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Morosinotto C, Stier A, Ruuskanen S, Garcin N, Karell P. Does colour-morph variation in metabolic physiology and oxidative stress match morph-specific life-history strategies? Oecologia 2025; 207:89. [PMID: 40418251 PMCID: PMC12106557 DOI: 10.1007/s00442-025-05728-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/04/2023] [Accepted: 05/09/2025] [Indexed: 05/27/2025]
Abstract
Understanding to what extent phenotypes vary in their physiological traits and their associations to life-history strategies may help to better understand how animals are adapted to their environment and how they can cope with changing conditions. Melanin-based colour polymorphism is a phenotypic trait closely associated with physiological characteristics and fitness, which in tawny owls (Strix aluco) is highly heritable and strongly associated with adult survival. Pheomelanic (brown) tawny owl adults raise heavier offspring, suggesting higher parental effort and/or faster growth of brown offspring, but have shorter lifespan than grey ones. Moreover, brown morphs show faster rate of telomere shortening than the grey morph, but only after reaching adulthood. To further explore the potential physiological mechanisms being involved in such trade-offs, we aimed at characterizing markers of metabolic physiology (thyroid hormones and mitochondrial density) and oxidative stress (reactive-oxygen metabolites) between brown and grey tawny owls, both at the nestling and adult stages. Although there was no significant effect of colour morph on thyroid hormones or mitochondrial density, brown nestlings had higher oxidative damage levels than grey individuals. Conversely in adults, mitochondrial density was higher in brown individuals, without a significant impact on oxidative stress levels. Morph-specific differences in physiological traits are thus life-stage dependent, but seem to match morph-specific life-history strategies since the higher oxidative stress observed in brown nestlings could result from their faster growth, while the higher mitochondrial density of brown adults could help in supporting their higher reproductive effort.
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Affiliation(s)
- Chiara Morosinotto
- Department of Biology, Lund University, Ecology Building, SE-223 62, Lund, Sweden
- Novia University of Applied Sciences, Faculty of Bioeconomy, FI-10600, Ekenäs, Finland
- Department of Biology, University of Padova, 35121, Padova, Italy
- National Biodiversity Future Center (NBFC), 90133, Palermo, Italy
| | - Antoine Stier
- Department of Biology, University of Turku, FI-20014, Turku, Finland
- Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, F-69622, Villeurbanne, France
- Institut Pluridisciplinaire Hubert Curien, UMR7178, Université de Strasbourg, CNRS, Strasbourg, France
| | - Suvi Ruuskanen
- Department of Biology, University of Turku, FI-20014, Turku, Finland
- Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland
| | - Natacha Garcin
- Department of Biology, University of Turku, FI-20014, Turku, Finland
| | - Patrik Karell
- Department of Biology, Lund University, Ecology Building, SE-223 62, Lund, Sweden.
- Novia University of Applied Sciences, Faculty of Bioeconomy, FI-10600, Ekenäs, Finland.
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2
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Marciau C, Bestley S, Costantini D, Hicks O, Hindell M, Kato A, Raclot T, Ribout C, Ropert-Coudert Y, Angelier F. Sibling similarity in telomere length in Adélie penguin chicks. Comp Biochem Physiol A Mol Integr Physiol 2025; 302:111818. [PMID: 39884423 DOI: 10.1016/j.cbpa.2025.111818] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/11/2024] [Revised: 01/23/2025] [Accepted: 01/24/2025] [Indexed: 02/01/2025]
Abstract
Early life telomere length is thought to influence and predict an individual's fitness. It has been shown to vary significantly in early life compared to adulthood. Investigating the factors influencing telomere length in young individuals is therefore of particular interest, especially as the relative importance of heredity compared to post-natal conditions remains largely uncertain. Adélie penguins are eco-indicators of the Antarctic ecosystem and their population are currently undergoing variable trajectories due to climate change. Here, we conducted a correlative study to investigate how telomere length was influenced by external and internal factors in Adélie penguin chicks. We found that most of the parameters we tested, including sex, body mass, brood size and hatching order as well as parental foraging trip duration, did not significantly influence chick telomere length at 32 days. However, siblings had similar telomere length, suggesting that hereditary factors play a stronger role in determining telomere length at this stage compared to the post-natal environment. In addition, telomere length and oxidative damage did not directly correlate but did interact in a complex way mediated by chick mass. High levels of oxidative damage were associated with longer telomeres in heavy chicks, whereas they were associated with shorter telomeres in light chicks. Although this mass-dependent relationship between telomere length and oxidative damage needs to be confirmed in future studies, it could reflect two different scenarios: (1) short telomeres may mimic the cost of poor nutritional conditions and oxidative damage in light chicks; (2) long telomeres may be maintained despite high oxidative damage in heavy chicks thanks to optimal nutritional conditions.
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Affiliation(s)
- Coline Marciau
- Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia; Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France.
| | - Sophie Bestley
- Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia
| | - David Costantini
- Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Universit'a, 01100 Viterbo, Italy; Unité Physiologie Moléculaire et Adaptation, UMR7221-Muséum National d'Histoire Naturelle-CNRS, 75005 Paris, France
| | - Olivia Hicks
- Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France
| | - Mark Hindell
- Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia
| | - Akiko Kato
- Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France
| | - Thierry Raclot
- Institut Pluridisciplinaire Hubert Curien, CNRS-UMR7178, Strasbourg, France
| | - Cécile Ribout
- Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France
| | - Yan Ropert-Coudert
- Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France
| | - Frederic Angelier
- Centre d'Etudes Biologiques de Chizé, UMR7372 CNRS-La Rochelle Université, Villiers en Bois, France
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Wolf SE, Woodruff MJ, Chang van Oordt DA, Clotfelter ED, Cristol DA, Derryberry EP, Ferguson SM, Stanback MT, Taff CC, Vitousek MN, Westneat DF, Rosvall KA. Among-population variation in telomere regulatory proteins and their potential role as hidden drivers of intraspecific variation in life history. J Anim Ecol 2025; 94:303-315. [PMID: 38509838 PMCID: PMC11415550 DOI: 10.1111/1365-2656.14071] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2023] [Accepted: 01/14/2024] [Indexed: 03/22/2024]
Abstract
Biologists aim to explain patterns of growth, reproduction and ageing that characterize life histories, yet we are just beginning to understand the proximate mechanisms that generate this diversity. Existing research in this area has focused on telomeres but has generally overlooked the telomere's most direct mediator, the shelterin protein complex. Shelterin proteins physically interact with the telomere to shape its shortening and repair. They also regulate metabolism and immune function, suggesting a potential role in life history variation in the wild. However, research on shelterin proteins is uncommon outside of biomolecular work. Intraspecific analyses can play an important role in resolving these unknowns because they reveal subtle variation in life history within and among populations. Here, we assessed ecogeographic variation in shelterin protein abundance across eight populations of tree swallow (Tachycineta bicolor) with previously documented variation in environmental and life history traits. Using the blood gene expression of four shelterin proteins in 12-day-old nestlings, we tested the hypothesis that shelterin protein gene expression varies latitudinally and in relation to both telomere length and life history. Shelterin protein gene expression differed among populations and tracked non-linear variation in latitude: nestlings from mid-latitudes expressed nearly double the shelterin mRNA on average than those at more northern and southern sites. However, telomere length was not significantly related to latitude. We next assessed whether telomere length and shelterin protein gene expression correlate with 12-day-old body mass and wing length, two proxies of nestling growth linked to future fecundity and survival. We found that body mass and wing length correlated more strongly (and significantly) with shelterin protein gene expression than with telomere length. These results highlight telomere regulatory shelterin proteins as potential mediators of life history variation among populations. Together with existing research linking shelterin proteins and life history variation within populations, these ecogeographic patterns underscore the need for continued integration of ecology, evolution and telomere biology, which together will advance understanding of the drivers of life history variation in nature.
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Affiliation(s)
- Sarah E. Wolf
- Department of BiologyIndiana UniversityBloomingtonIndianaUSA
- Institute of Evolutionary Biology, School of Biological SciencesUniversity of EdinburghEdinburghUK
| | | | - David A. Chang van Oordt
- Department of Ecology and Evolutionary BiologyCornell UniversityIthacaNew YorkUSA
- Cornell Lab of OrnithologyIthacaNew YorkUSA
| | | | | | | | - Stephen M. Ferguson
- Department of BiologyUniversity of KentuckyLexingtonKentuckyUSA
- Department of BiologyUniversity of RichmondRichmondVirginiaUSA
| | | | - Conor C. Taff
- Department of Ecology and Evolutionary BiologyCornell UniversityIthacaNew YorkUSA
- Cornell Lab of OrnithologyIthacaNew YorkUSA
| | - Maren N. Vitousek
- Department of Ecology and Evolutionary BiologyCornell UniversityIthacaNew YorkUSA
- Cornell Lab of OrnithologyIthacaNew YorkUSA
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4
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Shephard AM, Ledón-Rettig CC. A novel carnivorous diet reduces brain telomere length. Biol Lett 2025; 21:20240593. [PMID: 39933569 PMCID: PMC11813587 DOI: 10.1098/rsbl.2024.0593] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/15/2024] [Revised: 12/17/2024] [Accepted: 12/19/2024] [Indexed: 02/13/2025] Open
Abstract
Developmental conditions can profoundly influence adult survival or longevity. One established correlate of longevity is the length of telomeres-non-coding DNA regions that protect chromosomal ends. Telomere length in adulthood can be influenced by environmental conditions during development, such as nutrient restriction. Yet, we lack experimental studies of how adult telomere length is affected by a different form of nutritional variation: diet type. Here, we asked how diet-type variation during larval development affects telomere length in multiple post-metamorphic somatic tissues of the Mexican spadefoot (Spea multiplicata), an anuran species whose larvae develop on two qualitatively distinct diets: an ancestral omnivorous diet of detritus or a more novel carnivorous diet of live shrimp. We found that larvae developing on the novel shrimp diet developed into post-metamorphic frogs with shorter telomeres in the brain-a structure that is particularly vulnerable to harmful effects of nutritional adversity, such as oxidative stress. Given known links between telomere length and neurological health outcomes, our study suggests that a dietary transition to carnivory might carry costs in terms of compromised neural integrity later in life. This work highlights the lasting impact of a developmental diet on somatic maintenance and health.
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Sadler DE, Watts PC, Uusi-Heikkilä S. Directional selection, not the direction of selection, affects telomere length and copy number at ribosomal RNA loci. Sci Rep 2024; 14:12162. [PMID: 38802448 PMCID: PMC11130246 DOI: 10.1038/s41598-024-63030-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2024] [Accepted: 05/23/2024] [Indexed: 05/29/2024] Open
Abstract
Many fisheries exert directional selection on traits such as body size and growth rate. Whether directional selection impacts regions of the genome associated with traits related to growth is unknown. To address this issue, we characterised copy number variation in three regions of the genome associated with cell division, (1) telomeric DNA, (2) loci transcribed as ribosomal RNA (rDNA), and (3) mitochondrial DNA (mtDNA), in three selection lines of zebrafish reared at three temperatures (22 °C, 28 °C, and 34 °C). Selection lines differed in (1) the direction of selection (two lines experienced directional selection for large or small body size) and (2) whether they experienced any directional selection itself. Lines that had experienced directional selection were smaller, had lower growth rate, shorter telomeres, and lower rDNA copy number than the line that experiencing no directional selection. Neither telomere length nor rDNA copy number were affected by temperature. In contrast, mtDNA content increased at elevated temperature but did not differ among selection lines. Though directional selection impacts rDNA and telomere length, direction of such selection did not matter, whereas mtDNA acts as a stress marker for temperature. Future work should examine the consequences of these genomic changes in natural fish stocks.
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Affiliation(s)
- Daniel E Sadler
- Department of Biological and Environmental Science, University of Jyväskylä, 40014, Jyväskylä, Finland.
| | - Phillip C Watts
- Department of Biological and Environmental Science, University of Jyväskylä, 40014, Jyväskylä, Finland
| | - Silva Uusi-Heikkilä
- Department of Biological and Environmental Science, University of Jyväskylä, 40014, Jyväskylä, Finland
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Ravindran S, Underwood SL, Dorrens J, Seeker LA, Watt K, Wilbourn RV, Sparks AM, Sinclair R, Chen Z, Pilkington JG, McNeilly TN, Harrington L, Pemberton JM, Nussey DH, Froy H. No correlative evidence of costs of infection or immunity on leucocyte telomere length in a wild population of Soay sheep. Proc Biol Sci 2024; 291:20232946. [PMID: 38565156 PMCID: PMC10987235 DOI: 10.1098/rspb.2023.2946] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/29/2023] [Accepted: 03/04/2024] [Indexed: 04/04/2024] Open
Abstract
Telomere length (TL) is a biomarker hypothesized to capture evolutionarily and ecologically important physiological costs of reproduction, infection and immunity. Few studies have estimated the relationships among infection status, immunity, TL and fitness in natural systems. The hypothesis that short telomeres predict reduced survival because they reflect costly consequences of infection and immune investment remains largely untested. Using longitudinal data from a free-living Soay sheep population, we tested whether leucocyte TL was predicted by infection with nematode parasites and antibody levels against those parasites. Helminth parasite burdens were positively associated with leucocyte TL in both lambs and adults, which is not consistent with TL reflecting infection costs. We found no association between TL and helminth-specific IgG levels in either young or old individuals which suggests TL does not reflect costs of an activated immune response or immunosenescence. Furthermore, we found no support for TL acting as a mediator of trade-offs between infection, immunity and subsequent survival in the wild. Our results suggest that while variation in TL could reflect short-term variation in resource investment or environmental conditions, it does not capture costs of infection and immunity, nor does it behave like a marker of an individual's helminth-specific antibody immune response.
