Sperm production is negatively associated with muscle and sperm telomere length in a highly polyandrous species

Life history theory suggests that aging is one of the costs of reproduction. Accordingly, a higher reproductive allocation is expected to increase the deterioration of both the somatic and the germinal lines through enhanced telomere attrition. In most species, males’ reproductive allocation mainly regards traits that increase mating and fertilization success, i.e. sexually selected traits. In the current study, we tested the hypothesis that a higher investment in sexually selected traits is associated with a reduced telomere length in the guppy (Poecilia reticulata), an ectotherm species characterized by strong pre- and postcopulatory sexual selection. We first measured telomere length in both the soma and the sperm over the course of guppy’s lifespan to see if there was any variation in telomere length associated with age. Secondly, we investigated whether a greater expression of pre- and postcopulatory sexually selected traits is linked to shorter telomere length in both the somatic and the sperm germinal lines, and in young and old males. We found that telomeres lengthened with age in the somatic tissue, but there was no age-dependent variation in telomere length in the sperm cells. Telomere length in guppies was significantly and negatively correlated with sperm production in both tissues and life stages considered in this study. Our findings indicate that telomere erosion in male guppies is more strongly associated with their reproductive investment (sperm production) rather than their age, suggesting a trade-off between reproduction and maintenance is occurring at each stage of males’ life in this species.

[1]  D. Réale,et al.  Telomere length positively correlates with pace‐of‐life in a sex‐ and cohort‐specific way and elongates with age in a wild mammal , 2022, Molecular ecology.

[2]  S. Verhulst,et al.  Telomere length is highly repeatable and shorter in individuals with more elaborate sexual ornamentation in a short‐lived passerine , 2022, Molecular ecology.

[3]  M. Gaudry,et al.  A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout , 2021, bioRxiv.

[4]  J. Gaillard,et al.  Decline in telomere length with increasing age across nonhuman vertebrates: A meta‐analysis , 2021, Molecular ecology.

[5]  A. Vaiserman,et al.  Telomere Length as a Marker of Biological Age: State-of-the-Art, Open Issues, and Future Perspectives , 2021, Frontiers in Genetics.

[6]  J. L. Tomkins,et al.  How sperm competition shapes the evolution of testes and sperm: a meta-analysis , 2020, Philosophical Transactions of the Royal Society B.

[7]  J. Gaillard,et al.  The hidden ageing costs of sperm competition. , 2020, Ecology letters.

[8]  M. Magris,et al.  Trade-offs of strategic sperm adjustments and their consequences under phenotype–environment mismatches in guppies , 2020, Animal Behaviour.

[9]  S. Dobosz,et al.  Telomere Dynamics in the Diploid and Triploid Rainbow Trout (Oncorhynchus mykiss) Assessed by Q-FISH Analysis , 2020, Genes.

[10]  R. Shine,et al.  Covariation in superoxide, sperm telomere length and sperm velocity in a polymorphic reptile , 2020, Behavioral Ecology and Sociobiology.

[11]  A. Pilastro,et al.  Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish , 2020, Ecology and evolution.

[12]  N. Metcalfe,et al.  The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness , 2019, Proceedings of the Royal Society B.

[13]  A. Pilastro,et al.  Sexual selection and ageing: interplay between pre- and post-copulatory traits senescence in the guppy , 2019, Proceedings of the Royal Society B.

[14]  P. Opresko,et al.  The impact of oxidative DNA damage and stress on telomere homeostasis , 2019, Mechanisms of Ageing and Development.

[15]  E. Wapstra,et al.  Effects of male telomeres on probability of paternity in sand lizards , 2018, Biology Letters.

[16]  Petri T. Niemelä,et al.  Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis , 2018, Behavioral Ecology and Sociobiology.

[17]  A. Seluanov,et al.  Evolution of telomere maintenance and tumour suppressor mechanisms across mammals , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  A. Pilastro,et al.  Stabilizing selection on sperm number revealed by artificial selection and experimental evolution , 2018, Evolution; international journal of organic evolution.

