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Rapid evolution of sperm length in response to increased temperature in an ectothermic fish

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Abstract

The Intergovernmental Panel on Climate Change predicts an average global temperature increase of 1.8–4.0 °C by 2100. Tropical ectotherms are expected to be particularly sensitive to this temperature increase because they live close to their thermal limits. We investigated the phenotypic plasticity and evolutionary response of sperm traits in guppies (Poecilia reticulata) to increased temperatures after 6, 18, and 24 months. Guppies with evolution temperatures of 25 °C (control) or 28 °C were reared in either 25 or 28 °C in a 2 × 2 common garden design. The plastic response to increased temperature was a decreased sperm length, velocity, and path linearity. The evolutionary response was a subsequent increase in sperm length, resulting in complete compensation after just 6 months (at most four generations) in 28 °C water. Sperm velocity and linearity showed no sign of evolution even after 24 months. This study provides evidence that some reproductive traits can respond via rapid evolution to the temperature increase associated with climate change.

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References

  • Adriaenssens B, van Damme R, Seebacher F, Wilson RS (2012) Sex cells in changing environments: can organisms adjust the physiological function of gametes to different temperatures? Glob Chang Biol 18:1797–1803

    Article  Google Scholar 

  • Alkins-Koo M (2000) Reproductive timing of fishes in a tropical intermittent stream. Environ Biol Fish 57:49–66

    Article  Google Scholar 

  • Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Beirão J, Soares F, Herráez MP, Dinis MT, Cabrita E (2011) Changes in Solea senegalensis sperm quality throughout the year. Anim Reprod Sci 126:122–129

    Article  PubMed  Google Scholar 

  • Berger D, Bauerfeind SS, Blanckenhorn WU, Schäfer MA (2011) High temperatures reveal cryptic genetic variance in a polymorphic female sperm storage organ. Evolution 65:2830–2842

    Article  PubMed  Google Scholar 

  • Binet MT, Doyle CJ (2013) Effect of near-future seawater temperature rises on sea urchin sperm longevity. Mar Freshw Res 64:1–9

    Article  Google Scholar 

  • Blanckenhorn WU, Hellriegel B (2002) Against Bergmann’s rule: fly sperm increases with temperature. Ecol Lett 5:7–10

    Article  Google Scholar 

  • Boschetto C, Gasparini C, Pilastro A (2011) Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 65:813–821

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2006) Climate change—evolutionary response to rapid climate change. Science 312:1477–1478

    Article  PubMed  CAS  Google Scholar 

  • Breckels RD, Neff BD (2010) Pollution-induced behavioural effects in the brown bullhead (Ameiurus nebulosus). Ecotoxicology 19:1337–1346

    Article  PubMed  CAS  Google Scholar 

  • Breckels RD, Neff BD (2013) The effects of elevated temperature on the sexual traits, immunology, and survivorship of a tropical ectotherm. J Exp Biol 216:2658–2664

    Article  PubMed  Google Scholar 

  • Breckels RD, Garner SR, Neff BD (2014) Rapid evolution in response to increased temperature maintains population viability despite genetic erosion in a tropical ectotherm. Evol Ecol 28:141–155

    Article  Google Scholar 

  • Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc R Soc B 247:89–95

    Article  PubMed  CAS  Google Scholar 

  • Burness G, Moyes CD, Montgomerie R (2005) Motility, ATP levels and metabolic enzyme activity of sperm from bluegill (Lepomis macrochirus). Comp Biochem Physiol 140:11–17

    Article  CAS  Google Scholar 

  • Caissie D, El-Jabi N, Satish MG (2001) Modelling of maximum daily water temperatures in a small stream using air temperatures. J Hydrol 251:14–28

    Article  Google Scholar 

  • Casselman SJ, Schulte-Hostedde AI, Montgomerie R (2006) Sperm quality influences male fertilization success in walleye (Sander vitreus). Can J Fish Aquat Sci 63:2119–2125