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Affiliation(s)
- Sanjana Ravindran
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Sarah L. Underwood
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Jennifer Dorrens
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Luise A. Seeker
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Kathryn Watt
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Rachael V. Wilbourn
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Alexandra M. Sparks
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
- School of Biosciences, University of Sheffield, Sheffield S10 2TN, UK
| | - Rona Sinclair
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Zhulin Chen
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Jill G. Pilkington
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Tom N. McNeilly
- Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, UK
| | - Lea Harrington
- Institute for Research in Immunology and Cancer, Université de Montréal, Montréal, Canada H3C 3J7
| | - Josephine M. Pemberton
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Daniel H. Nussey
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
| | - Hannah Froy
- Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
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7
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Lunghi E, Bilandžija H. Telomere length and dynamics in Astyanax mexicanus cave and surface morphs. PeerJ 2024; 12:e16957. [PMID: 38435987 PMCID: PMC10908260 DOI: 10.7717/peerj.16957] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/13/2023] [Accepted: 01/25/2024] [Indexed: 03/05/2024] Open
Abstract
Background Telomeres are non-coding DNA repeats at the chromosome ends and their shortening is considered one of the major causes of aging. However, they also serve as a biomarker of environmental exposures and their length and attrition is affected by various stressors. In this study, we examined the average telomere length in Astyanax mexicanus, a species that has both surface-dwelling and cave-adapted populations. The cave morph descended from surface ancestors and adapted to a markedly different environment characterized by specific biotic and abiotic stressors, many of which are known to affect telomere length. Our objective was to explore whether telomere length differs between the two morphs and whether it serves as a biological marker of aging or correlates with the diverse environments the morphs are exposed to. Methods We compared telomere length and shortening between laboratory-reared Pachón cavefish and Rio Choy surface fish of A. mexicanus across different tissues and ages. Results Astyanax mexicanus surface fish exhibited longer average telomere length compared to cavefish. In addition, we did not observe telomere attrition in either cave or surface form as a result of aging in adults up to 9 years old, suggesting that efficient mechanisms prevent telomere-mediated senescence in laboratory stocks of this species, at least within this time frame. Our results suggest that telomere length in Astyanax may be considered a biomarker of environmental exposures. Cavefish may have evolved shorter and energetically less costly telomeres due to the absence of potential stressors known to affect surface species, such as predator pressure and ultra-violet radiation. This study provides the first insights into telomere dynamics in Astyanax morphs and suggests that shorter telomeres may have evolved as an adaptation to caves.
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Affiliation(s)
- Enrico Lunghi
- Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy
| | - Helena Bilandžija
- Division of Molecular Biology, Ruder Bošković Institute, Zagreb, Croatia
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8
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Pepke ML. Telomere length is not a useful tool for chronological age estimation in animals. Bioessays 2024; 46:e2300187. [PMID: 38047504 DOI: 10.1002/bies.202300187] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2023] [Revised: 11/16/2023] [Accepted: 11/20/2023] [Indexed: 12/05/2023]
Abstract
Telomeres are short repetitive DNA sequences capping the ends of chromosomes. Telomere shortening occurs during cell division and may be accelerated by oxidative damage or ameliorated by telomere maintenance mechanisms. Consequently, telomere length changes with age, which was recently confirmed in a large meta-analysis across vertebrates. However, based on the correlation between telomere length and age, it was concluded that telomere length can be used as a tool for chronological age estimation in animals. Correlation should not be confused with predictability, and the current data and studies suggest that telomeres cannot be used to reliably predict individual chronological age. There are biological reasons for why there is large individual variation in telomere dynamics, which is mainly due to high susceptibility to a wide range of environmental, but also genetic factors, rendering telomeres unfeasible as a tool for age estimation. The use of telomeres for chronological age estimation is largely a misguided effort, but its occasional reappearance in the literature raises concerns that it will mislead resources in wildlife conservation.
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Affiliation(s)
- Michael L Pepke
- Center for Evolutionary Hologenomics, Globe Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
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9
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Amir Abdul Nasir AF, Niehaus AC, Cameron SF, Ujvari B, Madsen T, von Hippel FA, Gao S, Dillon DM, Buck CL, Charters J, Heiniger J, Blomberg S, Wilson RS. Manganese Exacerbates Seasonal Health Declines in a Suicidally Breeding Mammal. ENVIRONMENTAL TOXICOLOGY AND CHEMISTRY 2024; 43:74-86. [PMID: 37750553 DOI: 10.1002/etc.5753] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/13/2022] [Revised: 03/31/2023] [Accepted: 09/20/2023] [Indexed: 09/27/2023]
Abstract
Reproductive costs must be balanced with survival to maximize lifetime reproductive rates; however, some organisms invest in a single, suicidal bout of breeding known as semelparity. The northern quoll (Dasyurus hallucatus) is an endangered marsupial in which males, but not females, are semelparous. Northern quolls living near mining sites on Groote Eylandt, Northern Territory, Australia, accumulate manganese (Mn) in their brains, testes, and hair, and elevated Mn impacts motor performance. Whether Mn is associated with other health declines is yet unknown. In the present study we show that male and female northern quolls with higher Mn accumulation had a 20% reduction in immune function and a trend toward reduced cortisol concentrations in hair. The telomere lengths of male quolls did not change pre- to postbreeding, but those with higher Mn levels had longer telomeres; in contrast, the telomeres of females shortened during the breeding season but recovered between the first year and second year of breeding. In addition, the telomeres of quolls that were recaptured declined at significantly higher rates in quolls with higher Mn between prebreeding, breeding, and/or postbreeding seasons. Future research should determine whether changes in cortisol, immune function, or telomere length affect reproductive output or survival-particularly for semelparous males. Environ Toxicol Chem 2024;43:74-86. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
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Affiliation(s)
- Ami F Amir Abdul Nasir
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
| | - Amanda C Niehaus
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
| | - Skye F Cameron
- Australian Wildlife Conservancy, Subiaco East, Western Australia, Australia
| | - Beata Ujvari
- Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Victoria, Australia
| | - Thomas Madsen
- Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Victoria, Australia
| | - Frank A von Hippel
- Department of Community, Environment and Policy, The University of Arizona, Tucson, Arizona, USA
| | - Sisi Gao
- Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA
| | - Danielle M Dillon
- Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
| | - C Loren Buck
- Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
| | - Jordan Charters
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
| | - Jaime Heiniger
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
| | - Simone Blomberg
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
| | - Robbie S Wilson
- School of Biological Sciences, The University of Queensland, Saint Lucia, Queensland, Australia
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10
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Westneat DF, Young RC, Cones AG, Kucera AC, Anacleto A, Heidinger BJ. Early-life telomeres are influenced by environments acting at multiple temporal and spatial scales. Mol Ecol 2023; 32:5959-5970. [PMID: 37837282 DOI: 10.1111/mec.17166] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/23/2023] [Revised: 09/22/2023] [Accepted: 10/03/2023] [Indexed: 10/15/2023]
Abstract
An individual's telomere length early in life may reflect or contribute to key life-history processes sensitive to environmental variation. Yet, the relative importance of genetic and environmental factors in shaping early-life telomere length is not well understood as it requires samples collected from multiple generations with known developmental histories. We used a confirmed pedigree and conducted an animal model analysis of telomere lengths obtained from nestling house sparrows (Passer domesticus) sampled over a span of 22 years. We found significant additive genetic variation for early-life telomere length, but it comprised a small proportion (9%) of the total biological variation. Three sources of environmental variation were important: among cohorts, among-breeding attempts within years, and among nestmates. The magnitude of variation among breeding attempts and among nestmates also differed by cohort, suggesting that interactive effects of environmental factors across time or spatial scales were important, yet we were unable to identify the specific causes of these interactions. The mean amount of precipitation during the breeding season positively predicted telomere length, but neither weather during a given breeding attempt nor date in the breeding season contributed to an offspring's telomere length. At the level of individual nestlings, offspring sex, size and mass at 10 days of age also did not predict telomere length. Environmental effects appear especially important in shaping early-life telomere length in some species, and more focus on how environmental factors that interact across scales may help to explain some of the variation observed among studies.
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Affiliation(s)
- David F Westneat
- Department of Biology, University of Kentucky, Lexington, Kentucky, USA
| | - Rebecca C Young
- Department of Biology, North Dakota State University, Fargo, North Dakota, USA
| | - Alexandra G Cones
- Department of Biology, University of Kentucky, Lexington, Kentucky, USA
| | - Aurelia C Kucera
- Department of Biology, North Dakota State University, Fargo, North Dakota, USA
| | - Angelo Anacleto
- Department of Biology, North Dakota State University, Fargo, North Dakota, USA
| | - Britt J Heidinger
- Department of Biology, North Dakota State University, Fargo, North Dakota, USA
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11
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Power ML, Ransome RD, Riquier S, Romaine L, Jones G, Teeling EC. Hibernation telomere dynamics in a shifting climate: insights from wild greater horseshoe bats. Proc Biol Sci 2023; 290:20231589. [PMID: 37817598 PMCID: PMC10565397 DOI: 10.1098/rspb.2023.1589] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/16/2023] [Accepted: 09/10/2023] [Indexed: 10/12/2023] Open
Abstract
Hibernation is linked with various hypotheses to explain the extended lifespan of hibernating mammals compared with their non-hibernating counterparts. Studies on telomeres, markers of ageing and somatic maintenance, suggest telomere shortening slows during hibernation, and lengthening may reflect self-maintenance with favourable conditions. Bats in temperate zones adjust body temperatures during winter torpor to conserve energy and exploit mild conditions for foraging. Climate change may impact the hibernation cycle of bats, but more research is needed regarding the role of telomeres in understanding their response to a changing climate. Here, relative telomere length (rTL) was measured in the long-lived greater horseshoe bat Rhinolophus ferrumequinum (n = 223 individuals) over three winters, considering climatic conditions. Cross-sectional analyses revealed between-individual variation in rTL with a strong year effect, likely linked to varying weather conditions and foraging success. Additionally, within-individual increases of rTL occurred in 51% of consecutive measurements, with evidence of increasing telomerase expression during hibernation in this species. These findings highlight the beneficial effects of hibernation on telomeres and potential consequences of changing climatic conditions for long-lived temperate bats. Understanding the interplay between hibernation, telomeres, and climate can provide insights into the adaptive capacity and survival of bat populations facing environmental challenges.
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Affiliation(s)
- Megan L. Power
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Republic of Ireland
| | - Roger D. Ransome
- School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
| | - Sébastien Riquier
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Republic of Ireland
| | - Luke Romaine
- School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
| | - Gareth Jones
- School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
| | - Emma C. Teeling
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Republic of Ireland
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12
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Sirman AE, Schmidt JE, Clark ME, Kittilson JD, Reed WL, Heidinger BJ. Compensatory Growth Is Accompanied by Changes in Insulin-Like Growth Factor 1 but Not Markers of Cellular Aging in a Long-Lived Seabird. Am Nat 2023; 202:78-91. [PMID: 37384761 DOI: 10.1086/724599] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2023]
Abstract
AbstractDeveloping organisms often plastically modify growth in response to environmental circumstances, which may be adaptive but is expected to entail long-term costs. However, the mechanisms that mediate these growth adjustments and any associated costs are less well understood. In vertebrates, one mechanism that may be important in this context is the highly conserved signaling factor insulin-like growth factor 1 (IGF-1), which is frequently positively related to postnatal growth and negatively related to longevity. To test this idea, we exposed captive Franklin's gulls (Leucophaeus pipixcan) to a physiologically relevant nutritional stressor by restricting food availability during postnatal development and examined the effects on growth, IGF-1, and two potential biomarkers of cellular and organismal aging (oxidative stress and telomeres). During food restriction, experimental chicks gained body mass more slowly and had lower IGF-1 levels than controls. Following food restriction, experimental chicks underwent compensatory growth, which was accompanied by an increase in IGF-1 levels. Interestingly, however, there were no significant effects of the experimental treatment or of variation in IGF-1 levels on oxidative stress or telomeres. These findings suggest that IGF-1 is responsive to changes in resource availability but is not associated with increased markers of cellular aging during development in this relatively long-lived species.
