Sex, shells, and weaponry: coercive reproductive tactics in the painted turtle, Chrysemys picta

Abstract

Males and females have divergent reproductive interests arising from their unequal investments in offspring. This sexual conflict drives an antagonistic arms race that influences sex-specific reproductive success. Alternative reproductive tactics are expected in long-lived species for which the reproductive strategy that maximizes mating success could differ across body sizes. The mating strategy of the painted turtle (Chrysemys picta) has been characterized as an elaborate and amiable male courtship display during which males use their elongate foreclaws to stroke females, coupled with female mate choice. Contrary to this long-held understanding, in situ field observations and experimental trials from our long-term study in Algonquin Provincial Park, Canada, demonstrate that males also exhibit an alternative, coercive mating strategy. Males are equipped with sexually size dimorphic tomiodonts, tooth-like cusps of the beak, as well as a weaponized anterior shell, with which they wound the head and neck of females. Behavioral trials during the breeding periods showed that male reproductive tactics shift from courtship (foreclaw display) to coercion (striking, biting, and forced submergence) across ontogeny, and male size predicts the occurrence and frequency of coercive behavior. We found phenotype-behavior matching whereby small males invest in putatively ornamental foreclaws used for courtship and large males invest in weaponry for coercion, challenging existing knowledge of this well-studied species. As a group with a long evolutionary history and varied mating systems, Testudines are a particularly interesting taxon in which to ask questions about mating system evolution.

Significance statement

Alternative reproductive tactics are hypothesized for long-lived species. We quantified a shift from apparent courtship to coercive tactics during the reproductive lifespan of a well-studied freshwater turtle. Male painted turtles (Chrysemys picta) have sexual weapons that are used to promote female acquiescence. Using behavioral trials with turtles from a long-term study population, we demonstrate that males match their morphology (ornament/weapons) to reproductive behavior (courtship/coercion) as their reproductive tactics shift. Our findings hint at the behavioral complexity of aquatic turtles, a challenging and often-overlooked group in behavioral studies.

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Data availability

Data and R code associated with this manuscript are deposited in the digital repository Zenodo. DOI: https://doi.org/10.5281/zenodo.4110623

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Acknowledgments

PDM thanks M.G. Keevil, J.L. Riley, and D.L. LeGros for their friendship, mentorship, and insightful discussions on all subjects tomiodonts and titillation. We thank reviewer R. Shine for thoughtful comments that improved the manuscript and stimulated novel thinking. T.C. Roth provided constrictive comments about research ethics and animal welfare. Additional thanks to M.G. Keevil, K.A. Henderson, S. Sanders, J. Flatt, M. Anagnostou, B. Hewitt, and S.J. Kell for assistance with field work and data collection. We value early record-keeping by K. Kasparian (Sari), M. Karch, J. Samson, P. Tran, T. Alkins, H. Kitching, J. Kellar, and E. Hughes about male turtle behavior and female wounding. We also wish to thank the Algonquin Wildlife Research Station and Ontario Parks for support of the long-term turtle studies in Algonquin Provincial Park.

Funding

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to JDL (grant number 311994) and RJB (grant number A5990), Ontario Ministry of Natural Resources and Forestry, and Ontario Parks. Additional support was provided by the Canadian Herpetological Society, Society for the Study of Amphibians and Reptiles, Ruffed Grouse Society, and the Sudbury Game and Fish Protective Association.

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Conceptualization: PDM, RJB, JDL; methodology: PDM, RJB, JDL; formal analysis and investigation: PDM; writing—original draft preparation: PDM; writing—review and editing: PDM, RJB, JDL; funding acquisition: RJB, JDL; supervision: JDL.

Corresponding author

Correspondence to Patrick D. Moldowan.

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The authors declare that they have no conflict of interest.

Ethics approval

Animal handling was approved by the Laurentian University Animal Care Committee (AUP #2008-12-02) and conforms to the guidelines of Canadian Council on Animal Care.

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All persons entitled to authorship have been included as authors and all authors have read and approved the submitted manuscript.

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Data and R code associated with this manuscript are deposited in the digital repository Zenodo. DOI: https://doi.org/10.5281/zenodo.4110623

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Communicated by S. Joy Downes

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Moldowan, P.D., Brooks, R.J. & Litzgus, J.D. Sex, shells, and weaponry: coercive reproductive tactics in the painted turtle, Chrysemys picta. Behav Ecol Sociobiol 74, 142 (2020). https://doi.org/10.1007/s00265-020-02926-w

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Keywords

  • Alternative reproductive tactics
  • Mating strategy
  • Sexual conflict
  • Sexual dimorphism
  • Sexual weapon
  • Titillation