    Article  Google Scholar 

  • Deutsch CS, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. PNAS 105:6668–6672

    Article  PubMed Central  PubMed  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limitations of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  PubMed  CAS  Google Scholar 

  • Dorts J, Grenouillet G, Douxfils J, Mandiki SNM, Milla S, Silvestre F, Kestemont P (2012) Evidence that elevated water temperature affects the reproductive physiology of the European bullhead Cottus gobio. Fish Physiol Biochem 38:389–399

    Article  PubMed  CAS  Google Scholar 

  • Emlen ST, Oring LW (1977) Sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  PubMed  CAS  Google Scholar 

  • Endler JA (1980) Natural selection of colour patterns in Poecilia reticulata. Evolution 34:76–91

    Article  Google Scholar 

  • Evans JP (2009) No evidence for sperm priming responses under varying sperm competition risk or intensity in guppies. Naturwissenschaften 96:771–779

    Article  PubMed  CAS  Google Scholar 

  • Evans JP (2011) Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies. Heredity 106:869–875

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. PNAS 106:1128–1132

    Article  PubMed Central  PubMed  Google Scholar 

  • Fuller A, Dawson T, Helmuth B, Hetem RS, Mitchell D, Maloney SK (2010) Physiological mechanisms in coping with climate change. Physiol Biochem Zool 83:713–720

    Article  PubMed  Google Scholar 

  • Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47

    PubMed  CAS  Google Scholar 

  • Gasparini C, Marino IAM, Boschetto C, Pilastro A (2010) Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata). J Evol Biol 23:124–135

    Article  PubMed  CAS  Google Scholar 

  • Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc B 243:181–185

    Article  PubMed  CAS  Google Scholar 

  • Hendry AP, Hensleigh JE, Reisenbichler RR (1998) Incubation temperature, developmental biology, and the divergence of sockeye salmon (Oncorhynchus nerka) within Lake Washington. Can J Fish Aquat Sci 55:1387–1394

    Article  Google Scholar 

  • Hendry AP, Wenburg JK, Bentzen P, Volk EC, Quinn TP (2000) Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290:516–518

    Article  PubMed  CAS  Google Scholar 

  • Houde AE (1997) Sex, colour, and mate choice in guppies. Princeton University Press, Princeton

    Google Scholar 

  • Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319

    Article  PubMed Central  PubMed  Google Scholar 

  • IPCC (2007) Climate change 2007: synthesis report. Cambridge University Press, Cambridge

    Google Scholar 

  • Kaushal SS, Likens GE, Jaworski NA, Pace ML, Sides AM, Seekell D, Belt KT, Secor DH, Wingate RL (2010) Rising stream and river temperatures in the United States. Front Ecol Environ 8:461–466

    Article  Google Scholar 

  • Kime DE, Van Look KJW, McAllister BG, Huyskens G, Rurangwa E, Ollevier F (2001) Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comp Biochem Physiol C 130:425–433

    CAS  Google Scholar 

  • Kobayashi H, Iwamatsu T (2002) Fine structure of the storage micropocket of spermatozoa in the ovary of the guppy Poecilia reticulata. Zool Sci 19:545–555

    Article  PubMed  Google Scholar 

  • Lahnsteiner F, Mansour N (2012) The effect of temperature on sperm motility and enzymatic activity in brown trout Salmo trutta, burbot Lota lota and grayling Thymallus thymallus. J Fish Biol 81:197–209

    Article  PubMed  CAS  Google Scholar 

  • Leal M, Gunderson AR (2012) Rapid change in thermal tolerance of a tropical lizard. Am Nat 180:815–822

    Article  PubMed  Google Scholar 

  • Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM, Pitnick S (2012) How multiple ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 22:1667–1672

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS (2006) Sperm design and sperm function. Biol Lett 2:246–249

    Article  PubMed Central  PubMed  Google Scholar 

  • Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233

    Article  PubMed  CAS  Google Scholar 

  • Morrow EH, Gage MJG (2000) The evolution of sperm length in moths. Proc R Soc B 267:307–313

