1932

Abstract

Using basic ecological concepts, we introduce sperm ecology as a framework to study sperm cells. First, we describe environmental effects on sperm and conclude that evolutionary and ecological research should not neglect the overwhelming evidence presented here (both in external and internal fertilizers and in terrestrial and aquatic habitats) that sperm function is altered by many environments, including the male environment. Second, we determine that the evidence for sperm phenotypic plasticity is overwhelming. Third, we find that genotype-by-environment interaction effects on sperm function exist, but their general adaptive significance (e.g., local adaptation) awaits further research. It remains unresolved whether sperm diversification occurs by natural selection acting on sperm function or by selection on male and female microenvironments that enable optimal plastic performance of sperm (sperm niches). Environmental effects reduce fitness predictability under sperm competition, predict species distributions under global change, explain adaptive behavior, and highlight the role of natural selection in behavioral ecology and reproductive medicine.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-120213-091611
2015-12-04
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/46/1/annurev-ecolsys-120213-091611.html?itemId=/content/journals/10.1146/annurev-ecolsys-120213-091611&mimeType=html&fmt=ahah

Literature Cited

  1. 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. Change Biol. 18:1797–803 [Google Scholar]
  2. Aitken RJ. 2006. Sperm function tests and fertility. Int. J. Androl. 29:60–75 [Google Scholar]
  3. Aitken RJ, Baker MA. 2013. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int. J. Dev. Biol. 57:265–72 [Google Scholar]
  4. Aitken RJ, Bronson R, Smith TB, De Iuliis GN. 2013. The source and significance of DNA damage in human spermatozoa; a commentary on diagnostic strategies and straw man fallacies. Mol. Hum. Reprod. 19:475–85 [Google Scholar]
  5. Aitken RJ, Clarkson JS. 1988. Significance of reactive oxygen species and anti-oxidants in defining the efficacy of sperm preparation techniques. J. Androl. 9:367–76 [Google Scholar]
  6. Aitken RJ, De Iuliis GN, McLachlan RI. 2009. Biological and clinical significance of DNA damage in the male germ line. Int. J. Androl. 32:46–56 [Google Scholar]
  7. Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS, De Iuliis GN. 2012. Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biol. Reprod. 87:110 [Google Scholar]
  8. Aitken RJ, Koppers AJ. 2011. Apoptosis and DNA damage in human spermatozoa. Asian J. Androl. 13:36–42 [Google Scholar]
  9. Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. 2014. Oxidative stress and male reproductive health. Asian J. Androl. 16:31–38 [Google Scholar]
  10. Alavi SMH, Cosson J. 2005. Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell Biol. Int. 29:101–10 [Google Scholar]
  11. Almbro M, Dowling DK, Simmons LW. 2011. Effects of vitamin E and beta-carotene on sperm competitiveness. Ecol. Lett. 14:891–95 [Google Scholar]
  12. Alvarez L, Dai L, Friedrich BM, Kashikar ND, Gregor I. et al. 2012. The rate of change in Ca2+ concentration controls sperm chemotaxis. J. Cell Biol. 196:653–63 [Google Scholar]
  13. Alvarez L, Friedrich BM, Gompper G, Kaupp UB. 2014. The computational sperm cell. Trends Cell Biol. 24:198–207 [Google Scholar]
  14. Aoki VW, Emery BR, Liu L, Carrell DT. 2006. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J. Androl. 27:890–98 [Google Scholar]
  15. Aranha I, Bhagya M, Yajurvedi HN. 2008. Concentration of cations in different parts of male reproductive system and their influence on in vitro sperm motility in lizard, Mabuya carinata Schneider. Ind. J. Exp. Biol. 46:720–24 [Google Scholar]
