Correlated evolution between targets of pre- and postcopulatory sexual selection across squamate reptiles

Ecology and Evolution

Volumn 6, Issue 18, 2016, Pages 6452-6459

  Kahrl, Ariel F ^a   Cox, Christian L ^b   Cox, Robert M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b GEORGIA SOUTHERN UNIVERSITY   (United States)

Author keywords

Phylogenetic comparative method; sexual size dimorphism; sperm competition; testis size

Indexed keywords

EID: 84982279544     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.2344     Document Type: Article

References (58)

1. Blomberg, S. P., T. Garland, and A. R. Ives. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745.
2. Calsbeek, R., C. Bonneaud, S. Prabhu, N. Manoukis, and T. B. Smith. 2007. Multiple paternity and sperm storage lead to increased genetic diversity in Anolis lizards. Evol. Ecol. 9:495–503.
3. Carothers, J. H. 1984. Sexual selection and sexual dimorphism in some herbivorous lizards. Am. Nat. 124:244–254.
4. Collet, J., D. S. Richardson, K. Worley, and T. Pizzari. 2012. Sexual selection and the differential effect of polyandry. Proc. Natl Acad. Sci. USA 109:8641–8645.
5. Cox, R. M., and A. F. Kahrl. 2014. Sexual selection and sexual dimorphism. Pp. 78–108 in J. L. Rheubert, D. S. Siegel, S. E. Trauth and B. G. Jamieson, eds. Reproductive biology and phylogeny of lizards and tuatara. CRC Press, Boca Raton, FL.
6. Cox, R. M., S. L. Skelley, and H. B. John-Alder. 2003. A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution 57:1653–1669.
7. Cox, R. M., M. A. Butler, and H. B. John-Alder. 2007. The evolution of sexual size dimorphism in reptiles. Pp. 38–49 in D. J. Fairbairn, W. U. Blankenhorn and T. Székely, eds. Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford Univ. Press, Oxford, U.K.
8. Devigili, A., J. P. Evans, A. Di Nisio, and A. Pilastro. 2015. Multivariate selection drives concordant patterns of pre- and postcopulatory sexual selection in a livebearing fish. Nat. Commun. 6:1–9.
9. Dines, J. P., S. L. Mesnick, K. Ralls, L. May-Collado, I. Agnarsson, and M. D. Dean. 2015. A trade-off between precopulatory and postcopulatory trait investment in male cetaceans. Evolution 69:1560–1572.
10. Dunn, J. C., L. B. Halenar, T. G. Davies, J. Cristobal-Azkarate, D. Reby, D. Sykes, et al. 2015. Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys. Curr. Biol. 25:2839–2844.
11. Ferrandiz-Rovira, M., J. F. Lemaître, S. Lardy, B. C. López, and A. Cohas. 2014. Do pre-and post-copulatory sexually selected traits covary in large herbivores? BMC Evol. Biol. 14:79.
12. Fitzpatrick, J. L., M. Almbro, A. Gonzalez-Voyer, N. Kolm, and L. W. Simmons. 2012. Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66:3595–3604.
13. Gage, M. 1994. Associations between body size, mating pattern, testis size, and sperm lengths across butterflies. Proc. R. Soc. Lond. B 258:247–254.
14. Garland, T., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:18–32.
15. Haenel, G. J., L. C. Smith, and H. B. John-Alder. 2003. Home-range analysis in Sceloporus undulatus II: a test of spatial relationships and reproductive success. Copeia 2003:113–123.
16. Harcourt, A. H., P. H. Harvey, S. G. Larson, and R. V. Short. 1981. Testis weight, body weight and breeding system in primates. Nature 293:55–57.
17. Harmon, L. J., J. T. Weir, C. D. Brock, R. E. Glor, and W. Challenger. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131.
18. Harvey, P. H., and A. H. Harcourt. 1984. Sperm competition, testes size, and breeding systems in primates. Pp. 589–599 in R. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, London, U.K.
19. Heske, E. J., and R. S. Ostfeld. 1990. Sexual dimorphism in size, relative size of testes, and mating systems in North American voles. J. Mammal. 71:510–519.
20. Hosken, D. J., and P. I. Ward. 2001. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4:10–13.
21. Hunt, J., C. J. Breuker, J. A. Sadowski, and A. J. Moore. 2009. Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22:13–26.
22. Kahrl, A. F., and R. M. Cox. 2015. Diet affects ejaculate traits in a lizard with condition-dependent fertilization success. Behav. Ecol. 26:1502–1511.
23. Kelly, C. D. 2008. Sperm investment in relation to weapon size in a male trimorphic insect? Behav. Ecol. 19:1018–1024.
24. Kembel, S. W., P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, et al. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464.
25. Kvarnemo, C., and L. W. Simmons. 2013. Polyandry as a mediator of sexual selection before and after mating. Phil. Trans. R. Soc. B. 368:20120042.
