Female monopolization mediates the relationship between pre- and postcopulatory sexual traits

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lüpold, Stefan ^a   Tomkins, Joseph L ^b   Simmons, Leigh W ^b   Fitzpatrick, John L ^b,c  

^a SYRACUSE UNIVERSITY   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TETRAHYDROLIPSTATIN;

BIOENERGETICS; CONTEST COMPETITION; COPULATION; LIFE HISTORY TRAIT; REPRODUCTIVE COST; SPERM COMPETITION; TRADE-OFF;

ACANTHOCEPHALA; ANATOMICAL VARIATION; ARTICLE; BIRD; BODY SIZE; COMPARATIVE STUDY; COPULATION; FEMALE MONOPOLIZATION; FISH; INSECT; INTERSPECIFIC COMPETITION; INTERSPECIFIC RELATIONSHIP; MONOGAMY; NONHUMAN; PHEASANT; PHYLOGENY; POSTCOPULATORY SEXUAL TRAIT; PRECOPULATORY SEXUAL TRAIT; PREDICTION; PRIMATE; SCHISTOSOMA; SEX DIFFERENCE; SEXUAL SELECTION; TESTIS; UNGULATE; ANIMAL; FEMALE; MALE; SEXUAL BEHAVIOR;

ANIMALS; COPULATION; FEMALE; MALE; SEXUAL BEHAVIOR, ANIMAL;

EID: 84897620649     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4184     Document Type: Article

References (70)