  16. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF. 2011. Insect seminal fluid proteins: identification and function. Annu. Rev. Entomol. 56:21–40 [Google Scholar]
  17. Axelsson J, Bonde JP, Giwercman YL, Rylander L, Giwercman A. 2010. Gene-environment interaction and male reproductive function. Asian J. Androl. 12:298–307 [Google Scholar]
  18. Babcock DF, Wandernoth PM, Wennemuth G. 2014. Episodic rolling and transient attachments create diversity in sperm swimming behavior. BMC Biol. 12:67 [Google Scholar]
  19. Bahat A, Eisenbach M. 2006. Sperm thermotaxis. Mol. Cell. Endocrinol. 252:115–19 [Google Scholar]
  20. Banks S, King SA, Irvine DS, Saunders PTK. 2005. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 129:505–14 [Google Scholar]
  21. Barros CM, Pegorer MF, Vasconcelos JLM, Eberhardt BG, Monteiro FM. 2006. Importance of sperm genotype (indicus versus taurus) for fertility and embryonic development at elevated temperatures. Theriogenology 65:210–18 [Google Scholar]
  22. Barros P, Sobral P, Range P, Chicharo L, Matias D. 2013. Effects of sea-water acidification on fertilization and larval development of the oyster Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 440:200–6 [Google Scholar]
  23. Beirao J, Purchase CF, Wringe BF, Fleming IA. 2014. Sperm plasticity to seawater temperatures in Atlantic cod Gadus morhua is affected more by population origin than individual environmental exposure. Mar. Ecol. Prog. Ser. 495:263–74 [Google Scholar]
  24. Bencic DC, Cloud JG, Ingermann RL. 2000. Carbon dioxide reversibly inhibits sperm motility and fertilizing ability in steelhead (Oncorhynchus mykiss). Fish Physiol. Biochem. 23:275–81 [Google Scholar]
  25. Bernasconi G, Ashman T-L, Birkhead TR, Bishop JDD, Grossniklaus U. et al. 2004. Evolutionary ecology of the prezygotic stage. Science 303:971–75 [Google Scholar]
  26. Bienkowska M, Panasiuk B, Wegrzynowicz P, Gerula D. 2011. The effect of different thermal conditions on drone semen quality and number of spermatozoa entering the spermatheca of queen bee. J. Apic. Res. 55:161–68 [Google Scholar]
  27. Billard R, Cosson MP. 1992. Some problems related to the assessment of sperm motility in freshwater fish. J. Exp. Zool. 261:122–31 [Google Scholar]
  28. Binet MT, Doyle CJ. 2013. Effect of near-future seawater temperature rises on sea urchin sperm longevity. Mar. Freshw. Res. 64:1–9 [Google Scholar]
  29. Birkhead TR, Fletcher F. 1995. Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc. R. Soc. Lond. B 262:329–34 [Google Scholar]
  30. Birkhead TR, Hosken DJ, Pitnick S. 2009. Sperm Biology: An Evolutionary Perspective. New York: Academic
  31. Birkhead TR, Martinez JG, Burke T, Froman DP. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B 266:1759–64 [Google Scholar]
  32. Birkhead TR, Møller AP, Sutherland WJ. 1993. Why do females make it so difficult for males to fertilize their eggs?. J. Theor. Biol. 161:51–60 [Google Scholar]
  33. Blanckenhorn WU, Hellriegel B. 2002. Against Bergmann's rule: fly sperm size increases with temperature. Ecol. Lett. 5:7–10 [Google Scholar]
  34. Blanco JM, Gee G, Wildt DE, Donoghue AM. 2000. Species variation in osmotic, cryoprotectant, and cooling rate tolerance in poultry, eagle, and peregrine falcon spermatozoa. Biol. Reprod. 63:1164–71 [Google Scholar]
  35. Breckels RD, Neff BD. 2013. The effects of elevated temperature on the sexual traits, immunology and survivorship of a tropical ectotherm. J. Exp. Biol. 216:2658–64 [Google Scholar]
  36. Breckels RD, Neff BD. 2014. Rapid evolution of sperm length in response to increased temperature in an ectothermic fish. Evol. Ecol. 28:521–33 [Google Scholar]
