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Discovery and description of a novel sexual weapon in the world’s most widely-studied freshwater turtle

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A Correction to this article was published on 11 December 2019

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Abstract

Sexually coercive reproductive tactics are widespread among animals, where one sex employs specialized structures, called sexual weapons, to harass, intimidate, and/or physically force the other sex to mate. Painted turtles (Chrysemys picta) have been extremely well-studied over the last two centuries, and their mating system has been described as female choice based on male courtship display. The present study arises from observation that males seemingly have more protracted and serrated anterior marginal scutes than females. We hypothesized that the anterior carapace is sexually dimorphic, and that this morphology is a weapon used by males in coercive mating. We quantified anterior carapacial morphology using geometric morphometric analysis of digital photographs, drawing on samples of painted turtles from North American museum collections and our field site in Algonquin Provincial Park. We found that the anterior carapace of males had a significantly more serrated and projected shape compared to females, consistent with the sexual weapon hypothesis. Additionally, anterior carapacial shape was more strongly related to body size in males. Behavioural field observations strongly suggest that males use this morphology as a weapon to harm females during reproduction. The present study complements and strengthens the recent hypothesis that male painted turtles engage in coercion as an alternative reproductive tactic, questioning the long-understood paradigm of exclusive female choice in this well-studied species. Our study invites new avenues of research on the evolution of female harm in a system with extreme selection on female longevity and for which operational sex ratios vary among populations. Further, our work underlines how basic natural history observations can transform our understanding of well-studied systems.

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Change history

  • 11 December 2019

    In the original publication of the article,<Emphasis Type="Bold"> Fig. 2</Emphasis> and<Emphasis Type="Bold"> Fig. 3</Emphasis> were published with an error.

  • 11 December 2019

    In the original publication of the article, Fig.��2 and Fig.��3 were published with an error.

References

  • Adams DC, Nistri A (2010) Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evol Biol 10:216

    PubMed  PubMed Central  Google Scholar 

  • Adams DC, Otárola-Castillo E (2012) geomorph: Software for geometric morphometric analyses. R package version 1.0. http://cran.r-project.org/web/packages/geomorph/index.html

  • Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Ital J Zool 71:5–16

    Google Scholar 

  • Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix Ital J Mammal 24(1):7–14

    Google Scholar 

  • Agassiz L (1857) Contributions to the Natural History of the United States of America (volume I). Little, Brown, New York (lii + 452d pp)

    Google Scholar 

  • Angeloni L, Bradbury J (1999) Body size influences mating strategies in simultaneously hermaphroditic sea slug, Aplysia vaccaria. Ethol Ecol Evol 11(187):195

    Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton

    Google Scholar 

  • Auffenberg W (1966) Courtship of Gopherus polyphemus. Herpetologica 22(2):113–117

    Google Scholar 

  • Auffenberg W (1977) Display behavior in tortoises. Am Zool 17:241–250

    Google Scholar 

  • Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (Order Testudines). Oecologia (Berl.) 44:185–191

    Google Scholar 

  • Bookstein FL (1986) Size and shape spaces for landmark data in two dimensions. Stat Sci 1(2):181–242

    Google Scholar 

  • Branch WR (1984) Preliminary observations on the ecology of the angulate tortoise (Chersina angulata) in the Eastern Cape Province, South Africa. Amphibia-Reptilia 5(1):43–55

    Google Scholar 

  • Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365

    Google Scholar 

  • Congdon JD, Nagle RD, Kinney OM, van Loben Sels RC, Quinter T, Tinkle DW (2003) Testing hypotheses of aging in long-lived painted turtles (Chrysemys picta). Exp Gerontol 38(7):765–772

    PubMed  Google Scholar 

  • Crother BI (ed) (2012) Scientific and Standard English Names of Amphibians and Reptiles of North America North of Mexico, with Comments Regarding Confidence in our Understanding, 7th edn. Society for the Study of Amphibians and Reptiles, USA, p 92

    Google Scholar 

  • Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature 407:885–886

    Google Scholar 

  • Darwin C (1871) The Descent of Man and Selection in Relation to Sex. Murray, London

    Google Scholar 

  • Douglass JF, Layne JN (1978) Activity and thermoregulation of the gopher tortoise (Gopherus polyphemus) in southern Florida. Herpetologica 34(4):359–374

    Google Scholar 

  • Ernst CH, Lovich JE (2009) Turtles of the United States and Canada, 2nd edn. John Hopkins University Press, Baltimore, p 827

