Nonlinear effects of female mate choice in wild threespine sticklebacks

Evolution

Volumn 58, Issue 11, 2004, Pages 2498-2510

  Blais, Jonatan ^a   Rico, Ciro ^b   Bernatchez, Louis ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

Author keywords

Gasterosteus aculeatus; Immunocompetence; Mate choice; Mean d2; Parasite load; Reproductive success; Sexual selection

Indexed keywords

BEHAVIORAL ECOLOGY; FISH; GENETIC VARIATION; IMMUNOCOMPETENCE; MATE CHOICE; MATING SUCCESS; SEXUAL SELECTION;

ANIMALIA; GASTEROSTEUS; GASTEROSTEUS ACULEATUS; TREMATODA;

EID: 9244233874     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb00879.x     Document Type: Article

References (83)

1. Aeschlimann, P. B., M. A. Haberli, T. B. H. Reusch, T. Boehm, and M. Milinski. 2003. Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav. Ecol. Sociobiol. 54:119-126.
2. Arnegard, M. E., and A. S. Kondrashov. 2004. Sympatric speciation by sexual selection alone is unlikely. Evolution 58:222-237.
3. Bakker, T. C. M., and M. Milinski. 1993. The advantages of being red: sexual selection in the stickleback. Mar. Behav. Physiol. 23:287-300.
4. Bakker, T. C. M., and B. Mundwiler. 1999. Pectoral fin size in a fish species with paternal care: a condition-dependent sexual trait revealing infection status. Freshwater Biol. 41:543-551.
5. Bell, M. A., and S. A. Foster. 1994. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford, U.K.
6. Bishop, Y. M. M., S. E. Fienberg., and P. W. Holland. 1975. Discrete multivariate analysis: theory and practice. MIT Press, Cambridge, MA.
7. Blanckenhorn, W. U., U. R. S. Kraushaar, Y. Teuschl, and C. T. Reim. 2004. Sexual selection on morphological and physiological traits and fluctuating asymmetry in the black scavenger fly Sepsis cynipsea. J. Evol. Biol. 17:629-641.
8. Blows, M. W., and R. Brooks. 2003. Measuring non-linear selection. Am. Nat. 162:815-820.
9. Blows, M. W., R. Brooks, and P. G. Kraft. 2003. Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies. Evolution 57:1622-1630.
10. Blows, M. W., S. F. Chenoweth, and E. Hine. 2004. Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 163:329-340.
11. Braithwaite, V. A., and I. Barber. 2000. Limitations to colour-based sexual preferences in three-spined sticklebacks. Behav. Ecol. Sociobiol. 47:413-416.
12. Brønseth, T., and I. Folstad. 1997. The effect of parasites on courtship dance in threespine sticklebacks: more than meets the eye? Can. J. Zool. 75:589-594.
13. Brooks, R., and J. A. Endler. 2001. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002-1015.
14. Candolin, U., and H.-R. Voigt. 2001. No effect of a parasite on reproduction in stickleback males: a laboratory artefact? Parasitology 122:457-464.
15. _. 2003. Size-dependent selection on arrival times in sticklebacks: why small males arrive first. Evolution 57:862-871.
16. Coltman, D. W., and J. Slate. 2003. Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971-983.
17. Coltman, D. W., J. G. Pilkington, J. A. Smith, and J. M. Pemberton. 1998. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B. Biol. Sci. 265:803-809.
18. Côté, I. M., and W. Hunte. 1989. Male and female mate choice in the redlip blenny: why bigger is better. Anim. Behav. 38:78-88.
19. Coulson, T. N., J. M. Pemberton, S. D. Albon, M. Beaumont, T. C. Marshall, J. Slate, F. E. Guinness, and T. H. Clutton-Brock. 1998. Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B. Biol. Sci. 265:489-495.
20. David, P. 1998. Heterozygosity-fitness correlations: new perspective on old problems. Heredity 80:531-537.
21. DeWoody, J. A., D. Walker, and J. C. Avise. 2000. Genetic parentage in large half-sib clutches: theoretical estimates and empirical appraisals. Genetics 154:1907-1912.
22. Doucet, S. M., and R. Montgomerie. 2003. Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav. Ecol. 14:503-509.
23. Dufresne, F., G. J. FitzGerald, and S. Lachance. 1990. Age and size-related differences in reproductive success and reproductive costs in threespine sticklebacks (Gasterosteus aculeatus). Behav. Ecol. 1:140-147.
24. FitzGerald, G. J. 1983. The reproductive ecology and behaviour of three sympatric sticklebacks (Gasterosteidae) in a saltmarsh. Biol. Behav. 8:67-79.