  37. Brito LFC, Silva AEDF, Rodrigues LH, Vieira FV, Deragon LAG, Kastelic JP. 2003. Effects of environmental factors, age and genotype on sperm production and semen quality in Bos indicus and Bos taurus AI bulls in Brazil. Anim. Reprod. Sci. 70:181–90 [Google Scholar]
  38. Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. 2014. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. PNAS 111:2200–5 [Google Scholar]
  39. Burness G, Casselman SJ, Schulte-Hostedde AI, Moyes CD, Montgomerie R. 2004. Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav. Ecol. Sociobiol. 56:65–70 [Google Scholar]
  40. Burruel V, Klooster KL, Chitwood J, Ross PJ, Meyers SA. 2013. Oxidative damage to rhesus macaque spermatozoa results in mitotic arrest and transcript abundance changes in early embryos. Biol. Reprod. 89:72 [Google Scholar]
  41. Byrne M, Soars NA, Ho MA, Wong E, McElroy D. et al. 2010. Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Mar. Biol. 157:2061–69 [Google Scholar]
  42. Caldwell GS, Fitzer S, Gillespie CS, Pickavance G, Turnbull E, Bentley MG. 2011. Ocean acidification takes sperm back in time. Invert. Reprod. Dev. 55:217–21 [Google Scholar]
  43. Chacur MGM, Mizusaki KT, Gabriel LRA, Oba E, Ramos AA. 2013. Seasonal effects on semen and testosterone in Zebu and Taurine bulls. Acta Sci. Vet. 41:1110 [Google Scholar]
  44. Clark AG, Begun DJ, Prout T. 1999. Female × male interactions in Drosophila sperm competition. Science 283:217–20 [Google Scholar]
  45. Crean AJ, Dwyer JM, Marshall DJ. 2013. Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94:2575–82 [Google Scholar]
  46. Crean AJ, Marshall DJ. 2008. Gamete plasticity in a broadcast spawning marine invertebrate. PNAS 105:13508–13 [Google Scholar]
  47. Dada R, Kumar M, Jesudasan R, Fernández JL, Agrawal A. 2012. Epigenetics and its role in male infertility. J. Assist. Reprod. Genet. 29:213–23 [Google Scholar]
  48. Delph LF, Johannson MH, Stephenson AG. 1997. How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78:1632–39 [Google Scholar]
  49. den Boer SPA, Baer B, Boomsma JJ. 2010. Seminal fluid mediates ejaculate competition in social insects. Science 327:1506–9 [Google Scholar]
  50. Dorado J, Acha D, Galvez MJ, Ortiz I, Carrasco JJ. et al. 2013. Sperm motility patterns in Andalusian donkey (Equus asinus) semen: effects of body weight, age, and semen quality. Theriogenology 79:1100–9 [Google Scholar]
  51. Dowling DK. 2014. Evolutionary perspectives on the links between mitochondrial genotype and disease phenotype. Biochim. Biophys. Acta 1840:1393–403 [Google Scholar]
  52. Dowling DK, Nowostawski AL, Arnqvist G. 2007. Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory?. J. Evol. Biol. 20:358–68 [Google Scholar]
  53. Dowling DK, Nystrand M, Simmons LW. 2010. Maternal effects, but no good or compatible genes for sperm competitiveness in Australian crickets. Evolution 64:1257–66 [Google Scholar]
  54. Elofsson H, Van Look K, Borg B, Mayer I. 2003. Influence of salinity and ovarian fluid on sperm motility in the fifteen-spined stickleback. J. Fish Biol. 63:1429–38 [Google Scholar]
  55. Fraga GG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames B. 1996. Smoking and low antioxidants levels increase oxidative damage to sperm DNA. Mutat. Res. 351:199–203 [Google Scholar]
  56. Friberg U, Dowling DK. 2008. No evidence of mitochondrial genetic variation for sperm competition within a population of Drosophila melanogaster. J. Evol. Biol. 21:1798–804 [Google Scholar]
  57. Friedrich BM, Jülicher F. 2007. Chemotaxis of sperm cells. PNAS 104:13256–61 [Google Scholar]
  58. Froman DP, Feltmann AJ. 1998. Sperm mobility: a quantitative trait of the domestic fowl (Gallus domesticus). Biol. Reprod. 58:379–84 [Google Scholar]
  59. Froman DP, Kirby JD. 2005. Sperm mobility: phenotype in roosters determined by mitochondrial function. Biol. Reprod. 72:562–67 [Google Scholar]