    Google Scholar 

  • Gibbons JW (1968) Reproductive potential, activity, and cycles in the painted turtle, Chrysemys picta. Ecology 49:399–409

    Google Scholar 

  • Golubović A, Arsovsko D, Tomović L, Bonnet X (2018) Is sexual brutality maladaptive under high population density? Biol J Lin Soc 124:394–402.s

    Google Scholar 

  • Goodall CR (1991) Procrustes methods in the statistical analysis of shape (with discussion and rejoinder). J Roy Stat Soc B 53:285–339

    Google Scholar 

  • Gower JC (1975) Generalized procrustes analysis. Psychometrika 40:33–51

    Google Scholar 

  • Gray JE (1831) Synopsis reptilium: or short descriptions of the species of reptiles. Part 1: Cataphracta; Tortoises, Crocodiles, and Enaliosaurians. G. B. Sowerby, UK

  • Holbrook JE (1836–1840) North American herpetology: or, a description of the reptiles inhabiting the United States (vol 2). J. Dobson, Philadelphia, PA, p 125

  • Iverson JB, Lewis EL (2018) How to measure a turtle. Herpetol Rev 49(3):453–460

    Google Scholar 

  • Jensen EL, Govindarajulu P, Russello MA (2015) Genetic assessment of taxonomic uncertainty in Painted Turtles. J Herpetol 49:314–324

    Google Scholar 

  • Kodric-Brown A, Sibly RM, Brown JH (1984) Truth in advertising: the kinds of traits favored by sexual selection. Am Nat 124(3):309–323

    Google Scholar 

  • Koga T, Murai M (1997) Size dependent mating behaviours of male sand-bubbler crab Scopimera globosa: alternative tactics in the life history. Ethology 103:578–587

    Google Scholar 

  • Leary CJ, Fox DJ, Shepard DB, Garcia AM (2005) Body size, age, growth and alternative mating tactics in toads: satellite males are smaller but not younger than calling males. Anim Behav 70:663–671

    Google Scholar 

  • Legler JM, Vogt RC (2013) The turtles of Mexico: land and freshwater forms. University of California Press, Berkeley

    Google Scholar 

  • Lovich JE, Ennen JR (2013) A quantitative analysis of the state of knowledge of turtles of the United States and Canada. Amphibia-Reptilia 34:11–23

    Google Scholar 

  • Lyson TR, Bhullar AAS, Bever GS, Joyce WG, de Queiroz K, Abzhanov A, Gauthier JA (2013) Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evol Dev 15(5):317–325

    PubMed  Google Scholar 

  • Mann GKH, O’Riain MJ, Hofmeyr MD (2006) Shaping up to fight: sexual selection influences body shape and size in the fighting tortoise (Chersina angulata). J Zool 269(3):373–379

    Google Scholar 

  • Maynard CJ (1869) Natural history miscellany. Am Nat 3(10):555–556

    Google Scholar 

  • McRae WA, Landers JL, Cleveland GD (1981) Sexual dimorphism in the Gopher Tortoise (Gopherus polyphemus). Herpetologica 37(1):46–52

    Google Scholar 

  • Miller L (1955) Further observations on the desert tortoise, Gopherus agassizii, of California. Copeia 1955:113–118

    Google Scholar 

  • Moldowan PD (2014) Sexual dimorphism and alternative reproductive tactics in the Midland Painted Turtle (Chrysemys picta marginata). Masters Thesis. Laurentian University Sudbury, Ontario

  • Moldowan PD, Brooks RJ, Litzgus JD (2016a) Turtles with “teeth”: beak morphology of Testudines with a focus on the tomiodonts of Painted Turtles (Chrysemys spp.). Zoomorphology 135:121–135

    Google Scholar 

  • Moldowan PD, Brooks RJ, Litzgus JD (2016b) Quantification of cranial and tomiodont dimorphism in Testudines using the Midland Painted Turtle, Chrysemys picta marginata. Zoomorphology 135:499–510

    Google Scholar 

  • Moldowan PD, Brooks RJ, Litzgus JD (in review) Demographics of injuries indicatre sexual coercion in a population of painted turtle (Chrysemys picta)

  • Polly PD (2012) Geometric morphometrics, an introduction. Department of Geology, Indiana University. Accessed 18 October 2017. http://www.indiana.edu/~g562/PBDB2013/Day%202A%20%20Introduction%20to%2Geometric%20Morphometrics.pdf

  • R Core Development Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Rico-Guevara A, Hurme KJ (2019) Intrasexually selected weapons. Biol Rev 94(1):60–101