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13
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Rouan A, Pousse M, Djerbi N, Porro B, Bourdin G, Carradec Q, Hume BC, Poulain J, Lê-Hoang J, Armstrong E, Agostini S, Salazar G, Ruscheweyh HJ, Aury JM, Paz-García DA, McMinds R, Giraud-Panis MJ, Deshuraud R, Ottaviani A, Morini LD, Leone C, Wurzer L, Tran J, Zoccola D, Pey A, Moulin C, Boissin E, Iwankow G, Romac S, de Vargas C, Banaigs B, Boss E, Bowler C, Douville E, Flores M, Reynaud S, Thomas OP, Troublé R, Thurber RV, Planes S, Allemand D, Pesant S, Galand PE, Wincker P, Sunagawa S, Röttinger E, Furla P, Voolstra CR, Forcioli D, Lombard F, Gilson E. Telomere DNA length regulation is influenced by seasonal temperature differences in short-lived but not in long-lived reef-building corals. Nat Commun 2023; 14:3038. [PMID: 37263999 DOI: 10.1038/s41467-023-38499-1] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/22/2022] [Accepted: 04/26/2023] [Indexed: 06/03/2023] Open
Abstract
Telomeres are environment-sensitive regulators of health and aging. Here,we present telomere DNA length analysis of two reef-building coral genera revealing that the long- and short-term water thermal regime is a key driver of between-colony variation across the Pacific Ocean. Notably, there are differences between the two studied genera. The telomere DNA lengths of the short-lived, more stress-sensitive Pocillopora spp. colonies were largely determined by seasonal temperature variation, whereas those of the long-lived, more stress-resistant Porites spp. colonies were insensitive to seasonal patterns, but rather influenced by past thermal anomalies. These results reveal marked differences in telomere DNA length regulation between two evolutionary distant coral genera exhibiting specific life-history traits. We propose that environmentally regulated mechanisms of telomere maintenance are linked to organismal performances, a matter of paramount importance considering the effects of climate change on health.
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Affiliation(s)
- Alice Rouan
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France.
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France.
| | - Melanie Pousse
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Nadir Djerbi
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Barbara Porro
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | | | - Quentin Carradec
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - Benjamin Cc Hume
- Department of Biology, University of Konstanz, Konstanz, Germany
| | - Julie Poulain
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - Julie Lê-Hoang
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - Eric Armstrong
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - Sylvain Agostini
- Shimoda Marine Research Center, University of Tsukuba, Shimoda, Japan
| | - Guillem Salazar
- Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich, 8092, Zurich, Switzerland
| | - Hans-Joachim Ruscheweyh
- Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich, 8092, Zurich, Switzerland
| | - Jean-Marc Aury
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - David A Paz-García
- Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Av. IPN 195, La Paz, Baja California Sur, 23096, La Paz, México
| | - Ryan McMinds
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- University of South Florida Center for Global Health and Infectious Diseases Research, Tampa, FL, USA
- Maison de la Modélisation, de la Simulation et des Interactions (MSI),, Université Côte d'Azur, Nice, France
| | - Marie-Josèphe Giraud-Panis
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Romane Deshuraud
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Alexandre Ottaviani
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Lycia Die Morini
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
| | - Camille Leone
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
| | - Lia Wurzer
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
| | - Jessica Tran
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
| | - Didier Zoccola
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Centre Scientifique de Monaco, Principality of Monaco, Monaco, Monaco
| | - Alexis Pey
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Clémentine Moulin
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Tara Ocean Foundation, 8 rue de Prague, 75012, Paris, France
| | - Emilie Boissin
- Laboratoire d'Excellence "CORAIL," PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan Cedex, France
| | - Guillaume Iwankow
- Laboratoire d'Excellence "CORAIL," PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan Cedex, France
| | - Sarah Romac
- Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, ECOMAP, Roscoff, France
| | - Colomban de Vargas
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, ECOMAP, Roscoff, France
| | - Bernard Banaigs
- Laboratoire d'Excellence "CORAIL," PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan Cedex, France
| | - Emmanuel Boss
- School of Marine Sciences, University of Maine, Orono, ME, USA
| | - Chris Bowler
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France
| | - Eric Douville
- Laboratoire des Sciences du Climat et de l'Environnement, LSCE/IPSL, CEA-CNRS-UVSQ, Université Paris-Saclay, 91191, Gif-sur-Yvette, France
| | - Michel Flores
- Weizmann Institute of Science, Department of Earth, and Planetary Sciences, 76100, Rehovot, Israel
| | - Stéphanie Reynaud
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Centre Scientifique de Monaco, Principality of Monaco, Monaco, Monaco
| | - Olivier P Thomas
- School of Biological and Chemical Sciences, Ryan Institute, University of Galway, University Road, H91TK33, Galway, Ireland
| | - Romain Troublé
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Tara Ocean Foundation, 8 rue de Prague, 75012, Paris, France
| | - Rebecca Vega Thurber
- Oregon State University, Department of Microbiology, 220 Nash Hall, Corvallis, OR, 97331, USA
| | - Serge Planes
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Laboratoire d'Excellence "CORAIL," PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan, Perpignan Cedex, France
| | - Denis Allemand
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Centre Scientifique de Monaco, Principality of Monaco, Monaco, Monaco
| | - Stephane Pesant
- European Bioinformatics Institute, Wellcome Genome Campus, European Molecular Biology Laboratory, Wellcome Genome Campus, Cambridge CB10 1SD, UK, UK
| | - Pierre E Galand
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Sorbonne Université, CNRS, Laboratoire d'Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls, Banyuls-sur-Mer, France
| | - Patrick Wincker
- Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
| | - Shinichi Sunagawa
- Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich, 8092, Zurich, Switzerland
| | - Eric Röttinger
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Paola Furla
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | | | - Didier Forcioli
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France
| | - Fabien Lombard
- Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GO-SEE, 75016, Paris, France
- Sorbonne Université, Institut de la Mer de Villefranche sur mer, Laboratoire d'Océanographie de Villefranche, Villefranche-sur-Mer, France
- Institut Universitaire de France, Ministère chargé de l'enseignement supérieur, Paris, France
| | - Eric Gilson
- Université Côte d'Azur-CNRS-Inserm-Institute for Research on Cancer and Ageing, Nice (IRCAN), Medical School, Nice, France.
- Laboratoire International Associé Université Côte d'Azur-Centre Scientifique de Monaco (LIA ROPSE), Monaco, Nice, France.
- Institut Fédératif de Recherche-Ressources Marines (IFR MARRES), Université Côte d'Azur, Nice, France.
- Department of Medical Genetics, CHU, Nice, France.
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14
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Byrjalsen A, Brainin AE, Lund TK, Andersen MK, Jelsig AM. Size matters in telomere biology disorders ‒ expanding phenotypic spectrum in patients with long or short telomeres. Hered Cancer Clin Pract 2023; 21:7. [PMID: 37189188 PMCID: PMC10184327 DOI: 10.1186/s13053-023-00251-7] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2023] [Accepted: 05/10/2023] [Indexed: 05/17/2023] Open
Abstract
The end of each chromosome consists of a DNA region termed the telomeres. The telomeres serve as a protective shield against degradation of the coding DNA sequence, as the DNA strand inevitably ‒ with each cell division ‒ is shortened. Inherited genetic variants cause telomere biology disorders when located in genes (e.g. DKC1, RTEL1, TERC, TERT) playing a role in the function and maintenance of the telomeres. Subsequently patients with telomere biology disorders associated with both too short or too long telomeres have been recognized. Patients with telomere biology disorders associated with short telomeres are at increased risk of dyskeratosis congenita (nail dystrophy, oral leukoplakia, and hyper- or hypo-pigmentation of the skin), pulmonary fibrosis, hematologic disease (ranging from cytopenia to leukemia) and in rare cases very severe multiorgan manifestations and early death. Patients with telomere biology disorders associated with too long telomeres have in recent years been found to confer an increased risk of melanoma and chronic lymphocytic leukemia. Despite this, many patients have an apparently isolated manifestation rendering telomere biology disorders most likely underdiagnosed. The complexity of telomere biology disorders and many causative genes makes it difficult to design a surveillance program which will ensure identification of early onset disease manifestation without overtreatment.
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Affiliation(s)
- Anna Byrjalsen
- Department of Clinical Genetics, Rigshospitalet, University Hospital of Copenhagen, Blegdamsvej 9, 2100, Copenhagen East, Denmark.
| | - Anna Engell Brainin
- Department of Clinical Genetics, Rigshospitalet, University Hospital of Copenhagen, Blegdamsvej 9, 2100, Copenhagen East, Denmark
| | - Thomas Kromann Lund
- Department of Cardiology, Section for Lung Transplantation, Rigshospitalet, University Hospital of Copenhagen, Blegdamsvej 9, Copenhagen East, 2100, Denmark
| | - Mette Klarskov Andersen
- Department of Clinical Genetics, Rigshospitalet, University Hospital of Copenhagen, Blegdamsvej 9, 2100, Copenhagen East, Denmark
| | - Anne Marie Jelsig
- Department of Clinical Genetics, Rigshospitalet, University Hospital of Copenhagen, Blegdamsvej 9, 2100, Copenhagen East, Denmark
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15
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Xu X, Li G, Zhang D, Zhu H, Liu G, Zhang Z. Gut Microbiota is Associated with Aging-Related Processes of a Small Mammal Species under High-Density Crowding Stress. ADVANCED SCIENCE (WEINHEIM, BADEN-WURTTEMBERG, GERMANY) 2023; 10:e2205346. [PMID: 36965140 PMCID: PMC10190659 DOI: 10.1002/advs.202205346] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/15/2022] [Revised: 02/15/2023] [Indexed: 05/18/2023]
Abstract
Humans and animals frequently encounter high-density crowding stress, which may accelerate their aging processes; however, the roles of gut microbiota in the regulation of aging-related processes under high-density crowding stress remain unclear. In the present study, it is found that high housing density remarkably increases the stress hormone (corticosterone), accelerates aging-related processes as indicated by telomere length (in brain and liver cells) and DNA damage or inflammation (as revealed by tumor necrosis factor-α and interleukin-10 levels), and reduces the lifespan of Brandt's vole (Lasiopodomys brandtii). Fecal microbiota transplantation from donor voles of habitats with different housing densities induces similar changes in aging-related processes in recipient voles. The elimination of high housing density or butyric acid administration delays the appearance of aging-related markers in the brain and liver cells of voles housed at high-density. This study suggests that gut microorganisms may play a significant role in regulating the density-dependent aging-related processes and subsequent population dynamics of animals, and can be used as potential targets for alleviating stress-related aging in humans exposed to high-density crowding stress.
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Affiliation(s)
- Xiaoming Xu
- State Key Laboratory of Integrated Management of Pest Insects and RodentsInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- University of Chinese Academy of SciencesBeijing100049China
| | - Guoliang Li
- State Key Laboratory of Integrated Management of Pest Insects and RodentsInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- CAS Center for Excellence in Biotic InteractionsUniversity of Chinese Academy of SciencesBeijing100049China
| | - Da Zhang
- State Key Laboratory of Integrated Management of Pest Insects and RodentsInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- University of Chinese Academy of SciencesBeijing100049China
| | - Hanyi Zhu
- State Key Laboratory of Integrated Management of Pest Insects and RodentsInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- University of Chinese Academy of SciencesBeijing100049China
| | - Guang‐hui Liu
- Institute for Stem cell and RegenerationCASBeijing100049China
- State Key Laboratory of Membrane BiologyInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- Beijing Institute for Stem Cell and Regenerative MedicineBeijing100101China
| | - Zhibin Zhang
- State Key Laboratory of Integrated Management of Pest Insects and RodentsInstitute of ZoologyChinese Academy of SciencesBeijing100101China
- CAS Center for Excellence in Biotic InteractionsUniversity of Chinese Academy of SciencesBeijing100049China
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16
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Voirin CJ, Tsunekage T, Liu Y, Alexy KF, Levin II. Brood size is associated with apparent telomere lengthening in nestling barn swallows. Oecologia 2023; 202:29-40. [PMID: 37087699 DOI: 10.1007/s00442-023-05375-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/15/2022] [Accepted: 04/12/2023] [Indexed: 04/24/2023]
Abstract
Early life for animals is often a time of rapid growth and development. In a resource-limited environment, life history theory predicts that there must be trade-offs between resource sinks in ways that optimize future survival and reproductive success. Telomeres have emerged as putative indicators of these early life trade-offs, but there are conflicting accounts as to how developmental traits and conditions impact telomere length and dynamics. For 2 years, we studied the nestlings of a breeding population of barn swallows from day 6 to day 12 of life, measuring various ontogenetic factors to understand to what extent they explain variation in telomere length and dynamics. We unexpectedly found that telomeres lengthened between the two sampling points. Nestlings in large broods had shorter telomeres, but surprisingly, individuals that grew faster from day 6 to day 12 had longer telomeres and more telomere lengthening. Nestlings with higher mass relative to their nestmates on d6 had shorter telomeres, suggesting that the relatively fast growth barn swallows experience early in development is more costly than the relatively slower growth later in development. These effects were only found in the first year of study. Telomere lengthening may be due to the initiation of new hematopoietic cell lines during development or the expression of telomerase early in life. Favorable early life conditions and high parental investment could allow for more growth with little to no cost to telomere length or dynamics.
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Affiliation(s)
| | - Toshi Tsunekage
- Department of Biology, Kenyon College, Gambier, OH, 43022, USA
| | - Yujie Liu
- Department of Biology, Kenyon College, Gambier, OH, 43022, USA
| | - Kate F Alexy
- Department of Biology, Kenyon College, Gambier, OH, 43022, USA
| | - Iris I Levin
- Department of Biology, Kenyon College, Gambier, OH, 43022, USA
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17
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D’Angiolo M, Yue JX, De Chiara M, Barré BP, Giraud Panis MJ, Gilson E, Liti G. Telomeres are shorter in wild Saccharomyces cerevisiae isolates than in domesticated ones. Genetics 2023; 223:iyac186. [PMID: 36563016 PMCID: PMC9991508 DOI: 10.1093/genetics/iyac186] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/02/2022] [Revised: 11/02/2022] [Accepted: 12/03/2022] [Indexed: 12/24/2022] Open
Abstract
Telomeres are ribonucleoproteins that cap chromosome-ends and their DNA length is controlled by counteracting elongation and shortening processes. The budding yeast Saccharomyces cerevisiae has been a leading model to study telomere DNA length control and dynamics. Its telomeric DNA is maintained at a length that slightly varies between laboratory strains, but little is known about its variation at the species level. The recent publication of the genomes of over 1,000 S. cerevisiae strains enabled us to explore telomere DNA length variation at an unprecedented scale. Here, we developed a bioinformatic pipeline (YeaISTY) to estimate telomere DNA length from whole-genome sequences and applied it to the sequenced S. cerevisiae collection. Our results revealed broad natural telomere DNA length variation among the isolates. Notably, telomere DNA length is shorter in those derived from wild rather than domesticated environments. Moreover, telomere DNA length variation is associated with mitochondrial metabolism, and this association is driven by wild strains. Overall, these findings reveal broad variation in budding yeast's telomere DNA length regulation, which might be shaped by its different ecological life-styles.