[19]  E. Wapstra,et al.  Ectothermic telomeres: it's time they came in from the cold , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  M. Haussmann,et al.  Experimental manipulation of telomere length: does it reveal a corner-stone role for telomerase in the natural variability of individual fitness? , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  Terry Burke,et al.  Spatio‐temporal variation in lifelong telomere dynamics in a long‐term ecological study , 2017, The Journal of animal ecology.

[22]  Mark R. Wilson,et al.  Telomere dynamics in a lizard with morph‐specific reproductive investment and self‐maintenance , 2017, Ecology and evolution.

[23]  A. Pilastro,et al.  Postcopulatory cost of immune system activation in Poecilia reticulata , 2017 .

[24]  C. R. Freeman-Gallant,et al.  Sexual signals reflect telomere dynamics in a wild bird , 2017, Ecology and evolution.

[25]  T. Ruf,et al.  Telomeres are elongated in older individuals in a hibernating rodent, the edible dormouse (Glis glis) , 2016, Scientific Reports.

[26]  D. Wells,et al.  Investigation of sperm telomere length as a potential marker of paternal genome integrity and semen quality. , 2016, Reproductive biomedicine online.

[27]  Mark R. Wilson,et al.  Ageing and the cost of maintaining coloration in the Australian painted dragon , 2016, Biology Letters.

[28]  J. Ruijter,et al.  Removal of between-run variation in a multi-plate qPCR experiment , 2015, Biomolecular detection and quantification.

[29]  S. Mendes,et al.  The efficacy of MS‐222 as anaesthetic agent in four freshwater aquarium fish species , 2015 .

[30]  L. Alibardi.  Immunolocalization of the telomerase‐1 component in cells of the regenerating tail, testis, and intestine of lizards , 2015, Journal of morphology.

[31]  S. Munch,et al.  Does Reproductive Investment Decrease Telomere Length in Menidia menidia? , 2015, PloS one.

[32]  Param Priya Singh,et al.  A Platform for Rapid Exploration of Aging and Diseases in a Naturally Short-Lived Vertebrate , 2015, Cell.

[33]  L. Schärer,et al.  Sperm competition and the evolution of spermatogenesis. , 2014, Molecular human reproduction.

[34]  J. Vaupel,et al.  Diversity of ageing across the tree of life , 2013, Nature.

[35]  A. Pilastro,et al.  Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits , 2013, Ecology and evolution.

[36]  M. Cayuela,et al.  Premature aging in telomerase-deficient zebrafish , 2013, Disease Models & Mechanisms.

[37]  D. Reznick,et al.  Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies , 2013, Proceedings of the Royal Society B: Biological Sciences.

[38]  Jean-Michel Gaillard,et al.  Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology , 2013, Ageing Research Reviews.

[39]  M. Kumar,et al.  Analysis of sperm telomere length in men with idiopathic infertility , 2013, Archives of Gynecology and Obstetrics.

[40]  E. Blackburn,et al.  The telomere syndromes , 2012, Nature Reviews Genetics.

[41]  Z. Varga,et al.  Anesthesia and euthanasia in zebrafish. , 2012, ILAR journal.

[42]  Pat Monaghan,et al.  Telomere length in early life predicts lifespan , 2012, Proceedings of the National Academy of Sciences.

[43]  G. Sorci,et al.  Sexually extravagant males age more rapidly. , 2011, Ecology letters.

[44]  A. Pilastro,et al.  Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata) , 2011, Behavioral Ecology and Sociobiology.

[45]  D. Shcherbakova,et al.  Telomerase: Structure, functions, and activity regulation , 2010, Biochemistry (Moscow).

[46]  A. Pilastro,et al.  Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata) , 2010, Journal of evolutionary biology.

[47]  A. Pilastro,et al.  Female presence influences sperm velocity in the guppy , 2009, Biology Letters.

[48]  J. Tolar,et al.  Expression of Telomerase and Telomere Length Are Unaffected by either Age or Limb Regeneration in Danio rerio , 2009, PloS one.

[49]  N. Metcalfe,et al.  Real-time quantitative PCR assay for measurement of avian telomeres , 2009 .

