A test for environmental effects on behavioral isolation in two species of killifish

Evolution

Volumn 66, Issue 10, 2012, Pages 3224-3237

  Berdan, Emma L ^a   Fuller, Rebecca C ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Behavior; Courtship; Reinforcement; Reproductive isolation; Speciation

Indexed keywords

BEHAVIORAL ECOLOGY; CONSPECIFIC; COURTSHIP; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL EFFECT; FERTILITY; FITNESS; HYBRID; INTRASPECIFIC COMPETITION; LIFE HISTORY TRAIT; RECOGNITION; REPRODUCTIVE ISOLATION; SALINITY; SALINITY TOLERANCE; TELEOST;

CYPRINODONTOIDEI; LUCANIA GOODEI; LUCANIA PARVA;

EID: 85027935976     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01646.x     Document Type: Article

References (93)

1. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ
2. Arndt, R. G. E. 1971. Ecology and behavior of the cyprinodont fishes Adinia xenica, Lucania parva, Lucania goodei, and Leptolucania ommata. Pp. 333. Zoology. Cornell, Ithaca, NY
3. Arnqvist, G., M. Edvardsson, U. Friberg, and T. Nilsson 2000. Sexual conflict promotes speciation in insects. Proc. Natl. Acad. Sci. USA 97:10460-10464.
4. Badyaev, A. V., and E. C. Snell-Rood 2006. Rapid evolutionary divergence of environment-dependent sexual traits in speciation: a paradox? Acta Zool. Sinica 52:315-319.
5. Boughman, J. W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944-948.
6. Boughman J.W.. 2002. How sensory drive can promote speciation. Trends Ecol. Evol. 17:571-577.
7. Boughman, J. W., H. D. Rundle, and D. Schluter 2005. Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361-373.
8. Burgess, G. H., and R. Franz 1978. Zoogeography of the aquatic fauna of the St. Johns River system with comments on adjacent peninsular faunas. Am. Midl. Nat. 100:160-170.
9. Byrne, P. G., and W. R. Rice 2006. Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc. R. Soc. B Biol. Sci. 273:917-922.
10. Carvajal-Rodriguez, A., and E. Rolan-Alvarez 2006. JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data. BMC Evol. Biol. 6:40.
11. Cocroft, R. B., R. L. Rodriguez, and R. E. Hunt 2010. Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant-feeding insects. Biol. J. Linn. Soc. 99:60-72.
12. Coyne, J. A., and H. A. Orr 2004. Speciation. Sinauer Associates, Inc., Sunderland, MA
13. Duggins, C. F., A. A. Karlin, and K. G. Relyea 1983. Electrophoretic variation in the killifish genus Lucania. Copeia 1983:564-570.
14. Dunson, W. A., and J. Travis 1991. The role of abiotic factors in community organization. Am. Nat. 138:1067-1091.
15. Endler, J. A. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139:S125-S153.
16. Endler, J. A., and A. L. Basolo 1998. Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13:415-420.
17. Engqvist, L., and K. P. Sauer 2001. Strategic male mating effort and cryptic male choice in a scorpionfly. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268:729-735.
18. Espinedo, C. M., C. R. Gabor, and A. S. Aspbury 2010. Males, but not females, contribute to sexual isolation between two sympatric species of Gambusia. Evol. Ecol. 24:865-878.
19. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35:124-138.
20. Fisher, H. S., B. B. M. Wong, and G. G. Rosenthal 2006. Alteration of the chemical environment disrupts communication in a freshwater fish. Proc. R. Soc. B Biol. Sci. 273:1187-1193.
21. Foster, N. R. 1967. Comparative studies on the biology of killifishes. Pp. 383. Zoology. Cornell, Ithaca, NY
22. Fuller, R. C. 2001. Patterns in male breeding behaviors in the bluefin killifish, Lucania goodei: A field study (Cyprinodontiformes : Fundulidae). Copeia 2001:823-828.
23. Fuller R.C. 2008a. Genetic incompatibilities in killifish and the role of environment. Evolution 62:3056-3068.
24. Fuller R.C.. 2008b. A test for a trade-off in salinity tolerance in early life-history stages in Lucania goodei and L. parva. Copeia 2008:154-157.
25. Fuller, R. C., and L. A. Noa 2008. Distribution and stability of sympatric populations of Lucania goodei and L. parva across Florida. Copeia 2008:699-707.
26. Fuller, R. C., K. E. McGhee, and M. Schrader 2007. Speciation in killifish and the role of salt tolerance. J. Evol. Biol. 20:1962-1975.
27. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJ
28. Gleeson, R. A., L. M. McDowell, and H. C. Aldrich 1996. Structure of the aesthetasc (olfactory) sensilla of the blue crab, Callinectes sapidus: Transformations as a function of salinity. Cell Tissue Res. 284:279-288.
29. Grizzle, J. M., and I. Altinok 2003. Effects of low salinities on oxygen consumption of selected euryhaline and stenohaline freshwater fish. J. World Aquacult. Soc. 34:113-117.