1. Darwin, C. The Descent of Man and Selection in Relation to Sex (John Murray, London, UK, 1871).
2. Andersson, M. Sexual Selection (Princeton University Press, Princeton, NJ, USA, 1994).
3. Jennions, M. D. & Petrie, M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21-64 (2000).
4. Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 526-567 (1970).
5. Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice (Princeton University Press, Princeton, NJ, USA, 1996).
6. Thornhill, R. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am. Nat. 122, 765-788 (1983).
7. Andersson, M. & Simmons, L. W. Sexual selection and mate choice. Trends Ecol. Evol. 21, 296-302 (2006).
8. Kvarnemo, C. & Simmons, L. W. Polyandry as a mediator of sexual selection before and after mating. Philos. Trans. R. Soc. Lond. B 368, 20120042 (2013).
9. Dewsbury, D. A. Ejaculate cost and male choice. Am. Nat. 119, 601-610 (1982).
10. Olsson, M., Madsen, T. & Shine, R. Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264, 455-459 (1997).
11. Emlen, D. J. Costs and the diversification of exaggerated animal structures. Science 291, 1534-1536 (2001).
12. Allen, B. J. & Levinton, J. S. Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Funct. Ecol. 21, 154-161 (2007).
13. Parker, G. A., Lessells, C. M. & Simmons, L. W. Sperm competition games: a general model for pre-copulatory male-male competition. Evolution 67, 95-109 (2013).
14. Simmons, L. W. & Emlen, S. T. Evolutionary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103, 16346-16351 (2006).
15. Puniamoorthy, N., Blanckenhorn, W. U. & Schäfer, M. A. Differential investment in pre- vs. post-copulatory sexual selection reinforces a cross-continental reversal of sexual size dimorphism in Sepsis punctum (Diptera: Sepsidae). J. Evol. Biol. 25, 2253-2263 (2012).
16. Galeotti, P. et al. Sperm traits negatively covary with size and asymmetry of a secondary sexual trait in a freshwater crayfish. PLoS One 7, e43771 (2012).
17. Malo, A. F., Roldan, E. R. S., Garde, J., Soler, A. J. & Gomendio, M. Antlers honestly advertise sperm production and quality. Proc. R. Soc. Lond. B 272, 149-157 (2005).
18. Kelly, C. D. Sperm investment in relation to weapon size in a male trimorphic insect? Behav. Ecol. 19, 1018-1024 (2008).
19. Poulin, R. & Morand, S. Testes size, body size and male-male competition in acanthocephalan parasites. J. Zool. 250, 551-558 (2000).
20. Fitzpatrick, J. L., Almbro, M., Gonzalez-Voyer, A., Kolm, N. & Simmons, L. W. Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66, 3595-3604 (2012).
21. Gage, M. J. G., Parker, G. A., Nylin, S. & Wiklund, C. Sexual selection and speciation in mammals, butterflies and spiders. Proc. R. Soc. Lond. B 269, 2309-2316 (2002).
22. Wedell, N. Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm. Evolution 47, 1203-1212 (1993).
23. Harcourt, A. H., Harvey, P. H., Larsen, S. G. & Short, R. V. Testis size, body weight and breeding system in primates. Nature 293, 55-57 (1981).
24. Soulsbury, C. D. Genetic patterns of paternity and testes size in mammals. PLoS One 5, e9581 (2010).
25. Birkhead, T. R. & Møller, A. P. Sperm Competition and Sexual Selection (Academic Press, San Diego, CA, USA, 1998).
26. Simmons, L. W. & Fitzpatrick, J. L. Sperm wars and the evolution of male fertility. Reproduction 144, 519-534 (2012).
27. Pyron, M., Pitcher, T. E. & Jacquemin, S. J. Evolution of mating systems and sexual size dimorphism in North American cyprinids. Behav. Ecol. Sociobiol. 67, 747-756 (2013).
28. Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269, 797-800 (1977).
29. Webster, M. S. Sexual dimorphism, mating system and body size in New World blackbirds (Icterinae). Evolution 46, 1621-1641 (1992).
30. Gonzalez-Voyer, A., Fitzpatrick, J. L. & Kolm, N. Sexual selection determines parental care patterns in cichlid fishes. Evolution 62, 2015-2026 (2008).
31. Shultz, S. & Dunbar, R. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl Acad. Sci. USA 107, 21582-21586 (2010).
32. Rosenthal, R. Meta-Analytic Procedures for Social Research (Sage, London, UK, 1991).
33. Gwynne, D. T. Katydids and Bush-Crickets: Reproductive Behavior and Evolution of the Tettigoniidae (Cornell University Press, Ithaca, 2001).
34. Kimball, R. T., St. Mary, C. M. & Braun, E. L. A macroevolutionary perspective on multiple sexual traits in the Phasianidae (Galliformes). Int. J. Evol. Biol. 2011, 423938 (2011).
35. Simmons, L. W. & Roberts, B. Bacterial immunity traded for sperm viability in male crickets. Science 309, 2031 (2005).
36. Kirkwood, T. B. L. & Austad, S. N. Why do we age? Nature 408, 233-238 (2000).
37. Roff, D. A. & Fairbairn, D. J. The evolution of trade-offs: where are we? J. Evol. Biol. 20, 433-447 (2007).
38. van Noordwijk, A. J. & de Jong, G. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137-142 (1986).
39. Fry, C. L. Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol. Dev. 8, 191-201 (2006).
40. Cotton, S., Small, J., Hashim, R. & Pomiankowski, A. Eyespan reflects reproductive quality in wild stalk-eyed flies. Evol. Ecol. 24, 83-95 (2010).
41. Osorio, S., Piulachs, M. D. & Bellés, X. Feeding and activation of corpora allata in the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). J. Insect Physiol. 44, 34-38 (1998).
42. Trumbo, S. T. & Robinson, G. E. Nutrition, hormones and life history in burying beetles. J. Insect Physiol. 50, 383-391 (2004).
43. Shutler, D. Sexual selection: when to expect trade-offs. Biol. Lett. 7, 101-104 (2011).
44. Leroi, A. M., Rose, M. R. & Lauder, G. V. What does the comparative method reveal about adaptation? Am. Nat. 143, 381-402 (1994).
45. Lüpold, S., Linz, G. M., Rivers, J. W., Westneat, D. F. & Birkhead, T. R. Sperm competition selects beyond relative testes size in birds. Evolution 63, 391-402 (2009).
46. Lüpold, S., Wistuba, J., Damm, O. S., Rivers, J. W. & Birkhead, T. R. Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality. Reproduction 141, 595-605 (2011).
47. Ramm, S. A. & Stockley, P. Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Lett. 6, 219-221 (2010).
48. Schärer, L. & Vizoso, D. B. Phenotypic plasticity in sperm production rate: there's more to it than testis size. Evol. Ecol. 21, 295-306 (2007).
49. Vahed, K. & Parker, D. J. The evolution of large testes: Sperm competition or male mating rate? Ethology 118, 107-117 (2012).
50. Preston, B. T., Stevenson, I. R., Pemberton, J. M. & Wilson, K. Dominant rams lose out by sperm depletion: a waning success in siring counters a ram's high score in competition for ewes. Nature 409, 681-682 (2001).
51. Wingfield, J. C., Hegner, R. E., Dufty, Jr A. M. & Ball, G. F. The 'challenge hypothesis': Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136, 829-846 (1990).
52. Costa, D. S., Paula, T. A. R. & Matta, S. L. P. The intertubular compartment morphometry in capybaras (Hydrochoerus hydrochaeris) testis. Anim. Reprod. Sci. 91, 173-179 (2006).
53. Herrera, E. A. & Macdonald, D. W. Aggression, dominance, and mating success among capybara males (Hydrochaeris hydrochaeris). Behav. Ecol. 4, 114-119 (1993).
54. Emlen, D. J. The evolution of animal weapons. Annu. Rev. Ecol. Syst. 39, 387-413 (2008).
55. Fairbairn, D. J. in Sex, Size and Gender Roles. (eds Blanckenhorn, W. U., Fairbairn, D. J. & Székely, T.) 1-10 (Oxford University Press, Oxford, UK, 2007).
56. Andersson, M. & Norberg, R. Å. Evolution of reversed sexual size dimorphism and role partitioning among predatory birds, with a size scaling of flight performance. Biol. J. Linn. Soc. 15, 105-130 (1981).
57. Székely, T., Reynolds, J. D. & Figuerola, J. Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection. Evolution 54, 1404-1413 (2000).
58. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. Red Deer: Behaviour and Ecology of Two Sexes (Edinburgh University Press, Edinburgh, 1985).
59. Lindenfors, P. Sexually antagonistic selection on primate size. J. Evol. Biol. 15, 595-607 (2002).
60. Lindenfors, P., Tullberg, B. S. & Biuw, M. Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav. Ecol. Sociobiol. 52, 188-193 (2002).
61. Shine, R. Sexual selection and size dimorphism in the Amphibia. Copeia 1979, 297-306 (1979).
62. Prenter, J., Elwood, R. W. & Montgomery, W. I. Sexual size dimorphism and reproductive investment by female spiders: a comparative analysis. Evolution 53, 1987-1994 (1999).
63. Selander, R. K. Sexual dimorphism and differential niche utilization in birds. Condor 68, 113-151 (1966).
64. Shine, R. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q. Rev. Biol. 64, 419-461 (1989).
65. Thom, M. D., Harrington, L. A. & Macdonald, D. W. Why are American mink sexually dimorphic? A role for niche separation. Oikos 105, 525-535 (2004).
66. Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712-726 (2002).
67. Freckleton, R. P. On the misuse of residuals in ecology: regression of residuals vs. multiple regression. J. Anim. Ecol. 71, 542-545 (2002).
68. García-Berthou, E. On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. J. Anim. Ecol. 70, 708-711 (2001).
69. R Development Core Team. R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2012).
70. Warton, D. I. & Hui, F. K. C. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3-10 (2011).