Correlated evolution of sexually selected traits: interspecific variation in ejaculates, sperm morphology, copulatory mate guarding, and body size in two sympatric species of garter snakes
- 379 Downloads
Male reproductive success is dependent on a correlated suite of traits related to a species’ ecology and mating system dynamics. Closely related species differing in their mating systems and ecology, such as the garter snakes (Thamnophis), are ideal for studying the correlated evolution of sexually selected traits. Here, we compare the degree of sexual size dimorphism (SSD), copulatory behavior, copulatory plug size, and traits associated with sperm competition between two sympatric and closely related Thamnophis species, T. sirtalis and T. radix with divergent mating aggregation size and density. Our findings indicate that T. sirtalis has greater female-biased SSD, shorter copulations, and larger, more strongly adhering copulatory plugs than T. radix. Our finding that T. sirtalis have longer sperm and higher numbers of sperm per ejaculate is further evidence of more intense sperm competition in this species than in T. radix. However, this reduced number of sperm in the ejaculate means that T. radix males are likely capable of more matings per season than T. sirtalis. This result may reflect differences in feeding during the breeding season (obligate aphagy in T. sirtalis) and the potential for sperm loss in T. radix during prolonged copulations that are prevented in T. sirtlais by their substantial copulatory plugs. Our findings demonstrate that ecological and mating system dynamics have the capacity to strongly influence correlated selection of pre- and postcopulatory traits.
Our findings demonstrate that ecological and mating system dynamics have the capacity to strongly influence correlated selection of, and trade-offs between, pre- and postcopulatory traits. For most postcopulatory selected traits we measured (sperm size, ejaculate size, effectiveness of their copulatory plug, and gamete-somatic index (but not relative testes mass)), the species predicted to experience strong sperm competition (T. sirtalis) has higher trait values. However, T. radix, which has a precopulatory mating advantage (larger male body size and less pronounced female-biased sexual size dimorphism), has enough stored sperm for many more matings. The large amount of stored sperm in T. radix may be due to sperm loss during prolonged matings or different energy budgets between the two species: T. sirtalis, with an evolutionary history of sperm competition, does not eat during the breeding season, which limits the time available for mating.
KeywordsSexual size dimorphism Sperm competition Copulatory plugs Prolonged copulation Reptile
Mariaelena Del Rio did the sperm counts and C.M. Whittington and two anonymous reviewers gave thoughtful comments and edits that improved the manuscript.
CRF is grateful for funding from the NSF (DDIG IOS 1011727 and IPRFB DIB-1308394).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures used in this research were approved by the Oregon State University Animal Care and Use Committee (ACUP no. 4317). This research complied with guidelines established by the National Institutes of Health Guide for the Care and Use of Laboratory Animals and was carried out under the authority of Manitoba Wildlife Scientific Permit WB12405.