25. FitzGerald, G. J., and N. Van-Havre. 1987. The adaptive significance of cannibalism in sticklebacks (Gasterosteidae: Pisces). Behav. Ecol. Sociobiol. 20:125-128.
26. FitzGerald, G. J., M. Fournier, and J. Morrissette. 1994. Sexual selection in an anadromous population of threespine sticklebacks: no role for parasites. Evol. Ecol. 8:348-356.
27. Folstad, I., and A. J. Karter. 1992. Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139:603-622.
28. Gawlik, D. E. 2002. The effects of prey availability on the numerical response of wading birds. Ecol. Monogr. 72:329-346.
29. Getty, T. 2002. Signalling health versus parasites. Am. Nat. 159:363-371.
30. Goldstein, D. B., A. R. Linares, L. L. Cavalli-Sforza, and M. Feldman. 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463-471.
31. Hall, D. W., M. Kirkpatrick, and B. West. 2000. Runaway sexual selection when female preferences are directly selected. Evolution 54:1862-1869.
32. Hamilton, W. D., and M. Zuk. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218:384-387.
33. 2), and reproductive traits in chinook salmon, Oncorhynchus tshawytscha. Can. J. Fish. Aquat. Sci. 59:77-84.
34. Hersch, E. I., and P. C. Phillips. 2004. Power and potential bias in field studies of natural selection. Evolution 58:479-485.
35. Higashi, M., G. Takimoto, and N. Yamamura. 1999. Sympatric speciation by sexual selection. Nature 402:523-536.
36. Höglund, J., S. B. Piertney, R. V. Alatalo, J. Lindell, A. Lundberg, and P. T. Rintamäki. 2002. Inbreeding depression and male fitness in black grouse. Proc. R. Soc. Lond. B. Biol. Sci. 269:711-715.
37. Hunt, J., L. F. Bussière, M. D. Jennions, and R. Brooks. 2004. What is genetic quality? Trends Ecol. Evol. 19:329-333.
38. Jamieson, I. G., D. M. Blouw, and P. W. Colgan. 1992. Parental care as a constraint on male mating success in fishes: a comparative study of threespine and white sticklebacks. Can. J. Zool. 70:956-962.
39. Johnstone, R. A. 1995. Honest advertisement of multiple qualities using multiple signals. J. Theor. Biol. 177:87-94.
40. Jones, A. G., S. Östlund-Nilsson, and J. C. Avise. 1998. A microsatellite assessment of sneaked fertilization and egg thievery in the fifteenspine stickleback. Evolution 5:848-858.
41. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157:245-261.
42. Kirkpatrick, M., and S. L. Nuismer. 2004. Sexual selection can constrain sympatric speciation. Proc. R. Soc. Lond. B. Biol. Sci. 271:687-693.
43. Kraak, S. B. M., and T. C. M. Bakker. 1998. Mutual mate choice in sticklebacks: attractive males choose big females, which lay big eggs. Anim. Behav. 56:859-866.
44. Kraak, S. B. M., T. C. M. Bakker, and B. Mundwiler. 1999a. Correlates of the duration of the egg collecting phase in the three-spined stickleback. J. Fish Biol. 54:1038-1049.
45. _. 1999b. Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success. Behav. Ecol. 10:696-706.
46. Künzler, R., and T. C. M. Bakker. 2000. Pectoral fin size and paternal quality in sticklebacks. Proc. R. Soc. Lond. B. Biol. Sci. 267:999-1004.
47. Lachance, S., and G. J. Fitzgerald. 1992. Parental care tactics of three-spined sticklebacks living in a harsh environment. Behav. Ecol. 3:360-366.
48. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
49. Lemly, A. D., and G. W. Esch. 1984. Effects of the trematode Uvulilfer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J. Parasitol. 70:475-492.
50. Marshall, T. C., and J. A. Spalton. 2000. Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim. Conserv. 3:241-248.
51. McCullagh, P., and J. Nelder. 1989. Generalized linear models. Chapman and Hall, London.
52. McKinnon, J. S., S. Mori, B. K. Blackman, L. David, D. M. Kingsley, L. Jamieson, J. Chou, and D. Schluter. 2004. Evidence for ecology's role in speciation. Nature 429:294-298.
53. Milinski, M., and T. C. M. Bakker. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330-333.
54. Mori, S. 1994. Nest site choice by the three-spined stickleback, Gasterosteus aculeatus (form leiurus), in spring-fed waters. J. Fish Biol. 45:279-289.
55. Neff, B. D. 2004. Stabilizing selection on genomic divergence in a wild fish population. Proc. Natl. Acad. Sci. USA 101:2381-2385.