  60. Froman DP, Wardell JC, Feltmann AJ. 2006. Sperm mobility: deduction of a model explaining phenotypic variation in roosters (Gallus domesticus). Biol. Reprod. 74:487–91 [Google Scholar]
  61. Frommel AY, Stiebens V, Clemmesen C, Havenhand J. 2010. Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua). Biogeosciences 7:3915–19 [Google Scholar]
  62. 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 [Google Scholar]
  63. Garcia-Tomas M, Sanchez J, Rafel O, Ramon J, Piles M. 2006. Variability, repeatability and phenotypic relationships of several characteristics of production and semen quality in rabbit. Anim. Reprod. Sci. 93:88–100 [Google Scholar]
  64. Gasparini C, Evans JP. 2014. Ovarian fluid mediates the temporal decline in sperm viability in a fish with sperm storage. PLOS ONE 8:e64431 [Google Scholar]
  65. Ghaleno LR, Valojerdi MR, Hassani F, Chehrazi M, Janzamin E. 2014. High level of intracellular sperm oxidative stress negatively influences embryo pronuclear formation after intracytoplasmic sperm injection treatment. Andrologia 46:1118–27 [Google Scholar]
  66. Glazener CM, Ford WC, Hull MG. 2000. The prognostic power of the post-coital test for natural conception depends on duration of infertility. Hum. Reprod. 15:1953–57 [Google Scholar]
  67. Havenhand JN, Schlegel P. 2009. Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences 6:3009–15 [Google Scholar]
  68. Hayes TB. 2011. Atrazine has been used safely for 50 years?. Emerg. Top. Ecotoxicol. 3:301–24 [Google Scholar]
  69. Heifetz Y, Rivlin PK. 2010. Beyond the mouse model: using Drosophila as a model for sperm interaction with the female reproductive tract. Theriogenology 73:723–39 [Google Scholar]
  70. Heise A, Kaehn W, Volkmann DH, Thompson PN, Gerber D. 2010. Influence of seminal plasma on fertility of fresh and frozen-thawed stallion epididymal spermatozoa. Anim. Reprod. Sci. 118:48–53 [Google Scholar]
  71. Hirsh A. 2003. Male subfertility. Br. Med. J. 327:669–72 [Google Scholar]
  72. Holman L, Snook RR. 2008. A sterile sperm caste protects brother fertile sperm from female-mediated death in Drosophila pseudoobscura. Curr. Biol. 18:292–96 [Google Scholar]
  73. Holt WV, Lloyd RE. 2010. Sperm storage in the vertebrate female reproductive tract: How does it work so well?. Theriogenology 73:713–22 [Google Scholar]
  74. Holt WV, van Look KJW. 2004. Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127:527–35 [Google Scholar]
  75. Hoornstra D, Andersson MA, Johansson T, Pirhonen T, Hatakka M, Salkinoja-Salonen MS. 2004. Mitochondrial toxicity detected in a health product with a boar spermatozoan bioassay. Altern. Lab. Anim. 32:407–16 [Google Scholar]
  76. Hughes M, Davey KG. 1969. The activity of spermatozoa of Periplaneta. J. Insect Physiol. 15:1607–16 [Google Scholar]
  77. Immler S, Hotzy C, Alavioon G, Petersson E, Arnqvist G. 2014. Sperm variation within a single ejaculate affects offspring development in Atlantic salmon. Biol. Lett. 10:20131040 [Google Scholar]
  78. Innocenti P, Morrow EH, Dowling DK. 2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332:845–48 [Google Scholar]
  79. Jenkins TG, Carrell DT. 2012. The sperm epigenome and potential implications for the developing embryo. Reproduction 143:727–34 [Google Scholar]
  80. Jensen N, Allen RM, Marshall DJ. 2014. Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Funct. Ecol. 28:724–33 [Google Scholar]
  81. Johnson GD, Lalancette C, Linnemann AK, Leduc F, Boissonneault G, Krawetz SA. 2011. The sperm nucleus: chromatin, RNA, and the nuclear matrix. Reproduction 141:21–36 [Google Scholar]
  82. Kang JH, Hakimov H, Ruiz A, Friendship RM, Buhr M, Golovan SP. 2008. The negative effects of exogenous DNA binding on porcine spermatozoa are caused by removal of seminal fluid. Theriogenology 70:1288–96 [Google Scholar]