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Affiliation(s)
- Melania D’Angiolo
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
| | - Jia-Xing Yue
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
- State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Sun Yat-sen University Cancer Center (SYSUCC), 651 Dongfeng Road East, China
| | - Matteo De Chiara
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
| | - Benjamin P Barré
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
| | - Marie-Josèphe Giraud Panis
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
| | - Eric Gilson
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
- Department of Genetics, CHU, 06107 Nice, France
| | - Gianni Liti
- Institute for Research on Cancer and Aging (IRCAN), Université Côte d’Azur, 28 Avenue de Valombrose, 06107 Nice, France
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18
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Wolf SE, Zhang S, Clotfelter ED. Experimental ectoparasite removal has a sex-specific effect on nestling telomere length. Ecol Evol 2023; 13:e9861. [PMID: 36911306 PMCID: PMC9992774 DOI: 10.1002/ece3.9861] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/09/2022] [Revised: 02/02/2023] [Accepted: 02/06/2023] [Indexed: 03/11/2023] Open
Abstract
Parasites are a strong selective force that can influence fitness-related traits. The length of chromosome-capping telomeres can be used to assess the long-term costs of parasitism, as telomere loss accelerates in response to environmental stressors and often precedes poorer survival prospects. Here, we explored the sex-specific effects of ectoparasite removal on morphology and telomere length in nestling tree swallows (Tachycineta bicolor). To do so, we experimentally removed blow fly (Protocalliphora spp.) larvae from nests using Permethrin, a broad-spectrum insecticide. Compared to water-treated controls, insecticide treatment of nests had a sex-biased effect on blood telomere length: ectoparasite removal resulted in significantly longer telomeres in males but not females. While this treatment did not influence nestling body mass, it was associated with reduced feather development regardless of sex. This may reflect a relaxed pressure to fledge quickly in the absence of parasites, or alternatively, could be a negative side effect of permethrin on morphology. Exploring robust sex-specific telomere dynamics in response to early-life environmental pressures such as parasitism will shed light on sexual dimorphism in adult life histories and aging.
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Affiliation(s)
- Sarah E. Wolf
- Department of BiologyIndiana UniversityBloomingtonIndianaUSA
- Department of Biobehavioral HealthPennsylvania State UniversityState CollegePennsylvaniaUSA
| | - Samuel Zhang
- Department of BiologyAmherst CollegeAmherstMassachusettsUSA
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19
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Armstrong E, Boonekamp J. Does oxidative stress shorten telomeres in vivo? A meta-analysis. Ageing Res Rev 2023; 85:101854. [PMID: 36657619 DOI: 10.1016/j.arr.2023.101854] [Citation(s) in RCA: 47] [Impact Index Per Article: 23.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/05/2022] [Revised: 12/18/2022] [Accepted: 01/15/2023] [Indexed: 01/18/2023]
Abstract
Telomere attrition is considered a hallmark of ageing. Untangling the proximate causes of telomere attrition may therefore reveal important aspects about the ageing process. In a landmark paper in 2002 Thomas von Zglinicki demonstrated that oxidative stress accelerates telomere attrition in cell culture. In the next 20 years, oxidative stress became firmly embedded into modern theories of ageing and telomere attrition. However, a recent surge of in vivo studies reveals an inconsistent pattern questioning the unequivocal role of oxidative stress in telomere length and telomere attrition (henceforth referred to as telomere dynamics), in living organisms. Here we report the results of the first formal meta-analysis on the association between oxidative stress and telomere dynamics in vivo, representing 37 studies, 4969 individuals, and 18,677 correlational measurements. The overall correlation between oxidative stress markers and telomere dynamics was indistinguishable from zero (r = 0.027). This result was independent of the type of oxidative stress marker, telomere dynamic, or taxonomic group. However, telomere measurement method affected the analysis and the subset of TRF-based studies showed a significant overall correlation (r = 0.09), supporting the prediction that oxidative stress accelerates telomere attrition. The correlation was more pronounced in short-lived species and during the adult life phase, when ageing becomes apparent. We then performed an additional meta-analysis of interventional studies (n = 7) manipulating oxidative stress. This revealed a significant effect of treatment on telomere dynamics (d=0.36). Our findings provide new support for the hypothesis that oxidative stress causes telomere attrition in living organisms.
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Affiliation(s)
- Emma Armstrong
- School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom; The Roslin Institute, The University of Edinburgh, Easter Bush Campus, Midlothian, United Kingdom
| | - Jelle Boonekamp
- School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.
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20
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Çelen İ, Jayasinghe A, Doh JH, Sabanayagam CR. Transcriptomic Signature of the Simulated Microgravity Response in Caenorhabditis elegans and Comparison to Spaceflight Experiments. Cells 2023; 12:270. [PMID: 36672205 PMCID: PMC9856674 DOI: 10.3390/cells12020270] [Citation(s) in RCA: 7] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2022] [Revised: 12/25/2022] [Accepted: 12/28/2022] [Indexed: 01/13/2023] Open
Abstract
Given the growing interest in human exploration of space, it is crucial to identify the effects of space conditions on biological processes. Here, we analyze the transcriptomic response of Caenorhabditis elegans to simulated microgravity and observe the maintained transcriptomic response after returning to ground conditions for four, eight, and twelve days. We show that 75% of the simulated microgravity-induced changes on gene expression persist after returning to ground conditions for four days while most of these changes are reverted after twelve days. Our results from integrative RNA-seq and mass spectrometry analyses suggest that simulated microgravity affects longevity-regulating insulin/IGF-1 and sphingolipid signaling pathways. Finally, we identified 118 genes that are commonly differentially expressed in simulated microgravity- and space-exposed worms. Overall, this work provides insight into the effect of microgravity on biological systems during and after exposure.
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Affiliation(s)
- İrem Çelen
- Center for Bioinformatics and Computational Biology, University of Delaware, Newark, DE 19711, USA
- Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, USA
| | - Aroshan Jayasinghe
- Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, USA
| | - Jung H. Doh
- Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, USA
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21
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Hope SF, Angelier F, Ribout C, Groffen J, Kennamer RA, Hopkins WA. Warmer incubation temperatures and later lay-orders lead to shorter telomere lengths in wood duck (Aix sponsa) ducklings. JOURNAL OF EXPERIMENTAL ZOOLOGY. PART A, ECOLOGICAL AND INTEGRATIVE PHYSIOLOGY 2023; 339:101-111. [PMID: 36214364 DOI: 10.1002/jez.2659] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/07/2022] [Revised: 07/27/2022] [Accepted: 09/19/2022] [Indexed: 12/15/2022]
Abstract
The environment that animals experience during development shapes phenotypic expression. In birds, two important aspects of the early-developmental environment are lay-order sequence and incubation. Later-laid eggs tend to produce weaker offspring, sometimes with compensatory mechanisms to accelerate their growth rate to catch-up to their siblings. Further, small decreases in incubation temperature slow down embryonic growth rates and lead to wide-ranging negative effects on many posthatch traits. Recently, telomeres, noncoding DNA sequences at the end of chromosomes, have been recognized as a potential proxy for fitness because longer telomeres are positively related to lifespan and individual quality in many animals, including birds. Although telomeres appear to be mechanistically linked to growth rate, little is known about how incubation temperature and lay-order may influence telomere length. We incubated wood duck (Aix sponsa) eggs at two ecologically-relevant temperatures (34.9°C and 36.2°C) and measured telomere length at hatch and 1 week after. We found that ducklings incubated at the lower temperature had longer telomeres than those incubated at the higher temperature both at hatch and 1 week later. Further, we found that later-laid eggs produced ducklings with shorter telomeres than those laid early in the lay-sequence, although lay-order was not related to embryonic developmental rate. This study contributes to our broader understanding of how parental effects can affect telomere length early in life. More work is needed to determine if these effects on telomere length persist until adulthood, and if they are associated with effects on fitness in this precocial species.
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Affiliation(s)
- Sydney F Hope
- Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, Virginia, USA.,Centre d'Etudes Biologiques de Chizé, CNRS-La Rochelle Université, UMR 7372, Villiers en Bois, France
| | - Frédéric Angelier
- Centre d'Etudes Biologiques de Chizé, CNRS-La Rochelle Université, UMR 7372, Villiers en Bois, France
| | - Cécile Ribout
- Centre d'Etudes Biologiques de Chizé, CNRS-La Rochelle Université, UMR 7372, Villiers en Bois, France
| | - Jordy Groffen
- Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, Virginia, USA
| | - Robert A Kennamer
- Savannah River Ecology Lab, University of Georgia, Aiken, South Carolina, USA
| | - William A Hopkins
- Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, Virginia, USA
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22
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Sepp T, Meitern R, Heidinger B, Noreikiene K, Rattiste K, Hõrak P, Saks L, Kittilson J, Urvik J, Giraudeau M. Parental age does not influence offspring telomeres during early life in common gulls (Larus canus). Mol Ecol 2022; 31:6197-6207. [PMID: 33772917 DOI: 10.1111/mec.15905] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/02/2020] [Revised: 02/27/2021] [Accepted: 03/22/2021] [Indexed: 01/31/2023]
Abstract
Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre- and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.
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Affiliation(s)
- Tuul Sepp
- Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Richard Meitern
- Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Britt Heidinger
- Biological Sciences Department, North Dakota State University, Fargo, ND, USA
| | - Kristina Noreikiene
- Institute of Veterinary Medicine, Estonian University of Life Sciences, Tartu, Estonia
| | - Kalev Rattiste
- Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia
| | - Peeter Hõrak
- Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
| | - Lauri Saks
- Estonian Marine Institute, University of Tartu, Tartu, Estonia
| | - Jeffrey Kittilson
- Biological Sciences Department, North Dakota State University, Fargo, ND, USA
| | - Janek Urvik
- Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia.,Institute of Biomedicine and Translational Medicine, University of Tartu, Tartu, Estonia
| | - Mathieu Giraudeau
- CREEC, Montpellier Cedex 5, France.,MIVEGEC, UMR IRD/CNRS/UM 5290, Montpellier Cedex 5, France
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23
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Friesen CR, Wapstra E, Olsson M. Of telomeres and temperature: Measuring thermal effects on telomeres in ectothermic animals. Mol Ecol 2022; 31:6069-6086. [PMID: 34448287 DOI: 10.1111/mec.16154] [Citation(s) in RCA: 15] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/03/2021] [Revised: 07/20/2021] [Accepted: 08/23/2021] [Indexed: 01/31/2023]
Abstract
Ectotherms are classic models for understanding life-history tradeoffs, including the reproduction-somatic maintenance tradeoffs that may be reflected in telomere length and their dynamics. Importantly, life-history traits of ectotherms are tightly linked to their thermal environment, with diverse or synergistic mechanistic explanations underpinning the variation. Telomere dynamics potentially provide a mechanistic link that can be used to monitor thermal effects on individuals in response to climatic perturbations. Growth rate, age and developmental stage are all affected by temperature, which interacts with telomere dynamics in complex and intriguing ways. The physiological processes underpinning telomere dynamics can be visualized and understood using thermal performance curves (TPCs). TPCs reflect the evolutionary history and the thermal environment during an individual's ontogeny. Telomere maintenance should be enhanced at or near the thermal performance optimum of a species, population and individual. The thermal sensitivity of telomere dynamics should reflect the interacting TPCs of the processes underlying them. The key processes directly underpinning telomere dynamics are mitochondrial function (reactive oxygen production), antioxidant activity, telomerase activity and telomere endcap protein status. We argue that identifying TPCs for these processes will significantly help design robust, repeatable experiments and field studies of telomere dynamics in ectotherms. Conceptually, TPCs are a valuable framework to predict and interpret taxon- and population-specific telomere dynamics across thermal regimes. The literature of thermal effects on telomeres in ectotherms is sparse and mostly limited to vertebrates, but our conclusions and recommendations are relevant across ectothermic animals.