30. Hall, D. W., M. Kirkpatrick, and B. West 2000. Runaway sexual selection when female preferences are directly selected. Evolution 54:1862-1869.
31. Herbert-Read, J. E., D. Logendran, and A. J. W. Ward 2010. Sensory ecology in a changing world: salinity alters conspecific recognition in an amphidromous fish, Pseudomugil signifer. Behav. Ecol. Sociobiol. 64:1107-1115.
32. Higashi, M., G. Takimoto, and N. Yamamura 1999. Sympatric speciation by sexual selection. Nature 402:523-526.
33. Hoskin, C. J., M. Higgie, K. R. McDonald, and C. Moritz 2005. Reinforcement drives rapid allopatric speciation. Nature 437:1353-1356.
34. Houde, A. E. 1997. Sex, color, and mate choice in guppies. Princeton Univ. Press, Princeton, NJ
35. Howard, D. J. 1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Pp. 46-69 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Inc., New York, NY
36. Hubbs, C., B. Walker, and R. Johnson 1943. Hybridization in nature between species of American cyprinodont fishes. Contrib. Lab. Vertebr. Biol.. 23:1-21.
37. Jaenike, J., K. A. Dyer, C. Cornish, and M. S. Minhas 2006. Asymmetrical reinforcement and Wolbachia infection in Drosophila. Plos Biology. 4:1852-1862.
38. Kelly, J. K., and M. A. F. Noor 1996. Speciation by reinforcement: a model derived from studies of Drosophila. Genetics 143:1485-1497.
39. Kilby, J. D. 1955. The fishes of two gulf coastal marsh areas of Florida. Tulane Stud. Zool. 2:175-247.
40. Kirkpatrick, M., and V. Ravigne 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159:S22-S35.
41. Kirkpatrick, M., and M. J. Ryan 1991. The evolution of mating preferences and the paradox of the lek. Nature 350:33-38.
42. Kitano, J., S. C. Lema, J. A. Luckenbach, S. Mori, Y. Kawagishi, M. Kusakabe, P. Swanson, and C. L. Peichel 2010. Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr. Biol. 20:2124-2130.
43. Kokko, H., and R. A. Johnstone 2002. Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 357:319-330.
44. Kozak, G. M., A. B. Rudolph, B. L. Colon, and R. C. Fuller 2012. Postzygotic isolation evolves before prezygotic isolation between fresh and saltwater populations of the rainwater killifish, Lucania parva. Intl. J. Evol. Biol 2012:523967.
45. Lande, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA Biol. Sci. 78:3721-3725.
46. Lee, D. S. 1980. Atlas of North American freshwater fishes, 1980-et seq. North Carolina State Museum of Natural History, Raleigh, NC
47. Lewandowski, E., and J. Boughman 2008. Effects of genetics and light environment on colour expression in threespine sticklebacks. Biol. J. Linn. Soc. 94:663-673.
48. Long, K. D., and A. E. Houde 1989. Orange spots as a visual cue for female mate choice in the guppy (Poecilia reticulata). Ethology 82:316-324.
49. Maan, M. E., and O. Seehausen 2011. Ecology, sexual selection and speciation. Ecol. Lett. 14:591-602.
50. Martin, O. Y., and D. J. Hosken 2003. The evolution of reproductive isolation through sexual conflict. Nature 423:979-982.
51. Mayr, E. 1963. Animal species and evolution. Belknap Press, Cambridge, MA
52. McGhee, K. E., and J. Travis 2010. Repeatable behavioural type and stable dominance rank in the bluefin killifish. Anim. Behav. 79:497-507.
53. McGhee, K. E., R. C. Fuller, and J. Travis 2007. Male competition and female choice interact to determine mating success in the bluefin killifish. Behav. Ecol. 18:822-830.
54. Mendelson, T. C. 2003. Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae : Etheostoma). Evolution 57:317-327.
55. Merrill, R. M., B. Van Schooten, J. A. Scott, and C. D. Jiggins 2011. Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies. Proc. R. Soc. B Biol. Sci. 278:511-518.
56. 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.
57. Noor, M. A. F. 1999. Reinforcement and other consequences of sympatry. Heredity 83:503-508.
58. Ord, T. J., and J. A. Stamps 2009. Species identity cues in animal communication. Am. Nat. 174:585-593.
59. Ord, T. J., L. King, and A. R. Young 2011. Contrasting theory with the empirical data of species recognition. Evolution 65:2572-2591.
60. Patten, M. A., J. T. Rotenberry, and M. Zuk 2004. Habitat selection, acoustic adaptation, and the evolution of reproductive isolation. Evolution 58:2144-2155.
61. Perez-Figueroa, A., A. Caballero, and E. Rolan-Alvarez 2005. Comparing the estimation properties of different statistics for measuring sexual isolation from mating frequencies. Biol. J. Linn. Soc. 85:307-318.