  83. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. 2008. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 93:3199–207 [Google Scholar]
  84. Kumar D, Upadhya D, Uppangala S, Salian SR, Kalthur G, Adiga SK. 2013. Nuclear DNA fragmentation negatively affects zona binding competence of Y bearing mouse spermatozoa. J. Assist. Reprod. Genet. 30:1611–15 [Google Scholar]
  85. Lane M, McPherson NO, Fullston T, Spillane M, Sandeman L. et al. 2014. Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PLOS ONE 9:e100832 [Google Scholar]
  86. Le Comber SC, Faulkes CG, van Look KJW, Holt WV, Smith C. 2004. Recovery of sperm activity after osmotic shock in the three-spined stickleback: implications for pre-oviposition ejaculation. Behaviour 141:1555–69 [Google Scholar]
  87. Leahy T, Gadella BM. 2011. Sperm surface changes and physiological consequences induced by sperm handling and storage. Reproduction 142:759–78 [Google Scholar]
  88. Levitan DR. 1995. The ecology of fertilization in free-spawning invertebrates. Ecology of Marine Invertebrate Larvae LR McEdward 56–123 Boca Raton, FL: CRC [Google Scholar]
  89. Levitan DR. 2000. Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc. R. Soc. Lond. B 267:531–34 [Google Scholar]
  90. Lewis C, Ford AT. 2012. Infertility in male aquatic invertebrates: a review. Aquat. Toxicol. 120:79–89 [Google Scholar]
  91. Lewis SM, Tigreros N, Fedina NT, Ming QL. 2012. Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles. J. Evol. Biol. 25:438–51 [Google Scholar]
  92. Lishko PV, Kirichok Y, Ren DJ, Navarro B, Chung JJ, Clapham DE. 2012. The control of male fertility by spermatozoan ion channels. Annu. Rev. Physiol. 74:453–75 [Google Scholar]
  93. Lindroth A. 1947. Time of activity of freshwater fish spermatozoa in relation to temperature. Zoologiska Bidrag från Uppsala 25:165–68 [Google Scholar]
  94. Lu XY, Wu RSS. 2005. Ultraviolet damages sperm mitochondrial function and membrane integrity in the sea urchin Anthocidaris crassispina. Ecotoxicol. Environ. Saf. 61:53–59 [Google Scholar]
  95. Manier MK, Lüpold S, Belote JM, Starmer WT, Berben KS. et al. 2013. Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr. Biol. 23:1853–62 [Google Scholar]
  96. Mann T. 1964. The Biochemistry of Semen and the Male Reproductive Tract London: Methuen
  97. Marshall DJ. 2015. Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects. J. Exp. Biol. 218:107–13 [Google Scholar]
  98. Mehlis M, Bakker TCM. 2014. The influence of ambient water temperature on sperm performance and fertilization success in three-spined sticklebacks (Gasterosteus aculeatus). Evol. Ecol. 28:655–67 [Google Scholar]
  99. Mita M, Uehara T, Nakamura M. 2002. Comparative studies on the energy metabolism in spermatozoa of four closely related species of sea urchins (genus Echinometra) in Okinawa. Zool. Sci. 19:419–27 [Google Scholar]
  100. Morita M, Awata S, Takahashi T, Takemura A, Kohda M. 2010. Sperm motility adaptation to ion-differing aquatic environments in the Tanganyikan cichlid, Astatotilapia burtoni. J. Exp. Zool. 313A:169–77 [Google Scholar]
  101. Morrell JM, Georgakas A, Lundeheim N, Nash D, Davies Morel MC, Johannisson A. 2014. Effect of heterologous and homologous seminal plasma on stallion sperm quality. Theriogenology 82:176–83 [Google Scholar]
  102. Morrow EH, Leijon A, Meerupati A. 2008. Hemiclonal analysis reveals significant genetic, environmental and genotype×environment effects on sperm size in Drosophila melanogaster. J. Evol. Biol. 21:1692–702 [Google Scholar]
  103. Mortimer ST, Swann M. 1995. Variable kinematics of capacitating human spermatozoa. Hum. Reprod. 10:3178–82 [Google Scholar]
  104. Mossman JA, Slate J, Birkhead TR. 2010. Mitochondrial haplotype does not affect sperm velocity in the zebra finch. Taeniopygia guttata. J. Evol. Biol. 23:422–32 [Google Scholar]