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mossman J, Slate J, Humphries S, Birkhead T (2009) Sperm morphology and velocity are genetically codetermined in the zebra finch. Evolution 63:2730–2737

    Article  PubMed  Google Scholar 

  • Parker GA (1993) Sperm competition games: sperm size and number under adult control. Proc R Soc B 253:245–254

    Article  PubMed  CAS  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  PubMed  CAS  Google Scholar 

  • Pilastro A, Evans JP, Sartorelli S, Bisazza A (2002) Male phenotype predicts insemination success in guppies. Proc R Soc B 269:1325–1330

    Article  PubMed Central  PubMed  Google Scholar 

  • Pitnick S, Markow T, Spicer GS (1999) Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53:1804–1822

    Article  Google Scholar 

  • Presgraves DC, Baker RH, Wilkinson GS (1999) Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proc R Soc B 266:1041–1047

    Article  PubMed Central  Google Scholar 

  • Réale D, Berteaux D, McAdam AG, Boutin S (2003) Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution 57:2416–2423

    Article  PubMed  Google Scholar 

  • Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937

    Article  PubMed  CAS  Google Scholar 

  • Reznick D, Buckwalter G, Groff J, Elder D (2001) The evolution of senescence in natural populations of guppies (Poecilia reticulata): a comparative approach. Exp Gerontol 36:791–812

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW, Fitzpatrick JL (2012) Sperm wars and the evolution of male fertility. Reproduction 144:519–534

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW, Moore AJ (2009) Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Elsevier, Oxford, pp 405–434

    Chapter  Google Scholar 

  • Singh B (1997) Climate-related global changes in the southern Caribbean: Trinidad and Tobago. Glob Planet Chang 15:93–111

    Article  Google Scholar 

  • Snook R (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:45–63

    Article  Google Scholar 

  • Stefan HG, Preudhomme EB (1993) Stream temperature estimation from air–temperature. J Am Water Resour Assoc 29:27–45

    Article  Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65

    Article  PubMed  CAS  Google Scholar 

  • Stoltz JA, Neff BD (2006) Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J Evol Biol 19:1873–1881

    Article  PubMed  CAS  Google Scholar 

  • Water Resources Agency (2001) National report on integrating the management of watersheds and coastal areas in Trinidad and Tobago. Ministry of Public Utilities and the Environment, Port of Spain

    Google Scholar 

  • West PM, Packer C (2002) Sexual selection, temperature, and the lion’s mane. Science 297:1339–1343

    Article  PubMed  CAS  Google Scholar 

  • Williot P, Kopeika EF, Goncharov BF (2000) Influence of testis state, temperature and delay in semen collection on spermatozoa motility in the cultured Siberian sturgeon (Acipenser baeri Brandt). Aquaculture 189:53–61

    Article  Google Scholar 

  • Zeh JA, Bonilla MM, Su EJ, Padua MV, Anderson RV, Kaur D, Yang DS, Zeh DW (2012) Degrees of disruption: projected temperature increase has catastrophic consequences for reproduction in a tropical ectotherm. Glob Chang Biol 18:1833–1842

    Article  Google Scholar 

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Acknowledgments

We thank J. Hung and M. Lau for their help with conducting sperm video analyses and S. Garner, T. Hain, N. Muñoz, C. Partridge, and three anonymous reviewers for providing comment that improved the manuscript. This research was funded by Natural Sciences and Engineering Research Council of Canada.

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  1. Department of Biology, University of Western Ontario, London, ON, N6A 5B7, Canada

    Ross D. Breckels & Bryan D. Neff

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  1. Ross D. Breckels
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Correspondence to Bryan D. Neff.

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Breckels, R.D., Neff, B.D. Rapid evolution of sperm length in response to increased temperature in an ectothermic fish. Evol Ecol 28, 521–533 (2014). https://doi.org/10.1007/s10682-014-9692-0

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