    Google Scholar 

  • Roddewig E (2014) Husbandry and breeding of the Southern Painted Turtle, Chrysemys picta dorsalis. Radiata 23:52–66

    Google Scholar 

  • Rohlf FJ, Slice DE (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

    Google Scholar 

  • Schneider JG (1783) Allgemeine Naturgeschichte der Schildkröten, nebst einem systematischen Verzeichnisse der einzelnen Arten und zwey Kupfern, Germany

  • Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N, Abramyan J, Amemiya CT, Badenhorst D, Biggar KK, Borchert GM, Wilson RK (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14(3):R28

    PubMed  Google Scholar 

  • Shine R, Mason RT (2005) Does large body size in males evolve to facilitate forcible insemination? A study on garter snakes. Evolution 59(11):2426–2432

    PubMed  Google Scholar 

  • Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Study Behav 22:1–63

    Google Scholar 

  • Starkey DE, Shaffer HB, Burke RL, Forstner MR, Iverson JB, Janzan FJ, Rhoden AGJ, Ultsch GR (2003) Molecular systematics, phylogeography, and the effects of Pleistocene glaciation in the Painted Turtle (Chrysemys picta) complex. Evolution 57:119–128

    CAS  PubMed  Google Scholar 

  • Thomas BR (2002) Conditional mating strategy in a long-lived vertebrate: ontogenetic shifts in the mating tactics of male slider turtles (Trachemys scripta). Copeia 2:456–461

    Google Scholar 

  • Tuma MW (2016) Evolution of body size and sexually dimorphic traits in North American Gopherus tortoises. Ph.D. dissertation, University of Southern California

  • Turtle Taxonomy Working Group (TTWG; van Dijk, P.P., J.B. Iverson, A.G.J. Rhodin, H.B. Shaffer, and R. Bour) (2014) Turtles of the world, 7th edition: annotated checklist of taxonomy, synonym, distribution with maps, and conservation status. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA (eds) Conservation Biology of Freshwater Turtles and Tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs, Arlington, pp 329–479

    Google Scholar 

  • Weir LK, Grant JW, Hutchings JA (2011) The influence of operational sex ratio on the intensity of competition for mates. Am Nat 177(2):167–176

    PubMed  Google Scholar 

Download references

Acknowledgements

We sincerely thank J. Claude and an anonymous reviewer for helpful comments on a previous version of this work. For facilitating access to museum collections, we thank: J. Friel and C. Dardia at Cornell Museum of Vertebrates; G. Watkins-Colwell at Yale Peabody Museum; C. Raxworthy and D. Kizirian at the American Museum of Natural History; J. Jacobs and G. Zug at the Smithsonian National Museum of Natural History; S. Rogers at the Carnegie Museum of Natural History; and C.M. Sheehy III and D. Blackburn at the Florida Museum of Natural History. PDM thanks E. and F. Gendreau, J. Dombroskie, C. Blair and B. Proshek for accommodation while visiting museums. We thank D. Berg and J. Claude for assistance with geometric morphometric analysis, and the Algonquin Wildlife Research Station for providing accommodations during field research. We thank C. Boccia and L. Mahler for their assistance in specimen radiography. Funding was provided by a NSERC CGS-D grant to PDM, and by NSERC Discovery grants to NR and JDL. The authors declare no conflict of interest. A Letter of Authorization to Conduct Research in a Provincial Park or Conservation Reserve was received from Algonquin Provincial Park (Ontario, Canada) prior to conducting research. Animal handling was approved by the Laurentian University Animal Care Committee (Protocol #20011948) and conforms to the Canadian Council on Animal Care guidelines.

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Author notes

  1. Deborah M. Hawkshaw and Patrick D. Moldowan have contributed equally to this work.

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada

    Deborah M. Hawkshaw, Patrick D. Moldowan & Njal Rollinson

  2. School of the Environment, University of Toronto, Toronto, ON, M5S 3E8, Canada

    Patrick D. Moldowan & Njal Rollinson

  3. Department of Biology, Laurentian University, 935 Ramsey Lake Road, Sudbury, ON, P3E 2C6, Canada

    Jacqueline D. Litzgus

  4. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Ronald J. Brooks

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  1. Deborah M. Hawkshaw
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Correspondence to Patrick D. Moldowan.

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Hawkshaw, D.M., Moldowan, P.D., Litzgus, J.D. et al. Discovery and description of a novel sexual weapon in the world’s most widely-studied freshwater turtle. Evol Ecol 33, 889–900 (2019). https://doi.org/10.1007/s10682-019-10014-3

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