  105. Murphy MP. 2009. How mitochondria produce reactive oxygen species. Biochem. J. 417:1–13 [Google Scholar]
  106. Nahon S, Porras VAC, Pruski AM, Charles F. 2009. Sensitivity to UV radiation in early life stages of the Mediterranean sea urchin Sphaerechinus granularis (Lamarck). Sci. Total Environ. 407:1892–900 [Google Scholar]
  107. Nosil P. 2012. Ecological Speciation New York: Oxford Univ. Press
  108. Okumura A, Fuse H, Kawauchi Y, Mizuno I, Akashi T. 2003. Changes in male reproductive function after high altitude mountaineering. High. Alt. Med. Biol. 4:349–53 [Google Scholar]
  109. Otti O, Johnston PR, Horsburgh GC, Galindo J, Reinhardt K. 2015. Female transcriptomic response to male genetic and nongenetic ejaculate variation. Behav. Ecol. 26:681–88 [Google Scholar]
  110. Otti O, McTighe AP, Reinhardt K. 2013. In vitro antimicrobial sperm protection by an ejaculate-like substance. Funct. Ecol. 27:219–26 [Google Scholar]
  111. Otti O, Naylor R, Siva-Jothy MT, Reinhardt K. 2009. Bacteriolytic activity in the ejaculate of an insect. Am. Nat. 174:292–95 [Google Scholar]
  112. Pacey AA, Hill C, Scudamore IW, Warren MA, Barratt CL, Cooke ID. 1995. Hyperactivation may assist human spermatozoa to detach from intimate association with the endosalpix. Hum. Reprod. 10:2603–9 [Google Scholar]
  113. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525–67 [Google Scholar]
  114. Parker GA. 2009. The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. The Genetics and Biology of Sexual Conflict WR Rice, S Gavrilets 1–22 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press [Google Scholar]
  115. Parker GA, Begon ME. 1993. Sperm competition games: sperm size and number under gametic control. Proc. R. Soc. Lond. B 253:255–62 [Google Scholar]
  116. Paul C, Murray AA, Spears N, Saunders PTK. 2008. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136:73–84 [Google Scholar]
  117. Peters A, Denk AG, Delhey K, Kempenaers B. 2004. Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J. Evol. Biol. 17:1111–20 [Google Scholar]
  118. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP. 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25:459–67 [Google Scholar]
  119. Pischedda A, Rice WR. 2012. Partitioning sexual selection into its mating success and fertilization success components. PNAS 109:2049–53 [Google Scholar]
  120. Pitnick S, Hosken DJ, Birkhead TR. 2009. Sperm morphological diversity. See Birkhead et al. 2009 69–149
  121. Pizzari T, Dean R, Pacey A, Moore H, Bonsall MB. 2008. The evolutionary ecology of pre- and post-meiotic sperm senescence. Trends Ecol. Evol. 23:131–40 [Google Scholar]
  122. Pizzari T, Parker GA. 2009. Sperm competition and sperm phenotype. See Birkhead et al. 2009 207–45
  123. Pizzol D, Ferlin A, Garolla A, Lenzi A, Bertoldo A, Foresta C. 2014. Genetic and molecular diagnostics of male infertility in the clinical practice. Front. Biosci. 19:291–303 [Google Scholar]
  124. Poiani A. 2006. Complexity of seminal fluid: a review. Behav. Ecol. Sociobiol. 60:289–310 [Google Scholar]
  125. Poland V, Eubel H, King M, Solheim C, Harvey Millar A, Baer B. 2011. Stored sperm differs from ejaculated sperm by proteome alterations associated with energy metabolism in the honeybee Apis mellifera. Mol. Ecol. 20:2643–54 [Google Scholar]
  126. Purchase CF, Butts IAE, Alonso-Fernández A, Trippel EA. 2010. Thermal reaction norms in sperm performance of Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 67:498–510 [Google Scholar]
  127. Purchase CF, Moreau DTR. 2012. Stressful environments induce novel phenotypic variation: hierarchical reaction norms for sperm performance of a pervasive invader. Ecol. Evol. 2:2562–71 [Google Scholar]
