Genetics of incipient speciation in Drosophila mojavensis. I. Male courtship song, mating success, and genotype X environment interactions

Evolution

Volumn 61, Issue 5, 2007, Pages 1106-1119

  Etges, William J ^a   De Oliveira, Cássia Cardoso ^a   Gragg, Erin ^b   Ortíz Barrientos, Daniel ^c   Noor, Mohamed A F ^b   Ritchie, Michael G ^d  

^a UNIVERSITY OF ARKANSAS   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Cactus; Courtship song; Desert; Drosophila mojavensis; GxE interaction; QTL; Sexual isolation; Speciation

Indexed keywords

ADAPTATION; CACTUS; CHROMOSOME; COURTSHIP; FLY; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; MALE BEHAVIOR; MATING SUCCESS; REPRODUCTIVE ISOLATION; SEXUAL SELECTION; SONG; SPECIATION (BIOLOGY);

ANIMAL; ARTICLE; CACTACEAE; DROSOPHILA; ECOSYSTEM; ENVIRONMENT; FEMALE; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOST PARASITE INTERACTION; MALE; PARASITOLOGY; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SEXUAL BEHAVIOR; SPECIES DIFFERENTIATION; STATISTICAL MODEL;

ANIMALS; CACTACEAE; DROSOPHILA; ECOSYSTEM; ENVIRONMENT; FEMALE; GENETIC SPECIATION; GENOTYPE; HOST-PARASITE RELATIONS; LIKELIHOOD FUNCTIONS; MALE; QUANTITATIVE TRAIT LOCI; REPRODUCTION; SELECTION (GENETICS); SEXUAL BEHAVIOR, ANIMAL; VARIATION (GENETICS);

BAJA CALIFORNIA [(PNN) MEXICO]; MEXICO [NORTH AMERICA]; NORTH AMERICA;

CACTACEAE; DROSOPHILA MOJAVENSIS;

EID: 34247898964     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2007.00104.x     Document Type: Article

References (102)