[50]  A. Moorman,et al.  Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data , 2009, Nucleic acids research.

[51]  N. Metcalfe,et al.  Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. , 2009, Ecology letters.

[52]  M. Blasco,et al.  Telomere lengthening early in development , 2007, Nature Cell Biology.

[53]  N. Metcalfe,et al.  Carotenoids, oxidative stress and female mating preference for longer lived males , 2007, Proceedings of the Royal Society B: Biological Sciences.

[54]  L. Kruuk,et al.  LIVE FAST, DIE YOUNG: TRADE‐OFFS BETWEEN FITNESS COMPONENTS AND SEXUALLY ANTAGONISTIC SELECTION ON WEAPONRY IN SOAY SHEEP , 2006 .

[55]  L. Kruuk,et al.  LIVE FAST, DIE YOUNG: TRADE-OFFS BETWEEN FITNESS COMPONENTS AND SEXUALLY ANTAGONISTIC SELECTION ON WEAPONRY IN SOAY SHEEP , 2006, Evolution; international journal of organic evolution.

[56]  J. Evans,et al.  Colourful male guppies produce faster and more viable sperm , 2006, Journal of evolutionary biology.

[57]  C. Autexier,et al.  The structure and function of telomerase reverse transcriptase. , 2006, Annual review of biochemistry.

[58]  L. Simmons,et al.  Sexual selection and mate choice. , 2006, Trends in ecology & evolution.

[59]  P. Monaghan,et al.  Do telomere dynamics link lifestyle and lifespan? , 2006, Trends in ecology & evolution.

[60]  A. Magurran.  Evolutionary Ecology: The Trinidadian Guppy , 2005 .

[61]  Luc F. Bussière,et al.  High-quality male field crickets invest heavily in sexual display but die young , 2004, Nature.

[62]  S. Baatout,et al.  Telomere biology in mammalian germ cells and during development. , 2004, Developmental biology.

[63]  S. Oikawa,et al.  Mechanism of Telomere Shortening by Oxidative Stress , 2004, Annals of the New York Academy of Sciences.

[64]  E. Cooper,et al.  Sex–specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata) , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[65]  P. Nicoletto,et al.  The Relationship Among Swimming Performance, Courtship Behavior, and Carotenoid Pigmentation of Guppies in Four Rivers of Trinidad , 1999, Environmental Biology of Fishes.

[66]  J. Evans,et al.  Directional postcopulatory sexual selection revealed by artificial insemination , 2003, Nature.

[67]  R. Cawthon.  Telomere measurement by quantitative PCR. , 2002, Nucleic acids research.

[68]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[69]  Steven N. Austad,et al.  Why do we age? , 2000, Nature.

[70]  D. Franck.  Sex, Color, and Mate Choice in Guppies , 2000 .

[71]  C. Greider,et al.  Recombination in telomere-length maintenance. , 2000, Trends in biochemical sciences.

[72]  Ulrika Candolin,et al.  Reproduction under predation risk and the trade–off between current and future reproduction in the threespine stickleback , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  H. Greven,et al.  Notes on the mechanically stimulated discharge of spermiozeugmata in the guppy, Poecilia reticulata: a quantitative approach , 1997 .

[74]  Alexey M. Olovnikov,et al.  Telomeres, telomerase, and aging: Origin of the theory , 1996, Experimental Gerontology.

[75]  W. V. Van Voorhies.  Production of sperm reduces nematode lifespan , 1992, Nature.

[76]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[77]  V A Zakian,et al.  Structure and function of telomeres. , 1989, Annual review of genetics.

[78]  M. Andersson.  EVOLUTION OF CONDITION‐DEPENDENT SEX ORNAMENTS AND MATING PREFERENCES: SEXUAL SELECTION BASED ON VIABILITY DIFFERENCES , 1986, Evolution; international journal of organic evolution.

[79]  J. D. Watson.  Origin of Concatemeric T7DNA , 1972 .

[80]  L. Hayflick.  THE LIMITED IN VITRO LIFETIME OF HUMAN DIPLOID CELL STRAINS. , 1965, Experimental cell research.