Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1718, 2011, Pages 2611-2620

  Evans, Jonathan P ^a   Gasparini, Clelia ^b   Holwell, Gregory I ^c   Ramnarine, Indar W ^d   Pitcher, Trevor E ^e   Pilastro, Andrea ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF THE WEST INDIES   (Trinidad and Tobago)

^e UNIVERSITY OF WINDSOR   (Canada)

Author keywords

Coevolution; Genitalia; Sexual conflict; Sexual selection

Indexed keywords

ANTAGONISM; COEVOLUTION; COPULATION; INTRASPECIFIC VARIATION; LIFE HISTORY TRAIT; MALE BEHAVIOR; MORPHOLOGY; MORPHOMETRY; PREDATION; REPRODUCTIVE BIOLOGY; SEXUAL BEHAVIOR; SEXUAL CONFLICT; SEXUAL SELECTION; TELEOST;

ANIMAL; ARTICLE; CYPRINODONTIFORMES; EVOLUTION; FEMALE; FEMALE GENITAL SYSTEM; GENETIC SELECTION; GENETICS; HISTOLOGY; MALE; MALE GENITAL SYSTEM; PHENOTYPE; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; MALE; PHENOTYPE; POECILIA; SELECTION, GENETIC; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

CYPRINODONTIFORMES; POECILIA RETICULATA;

EID: 79960688305     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.2453     Document Type: Article

References (60)

