Multiple sexual selection pressures drive the rapid evolution of complex morphology in a male secondary genital structure

Ecology and Evolution

Volumn 5, Issue 19, 2015, Pages 4437-4450

  Frazee, Stephen R ^a   Masly, John P ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Competitive fertilization; Mating success; Morphological evolution; Secondary genitalia

Indexed keywords

EID: 84942901482     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1721     Document Type: Article

References (76)

1. Andersson, M. 1994. Sexual selection. Princeton University Press, Pinceton, NJ.
2. Arnqvist, G., R. Thornhill, and L. Rowe . 1997. Evolution of animal genitalia: morphological correlates of fitness components in a water strider. J. Evol. Biol. 10:613-640.
3. Ashburner, M., K. G. Golic, and R. S. Hawley . 2005. Drosophila: a laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
4. Avila, F. W., L. K. Sirot, B. A. LaFlamme, C. D. Rubinstein, and M. F. Wolfner . 2011. Insect seminal fluid proteins: identification and function. Ann. Rev. Entomol. 56:21-40.
5. Billeter, J. C., and S. F. Goodwin . 2004. Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. J. Comp. Neurol. 475:270-287.
6. Boll, W., and M. Noll . 2002. The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129:5667-5681.
7. Bopp, D., E. Jamet, S. Baumgartner, M. Burri, and M. Noll . 1989. Isolation of two tissue-specific Drosophila paired box genes, Pox meso and Pox neuro. EMBO J. 8:3447-3457.
8. Boughman, J. W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944-948.
9. Briceño, R. D., and W. G. Eberhard . 2009a. Experimental modifications imply a stimulatory function for male tsetse fly genitalia, supporting cryptic female choice theory. J. Evol. Biol. 22:1516-1525.
10. Briceño, R. D., and W. G. Eberhard . 2009b. Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia. J. Insect Physiol. 55:989-996.
11. Briceño, R. D., W. G. Eberhard, E. Chinea-Cano, D. Wegrzynek, and T. dos Santos Rolo . 2015. Species-specific differences in the behavior of male tsetse fly genitalia hidden in the female during copulation. Etho. Ecol. Evol. doi:10.1080/03949370.2014.1002114.
12. Castillo, D. M., and L. C. Moyle . 2014. Intraspecific sperm competition genes enforce post-mating species barriers in Drosophila. Proc. Biol. Sci. 281:20142050.
13. Catchpole, R. D. J. 1994. Wing length is not the best predictor of body size. Dros. Inf. Ser. 75:84-86.
14. Choe, J. C., and B. J. Crespi . 1997. The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, UK.
15. Cohen, B., M. E. McGuffin, C. Pfeifle, D. Segal, and S. M. Cohen . 1992. Apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Gen. Dev. 6:715-729.
16. Córdoba-Aguilar, A., E. Uhía, and A. C. Rivera . 2003. Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals' sperm displacement. J. Zool. 261:381-398.
17. Coyne, J. A., and H. A. Orr . 2004. Speciation. Sinauer Associates, Sunderland, MA.
18. Drapeau, M. D., A. Radovic, P. J. Wittkopp, and A. D. Long . 2003. A gene necessary for normal male courtship, yellow, acts downstream of fruitless in the Drosophila melanogaster larval brain. J. Neurobiol. 55:53-72.
19. Duffy, J. B.. 2002. GAL4 system in Drosophila: a fly geneticist's swiss army knife. Genesis 34:1-15.
20. Dyer, K. A., B. E. White, J. L. Sztepanacz, E. R. Bewick, and H. D. Rundle . 2014. Reproductive character displacement of epicuticular compounds and their contribution to mate choice in Drosophila subquinaria and Drosophila recens. Evolution 68:1163-1175.
21. Eberhard, W. G. 1985. Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA.
22. Ferson, S., F. J. Rohlf, and R. K. Koehn . 1985. Measuring shape variation of two-dimensional outlines. Syst. Zool. 34:59-68.
23. Firman, R. C., and L. W. Simmons . 2008. The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J. Evol. Biol. 21:1524-1533.
24. Grieshop, K., and M. Polak . 2012. The precopulatory function of male genital spines in Drosophila ananassae [Doleschall] (Diptera: Drosophilidae) revealed by laser surgery. Evolution 66:2637-2645.