1. Alcorn, S. M., T. V. Orum, A. G. Steigerwalt, J. L. M. Foster, J. C. Fogleman, and D. J. Brenner. 1991. Taxonomy and pathogenicity of Erwinia cacticida sp. nov. Int. J. Syst. Bacteriol. 41: 197 212.
2. Alonso-Pimentel, H., and T. R. Tobin. 1992. Discriminant function analysis of the courtship behavior of Drosophila mojavensis (Diptera: Drosophilidae). J. Insect Behav. 5: 131 139.
3. Basten, C. J., B. S. Weir, and Z.-B. Zeng. 2002. QTL cartographer: A reference manual and tutorial for QTL mapping. Dept. of Statistics, North Carolina State Univ., Raleigh, NC.
4. Bennet-Clark, H. C., and A. W. Ewing. 1969. Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster. Anim. Behav. 17: 755 759.
5. Berlocher, S. H., and J. L. Feder. 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47: 773 815.
6. Billeter, J.-C., E. J. Rideout, A. J. Dornan, and S. F. Goodwin. 2006. Control of male sexual behavior in Drosophila by the sex determination pathway. Curr. Biol. 16: R766 R776.
7. Boughman, J. W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411: 944 948.
8. Brazner, J. C., and W. J. Etges. 1993. Pre-mating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. II. Effects of larval substrates on time to copulation, mate choice, and mating propensity. Evol. Ecol. 7: 605 624.
9. Brodie, E. D., A. J. Moore, and F. J. Janzen. 1995. Visualising and quantifying natural selection. Trends Ecol. Evol. 10: 313 318.
10. Bush, G. L. 1969. Sympatric host race formation and specialization in frugivorous flies of the genus Rhagoletis (Diptera, Tephriditae). Evolution 23: 237 251.
11. Byrne, B. C. 1999. Behaviour-genetic analysis of lovesongs in desert species of Drosophila. Ph.D. thesis, University of Leicester, Leicester, U.K.
12. Chenoweth, S. F., and M. W. Blows. 2006. Dissecting the complex genetic basis of mate choice. Nat. Rev. Genet. 7: 681 692.
13. Cotton, S., J. Small, and A. Pomiankowski. 2006. Sexual selection and condition-dependent mate preferences. Curr. Biol. 16: R755 R765.
14. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43: 362 381.
15. Coyne, J. A., and H. A. Orr. 1997. "Patterns of speciation in Drosophila" revisited. Evolution 51: 295 303.
16. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.
17. Danielson-Francois, A. M., J. K. Kelly, and M. D. Greenfield. 2006. Genotype × environment interaction for male attractiveness in an acoustic moth: evidence for plasticity and canalization. J. Evol. Biol. 19: 532 542.
18. Dobzhansky, T. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
19. Endler, J. A. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139: S125 S153.
20. Etges, W. J. 1989. Evolution of developmental homeostasis in Drosophila mojavensis. Evol. Ecol. 3: 189 201.
21. Etges, W. J. 1990. Direction of life history evolution in Drosophila mojavensis. Pp. 37 56 in J. S. F. Barker, W. T. Starmer, and R. J. MacIntyre, eds. Ecological and evolutionary genetics of Drosophila. Plenum, New York.
22. Etges, W. J. 1992. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. Evolution 46: 1945 1950.
23. Etges, W. J. 1993. Genetics of host-cactus response and life-history evolution among ancestral and derived populations of cactophilic Drosophila mojavensis. Evolution 47: 750 767.
24. Etges, W. J. 1998. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IV. Correlated responses in behavioral isolation to artificial selection on a life history trait. Am. Nat. 152: 129 144.
25. Etges, W. J. 2002. Divergence in mate choice systems: does evolution play by rules? Genetica 116: 151 166.
26. Etges, W. J., and M. A. Ahrens. 2001. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. V. Deep geographic variation in epicuticular hydrocarbons among isolated populations. Am. Nat. 158: 585 598.
27. Etges, W. J., and W. B. Heed. 1987. Sensitivity to larval density in populations of Drosophila mojavensis: influences of host plant variation on components of fitness. Oecologia 71: 375 381.
28. Etges, W. J., and C. S. Klassen. 1989. Influences of atmospheric ethanol on adult Drosophila mojavensis: altered metabolic rates and increases in fitness among populations. Physiol. Zool. 62: 170 193.
29. Etges, W. J., W. R. Johnson, G. A. Duncan, G. Huckins, and W. B. Heed. 1999. Ecological genetics of cactophilic Drosophila. Pp. 164 214 in R. Robichaux, ed. Ecology of Sonoran Desert plants and plant communities. Univ. of Arizona Press, Tucson, AZ.
30. Etges, W. J., K. F. Over, C. C. De Oliveira, and M. G. Ritchie. 2006. Inheritance of courtship song variation among geographically isolated populations of Drosophila mojavensis. Anim. Behav. 71: 1205 1214.
31. Ewing, A. W., and H. C. Bennet-Clark. 1968. The courtship songs of Drosophila. Behaviour 31: 288 301.
32. Ewing, A. W., and J. A. Miyan. 1986. Sexual selection, sexual isolation and the evolution of song in the Drosophila repleta group of species. Anim. Behav. 34: 421 429.