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Affiliation(s)
- Christopher R Friesen
- School of Earth, Atmospheric and Life Sciences, The University of Wollongong, Wollongong, New South Wales, Australia.,School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia
| | - Erik Wapstra
- School of Natural Sciences, University of Tasmania, Hobart, Tasmania, Australia
| | - Mats Olsson
- School of Earth, Atmospheric and Life Sciences, The University of Wollongong, Wollongong, New South Wales, Australia.,Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden
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24
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Vedder O, Moiron M, Bichet C, Bauch C, Verhulst S, Becker PH, Bouwhuis S. Telomere length is heritable and genetically correlated with lifespan in a wild bird. Mol Ecol 2022; 31:6297-6307. [PMID: 33460462 DOI: 10.1111/mec.15807] [Citation(s) in RCA: 25] [Impact Index Per Article: 8.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/09/2020] [Revised: 12/18/2020] [Accepted: 01/08/2021] [Indexed: 01/31/2023]
Abstract
Telomeres are protective caps at the end of eukaryotic chromosomes that shorten with age and in response to stressful or resource-demanding conditions. Their length predicts individual health and lifespan across a wide range of animals, but whether the observed positive association between telomere length and lifespan is environmentally induced, or set at conception due to a shared genetic basis, has not been tested in wild animals. We applied quantitative genetic "animal models" to longitudinal telomere measurements collected over a 10-year period from individuals of a wild seabird (common tern; Sterna hirundo) with known pedigree. We found no variation in telomere shortening with age among individuals at the phenotypic and genetic level, and only a small permanent environmental effect on adult telomere length. Instead, we found telomere length to be highly heritable and strongly positively genetically correlated with lifespan. Such heritable differences between individuals that are set at conception may present a hitherto underappreciated component of variation in somatic state.
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Affiliation(s)
- Oscar Vedder
- Institute of Avian Research, Wilhelmshaven, Germany.,Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
| | - Maria Moiron
- Institute of Avian Research, Wilhelmshaven, Germany.,CEFE, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul Valéry Montpellier 3, Montpellier, France
| | | | - Christina Bauch
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
| | - Simon Verhulst
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
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25
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Tobler M, Gómez-Blanco D, Hegemann A, Lapa M, Neto JM, Tarka M, Xiong Y, Hasselquist D. Telomeres in ecology and evolution: A review and classification of hypotheses. Mol Ecol 2022; 31:5946-5965. [PMID: 34865259 DOI: 10.1111/mec.16308] [Citation(s) in RCA: 22] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2021] [Revised: 11/19/2021] [Accepted: 12/01/2021] [Indexed: 01/31/2023]
Abstract
Research on telomeres in the fields of ecology and evolution has been rapidly expanding over the last two decades. This has resulted in the formulation of a multitude of, often name-given, hypotheses related to the associations between telomeres and life-history traits or fitness-facilitating processes (and the mechanisms underlying them). However, the differences (or similarities) between the various hypotheses, which can originate from different research fields, are often not obvious. Our aim here is therefore to give an overview of the hypotheses that are of interest in ecology and evolution and to provide two frameworks that help discriminate among them. We group the hypotheses (i) based on their association with different research questions, and (ii) using a hierarchical approach that builds on the assumptions they make, such as about causality of telomere length/shortening and/or the proposed functional consequences of telomere shortening on organism performance. Both our frameworks show that there exist parallel lines of thoughts in different research fields. Moreover, they also clearly illustrate that there are in many cases competing hypotheses within clusters, and that some of these even have contradictory assumptions and/or predictions. We also touch upon two topics in telomere research that would benefit from further conceptualization. This review should help researchers, both those familiar with and those new to the subject, to identify future avenues of research.
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Affiliation(s)
| | | | - Arne Hegemann
- Department of Biology, Lund University, Lund, Sweden
| | - Mariana Lapa
- Department of Biology, Lund University, Lund, Sweden
| | - Júlio M Neto
- Department of Biology, Lund University, Lund, Sweden
| | - Maja Tarka
- Department of Biology, Lund University, Lund, Sweden
| | - Ye Xiong
- Department of Biology, Lund University, Lund, Sweden
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26
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Kauzálová T, Tomášek O, Mulder E, Verhulst S, Albrecht T. Telomere length is highly repeatable and shorter in individuals with more elaborate sexual ornamentation in a short-lived passerine. Mol Ecol 2022; 31:6172-6183. [PMID: 35150467 DOI: 10.1111/mec.16397] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2021] [Revised: 01/18/2022] [Accepted: 02/01/2022] [Indexed: 01/31/2023]
Abstract
Quantifying an individual's state as a fitness proxy has proven challenging, but accumulating evidence suggests that telomere length and attrition may indicate individual somatic state and success at self-maintenance, respectively. Sexual ornamentation is also thought to signal phenotypic quality, but links between telomeres and sexual ornamentation have been little explored. To address this issue, we examined whether telomere length and dynamics are predicted by the expression of a sexually selected ornament, the length of the outermost tail feathers (streamers), using longitudinal data from a population of European barn swallows (Hirundo rustica). In 139 adult individuals, each measured twice, we further assessed associations of telomere length with age, sex, breeding status and survival. Telomere length showed high individual repeatability (R = .97) across years while shortening with age in both sexes. Telomere length and dynamics were not significantly associated with survival to the next year, remaining lifespan or reproduction status (comparing breeding and nonbreeding yearlings). Tail streamer length, a sexually selected trait in barn swallows, was negatively associated with telomere length, independent of sex. Thus, telomere length may reflect the costs of carrying an elaborated sexual ornament, although ornament size did not significantly predict telomere shortening. In conclusion, telomere length in adult barn swallows is a highly consistent trait that shows a negative relationship with sexual ornamentation, suggesting a trade-off between sexual ornamentation and telomere length.
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Affiliation(s)
- Tereza Kauzálová
- Institute of Vertebrate Biology, The Czech Academy of Sciences, Brno, Czech Republic.,Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic
| | - Oldřich Tomášek
- Institute of Vertebrate Biology, The Czech Academy of Sciences, Brno, Czech Republic.,Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic
| | - Ellis Mulder
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
| | - Simon Verhulst
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
| | - Tomáš Albrecht
- Institute of Vertebrate Biology, The Czech Academy of Sciences, Brno, Czech Republic.,Department of Zoology, Faculty of Science, Charles University in Prague, Praha, Czech Republic
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27
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Sheldon EL, Eastwood JR, Teunissen N, Roast MJ, Aranzamendi NH, Fan M, Louise Hall M, Kingma SA, Verhulst S, Peters A. Telomere dynamics in the first year of life, but not later in life, predict lifespan in a wild bird. Mol Ecol 2022; 31:6008-6017. [PMID: 34850488 DOI: 10.1111/mec.16296] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2021] [Revised: 10/15/2021] [Accepted: 11/09/2021] [Indexed: 02/02/2023]
Abstract
Telomeres are protective, nucleoprotein structures at the end of chromosomes that have been associated with lifespan across taxa. However, the extent to which these associations can be attributed to absolute length vs. the rate of telomere shortening prior to sampling remains unresolved. In a longitudinal study, we examined the relationship between lifespan, telomere length and the rate of telomere shortening in wild, purple-crowned fairy-wrens (Malurus coronatus coronatus). To this end, we measured telomere length using quantitative polymerase chain reaction in the blood of 59 individuals sampled as nestlings and 4-14 months thereafter, and in 141 known-age individuals sampled on average three times across adulthood. We applied within-subject centring analyses to simultaneously test for associations between lifespan and average telomere length and telomere shortening. We reveal that the rate of telomere shortening and to a lesser extent telomere length in the first year of life independently predicted lifespan, with individuals with faster shortening rates and/or shorter telomeres living less long. In contrast, in adulthood neither telomere shortening nor telomere length predicted lifespan, despite a considerably larger data set. Our results suggest that telomere length measured very early in life (during development) and longitudinal assessments of telomere shortening during the first year of life constitute more useful biomarkers of total life expectancy than either telomere length measured after development, or telomere shortening later in adulthood.
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Affiliation(s)
| | | | - Niki Teunissen
- School of Biological Sciences, Monash University, Clayton, Vic, Australia
| | | | | | - Marie Fan
- School of Biological Sciences, Monash University, Clayton, Vic, Australia
| | - Michelle Louise Hall
- Max Planck Institute for Ornithology, Vogelwarte Radolfzell, Radolfzell, Germany.,Bush Heritage Australia, Melbourne, Vic, Australia.,School of Biological Sciences, University of Western Australia, Crawley, WA, Australia
| | - Sjouke Anne Kingma
- Max Planck Institute for Ornithology, Vogelwarte Radolfzell, Radolfzell, Germany
| | - Simon Verhulst
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands
| | - Anne Peters
- School of Biological Sciences, Monash University, Clayton, Vic, Australia.,Max Planck Institute for Ornithology, Vogelwarte Radolfzell, Radolfzell, Germany
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28
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Pepke ML, Kvalnes T, Lundregan S, Boner W, Monaghan P, Saether BE, Jensen H, Ringsby TH. Genetic architecture and heritability of early-life telomere length in a wild passerine. Mol Ecol 2022; 31:6360-6381. [PMID: 34825754 DOI: 10.1111/mec.16288] [Citation(s) in RCA: 11] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2021] [Revised: 10/01/2021] [Accepted: 11/09/2021] [Indexed: 01/31/2023]
Abstract
Early-life telomere length (TL) is associated with fitness in a range of organisms. Little is known about the genetic basis of variation in TL in wild animal populations, but to understand the evolutionary and ecological significance of TL it is important to quantify the relative importance of genetic and environmental variation in TL. In this study, we measured TL in 2746 house sparrow nestlings sampled across 20 years and used an animal model to show that there is a small heritable component of early-life TL (h2 = 0.04). Variation in TL among individuals was mainly driven by environmental (annual) variance, but also brood and parental effects. Parent-offspring regressions showed a large maternal inheritance component in TL ( h maternal 2 = 0.44), but no paternal inheritance. We did not find evidence for a negative genetic correlation underlying the observed negative phenotypic correlation between TL and structural body size. Thus, TL may evolve independently of body size and the negative phenotypic correlation is likely to be caused by nongenetic environmental effects. We further used genome-wide association analysis to identify genomic regions associated with TL variation. We identified several putative genes underlying TL variation; these have been inferred to be involved in oxidative stress, cellular growth, skeletal development, cell differentiation and tumorigenesis in other species. Together, our results show that TL has a low heritability and is a polygenic trait strongly affected by environmental conditions in a free-living bird.
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Affiliation(s)
- Michael Le Pepke
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
| | - Thomas Kvalnes
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
| | - Sarah Lundregan
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
| | - Winnie Boner
- Institute of Biodiversity, Animal Health and Comparative Medicine (IBAHCM), University of Glasgow, Glasgow, UK
| | - Pat Monaghan
- Institute of Biodiversity, Animal Health and Comparative Medicine (IBAHCM), University of Glasgow, Glasgow, UK
| | - Bernt-Erik Saether
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
| | - Henrik Jensen
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
| | - Thor Harald Ringsby
- Department of Biology, Centre for Biodiversity Dynamics (CBD), Norwegian University of Science and Technology (NTNU), Trondheim, Norway
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29
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Sheldon EL, Ton R, Boner W, Monaghan P, Raveh S, Schrey AW, Griffith SC. Associations between DNA methylation and telomere length during early life: Insight from wild zebra finches (Taeniopygia guttata). Mol Ecol 2022; 31:6261-6272. [PMID: 34551154 DOI: 10.1111/mec.16187] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2021] [Accepted: 09/10/2021] [Indexed: 01/31/2023]
Abstract
Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, especially during early life, yet surprisingly little is known about their reciprocal association, especially in natural populations. Here, we explore how variation in DNAm, growth rate, and early-life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere length dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in-gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between DNA based biomarkers of ageing, and of physiological reactions to environmental change.
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Affiliation(s)
- Elizabeth L Sheldon
- Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia
| | - Riccardo Ton
- Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia
| | - Winnie Boner
- Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
| | - Pat Monaghan
- Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
| | - Shirley Raveh
- Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
| | - Aaron W Schrey
- Department of Biology, Georgia Southern University, Armstrong Campus, Savannah, Georgia, USA
| | - Simon C Griffith
- Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia
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McLennan D, Auer SK, McKelvey S, McKelvey L, Anderson G, Boner W, Duprez JS, Metcalfe NB. Habitat restoration weakens negative environmental effects on telomere dynamics. Mol Ecol 2022; 31:6100-6113. [PMID: 33973299 DOI: 10.1111/mec.15980] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2021] [Revised: 04/16/2021] [Accepted: 04/27/2021] [Indexed: 02/01/2023]
Abstract
Habitat quality can have far-reaching effects on organismal fitness, an issue of concern given the current scale of habitat degradation. Many temperate upland streams have reduced nutrient levels due to human activity. Nutrient restoration confers benefits in terms of invertebrate food availability and subsequent fish growth rates. Here we test whether these mitigation measures also affect the rate of cellular ageing of the fish, measured in terms of the telomeres that cap the ends of eukaryotic chromosomes. We equally distributed Atlantic salmon eggs from the same 30 focal families into 10 human-impacted oligotrophic streams in northern Scotland. Nutrient levels in five of the streams were restored by simulating the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period, while five reference streams were left as controls. Telomere lengths and expression of the telomerase reverse transcriptase (TERT) gene that may act to lengthen telomeres were then measured in the young fish when 15 months old. While TERT expression was unrelated to any of the measured variables, telomere lengths were shorter in salmon living at higher densities and in areas with a lower availability of the preferred substrate (cobbles and boulders). However, the adverse effects of these habitat features were much reduced in the streams receiving nutrients. These results suggest that adverse environmental pressures are weakened when nutrients are restored, presumably because the resulting increase in food supply reduces levels of both competition and stress.