25. Grieshop, K., and M. Polak . 2014. Evaluating the post-copulatory sexual selection hypothesis for genital evolution reveals evidence for pleiotropic harm exerted by the male genital spines of Drosophila ananassae. J. Evol. Biol. 27:2676-2686.
26. Head, M. L., G. M. Kozak, and J. W. Boughman . 2013. Female mate preferences for male body size and shape promote sexual isolation in threespine sticklebacks. Ecol. Evol. 3:2183-2196.
27. Heifetz, Y., U. Tram, and M. F. Wolfner . 2001. Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc. Biol. Sci. 268:175-180.
28. Hosken, D. J., and P. Stockley . 2004. Sexual selection and genital evolution. Trends Ecol. Evol. 19:87-93.
29. Hoskin, C. J., and M. Higgie . 2010. Speciation via species interactions: the divergence of mating traits within species. Ecol. Lett. 13:409-420.
30. Hotzy, C., M. Polak, J. L. Rönn, and G. Arnqvist . 2012. Phenotypic engineering unveils the function of genital morphology. Curr. Biol. 22:2258-2261.
31. House, C. M., and L. W. Simmons . 2003. Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proc. Biol. Sci. 270:447-455.
32. House, C. M., and L. W. Simmons . 2006. Offensive and defensive sperm competition roles in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Behav. Ecol. Socio. 60:131-136.
33. House, C. M., Z. Lewis, D. J. Hodgson, N. Wedell, M. D. Sharma, J. Hunt, et al. 2013. Sexual and natural selection both influence male genital evolution. PLoS ONE 8:e63807.
34. Howard, D. J., and P. G. Gregory . 1993. Post-insemination signaling systems and reinforcement. Philos. Trans. R. Soc. B 340:231-236.
35. Hudson, E. J., and T. D. Price . 2014. Pervasive reinforcement and the role of sexual selection in biological speciation. J. Hered. 105:821-833.
36. Jagadeeshan, S., and R. S. Singh . 2006. A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of genitalia. J. Evol. Biol. 19:1058-1070.
37. Kamimura, Y. 2010. Copulation anatomy of Drosophila melanogaster (Diptera: Drosophilidae): wound-making organs and their possible roles. Zoomorphology 129:163-174.
38. Kuhl, F. P., and C. R. Giardina . 1982. Elliptical Fourier features of a closed contour. Comp. Graph. Image Proc. 18:236-258.
39. Latour, Y., M. Perriat-Sanguinet, P. Caminade, P. Boursot, C. M. Smadja, and G. Ganem . 2014. Sexual selection against natural hybrids may contribute to reinforcement in a house mouse hybrid zone. Proc. Biol. Sci. 281:20132733.
40. Lestrel, P. E. 1997. Fourier descriptors and their applications in biology. Cambridge University Press, Cambridge, UK.
41. LeVasseur-Viens, H., M. Polak, and A. J. Moehring . 2015. No evidence for external genital morphology affecting cryptic female choice and reproductive isolation in Drosophila. Evolution 69:1797-1807.
42. Liu, J., J. M. Mercer, L. F. Stam, G. C. Gibson, Z. B. Zeng, and C. C. Laurie . 1996. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics 142:1129-1145.
43. Lundgren, S. E., C. A. Callahan, S. Thor, and J. B. Thomas . 1995. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121:1769-1773.
44. Lüpold, S., M. K. Manier, O. Ala-Honkola, J. M. Belote, and S. Pitnick . 2011. Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behav. Ecol. 22:184-191.
45. Lüpold, S., M. K. Manier, K. S. Berben, K. J. Smith, B. D. Daley, S. H. Buckley, et al. 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr. Biol. 22:1667-1672.
46. Manier, M. K., J. M. Belote, K. S. Berben, D. Novikov, W. T. Stuart, and S. Pitnick . 2010. Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328:354-357.
47. Manier, M. K., J. M. Belote, K. S. Berben, S. Lüpold, O. Ala-Honkola, W. F. Collins, et al. 2013a. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67:2348-2362.
48. Manier, M. K., S. Lüpold, J. M. Belote, W. T. Starmer, K. S. Berben, O. Ala-Honkola, et al. 2013b. Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr. Biol. 23:1853-1862.
49. Masly, J. P. 2012. 170 Years of "Lock-and-Key": genital morphology and reproductive isolation. Int. J. Evol. Biol. 2012:247352.