62. Peterson, M. A., B. M. Honchak, S. E. Locke, T. E. Beeman, J. Mendoza, J. Green, K. J. Buckingham, M. A. White, and K. J. Monsen 2005. Relative abundance and the species-specific reinforcement of male mating preference in the Chrysochus (Coleoptera : Chrysomelidae) hybrid zone. Evolution 59:2639-2655.
63. Plath, M., R. Riesch, A. Oranth, J. Dzienko, N. Karau, A. Schiessl, S. Stadler, A. Wigh, C. Zimmer, L. Arias-Rodriguez, et al. 2010. Complementary effect of natural and sexual selection against immigrants maintains differentiation between locally adapted fish. Naturwissenschaften 97:769-774.
64. R Development Core Team, 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
65. Ramsey, J., H. D. Bradshaw, and D. W. Schemske 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520-1534.
66. Ritchie, M. G. 2007. Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38:79-102.
67. Rolan-Alvarez, E., and M. Caballero 2000. Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution 54:30-36.
68. Rundle, H. D., and J. W. Boughman 2010. Behavioral ecology and speciation. Pp. 471-487 in D. F. Westneat and C. W. Fox, eds. Evolutionary behavioral ecology. Oxford Univ. Press, New York, NY
69. Sakamoto, T., K. Uchida, and S. Yokota 2001. Regulation of the ion-transporting mitochondrion-rich cell during adaptation of teleost fishes to different salinities. Zool. Sci. 18:1163-1174.
70. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372-380.
71. Scott, G. R., J. G. Richards, B. Forbush, P. Isenring, and P. M. Schulte 2004a. Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am. J. Physiol. Cell Physiol. 287:C300-9.
72. Scott, G. R., J. T. Rogers, J. G. Richards, C. M. Wood, and P. M. Schulte 2004b. Intraspecific divergence of ionoregulatory physiology in the euryhaline teleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. J. Exp. Biol. 207:3399-410.
73. Seehausen, O., J. J. M. vanAlphen, and F. Witte 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808-1811.
74. Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. van der Sluijs, M. V. Schneider, M. E. Maan, H. Tachida, et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620-626.
75. Servedio, M. R. 2007. Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement. Evolution 61:2772-2789.
76. Servedio M.R.. 2009. The role of linkage disequilibrium in the evolution of premating isolation. Heredity 102:51-56.
77. Servedio, M. R., and M. Kirkpatrick 1997. The effects of gene flow on reinforcement. Evolution 51:1764-1772.
78. Servedio, M. R., and M. A. F. Noor 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Syst. 34:339-364.
79. Slabbekoorn, H., and T. B. Smith 2002. Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution 56:1849-1858.
80. Sokal, R. R., and F. J. Rohlf 1981. Biometry: the principles and practice of statistics in biological research. W. H. Freeman, San Francisco
81. Sola, C., and P. Tongiorgi 1996. The effect of salinity on the chemotaxis of glass eels, Anguilla anguilla, to organic earthy and green odorants. Environ. Biol. Fishes 47:213-218.
82. Stelkens, R. B., K. A. Young, and O. Seehausen 2010. The accumulation of reproductive incompatibilities in African cichlid fish. Evolution 64:617-632.
83. Svensson, E. I., K. Karlsson, M. Friberg, and F. Eroukhmanoff 2007. Gender differences in species recognition and the evolution of asymmetric sexual isolation. Curr. Biol. 17:1943-1947.
84. Tobias, J. A., J. Aben, R. T. Brumfield, E. P. Derryberry, W. Halfwerk, H. Slabbekoorn, and N. Seddon 2010. Song divergence by sensory drive in Amazonian birds. Evolution 64:2820-2839.
85. Tobler, M., I. Schlupp, and M. Plath 2008. Does divergence in female mate choice affect male size distributions in two cave fish populations?Biol. Lett. 4:452-454.
86. van Doorn, G. S., P. Edelaar, and F. J. Weissing 2009. On the origin of species by natural and sexual selection. Science 326:1704-1707.
87. Walker, T. J. 1974. Character displacement and acoustic insects. Am. Zool. 14:1137-1150.
88. Wedell, N., M. J. G. Gage, and G. A. Parker 2002. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17:313-320.
89. Whitehead, A. 2010. The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus Sp.). Evolution 64:2070-2085.
90. Wiley, C., A. Qvarnstrom, G. Andersson, T. Borge, and G. P. Saetre 2009. Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution 63:1731-1739.
91. Wong, B. B. M., and M. D. Jennions 2003. Costs influence male mate choice in a freshwater fish. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270:S36-S38.
92. Yukilevich, R. Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution, 10.1111/j.1558-5646.2011.01534.x
93. Zuur, A. F. 2009. Mixed effects models and extensions in ecology with R. Springer, New York ; London