- Alcock J (1994) Postinsemination associations between males and females in insects: the mate-guarding hypothesis. Annu Rev Entomol 39(1):1–21. https://doi.org/10.1146/annurev.en.39.010194.000245 CrossRefGoogle Scholar
- Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
- Arnqvist G (2014) Cryptic female choice. In: Shuker DM, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, Oxford, pp 204–220. https://doi.org/10.1093/acprof:oso/9780199678020.003.0011 CrossRefGoogle Scholar
- Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, San DiegoGoogle Scholar
- Brennan PL, Prum RO (2014) Mechanisms and evidence of genital coevolution: the roles of natural selection, mate choice, and sexual conflict. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 385–406Google Scholar
- Cox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford, pp 38–49. https://doi.org/10.1093/acprof:oso/9780199208784.003.0005 CrossRefGoogle Scholar
- Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, LondonGoogle Scholar
- Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol S 39(1):387–413. https://doi.org/10.1146/annurev.ecolsys.39.110707.173502 CrossRefGoogle Scholar
- Fairbairn DJ, Blanckenhorn WU, Székely T (eds) (2007) Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199208784.001.0001 CrossRefGoogle Scholar
- Fitch HS (1965) An ecological study of the garter snake, Thamnophis sirtalis. Univ Kansas Publ Mus Nat Hist 15:493–564Google Scholar
- Friesen CR, Shine R, Krohmer RW, Mason RT (2013) Not just a chastity belt: the functional significance of mating plugs in garter snakes, revisited. Biol J Linn Soc 109(4):893–907. https://doi.org/10.1111/bij.12089
- Ghiselin MT (1976) The economy of nature and the evolution of sex. University of California Press, Los AngelesGoogle Scholar
- Gregory PT (1977) Life history parameters of the red-sided garter snake (Thamnophis sirtalis pairetalis) in an extreme environment, the Interlake region of Manitoba Canada. National Museum of Canada, OttawaGoogle Scholar
- Gregory PG (1984) Communal denning in snakes. In: Fitch HS, Seigel RA (eds) Vertebrate ecology and systematics: a tribute to Henry S. Fitch. University of Kansas, Lawrence, pp 57–76Google Scholar
- Hosokawa T, Nobuhiko S (2001) Significance of prolonged copulation under the restriction of daily reproductive time in the stink bug Megacopta punctatissima (Heteroptera: Plataspidae). Behaviour 94:750–754Google Scholar
- King RB, Bittner TD, Queral-Regil A, Cline JH (1999) Sexual dimorphism in neonate and adult snakes. J Zool 247(1):19–28. https://doi.org/10.1111/j.1469-7998.1999.tb00189.x CrossRefGoogle Scholar
- Kokko H, Jennions MD (2014) The relationship between sexual selection and sexual conflict. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 23–35Google Scholar
- Madsen T, Shine R (1994) Costs of reproduction influence the evolution of sexual size dimorphism in snakes. Evolution 48(4):1389–1397. https://doi.org/10.1111/j.1558-5646.1994.tb05323.x PubMedCrossRefGoogle Scholar
- Mason R, MacMillan S, Whittier J, Krohmer R, Koonz W (1991) Thamnophis sirtalis parietalis (red-sided garter snake) population morph variation. Herpetol Rev 22:61Google Scholar
- Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45(4):525–567. https://doi.org/10.1111/j.1469-185X.1970.tb01176.x CrossRefGoogle Scholar
- Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 123–163Google Scholar
- Parker GA (2014) The sexual cascade. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 23–35Google Scholar
- Rossman DA, Ford NB, Seigel RA (1996) The garter snakes: evolution and ecology. University of Oklahoma Press, NormanGoogle Scholar
- Shine R, Olsson MM, Mason RT (2000b) Chastity belts in gartersnakes: the functional significance of mating plugs. Biol J Linn Soc 70(3):377–390. https://doi.org/10.1111/j.1095-8312.2000.tb01229.x CrossRefGoogle Scholar
- Shine R, Elphick MJ, Harlow PS, Moore IT, LeMaster MP, Mason RT (2001) Movements, mating, and dispersal of red-sided gartersnakes (Thamnophis sirtalis parietalis) from a communal den in Manitoba. Copeia 2001(1):82–91. https://doi.org/10.1643/0045-8511(2001)001[0082:MMADOR]2.0.CO;2 CrossRefGoogle Scholar
- Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, PrincetonGoogle Scholar
- Tourmente M, Giojalas LC, Chiaraviglio M (2011) Sperm parameters associated with reproductive ecology in two snake species. Herpetologica 67(1):58–70. https://doi.org/10.1655/HERPETOLOGICA-D-10-00052.1 CrossRefGoogle Scholar
- Wusterbarth T, King RB, Duvall MR, Grayburn WS, Burghardt GM (2010) Phylogenetically widespread multiple paternity in new world natricine snakes. Herpetol Conserv Biol 2010:86–93Google Scholar