50. Masly, J. P., and Y. Kamimura . 2014. Asymmetric mismatch in strain-specific genital morphology causes increased harm to Drosophila females. Evolution 68:2401-2411.
51. McNeil, C. L., C. L. Bain, and S. J. Macdonald . 2011. Multiple Quantitative Trait Loci Influence the Shape of a Male-Specific Genital Structure in Drosophila melanogaster. G3 (Bethesda) 1:343-351.
52. McPeek, M. A., L. B. Symes, D. M. Zong, and C. L. McPeek . 2011. Species recognition and patterns of population variation in the reproductive structures of a damselfly genus. Evolution 65:419-428.
53. Melcher, K. 1997. Galactose metabolism in Saccharomyces cerevisiae: a paradigm for eukaryotic gene regulation. Pp. 235-269 in F. K. Zimmermann and K. D. Entian, eds. Yeast sugar metabolism. Technomic Publishing Inc., Lancaster, PA.
54. Mosca, T. J., W. Hong, V. S. Dani, V. Favaloro, and L. Luo . 2012. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 484:237-241.
55. Phelan, P. L., and T. C. Baker . 1987. Evolution of male pheromones in moths: reproductive isolation through sexual selection? Science 235:205-207.
56. Polak, M., and A. Rashed . 2010. Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc. Biol. Sci. 277:1371-1376.
57. Questiau, S. 1999. How can sexual selection promote population divergence? Ethol. Ecol. Evol. 11:313-324.
58. R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
59. Rasband, W. S. 1997-2014. ImageJ. U. S. National Institutes of Health, Bethesda, MD, USA.
60. Rowe, L., and G. Arnqvist . 2012. Sexual selection and the evolution of genital shape and complexity in water striders. Evolution 66:40-54.
61. Schwander, T., D. Arbuthnott, R. Gries, G. Gries, P. Nosil, and B. Crespi . 2013. Hydrocarbon divergence and reproductive isolation in Timema stick insects. BMC Evol. Biol. 13:151.
62. Seddon, N., C. A. Botero, J. A. Tobias, P. O. Dunn, H. E. A. MacGregor, D. R. Rubenstein, et al. 2013. Sexual selection accelerates signal evolution during speciation in birds. Proc. Biol. Sci. 280:20131065.
63. Servedio, M. R., and M. A. F. Noor . 2003. The role of reinforcement in speciation: theory and data. Ann. Rev. Ecol. Evol. Syst. 34:339-364.
64. Shapiro, A. M., and A. H. Porter . 1989. The lock-and-key hypothesis: evolutionary and biosystematic interpretation of insect genitalia. Ann. Rev. Entomol. 34:231-245.
65. Siegel, R. W., and J. C. Hall . 1979. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 76:3430-3434.
66. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJ.
67. Simmons, L. W. 2014. Sexual selection and genital evolution. Aus. Ent. 53:1-17.
68. Simmons, L. W., and R. C. Firman . 2014. Experimental evidence for the evolution of the Mammalian baculum by sexual selection. Evolution 68:276-283.
69. Simmons, L. W., C. M. House, J. Hunt, and F. García-González . 2009. Evolutionary response to sexual selection in male genital morphology. Curr. Biol. 19:1442-1446.
70. Singh, S. R., B. N. Singh, and H. F. Hoenigsberg . 2002. Female remating, sperm competition and sexual selection in Drosophila. Gen. Mol. Res. 1:178-215.
71. Snook, R. R., and D. J. Hosken . 2004. Sperm death and dumping in Drosophila. Nature 428:939-941.
72. Stockley, P., S. Ramm, A. Sherborne, M. D. Thom, S. Paterson, and J. Hurst . 2013. Baculum morphology predicts reproductive success of male house mice under sexual selection. BMC Biol. 11:66.
73. Svedin, N., C. Wiley, T. Veen, L. Gustafsson, and A. Qvarnström . 2008. Natural and sexual selection against hybrid flycatchers. Proc. Biol. Sci. 275:735-744.
74. Taylor, B. J. 1989. Sexually dimorphic neurons in the terminalia of Drosophila melanogaster: I. Development of sensory neurons in the genital disc during metamorphosis. J. Neurogenet. 5:173-192.
75. Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York, NY.
76. Wojcieszek, J. M., and L. W. Simmons . 2013. Divergence in genital morphology may contribute to mechanical reproductive isolation in a millipede. Ecol. Evol. 3:334-343.