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

Abstract

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.

Significance statement

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.

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Acknowledgments

Mariaelena Del Rio did the sperm counts and C.M. Whittington and two anonymous reviewers gave thoughtful comments and edits that improved the manuscript.

Funding

CRF is grateful for funding from the NSF (DDIG IOS 1011727 and IPRFB DIB-1308394).

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Correspondence to Christopher R. Friesen.

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The authors declare that they have no conflict of interest.

Ethical approval

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.

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Communicated by S. J. Downes

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Friesen, C.R., Uhrig, E.J., Bentz, E.J. et al. 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. Behav Ecol Sociobiol 71, 180 (2017). https://doi.org/10.1007/s00265-017-2414-1

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Keywords

  • Sexual size dimorphism
  • Sperm competition
  • Copulatory plugs
  • Prolonged copulation
  • Reptile