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Affiliation(s)
- Darryl McLennan
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK
| | - Sonya K Auer
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK.,Department of Biology, Williams College, Williamstown, MA, USA
| | | | | | - Graeme Anderson
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK
| | - Winnie Boner
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK
| | - Jessica S Duprez
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK
| | - Neil B Metcalfe
- Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK
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31
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Vernasco BJ, Watts HE. Telomere length predicts timing and intensity of migratory behaviour in a nomadic songbird. Biol Lett 2022; 18:20220176. [PMID: 35920029 PMCID: PMC9346355 DOI: 10.1098/rsbl.2022.0176] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/04/2022] [Accepted: 07/14/2022] [Indexed: 12/04/2022] Open
Abstract
Our understanding of state-dependent behaviour is reliant on identifying physiological indicators of condition. Telomeres are of growing interest for understanding behaviour as they capture differences in biological state and residual lifespan. To understand the significance of variable telomere lengths for behaviour and test two hypotheses describing the relationship between telomeres and behaviour (i.e. the causation and the selective adoption hypotheses), we assessed if telomere lengths are longitudinally repeatable traits related to spring migratory behaviour in captive pine siskins (Spinus pinus). Pine siskins are nomadic songbirds that exhibit highly flexible, facultative migrations, including a period of spring nomadism. Captive individuals exhibit extensive variation in spring migratory restlessness and are an excellent system for mechanistic studies of migratory behaviour. Telomere lengths were found to be significantly repeatable (R = 0.51) over four months, and shorter pre-migratory telomeres were associated with earlier and more intense expression of spring nocturnal migratory restlessness. Telomere dynamics did not vary with migratory behaviour. Our results describe the relationship between telomere length and migratory behaviour and provide support for the selective adoption hypothesis. More broadly, we provide a novel perspective on the significance of variable telomere lengths for animal behaviour and the timing of annual cycle events.
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Affiliation(s)
- Ben J. Vernasco
- School of Biological Sciences, Washington State University, Pullman, WA, USA
| | - Heather E. Watts
- School of Biological Sciences, Washington State University, Pullman, WA, USA
- Center for Reproductive Biology, Washington State University, Pullman, WA, USA
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32
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Marasco V, Smith S, Angelier F. How does early-life adversity shape telomere dynamics during adulthood? Problems and paradigms. Bioessays 2022; 44:e2100184. [PMID: 35122449 DOI: 10.1002/bies.202100184] [Citation(s) in RCA: 17] [Impact Index Per Article: 5.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/30/2021] [Revised: 01/18/2022] [Accepted: 01/20/2022] [Indexed: 01/06/2023]
Abstract
Although early-life adversity has been associated with negative consequences during adulthood, growing evidence shows that such adversity can also lead to subsequent stress resilience and positive fitness outcomes. Telomere dynamics are relevant in this context because of the link with developmental conditions and longevity. However, few studies have assessed whether the effects of early-life adversity on developmental telomere dynamics may relate to adult telomere dynamics. We propose that the potential links between early-life adversity and adult telomere dynamics could be driven by developmental constraints (the Constraint hypothesis), by the nature/severity of developmental adversity (the Resilience hypothesis), or by developmental-mediated changes in individual life-history strategies (the Pace of Life hypothesis). We discuss these non-mutually exclusive hypotheses, explore future research directions, and propose specific studies to test these hypotheses. Our article aims to expand our understanding of the evolutionary role of developmental conditions on adult telomere dynamics, stress resilience and ageing.
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Affiliation(s)
- Valeria Marasco
- Konrad Lorenz Institute of Ethology (KLIVV), University of Veterinary Medicine Vienna, Vienna, Austria
| | - Steve Smith
- Konrad Lorenz Institute of Ethology (KLIVV), University of Veterinary Medicine Vienna, Vienna, Austria
| | - Frédéric Angelier
- Centre d'Etudes Biologiques de Chizé, Centre National de la Recherche Scientifique (CNRS)-La Rochelle Université (LRU), UMR 7372, Villiers en Bois, France
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33
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Roast MJ, Eastwood JR, Aranzamendi NH, Fan M, Teunissen N, Verhulst S, Peters A. Telomere length declines with age, but relates to immune function independent of age in a wild passerine. ROYAL SOCIETY OPEN SCIENCE 2022; 9:212012. [PMID: 35601455 PMCID: PMC9043702 DOI: 10.1098/rsos.212012] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 12/22/2021] [Accepted: 04/01/2022] [Indexed: 05/03/2023]
Abstract
Telomere length (TL) shortens with age but telomere dynamics can relate to fitness components independent of age. Immune function often relates to such fitness components and can also interact with telomeres. Studying the link between TL and immune function may therefore help us understand telomere-fitness associations. We assessed the relationships between erythrocyte TL and four immune indices (haptoglobin, natural antibodies (NAbs), complement activity (CA) and heterophil-lymphocyte (HL) ratio; n = 477-589), from known-aged individuals of a wild passerine (Malurus coronatus). As expected, we find that TL significantly declined with age. To verify whether associations between TL and immune function were independent of parallel age-related changes (e.g. immunosenescence), we statistically controlled for sampling age and used within-subject centring of TL to separate relationships within or between individuals. We found that TL positively predicted CA at the between-individual level (individuals with longer average TL had higher CA), but no other immune indices. By contrast, age predicted the levels of NAbs and HL ratio, allowing inference that respective associations between TL and age with immune indices are independent. Any links existing between TL and fitness are therefore unlikely to be strongly mediated by innate immune function, while TL and immune indices appear independent expressions of individual heterogeneity.
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Affiliation(s)
- Michael J. Roast
- School of Biological Sciences, Monash University, Victoria 3800, Australia
| | - Justin R. Eastwood
- School of Biological Sciences, Monash University, Victoria 3800, Australia
| | | | - Marie Fan
- School of Biological Sciences, Monash University, Victoria 3800, Australia
| | - Niki Teunissen
- School of Biological Sciences, Monash University, Victoria 3800, Australia
| | - Simon Verhulst
- Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands
| | - Anne Peters
- School of Biological Sciences, Monash University, Victoria 3800, Australia
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34
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Morosinotto C, Bensch S, Tarka M, Karell P. Heritability and parental effects in telomere length in a color polymorphic long-lived bird. Physiol Biochem Zool 2022; 95:350-364. [DOI: 10.1086/720161] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/03/2022]
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35
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Pisanu C, Vitali E, Meloni A, Congiu D, Severino G, Ardau R, Chillotti C, Trabucchi L, Bortolomasi M, Gennarelli M, Minelli A, Squassina A. Investigating the Role of Leukocyte Telomere Length in Treatment-Resistant Depression and in Response to Electroconvulsive Therapy. J Pers Med 2021; 11:jpm11111100. [PMID: 34834452 PMCID: PMC8622097 DOI: 10.3390/jpm11111100] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2021] [Revised: 10/19/2021] [Accepted: 10/25/2021] [Indexed: 12/15/2022] Open
Abstract
Psychiatric disorders seem to be characterized by premature cell senescence. However, controversial results have also been reported. In addition, the relationship between accelerated aging and treatment-resistance has scarcely been investigated. In the current study, we measured leukocyte telomere length (LTL) in 148 patients with treatment-resistant depression (TRD, 125 with major depressive disorder, MDD, and 23 with bipolar disorder, BD) treated with electroconvulsive therapy (ECT) and analyzed whether LTL was associated with different response profiles. We also compared LTL between patients with TRD and 335 non-psychiatric controls. For 107 patients for which genome-wide association data were available, we evaluated whether a significant overlap among genetic variants or genes associated with LTL and with response to ECT could be observed. LTL was negatively correlated with age (Spearman’s correlation coefficient = −0.25, p < 0.0001) and significantly shorter in patients with treatment-resistant MDD (Quade’s F = 35.18, p < 0.0001) or BD (Quade’s F = 20.84, p < 0.0001) compared to controls. Conversely, baseline LTL was not associated with response to ECT or remission. We did not detect any significant overlap between genetic variants or genes associated with LTL and response to ECT. Our results support previous findings suggesting premature cell senescence in patients with severe psychiatric disorders and suggest that LTL could not be a predictive biomarker of response to ECT.
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Affiliation(s)
- Claudia Pisanu
- Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, 09042 Cagliari, Italy; (C.P.); (A.M.); (D.C.); (G.S.)
| | - Erika Vitali
- Department of Molecular and Translational Medicine, University of Brescia, 25121 Brescia, Italy; (E.V.); (M.G.); (A.M.)
- Genetics Unit, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, 25125 Brescia, Italy
| | - Anna Meloni
- Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, 09042 Cagliari, Italy; (C.P.); (A.M.); (D.C.); (G.S.)
| | - Donatella Congiu
- Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, 09042 Cagliari, Italy; (C.P.); (A.M.); (D.C.); (G.S.)
| | - Giovanni Severino
- Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, 09042 Cagliari, Italy; (C.P.); (A.M.); (D.C.); (G.S.)
| | - Raffaella Ardau
- Unit of Clinical Pharmacology, University Hospital Agency of Cagliari, 09123 Cagliari, Italy; (R.A.); (C.C.)
| | - Caterina Chillotti
- Unit of Clinical Pharmacology, University Hospital Agency of Cagliari, 09123 Cagliari, Italy; (R.A.); (C.C.)
| | - Luigi Trabucchi
- Psychiatric Hospital “Villa Santa Chiara”, 37142 Verona, Italy; (L.T.); (M.B.)
| | - Marco Bortolomasi
- Psychiatric Hospital “Villa Santa Chiara”, 37142 Verona, Italy; (L.T.); (M.B.)
| | - Massimo Gennarelli
- Department of Molecular and Translational Medicine, University of Brescia, 25121 Brescia, Italy; (E.V.); (M.G.); (A.M.)
- Genetics Unit, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, 25125 Brescia, Italy
| | - Alessandra Minelli
- Department of Molecular and Translational Medicine, University of Brescia, 25121 Brescia, Italy; (E.V.); (M.G.); (A.M.)
- Genetics Unit, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, 25125 Brescia, Italy
| | - Alessio Squassina
- Department of Biomedical Science, Section of Neuroscience and Clinical Pharmacology, University of Cagliari, 09042 Cagliari, Italy; (C.P.); (A.M.); (D.C.); (G.S.)
- Correspondence: ; Tel.: +39-070-675-4323
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36
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Brown AM, Wood EM, Capilla-Lasheras P, Harrison XA, Young AJ. Longitudinal evidence that older parents produce offspring with longer telomeres in a wild social bird. Biol Lett 2021; 17:20210409. [PMID: 34665991 PMCID: PMC8526163 DOI: 10.1098/rsbl.2021.0409] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2021] [Accepted: 09/29/2021] [Indexed: 02/07/2023] Open
Abstract
As telomere length (TL) often predicts survival and lifespan, there is considerable interest in the origins of inter-individual variation in TL. Cross-generational effects of parental age on offspring TL are thought to be a key source of variation, but the rarity of longitudinal studies that examine the telomeres of successive offspring born throughout the lives of parents leaves such effects poorly understood. Here, we exploit TL measures of successive offspring produced throughout the long breeding tenures of parents in wild white-browed sparrow weaver (Plocepasser mahali) societies, to isolate the effects of within-parent changes in age on offspring TLs. Our analyses reveal the first evidence to date of a positive within-parent effect of advancing age on offspring TL: as individual parents age, they produce offspring with longer telomeres (a modest effect that persists into offspring adulthood). We consider the potential for pre- and post-natal mechanisms to explain our findings. As telomere attrition predicts offspring survival to adulthood in this species, this positive parental age effect could impact parent and offspring fitness if it arose via differential telomere attrition during offspring development. Our findings support the view that cross-generational effects of parental age can be a source of inter-individual variation in TL.
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Affiliation(s)
- Antony M. Brown
- Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK
| | - Emma M. Wood
- Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK
| | - Pablo Capilla-Lasheras
- Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK
| | - Xavier A. Harrison
- Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK
| | - Andrew J. Young
- Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK
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37
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Badmus KA, Idrus Z, Meng GY, Sazili AQ, Mamat-Hamidi K. Telomere Length and Regulatory Genes as Novel Stress Biomarkers and Their Diversities in Broiler Chickens ( Gallus gallus domesticus) Subjected to Corticosterone Feeding. Animals (Basel) 2021; 11:ani11102759. [PMID: 34679783 PMCID: PMC8532957 DOI: 10.3390/ani11102759] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/22/2021] [Revised: 08/16/2021] [Accepted: 08/23/2021] [Indexed: 12/15/2022] Open
Abstract
Simple Summary Assessment of poultry welfare is very crucial for sustainable production in the tropics. There is a demand for alternatives to plasma corticosterone levels as they have received much criticism as an unsuitable predictor of animal welfare due to inconsistency. In this study, we noticed no effect of age on plasma corticosterone (CORT) although it was altered by CORT treatment. However, growth performances and organ weight were affected by CORT treatment and age. The broad sense evaluation of telomere length in this study revealed that telomere length in the blood, muscle, liver and heart was shortened by chronic stress induced by corticosterone administration. The expression profile of the telomere regulatory genes was altered by chronic stress. This study informed us of the potential of telomere length and its regulatory genes in the assessment of animal welfare in the poultry sector for sustainable production. Abstract This study was designed to characterize telomere length and its regulatory genes and to evaluate their potential as well-being biomarkers. Chickens were fed a diet containing corticosterone (CORT) for 4 weeks and performances, organ weight, plasma CORT levels, telomere lengths and regulatory genes were measured and recorded. Body weights of CORT-fed chickens were significantly suppressed (p < 0.05), and organ weights and circulating CORT plasma levels (p < 0.05) were altered. Interaction effect of CORT and duration was significant (p < 0.05) on heart and liver telomere length. CORT significantly (p < 0.05) shortened the telomere length of the whole blood, muscle, liver and heart. The TRF1, chTERT, TELO2 and HSF1 were significantly (p < 0.05) upregulated in the liver and heart at week 4 although these genes and TERRA were downregulated in the muscles at weeks 2 and 4. Therefore, telomere lengths and their regulators are associated and diverse, so they can be used as novel biomarkers of stress in broiler chickens fed with CORT.