1. Eberhard, W. G. 1985 Sexual selection and animal genitalia. Cambridge, MA: Harvard University Press.
2. Hosken, D. J. & Stockley, P. 2004 Sexual selection and genital evolution. Trends Ecol. Evol. 19, 87-93. (doi:10.1016/j.tree.2003.11.012)
3. Bertin, A. & Fairbairn, D. J. 2005 One tool, many uses: precopulatory sexual selection on genital morphology in Aquarius remigis. J. Evol. Biol. 18, 949-961. (doi:10.1111/j.1420-9101.2005.00913.x)
4. Langerhans, R. B., Layman, C. A. & DeWitt, T. J. 2005 Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proc. Natl Acad. Sci. USA 102, 7618-7623. (doi:10.1073/pnas.0500935102)
5. Brooks, R. & Caithness, N. 1995 Female choice in a feral guppy population: are there multiple cues. Anim. Behav. 50, 301-307. (doi:10.1006/anbe.1995.0246)
6. Preziosi, R. F. & Fairbairn, D. J. 1996 Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: body size, components of body size and male mating success. J. Evol. Biol. 9, 317-336. (doi:10.1046/j.1420-9101.1996.9030317.x)
7. Arnqvist, G. & Danielsson, I. 1999 Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution 53, 147-156. (doi:10.2307/2640927)
8. Danielsson, I. & Askenmo, C. 1999 Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris. Behav. Ecol. Sociobiol. 46, 149-156. (doi:10.1007/s002650050604)
9. House, C. M. & Simmons, L. W. 2005 Relative influence of male and female genital morphology on paternity in the dung beetle Onthophagus taurus. Behav. Ecol. 16, 889-897. (doi:10.1093/beheco/ari066)
10. Wenninger, E. J. & Averill, A. L. 2006 Influence of body and genital morphology on relative male fertilization success in oriental beetles. Behav. Ecol. 17, 656-663. (doi:10.1093/beheco/ark013)
11. Hotzy, C. & Arnqvist, G. 2009 Sperm competition favors harmful males in seed beetles. Curr. Biol. 19, 404-407. (doi:10.1016/j.cub.2009.01.045)
12. Arnqvist, G. 1998 Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784-786. (doi:10.1038/31689)
13. Brennan, P., Prum, R., McCracken, K., Sorenson, M., Wilson, R. & Birkhead, T. 2007 Coevolution of male and female genital morphology in waterfowl. PLoS ONE, e418. (doi:10.1371/journal.pone.0000418)
14. Co ́rdoba-Aguilar, A. 2005 Possible coevolution of male and female genital form and function in a calopterygid damselfly. J. Evol. Biol. 18, 132-137. (doi:10.1111/j.1420-9101.2004.00796.x)
15. Huber, B. A. 2003 Southern African pholcid spiders: revision and cladistic analysis of Quamtana gen. and Spermophora Hentz (Araneae: Pholcidae), male-female covariation. Zool. J. Linn. Soc. 139, 477-527. (doi:10.1046/j.0024-4082.2003.00082.x)
16. Arnqvist, G. & Rowe, L. 2002 Correlated evolution of male and female morphologies in water striders. Evolution 56, 936-947. (doi:10.1111/j.0014-3820.2002.tb01406.x)
17. Arnqvist, G. & Rowe, L. 2002 Antagonistic coevolution between the sexes in a group of insects. Nature 415, 787-789. (doi:10.1038/415787a)
18. Peden, A. E. 1972 The function of gonopodial parts and behavioural pattern during copulation by Gambusia (Poeciliidae). Can. J. Zool. 50, 955-968. (doi:10.1139/z72-128)
19. Tatarnic, N. J. & Cassis, G. 2010 Sexual coevolution in the traumatically inseminating plant bug genus Coridromius [transl. from English]. J. Evol. Biol. 23, 1321-1326. (doi:10.1111/j.1420-9101.2010.01991.x)
20. Rönn, J., Katvala, A. & Arnqvist, G. 2007 Coevolution between harmful male genitalia and female resistance in seed beetles. Proc. Natl Acad. Sci. USA 104, 10 921-10 925. (doi:10.1073/pnas.0701170104)
21. Andrade, C. A. C., Vieira, R. D., Ananina, G. & Klaczko, L. B. 2009 Evolution of the male genitalia: morphological variation of the aedeagi in a natural population of Drosophila mediopunctata. Genetica 135, 13-23. (doi:10. 1007/s10709-008-9247-9)
22. Mutanen, M. & Kaitala, A. 2006 Genital variation in a dimorphic moth Selenia tetralunaria (Lepidoptera, Geometridae). Biol. J. Linn. Soc. 87, 297-307. (doi:10.1111/j.1095-8312.2006.00578.x)
23. Mutanen, M., Kaitala, A. & Monkkonen, M. 2006 Genital variation within and between three closely related Euxoa moth species: testing the lock-and-key hypothesis. J. Zool. 268, 109-119. (doi:10.1111/j.1469-7998.2005.00029.x)
24. Mutanen, M., Rytkonen, S., Linden, J. & Sinkkonen, J. 2007 Male genital variation in a moth Pammene luedersiana (Lepidoptera: Tortricidae). Eur. J. Entomol. 104, 259-265.
25. Greven, H. 2005 Structural and behavioral traits associated with sperm transfer in Poeciliinae. In Viviparous fishes (eds M. C. Uribe & H. J. Grier), pp. 145-163. Homestead, FL: New Life Publications.
26. Rosen, D. E. & Bailey, R. M. 1963 The poeciliid fishes (cypridontiformes). Their structure, zoogeography, and systematics. Bull. Am. Mus. Nat. Hist. 126, 1-176.
27. Ptacek, M. B. & Travis, J. 1998 Hierarchical patterns of covariance between morphological and behavioural traits. Anim. Behav. 56, 1044. (doi:10.1006/anbe.1998.0874)
28. Evans, J. P. & Meisner, A. D. 2009 Copulatory structures: taxonomic overview and the potential for sexual selection. In Reproductive biology and phylogeny of fishes (ed. B. G. M. Jamieson), pp. 138-180. Enfield, NH: Science Publishers.