  128. Rahman MS, Tsuchiya M, Uehara T. 2009. Effects of temperature on gamete longevity and fertilization success in two sea urchin species, Echinometra mathaei and Tripneustes gratilla. Zool. Sci. 26:1–8 [Google Scholar]
  129. Rajkovic J, Uyttendaele A, Deley M, Van Soom W, Rijsselaere A. et al. 2006. Dynamics of boar semen motility inhibition as a semi-quantitative measurement of Bacillus cereus emetic toxin (Cereulide). J. Microbiol. Methods 65:525–34 [Google Scholar]
  130. Ramon M, Salces-Ortiz J, Gonzalez C, Perez-Guzman MD, Garde JJ. et al. 2014. Influence of the temperature and the genotype of the HSP90AA1 gene over sperm chromatin stability in Manchega rams. PLOS ONE 9:e86107 [Google Scholar]
  131. Rand DM. 2001. The units of selection on mitochondrial DNA. Annu. Rev. Ecol. Evol. Syst. 32:415–48 [Google Scholar]
  132. Reinhardt K. 2007. Evolutionary consequences of sperm cell aging. Q. Rev. Biol. 82:375–93 [Google Scholar]
  133. Reinhardt K, Otti O. 2012. Comparing sperm swimming speed. Evol. Ecol. Res. 14:1039–56 [Google Scholar]
  134. Reinhardt K, Ribou A-C. 2013. Females become infertile as the stored sperm's oxygen radicals increase. Sci. Rep. 3:2888 [Google Scholar]
  135. Reinhardt K, Siva-Jothy MT. 2005. An advantage for young sperm in the house cricket Acheta domesticus. Am. Nat. 165:718–23 [Google Scholar]
  136. Renieri T, Vegni Talluri M. 1974. Sperm modification in the female ducts of a grasshopper. Monit. Zool. Ital. 8:1–9 [Google Scholar]
  137. Ribou A-C, Reinhardt K. 2012. Reduced metabolic rate and oxygen radicals production in stored insect sperm. Proc. R. Soc. Lond. B 279:2196–203 [Google Scholar]
  138. Rick IP, Mehlis M, Esser E, Bakker TCM. 2014. The influence of ambient ultraviolet light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Oecologia 174:393–402 [Google Scholar]
  139. Rickard JP, Pini T, Soleilhavoup C, Cognie J, Bathgate R. et al. 2014. Seminal plasma aids the survival and cervical transit of epididymal ram spermatozoa. Reproduction 148:468–78 [Google Scholar]
  140. Riemann JG, Thorson BJ. 1971. Sperm maturation in the male and female genital tracts of Anagasta kühniella (Lepidoptera: Pyralidae). Int. J. Insect Morphol. Embryol. 1:1–19 [Google Scholar]
  141. Ritchie H, Marshall DJ. 2013. Fertilisation is not a new beginning: sperm environment affects offspring development success. J. Exp. Biol. 216:3104–9 [Google Scholar]
  142. Rohmer C, David JR, Moreteau B, Joly D. 2004. Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J. Exp. Biol. 207:2735–43 [Google Scholar]
  143. Roldan ERS, Gomendio M. 2009. Sperm and conservation. See Birkhead et al. 2009 539–64
  144. Rosengrave P, Taylor H, Montgomerie R, Metcalf V, McBride K, Gemmell NJ. 2009. Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp. Biochem. Physiol. A 152:123–29 [Google Scholar]
  145. Satake N, Elliott RMA, Watson PF, Holt WV. 2006. Sperm selection and competition in pigs may be mediated by the differential motility activation and suppression of sperm subpopulations within the oviduct. J. Exp. Biol. 209:1560–72 [Google Scholar]
  146. Scaggiante M, Mazzoldi C, Petersen CW, Rasotto MB. 1999. Sperm competition and mode of fertilization in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae). J. Exp. Zool. 283:81–90 [Google Scholar]
  147. Schlegel P, Havenhand JN, Gillings MR, Williamson JE. 2012. Individual variability in reproductive success determines winners and losers under ocean acidification: a case study with sea urchins. PLOS ONE 7:e53118 [Google Scholar]
  148. Schlegel P, Havenhand JN, Obadia N, Williamson JE. 2014. Sperm swimming in the polychaete Galeolaria caespitosa shows substantial inter-individual variability in response to future ocean acidification. Mar. Pollut. Bull. 78:213–17 [Google Scholar]