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Affiliation(s)
- Kazeem Ajasa Badmus
- Department of Animal Science, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia; (K.A.B.); (Z.I.); (A.Q.S.)
- Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia;
| | - Zulkifli Idrus
- Department of Animal Science, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia; (K.A.B.); (Z.I.); (A.Q.S.)
- Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia;
| | - Goh Yong Meng
- Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia;
- Department of Veterinary Pre-Clinical Science, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia
| | - Awis Qurni Sazili
- Department of Animal Science, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia; (K.A.B.); (Z.I.); (A.Q.S.)
- Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia;
| | - Kamalludin Mamat-Hamidi
- Department of Animal Science, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia; (K.A.B.); (Z.I.); (A.Q.S.)
- Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia;
- Correspondence:
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38
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Noguera JC, Velando A. Telomerase activity can mediate the effects of growth on telomeres during post-natal development in a wild bird. J Exp Biol 2021; 224:269201. [PMID: 34142138 DOI: 10.1242/jeb.242465] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/18/2021] [Accepted: 05/24/2021] [Indexed: 01/14/2023]
Abstract
In wild animals, telomere attrition during early development has been linked with several fitness disadvantages throughout life. Telomerase enzyme can elongate telomeres, but it is generally assumed that its activity is suppressed in most somatic tissues upon birth. However, recent evidence suggests that this may not be the case for long-lived bird species. We have therefore investigated whether telomerase activity is maintained during the postnatal growth period in a wild yellow-legged gull (Larus michahellis) population. Our results indicate that telomerase activity is not negligible in the blood cells, but activity levels sharply decline from hatching to fledging following a similar pattern to the reduction observed in telomere length. Our results further suggest that the observed variation in telomere length may be the result of a negative effect of fast growth on telomerase activity, thus providing a new mechanism through which growth rates may affect telomere dynamics and potentially life-history trajectories.
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Affiliation(s)
- Jose C Noguera
- Grupo de Ecología Animal (GEA), Centro de Investigacion Mariña (CIM), Universidad de Vigo, Vigo 36310, Spain
| | - Alberto Velando
- Grupo de Ecología Animal (GEA), Centro de Investigacion Mariña (CIM), Universidad de Vigo, Vigo 36310, Spain
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39
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Ingles ED, Deakin JE. Telomeres, species differences, and unusual telomeres in vertebrates: presenting challenges and opportunities to understanding telomere dynamics. AIMS GENETICS 2021. [DOI: 10.3934/genet.2016.1.1] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/26/2022]
Abstract
AbstractThere has been increasing interest in the use of telomeres as biomarkers of stress, cellular ageing and life-histories. However, the telomere landscape is a diverse feature, with noticeable differences between species, a fact which is highlighted by the unusual telomeres of various vertebrate organisms. We broadly review differences in telomere dynamics among vertebrates, and emphasize the need to understand more about telomere processes and trends across species. As part of these species differences, we review unusual telomeres in vertebrates. This includes mega-telomeres, which are present across a diverse set of organisms, but also focusing on the unusual telomeres traits of marsupials and monotremes, which have seen little to no prior discussion, yet uniquely stand out from other unusual telomere features discovered thus far. Due to the presence of at least two unique telomere features in the marsupial family Dasyuridae, as well as to the presence of physiological strategies semelparity and torpor, which have implications for telomere life-histories in these species, we suggest that this family has a very large potential to uncover novel information on telomere evolution and dynamics.
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Affiliation(s)
- Emory D. Ingles
- Institute of Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia
| | - Janine E. Deakin
- Institute of Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia
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40
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Friesen CR, Wilson M, Rollings N, Sudyka J, Giraudeau M, Whittington CM, Olsson M. Exercise training has morph-specific effects on telomere, body condition and growth dynamics in a color-polymorphic lizard. J Exp Biol 2021; 224:jeb.242164. [PMID: 33785504 DOI: 10.1242/jeb.242164] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/18/2020] [Accepted: 03/22/2021] [Indexed: 12/12/2022]
Abstract
Alternative reproductive tactics (ARTs) are correlated suites of sexually selected traits that are likely to impose differential physiological costs on different individuals. While moderate activity might be beneficial, animals living in the wild often work at the margins of their resources and performance limits. Individuals using ARTs may have divergent capacities for activity. When pushed beyond their respective capacities, they may experience condition loss, oxidative stress, and molecular damage that must be repaired with limited resources. We used the Australian painted dragon lizard that exhibits color polymorphism as a model to experimentally test the effect of exercise on body condition, growth, reactive oxygen species (ROS) and telomere dynamics - a potential marker of stress and aging and a correlate of longevity. For most males, ROS levels tended to be lower with greater exercise; however, males with yellow throat patches - or bibs - had higher ROS levels than non-bibbed males. At the highest level of exercise, bibbed males exhibited telomere loss, while non-bibbed males gained telomere length; the opposite pattern was observed in the no-exercise controls. Growth was positively related to food intake but negatively correlated with telomere length at the end of the experiment. Body condition was not related to food intake but was positively correlated with increases in telomere length. These results, along with our previous work, suggest that aggressive - territory holding - bibbed males suffer physiological costs that may reduce longevity compared with non-bibbed males with superior postcopulatory traits.
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Affiliation(s)
- Christopher R Friesen
- School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.,Illawarra Health and Medical Research Institute (IHMRI), University of Wollongong, Wollongong, NSW 2522, Australia.,Faculty of Science, School of Life and Environmental Sciences, The University of Sydney, NSW 2006, Australia
| | - Mark Wilson
- Illawarra Health and Medical Research Institute (IHMRI), University of Wollongong, Wollongong, NSW 2522, Australia.,Molecular Horizons and School of Chemistry and Molecular Bioscience, University of Wollongong, Wollongong, NSW 2522, Australia
| | - Nicky Rollings
- Faculty of Science, School of Life and Environmental Sciences, The University of Sydney, NSW 2006, Australia
| | - Joanna Sudyka
- Institute of Environmental Sciences, Jagiellonian University, 30-060 Krakow, Poland
| | - Mathieu Giraudeau
- CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, F34394 Montpellier, France.,CREES Centre for Research on the Ecology and Evolution of Disease, 34394 Montpellier, France
| | - Camilla M Whittington
- Faculty of Science, School of Life and Environmental Sciences, The University of Sydney, NSW 2006, Australia
| | - Mats Olsson
- School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.,Department of Biological & Environmental Sciences, University of Gothenburg, 405 30 Gothenburg, Sweden
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41
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Ensminger DC, Siegel SR, Owen DAS, Sheriff MJ, Langkilde T. Elevated glucocorticoids during gestation suggest sex-specific effects on offspring telomere lengths in a wild lizard. Comp Biochem Physiol A Mol Integr Physiol 2021; 257:110971. [PMID: 33933630 DOI: 10.1016/j.cbpa.2021.110971] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2021] [Revised: 04/06/2021] [Accepted: 04/26/2021] [Indexed: 12/30/2022]
Abstract
The effects of maternal glucocorticoids (e.g. corticosterone, CORT) on offspring interest biologists due to increasing environmental perturbations. While little is known about the impact of maternal CORT on offspring fitness, it may modulate telomere length and compromise offspring health. Here, we use a modified real-time quantitative PCR assay to assess telomere length using small DNA quantities (<60 ng). We tested the hypothesis that increased maternal CORT during gestation decreases offspring telomere length. While CORT-driven telomere shortening is well established within individuals, cross-generational effects remain unclear. We treated wild-caught gravid female eastern fence lizards (Sceloporus undulatus) with daily transdermal applications of CORT, at ecologically relevant levels, from capture to laying. Maternal CORT treatment did not alter maternal telomere length, although baseline maternal CORT concentrations had a weak, negative correlation with maternal telomere length. There was no relation between mother and offspring telomere length. There was a trend for maternal CORT treatment to shorten telomeres of sons but not daughters. Our treatment replicated exposure to a single stressor per day, likely underestimating effects seen in the wild where stressors may be more frequent. Future research should further explore fitness consequences of maternal CORT effects.
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Affiliation(s)
- David C Ensminger
- Department of Ecosystem Science and Management, The Pennsylvania State University, Forest Resources Building, University Park, PA 16802, United States of America; Department of Biology, The Pennsylvania State University, Mueller Laboratory, University Park, PA 16802, United States of America.
| | - Sue R Siegel
- Department of Biobehavioral Health, The Pennsylvania State University, Biomarker Core Lab, University Park, PA 16802, United States of America
| | - Dustin A S Owen
- Department of Ecosystem Science and Management, The Pennsylvania State University, Forest Resources Building, University Park, PA 16802, United States of America; Department of Biology, The Pennsylvania State University, Mueller Laboratory, University Park, PA 16802, United States of America; Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, PA 16802, United States of America
| | - Michael J Sheriff
- Biology Department, University of Massachusetts Dartmouth, Dartmouth, MA 02747, United States of America
| | - Tracy Langkilde
- Department of Biology, The Pennsylvania State University, Mueller Laboratory, University Park, PA 16802, United States of America; Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, PA 16802, United States of America
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42
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Telomere lengths correlate with fitness but assortative mating by telomeres confers no benefit to fledgling recruitment. Sci Rep 2021; 11:5463. [PMID: 33750872 PMCID: PMC7943796 DOI: 10.1038/s41598-021-85068-x] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2020] [Accepted: 02/22/2021] [Indexed: 02/07/2023] Open
Abstract
Assortative mating by telomere lengths has been observed in several bird species, and in some cases may increase fitness of individuals. Here we examined the relationship between telomere lengths of Blue-footed Booby (Sula nebouxii) mates, long-lived colonial seabirds with high annual divorce rates. We tested the hypothesis that interactions between maternal and paternal telomere lengths affect offspring and parental survival. We found that relative telomere lengths (RTL) were strongly positively correlated between members of a breeding pair. In addition, RTL of both parents interacted to predict fledgling recruitment, although fledglings with two very long-RTL parents performed only averagely. Telomere lengths also predicted adult survival: birds with long telomeres were more likely to survive, but birds whose mate had long telomeres were less likely to survive. Thus, having long telomeres benefits survival, while choosing a mate with long telomeres benefits reproductive output while penalizing survival. These patterns demonstrate that while a breeder's RTL predicts offspring quality, assortative mating by RTL does not enhance fitness, and a trade-off between different components of fitness may govern patterns of assortative mating by telomere length. They also illustrate how testing the adaptive value of only one parent’s telomere length on either survival or reproductive success alone may provide equivocal results.
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Álvarez‐Quintero N, Velando A, Noguera JC, Kim S. Environment-induced changes in reproductive strategies and their transgenerational effects in the three-spined stickleback. Ecol Evol 2021; 11:771-783. [PMID: 33520165 PMCID: PMC7820166 DOI: 10.1002/ece3.7052] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2020] [Revised: 10/23/2020] [Accepted: 10/23/2020] [Indexed: 01/10/2023] Open
Abstract
An organism may increase its fitness by changing its reproductive strategies in response to environmental cues, but the possible consequences of those changes for the next generation have rarely been explored. By using an experiment on the three-spined stickleback (Gasterosteus aculeatus), we studied how changes in the onset of breeding photoperiod (early versus late) affect reproductive strategies of males and females, and life histories of their offspring. We also explored whether telomeres are involved in the within- and transgenerational effects. In response to the late onset of breeding photoperiod, females reduced their investment in the early clutches, but males increased their investment in sexual signals. Costs of increased reproductive investment in terms of telomere loss were evident only in the late females. The environmentally induced changes in reproductive strategies affected offspring growth and survival. Most notably, offspring growth rate was the fastest when both parents experienced a delayed (i.e., late) breeding photoperiod, and survival rate was the highest when both parents experienced an advanced (i.e., early) breeding photoperiod. There was no evidence of transgenerational effects on offspring telomere length despite positive parents-offspring relationships in this trait. Our results highlight that environmental changes may impact more than one generation by altering reproductive strategies of seasonal breeders with consequences for offspring viability.