26. Licht, P., and A. K. Pearson. 1969. Effects of adenohypophysectomy on testicular function in the lizard Anolis carolinensis. Biol. Reprod. 1:107–119.
27. Losos, J. B. 1994. Historical contingency and lizard community ecology. Pp. 319–333 in L. J. Vitt and E. R. Pianka, eds. Lizard ecology: historical and experimental perspectives. Princeton Univ. Press, Princeton, NJ.
28. Lüpold, S., J. L. Tomkins, L. W. Simmons, and J. L. Fitzpatrick. 2014. Female monopolization mediates the relationship between pre- and postcopulatory sexual traits. Nat. Commun. 5:3184–3191.
29. Moczek, A. P., and H. F. Nijhout. 2004. Trade-offs during the development of primary and secondary sexual traits in a horned beetle. Evolution 163:184–191.
30. Møller, A. P. 1989. Ejaculate quality, testes size and sperm production in mammals. Funct. Ecol. 3:91–96.
31. Møller, A. P. 1991. Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am. Nat. 137:882–906.
32. Møller, A. P., and J. V. Briskie. 1995. Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36:357–365.
33. Olsson, M., T. Madsen, and R. Shine. 1997. Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264:455–459.
34. Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877–884.
35. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.
36. Parker, G. A., and T. Pizzari. 2010. Sperm competition and ejaculate economics. Biol. Rev. 85:897–934.
37. Parker, G. A., C. M. Lessells, and L. W. Simmons. 2013. Sperm competition games: a general model for pre-copulatory male-male competition. Evolution 67:95–109.
38. Pélissié, B., P. Jarne, V. Sarda, and P. David. 2014. Disentangling precopulatory and postcopulatory sexual selection in polyandrous species. Evolution 68:1320–1331.
39. Pischedda, A., and W. R. Rice. 2012. Partitioning sexual selection into its mating success and fertilization success components. Proc. Natl Acad. Sci. USA 109:2049–2053.
40. Poulin, R., and S. Morand. 2000. Testes size, body size and male–male competition in acanthocephalan parasites. J. Zool. 250:551–558.
41. Preston, B. T., I. R. Stevenson, J. M. Pemberton, D. W. Coltman, and K. Wilson. 2003. Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc. R. Soc. Lond. B 270:633–640.
42. Pyron, R. A., F. T. Burbrink, and J. J. Wiens. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13:93.
43. R Development Core Team 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
44. Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217–223.
45. Rose, E., K. A. Paczolt, and A. G. Jones. 2013. The contributions of premating and postmating selection episodes to total selection in sex-role-reversed Gulf Pipefish. Am. Nat. 182:410–420.
46. Rowe, M., and S. Pruett-Jones. 2011. Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS ONE 6:e15720.
47. Shine, R. 1994. Sexual size dimorphism in snakes revisited. Copeia 1994:326–346.
48. Simmons, L. W., and D. J. Emlen. 2006. Evolutionary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103:16346–16351.
49. Somjee, U., P. E. Allen, and C. W. Miller. 2015. Different environments lead to a reversal in the expression of weapons and testes in the heliconia bug, Leptoscelis tricolor (Hemiptera: Coreidae). Biol. J. Linn. Soc. 115:802–809.
50. South, A., and S. M. Lewis. 2012. Determinants of reproductive success across sequential episodes of sexual selection in a firefly. Proc. R. Soc. B 279:3201–3208.
51. Stamps, J. A. 1983. Sexual selection, sexual dimorphism and territoriality. Pp. 169–204 in L. J. Vitt and E. R. Pianka, eds. Lizard ecology: historical and experimental perspectives. Princeton Univ. Press, Princeton, NJ.
52. Stockley, P., M. Gage, G. A. Parker, and A. P. Møller. 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 45:933–954.
53. Todd, A. C. 2008. Using testis size to predict the mating systems of New Zealand geckos. New Zeal. J. Zool. 35:103–114.
54. Turnell, B. R., and K. L. Shaw. 2015. High opportunity for postcopulatory sexual selection under field conditions. Evolution 69:2094–2104.
55. Uller, T., and M. Olsson. 2008. Multiple paternity in reptiles: patterns and processes. Mol. Ecol. 17:2566–2580.
56. Uller, T., D. Stuart-Fox, and M. Olsson. 2010. Evolution of primary sexual characters in reptiles. Pp. 426–429 in J. L. Leonard and A. Córdoba-Agulliar, eds. The evolution of primary sexual characteristics in animals. Oxford Univ. Press, Oxford, U.K.
57. Wedell, N. 1993. Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47:1203–1212.
58. Yamane, T., K. Okada, S. Nakayama, and T. Miyatake. 2010. Dispersal and ejaculatory strategies associated with exaggeration of weapon in an armed beetle. Proc. R. Soc. Lond. B 277: 1705–1710.