  149. Schramm GP. 2008. Studies on genotype specific modified methods for cryopreservation of cock semen. Züchtungskunde 80:137–45 [Google Scholar]
  150. Shaliutina-Kolesova A, Gazo I, Cosson J, Linhart O. 2014. Protection of common carp (Cyprinus carpio L.) spermatozoa motility under oxidative stress by antioxidants and seminal plasma. Fish Physiol. Biochem. 40:1771–81 [Google Scholar]
  151. Simmons LW, Lovegrove M, Almbro M. 2014. Female effects, but no intrinsic male effects on paternity outcome in crickets. J. Evol. Biol. 27:1644–49 [Google Scholar]
  152. Simmons LW, Moore AJ. 2009. Evolutionary quantitative genetics of sperm. See Birkhead et al. 2009 405–34 [Google Scholar]
  153. Siva-Jothy MT. 2000. The young sperm gambit. Ecol. Lett. 3:172–74 [Google Scholar]
  154. Stürup M, Baer-Imhoof B, Nash DR, Boomsma JJ, Baer B. 2013. When every sperm counts: factors affecting male fertility in the honeybee Apis mellifera. Behav. Ecol. 24:1192–98 [Google Scholar]
  155. Sung CG, Kim TW, Park YG, Kang SG, Inaba K. et al. 2014. Species and gamete-specific fertilization success of two sea urchins under near future levels of pCO2. J. Mar. Syst. 137:67–73 [Google Scholar]
  156. Tarín JJ, Pérez-Albalá S, Cano A. 2000. Consequences on offspring of abnormal function in ageing gametes. Hum. Reprod. Update 6:532–49 [Google Scholar]
  157. Tavares RS, Mansell S, Barratt CL, Wilson SM, Publicover SJ, Ramalho-Santos J. 2013. p,p′-DDE activates CatSper and compromises human sperm function at environmentally relevant concentrations. Hum. Reprod. 28:3167–77 [Google Scholar]
  158. Usinger RL. 1966. Monograph of the Cimicidae Philadelphia: Entomol. Soc. Am.
  159. Uthicke S, Pecorino D, Albright R, Negri AP, Cantin N. et al. 2013. Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci. PLOS ONE 8:e82938 [Google Scholar]
  160. Vasudeva R, Deeming DC, Eady PE. 2014. Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus. J. Evol Biol. 27:1811–18 [Google Scholar]
  161. Vihtakari M, Hendriks IE, Holding J, Renaud PE, Duarte CM, Havenhand JN. 2013. Effects of ocean acidification and warming on sperm activity and early life stages of the Mediterranean mussel (Mytilus galloprovincialis). Water 5:1890–915 [Google Scholar]
  162. Villegas J, Kehr K, Soto L, Henkel R, Miska W, Sanchez R. 2003. Reactive oxygen species induce reversible capacitation in human spermatozoa. Andrologia 35:227–32 [Google Scholar]
  163. Wallace DC, Fan W, Procaccio P. 2011. Mitochondrial energetics and therapeutics. Annu. Rev. Pathol. Mech. Dis. 5:297–348 [Google Scholar]
  164. West-Eberhard MJ. 2003. Developmental Plasticity and Evolution Oxford, UK: Oxford Univ. Press
  165. Wolff JN, Ladoukakis ED, Enriquez JA, Dowling DK. 2014. Mitonuclear interactions: evolutionary consequences over multiple biological scales. Philos. Trans. R. Soc. B 369:20130443 [Google Scholar]
  166. World Health Organ 2010. WHO Laboratory Manual for the Examination and Processing of Human Sperm Geneva: WHO, 5th ed..
  167. Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW. et al. 2008. Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. PNAS 105:605–10 [Google Scholar]
  168. Yee WKW, Sutton KL, Dowling DK. 2013. In vivo male fertility is affected by naturally occurring mitochondrial haplotypes. Curr. Biol. 23:R55–56 [Google Scholar]
  169. Yeung CH, Barfield JP, Cooper TG. 2006. Physiological volume regulation by spermatozoa. Mol. Cell. Endocrinol. 250:98–110 [Google Scholar]
  170. Zini A, Al-Hathal N. 2011. Antioxidant therapy in male infertility: fact or fiction?. Asian J. Androl. 13:374–81 [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-120213-091611
Loading
/content/journals/10.1146/annurev-ecolsys-120213-091611
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error