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Affiliation(s)
- Náyade Álvarez‐Quintero
- Grupo Ecoloxía Animal (Lab 97)Torre CACTICentro de Investigación MariñaUniversidade de VigoVigoSpain
| | - Alberto Velando
- Grupo Ecoloxía Animal (Lab 97)Torre CACTICentro de Investigación MariñaUniversidade de VigoVigoSpain
| | - Jose C. Noguera
- Grupo Ecoloxía Animal (Lab 97)Torre CACTICentro de Investigación MariñaUniversidade de VigoVigoSpain
| | - Sin‐Yeon Kim
- Grupo Ecoloxía Animal (Lab 97)Torre CACTICentro de Investigación MariñaUniversidade de VigoVigoSpain
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Vernasco BJ, Dakin R, Majer AD, Haussmann MF, Brandt Ryder T, Moore IT. Longitudinal dynamics and behavioural correlates of telomeres in male wire‐tailed manakins. Funct Ecol 2020. [DOI: 10.1111/1365-2435.13715] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/26/2022]
Affiliation(s)
- Ben J. Vernasco
- Department of Biological Sciences Virginia Tech Blacksburg VA USA
| | - Roslyn Dakin
- Migratory Bird Center Smithsonian Conservation Biology Institute Washington DC USA
| | | | | | - T. Brandt Ryder
- Migratory Bird Center Smithsonian Conservation Biology Institute Washington DC USA
| | - Ignacio T. Moore
- Department of Biological Sciences Virginia Tech Blacksburg VA USA
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Petitjean Q, Jean S, Côte J, Larcher T, Angelier F, Ribout C, Perrault A, Laffaille P, Jacquin L. Direct and indirect effects of multiple environmental stressors on fish health in human-altered rivers. THE SCIENCE OF THE TOTAL ENVIRONMENT 2020; 742:140657. [PMID: 32721751 DOI: 10.1016/j.scitotenv.2020.140657] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/26/2020] [Revised: 06/24/2020] [Accepted: 06/29/2020] [Indexed: 06/11/2023]
Abstract
Freshwater fish face multiple challenges in human-altered rivers such as trace metal contamination, temperature increase and parasitism. These multiple stressors could have unexpected interactive effects on fish health due to shared physiological pathways, but few studies investigated this question in wild fish populations. In this study, we compared 16 populations of gudgeon (Gobio occitaniae) distributed along perturbation gradients in human-altered rivers in the South of France. We tested the effects of single and combined stressors (i.e., metal contamination, temperature, parasitism) on key traits linked to fish health across different biological levels using a Structural Equation Modelling approach. Parasitism and temperature alone had limited deleterious effects on fish health. In contrast, fish living in metal-contaminated sites had higher metal bioaccumulation and higher levels of cellular damage in the liver through the induction of an inflammatory response. In addition, temperature and contamination had interactive negative effects on growth. These results suggest that trace metal contamination has deleterious effects on fish health at environmentally realistic concentrations and that temperature can modulate the effects of trace metals on fish growth. With this study, we hope to encourage integrative approaches in realistic field conditions to better predict the effects of natural and anthropogenic stressors on aquatic organisms.
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Affiliation(s)
- Quentin Petitjean
- EcoLab, Laboratoire écologie fonctionnelle et environnement, UMR5245, Université de Toulouse, CNRS, Toulouse, France; EDB, UMR5174 EDB, Université de Toulouse, CNRS, IRD, UPS, 118 route de Narbonne, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France.
| | - Séverine Jean
- EcoLab, Laboratoire écologie fonctionnelle et environnement, UMR5245, Université de Toulouse, CNRS, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France
| | - Jessica Côte
- EDB, UMR5174 EDB, Université de Toulouse, CNRS, IRD, UPS, 118 route de Narbonne, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France
| | - Thibaut Larcher
- INRA-Oniris, PAnTher APEX, La Chantrerie, 44307 Nantes, France
| | - Fréderic Angelier
- Centre d'Etudes Biologiques de Chizé, UMR 7372, Université de la Rochelle, CNRS, Villiers en Bois, France
| | - Cécile Ribout
- Centre d'Etudes Biologiques de Chizé, UMR 7372, Université de la Rochelle, CNRS, Villiers en Bois, France
| | - Annie Perrault
- EcoLab, Laboratoire écologie fonctionnelle et environnement, UMR5245, Université de Toulouse, CNRS, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France
| | - Pascal Laffaille
- EcoLab, Laboratoire écologie fonctionnelle et environnement, UMR5245, Université de Toulouse, CNRS, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France
| | - Lisa Jacquin
- EDB, UMR5174 EDB, Université de Toulouse, CNRS, IRD, UPS, 118 route de Narbonne, Toulouse, France; LTSER France, Zone Atelier PYGAR "Pyrénées-Garonne", Auzeville-Tolosane, France
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46
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Power ML, Power S, Bertelsen MF, Jones G, Teeling EC. Wing: A suitable nonlethal tissue type for repeatable and rapid telomere length estimates in bats. Mol Ecol Resour 2020; 21:421-432. [PMID: 33049101 DOI: 10.1111/1755-0998.13276] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/12/2020] [Revised: 09/10/2020] [Accepted: 09/23/2020] [Indexed: 12/31/2022]
Abstract
Telomeres are used increasingly in ecology and evolution as biomarkers for ageing and environmental stress, and are typically measured from DNA extracted from nonlethally sampled blood. However, obtaining blood is not always possible in field conditions and only limited amounts can be taken from small mammals, such as bats, which moreover lack nucleated red blood cells and hence yield relatively low amounts of DNA. As telomere length can vary within species according to age and tissue, it is important to determine which tissues serve best as a representation of the organism as a whole. Here, we investigated whether wing tissue biopsies, a rapid and relatively noninvasive tissue collection method, could serve as a proxy for other tissues when measuring relative telomere length (rTL) in the Egyptian fruit bat (Rousettus aegyptiacus). Telomeres were measured from blood, brain, heart, kidney, liver lung, muscle and wing, and multiple wing biopsies were taken from the same individuals to determine intra-individual repeatability of rTL measured by using qPCR. Wing rTL correlated with rTL estimates from most tissues apart from blood. Blood rTL was not significantly correlated with rTL from any other tissue. Blood and muscle rTLs were significantly longer compared with other tissues, while lung displayed the shortest rTLs. Individual repeatability of rTL measures from wing tissue was high (>70%). Here we show the relationships between tissue telomere dynamics for the first time in a bat, and our results provide support for the use of wing tissue for rTL measurements.
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Affiliation(s)
- Megan L Power
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin, Ireland
| | - Sarahjane Power
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin, Ireland
| | - Mads F Bertelsen
- Center for Zoo and Wild Animal Health, Copenhagen Zoo, Frederiksberg, Denmark
| | - Gareth Jones
- School of Biological Sciences, University of Bristol, Bristol, UK
| | - Emma C Teeling
- School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin, Ireland
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Gaikwad AS, Mahmood R, B R, Kondhalkar S. Evaluation of telomere length and genotoxicity among asphalt associated workers. Mutat Res 2020; 858-860:503255. [PMID: 33198936 DOI: 10.1016/j.mrgentox.2020.503255] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/22/2019] [Revised: 08/21/2020] [Accepted: 08/25/2020] [Indexed: 10/23/2022]
Abstract
There are contradictory reports about bitumen exposure and malignancy risk worldwide. Also, the evidence for genotoxicity risk among workers occupationally exposed to asphalt is insufficient. The study intended to evaluate particulate matter 10 (PM10) at the workplace and biomarkers of genotoxicity effects among a group of asphalt workers in and around Bangalore, India. This study involved a total of 107 participants (54 exposed group and 53 unexposed control group). To evaluate the genotoxicity, the urinary 8-OHdG and relative telomere length as oxidative damage while micronucleus (MN) assay for cytogenetic damage was carried out during the study. The majority of workers have reported health complaints and 57.4% of them were not using any personal protective equipments (PPE's). The level of PM10 detected was 104 ± 9.5 μg/m3 and 619 ± 22.7 μg/m3 in the road paving and asphalt mixing sites respectively. The biomonitoring study observed a highly significant (p = <0.001) increase in the level of 8-hydroxy-2-deoxyguanosine (8-OHdG) in the exposed group (23.17 ± 8.65 ng/mg creatinine) compared to the control (13.6 ± 7.12 ng/mg creatinine), revealed age significant associated and non-smoking borderline significant associated for oxidative stress. The relative telomere length (TL) analysis revealed its highly significant (p = 0.004) reduction in the exposed group, adjusted mean 0.95 (95% CI 0.83-1.07) compared to the control 1.06 (95% CI 0.91-1.26). The job category (p = 0.028), non-smoking (p = 0.026), and tobacco chewing (p = 0.013) were associated with reduced relative TL in the asphalt exposed group. In cytogenotoxicity analysis, the mean micronucleus (MN) frequency per 100 cells in the exposed group (26.46 ± 19.8) was significantly (p = <0.001) increased over the control group (8.56 ± 7.18). Neither smoking habit nor age appeared to influence the MN frequencies in either group. In the present study, we have demonstrated genetic damage in workers occupationally exposed to asphalt and particulate matter, raising concern for an increased risk of malignancy in these workers.
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Affiliation(s)
- Avinash S Gaikwad
- ICMR-Regional Occupational Health Centre (Southern), ICMR Complex, Devanahalli TK, Bangalore 562 110, India.
| | - Riaz Mahmood
- Department of Biotechnology and Bioinformatics, Kuvempu University, Shimoga 577451, India.
| | - Ravichandran B
- ICMR-Regional Occupational Health Centre (Southern), ICMR Complex, Devanahalli TK, Bangalore 562 110, India.
| | - Shridhar Kondhalkar
- ICMR-Regional Occupational Health Centre (Southern), ICMR Complex, Devanahalli TK, Bangalore 562 110, India.
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48
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Casagrande S, Stier A, Monaghan P, Loveland JL, Boner W, Lupi S, Trevisi R, Hau M. Increased glucocorticoid concentrations in early life cause mitochondrial inefficiency and short telomeres. J Exp Biol 2020; 223:jeb222513. [PMID: 32532864 DOI: 10.1242/jeb.222513] [Citation(s) in RCA: 48] [Impact Index Per Article: 9.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/28/2020] [Accepted: 06/04/2020] [Indexed: 12/13/2022]
Abstract
Telomeres are DNA structures that protect chromosome ends. However, telomeres shorten during cell replication and at critically low lengths can reduce cell replicative potential, induce cell senescence and decrease fitness. Stress exposure, which elevates glucocorticoid hormone concentrations, can exacerbate telomere attrition. This phenomenon has been attributed to increased oxidative stress generated by glucocorticoids ('oxidative stress hypothesis'). We recently suggested that glucocorticoids could increase telomere attrition during stressful periods by reducing the resources available for telomere maintenance through changes in the metabolic machinery ('metabolic telomere attrition hypothesis'). Here, we tested whether experimental increases in glucocorticoid levels affected telomere length and mitochondrial function in wild great tit (Parus major) nestlings during the energy-demanding early growth period. We monitored resulting corticosterone (Cort) concentrations in plasma and red blood cells, telomere lengths and mitochondrial metabolism (metabolic rate, proton leak, oxidative phosphorylation, maximal mitochondrial capacity and mitochondrial inefficiency). We assessed oxidative damage caused by reactive oxygen species (ROS) metabolites as well as the total non-enzymatic antioxidant protection in plasma. Compared with control nestlings, Cort-nestlings had higher baseline corticosterone, shorter telomeres and higher mitochondrial metabolic rate. Importantly, Cort-nestlings showed increased mitochondrial proton leak, leading to a decreased ATP production efficiency. Treatment groups did not differ in oxidative damage or antioxidants. Hence, glucocorticoid-induced telomere attrition is associated with changes in mitochondrial metabolism, but not with ROS production. These findings support the hypothesis that shortening of telomere length during stressful periods is mediated by glucocorticoids through metabolic rearrangements.
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Affiliation(s)
- Stefania Casagrande
- Max Planck Institute for Ornithology, Evolutionary Physiology Group, 82319 Seewiesen, Germany
| | - Antoine Stier
- Institute of Biodiversity Animal Health and Comparative Medicine, University of Glasgow, Glasgow, G12 8QQ, UK
- Department of Biology, University of Turku, FI-20014 Turku, Finland
| | - Pat Monaghan
- Institute of Biodiversity Animal Health and Comparative Medicine, University of Glasgow, Glasgow, G12 8QQ, UK
| | - Jasmine L Loveland
- Max Planck Institute for Ornithology, Behavioural Genetics and Evolutionary Ecology Group, 82319 Seewiesen, Germany
| | - Winifred Boner
- Institute of Biodiversity Animal Health and Comparative Medicine, University of Glasgow, Glasgow, G12 8QQ, UK
| | - Sara Lupi
- Max Planck Institute for Ornithology, Evolutionary Physiology Group, 82319 Seewiesen, Germany
- Konrad Lorenz Institute of Ethology, University of Veterinary Medicine, Vienna, A-1160 Vienna, Austria
| | - Rachele Trevisi
- Max Planck Institute for Ornithology, Evolutionary Physiology Group, 82319 Seewiesen, Germany
| | - Michaela Hau
- Max Planck Institute for Ornithology, Evolutionary Physiology Group, 82319 Seewiesen, Germany
- Department of Biology, University of Konstanz, D-78464 Konstanz, Germany
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49
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Heidinger BJ, Young RC. Cross‐Generational Effects of Parental Age on Offspring Longevity: Are Telomeres an Important Underlying Mechanism? Bioessays 2020; 42:e1900227. [DOI: 10.1002/bies.201900227] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2019] [Revised: 05/20/2020] [Indexed: 01/04/2023]
Affiliation(s)
- Britt J. Heidinger
- Biological Sciences Department North Dakota State University Fargo ND 58108 USA
| | - Rebecca C. Young
- Biological Sciences Department North Dakota State University Fargo ND 58108 USA
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50
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Sex-Specific Associations of Harsh Childhood Environment with Psychometrically Assessed Life History Profile: no Evidence for Mediation through Developmental Timing or Embodied Capital. ADAPTIVE HUMAN BEHAVIOR AND PHYSIOLOGY 2020. [DOI: 10.1007/s40750-020-00144-2] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
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