56. Peichel, C. L., K. S. Nereng, K. A. Ohgi, B. L. E. Cole, P. F. Colosimo, C. A. Buerkle, D. Schluter, and D. M. Kingsley. 2001. The genetic architecture of divergence between threespine stickleback species. Nature 414:901-905.
57. Peters, A. 2000. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc. R. Soc. Lond. B. Biol. Sci. 267:884-889.
58. Phillips, P. C., and S. J. Arnold. 1989. Visualizing multivariate selection. Evolution 43:1209-1222.
59. Pomiankowski, A., and A. P. Møller. 1995. A resolution of the lek paradox. Proc. R. Soc. Lond. B. Biol. Sci. 260:21-29.
60. Powell, G. V. N. 1987. Habitat use by wading birds in a subtropical estuary: implications of hydrography. Auk 104:740-749.
61. Price, T. 1998. Sexual selection and natural selection in bird speciation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353:1-12.
62. Pryke, S. R., S. Andersson, and M. J. Lawes. 2001. Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display. Evolution 55:1452-1463.
63. Reusch, T. B. H., M. A. Häberli, P. B. Aeschlimann, and M. Milinski. 2001. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300-302.
64. Rico, C., U. Kuhnlein, and G. J. FitzGerald. 1992. Male reproductive tactics in the threespine stickleback-an evaluation by DNA fingerprinting. Mol. Ecol 1:79-87.
65. Rico, C., D. Zadworny, U. Kuhnlein, and G. J. FitzGerald. 1993. Characterization of hypervariable microsatellite loci in the threespine stickleback Gasterosteus aculeatus. Mol. Ecol. 2:271-272.
66. Rossiter, S. J., G. Jones, R. D. Ransome, and E. M. Barratt. 2001. Outbreeding increases offspring survival in wild greater horse-shoe bats (Rhinolophus ferrumequinum). Proc. R. Soc. Lond. B. Biol. Sci. 268:1055-1061.
67. Rowland, W. J. 1995. Do female stickleback care about male courtship vigour? Manipulation of display tempo using video playback. Behaviour 132:951-961.
68. Schaffer, C. 1993. Overfitting avoidance as bias. Mach. Learn. 10:153-178.
69. Schluter, D., and D. Nychka. 1994. Exploring fitness surfaces. Am. Nat. 143:597-616.
70. Saether, S. A., P. Fiske, J. A. Kalas, and J. M. Gjul. 2000. Females of the lekking great snipe do not prefer males with whiter tails. Anim. Behav. 59:273-280.
71. Sherman, P. W., and H. K. Reeve. 1999. Sexual selection and sensory exploitation. Science 283:1083a.
72. Swarup, H. 1958. Stages in the development of the stickleback Gasterosteus aculeatus (L.). J. Embryol. Exp. Morph. 6:373-383.
73. Takimoto, G., M. Higashi, and N. Yamamura. 2000. A deterministic genetic model for sympatric speciation by sexual selection. Evolution 54:1870-1881.
74. Taylor, E. B. 1998. Microsatellites isolated from the threespine stickleback Gasterosteus aculeatus. Mol. Ecol. 7:930-931.
75. Tsitrone, A., F. Rousset, and P. David. 2001. Heterosis, marker mutational processes and population inbreeding history. Genetics 159:1845-1859.
76. Turner, G. F., and M. T. Burrows. 1995. A model of sympatric speciation by sexual selection. Proc. R. Soc. Lond. B. Biol. Sci. 260:287-292.
77. Webberley, K. M., G. D. D. Hurst, J. Buszko, and M. E. N. Majerus. 2002. Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system. Anim. Behav. 63:131-141.
78. Wegner, K. M., M. Kalbe, J. Kurtz, T. B. H. Reusch, and M. Milinski. 2003. Parasite selection for immunogenetic optimality. Science 301:1343.
79. Whoriskey, F. G., and G. J. FitzGerald. 1985a. Nest sites of the threespine stickleback: can site characters alone protect the nest against egg predators and are nest sites a limiting resource? Can. J. Zool. 63:1991-1994.
80. _. 1985b. The effects of bird predation on an estuarine stickleback (Pisces: Gasterosteidae) community. Can. J. Zool. 63:301-307.
81. Wiegmann, D. D., and J. R. Baylis. 1995. Male body size and paternal behaviour in smallmouth bass, Micropterus dolomieui (Pisces: Centrarchidae). Anim. Behav. 50:1543-1555.
82. Zhang, X. S., and W. G. Hill. 2003. Multivariate stabilizing selection and pleiotropy in the maintenance of quantitative genetic variation. Evolution 57:1761-1775.
83. Zuk, M., and K. A. McKean. 1996. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26:1009-1023.