29. Reynolds, J. D., Gross, M. R. & Coombs, M. J. 1993 Environmental conditions and male morphology determine alternative mating behaviour in Trinidadian guppies. Anim. Behav. 45, 145-152. (doi:10.1006/anbe.1993.1013)
30. Rosen, D. E. & Gordon, M. 1953 Functional anatomy and evolution of male genitalia in poeciliid fishes. Zoologica 38, 1-47.
31. Rosen, D. E. & Tucker, A. 1961 Evolution of secondary sexual characters and sexual behavior patterns in a family of viviparous fishes (Cyprinodontiformes: Poeciliidae). Copeia 1961, 201-212. (doi:10.2307/1439999)
32. Kelly, C. D., Godin, J. G. & Abdallah, G. 2000 Geographic variation in the male intromittent organ of the Trinidadian guppy (Poecilia reticulata). Can. J. Zool. 78, 1674-1680. (doi:10.1139/cjz-78-9-1674)
33. Magurran, A. E. 2005 Evolutionary ecology: the Trinidadian guppy. Oxford, UK: Oxford University Press.
34. Endler, J. A. 1995 Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol. Evol. 10, 22-29. (doi:10.1016/S0169-5347(00)88956-9)
35. Magurran, A. E. & Seghers, B. H. 1994 A cost of sexual harassment in the guppy, Poecilia reticulata. Proc. R. Soc. Lond. B 258, 89-92. (doi:10.1098/rspb.1994.0147)
36. Constantz, G. D. 1984 Sperm competition in poeciliid fishes. In Sperm competition and the evolution of animal mating systems (ed. R. L. Smith), pp. 465-485. Orlando, FL: Academic Press.
37. Clark, E., Aronson, L. R. & Gordon, M. 1954 Mating behavior pattern in two sympatric species of xiphophorin fishes: their inheritance and significance in sexual isolation. Bull. Am. Mus. Nat. Hist. 103, 135-226.
38. Magurran, A. E. & Seghers, B. H. 1994 Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc. R. Soc. Lond. B 255, 31-36. (doi:10.1098/rspb.1994.0005)
39. Houde, A. E. 1997 Sex, color, and mate choice in guppies, p. 210. Princeton, NJ: Princeton University Press.
40. Kuckuck, C. & Greven, H. 1997 Notes on the mechanically stimulated discharge of spermiozeugmata in the guppy, Poecilia reticulata: a quantitative approach. Zeitschrift für Fischkunde 4, 73-88.
41. Matthews, I. M. & Magurran, A. E. 2000 Evidence for sperm transfer during sneaky mating in wild Trinidadian guppies. J. Fish Biol. 56, 1381-1386. (doi:10.1111/j.1095-8649.2000.tb02150.x)
42. Clark, E. & Aronson, L. R. 1951 Sexual behaviour in the guppy, Lebistes reticulatus. Zoologica 36, 49-66.
43. Pilastro, A. & Bisazza, A. 1999 Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc. R. Soc. Lond. B 266, 1887-1891. (doi:10.1098/rspb.1999.0862)
44. Matthews, I. M., Evans, J. P. & Magurran, A. E. 1997 Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proc. R. Soc. Lond. B 264, 695-700. (doi:10.1098/rspb.1997.0099)
45. Endler, J. A. & Houde, A. E. 1995 Geographical variation in female preferences for male traits in Poecilia reticulata. Evolution 49, 456-468. (doi:10.2307/2410270)
46. Evans, J. P., Pilastro, A. & Ramnarine, I. W. 2003 Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata) populations. Biol. J. Linn. Soc. 78, 605-612. (doi:10.1046/j.0024-4066.2002.00193.x)
47. Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. 2004 Geometric morphometrics for biologists. p. 443. London, UK: Elsevier Academic Press.
48. Rohlf, F. J. 2005 TPSDIG2, digitize landmarks and outlines, v. 2.10. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
49. Rohlf, F. J. 2005 TPSRELW, relative warps analysis, v. 1.45. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
50. Lessells, C. M. & Boag, P. T. 1987 Unrepeatable repeatabilities: a common mistake. Auk 104, 116-121.
51. Neff, B. D., Pitcher, T. E. & Ramnarine, I. W. 2008 Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol. Ecol. 17, 2975-2984. (doi:10.1111/j.1365-294X.2008.03816.x)
52. Lukacs, P. M., Burnham, K. P. & Anderson, D. R. 2010 Model selection bias and Freedman's paradox. Ann. Inst. Stat. Math. 62, 117-125. (doi:10.1007/s10463-009- 0234-4)
53. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. New York, NY: Springer-Verlag.
54. Rohlf, F. J. 2007 TPSREGR, thin plate spline regression, v. 1.35. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
55. Reznick, D. N. & Endler, J. A. 1982 The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 125-148.
56. Cheng, Y. Y. 2004 Sexual selection and the evolution of genitalia in the guppy (Poecilia reticulata). MSc thesis, University of Toronto, Toronto.
57. Pilastro, A., Giacomello, E. & Bisazza, A. 1997 Sexual selection for small size in the male mosquitofish (Gambusia holbrooki). Proc. R. Soc. Lond. B 264, 1125-1129. (doi:10.1098/rspb.1997. 0155)
58. Herdman, E. J. E., Kelly, C. D. & Godin, J. G. J. 2004 Male mate choice in the guppy (Poecilia reticulata): do males prefer larger females as mates? Ethology 110, 97-111. (doi:10.1111/j.1439-0310.2003.00960.x)
59. Rowe, L., Cameron, E. & Day, T. 2003 Detecting sexually antagonistic coevolution with population crosses. Proc. R. Soc. Lond. B 270, 2009-2016. (doi:10.1098/ rspb.2003.2453)
60. Eberhard, W. 2010 Evolution of genitalia: theories, evidence, and new directions. Genetica 138, 5-18. (doi:10. 1007/s10709-009-9358-y)