33. Fairbairn, D. J., and R. F. Preziosi. 1996. Sexual selection and the evolution of sexual size dimorphism in the water strider, Aquarius remigis. Evolution 50: 1549 1559.
34. Feder, J. L. 1998. The apple maggot fly, Rhagoletis pomenella: flies in the face of conventional wisdom about speciation? Pp. 130 144 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, New York.
35. Fellows, D. P., and W. B. Heed. 1972. Factors affecting host plant selection in desert-adapted cactophilic Drosophila. Ecology 53: 850 858.
36. Genstat5-Committee. 1993. Genstat 5 release 3 reference manual. Oxford Univ. Press, Oxford, U.K.
37. Gerhardt, H. C. 1992. Multiple messages in acoustic signals. Semin. Neurosci. 4: 391 400.
38. Gerhardt, H. C., and F. Huber. 2002. Acoustic communication in insects and anurans. Univ. of Chicago Press, Chicago.
39. Gilbert, D. G. 2005. DroSpeGe, a public database of Drosophila species genomes. Available at http://insects.eugenes.org/DroSpeGe/.
40. Gillespie, J. H., and M. Turelli. 1989. Genotype - environment interactions and the maintenance of polygenic variation. Genetics 121: 129 138.
41. Gleason, J. M. 2005. Mutations and natural genetic variation in the courtship song of Drosophila. Behav. Genet. 35: 265 277.
42. Gleason, J. M., and M. G. Ritchie. 1998. Evolution of courtship song and reproductive isolation in the Drosophila willistoni species complex: do sexual signals diverge the most quickly? Evolution 52: 1493 1500.
43. Gleason, J. M., and M. G. Ritchie. 2004. Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL? Genetics 166: 1303 1311.
44. Gleason, J. M., S. V. Nuzhdin, and M. G. Ritchie. 2002. Quantitative trait loci affecting a courtship signal in Drosophila melanogaster. Heredity 89: 1 6.
45. Gomulkiewicz, R., R. D. Holt, and M. Barfield. 1999. The effect of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theor. Popul. Biol. 55: 283 296.
46. Gorczyca, M., and J. C. Hall. 1987. The INSECTAVOX, an integrated device for recording and amplifying courtship song. Drosophila Inf. Serv. 66: 157 160.
47. Gray, D. A., and W. H. Cade. 1999. Quantitative genetics of sexual selection in the field cricket, Gryllus integer. Evolution 53: 848 854.
48. Greenfield, M. D., and R. L. Rodriguez. 2004. Genotype-environment interaction and the reliability of mating signals. Anim. Behav. 68: 1461 1468.
49. Griffith, S. C., I. P. F. Owens, and T. Burke. 1999. Environmental determination of a sexually selected trait. Nature 400: 358 360.
50. Hall, D. W., and M. Kirkpatrick. 2006. Reinforcement and sex linkage. Evolution 60: 908 921.
51. Heed, W. B. 1978. Ecology and genetics of Sonoran Desert Drosophila. Pp. 109 126 in P. F. Brussard, ed. Ecological genetics: the interface. Springer-Verlag, New York.
52. Heed, W. B., and R. L. Mangan. 1986. Community ecology of the Sonoran Desert Drosophila. Pp. 311 345 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Academic Press, New York.
53. Henry, C., S., M. L. M. Wells, and K. E. Holsinger. 2002. The inheritance of mating songs in two cryptic, sibling lacewing species (Neuroptera: Chrysopidae: Chrysoperla). Genetica 116: 269 289.
54. Hoikkala, A., J. Aspi, and L. Suvanto. 1998. Male courtship song frequency as an indicator of male genetic quality in an insect species, Drosophila montana. Proc. R. Soc. Lond. B 265: 503 508.
55. Hoikkala, A., K. Klappert, and D. Mazzi. 2005. Factors affecting male song evolution in Drosophila montana. Curr. Top. Dev. Biol. 67: 225 250.
56. Jia, F. Y., and M. D. Greenfield. 1997. When are good genes good? Variable outcomes of female choice in wax moths. Proc. R. Soc. B: Biol. Sci. 264: 1057 1063.
57. Jia, F.-Y., M. D. Greenfield, and R. D. Collins. 2000. Genetic variance of sexually selected traits in waxmoths: maintenance by genotype X environment interaction. Evolution 54: 953 967.
58. Kirkpatrick, M. 1987. Sexual selection by female choice in polygynous animals. Annu. Rev. Ecol. Syst. 18: 43 70.
59. Kokko, H., R. Brooks, J. M. McNamara, and A. I. Houston. 2002. The sexual selection continuum. Proc. R. Soc. Lond. B 269: 1331 1340.
60. Lande, R. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78: 3721 3725.
61. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37: 1210 1226.
62. Lander, E. S., P. Green, J. Abrahamson, A. Barlow, M. J. Daly, S. E. Lincoln, and L. Newburg. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174 181.
63. Lesna, I., and M. W. Sabelis. 1999. Diet-dependent female choice for males with 'good genes' in a soil predatory mite. Nature 401: 581.
64. Liimatainen, J., A. Hoikkala, J. Aspi, and P. Welbergen. 1992. Courtship in Drosophila montana: the effects of male auditory signals on the behaviour of flies. Anim. Behav. 43: 35 48.
65. Markow, T. A. 1991. Sexual isolation among populations of Drosophila mojavensis. Evolution 45: 1525 1529.
66. Markow, T. A., J. C. Fogleman, and W. B. Heed. 1983. Reproductive isolation in Sonoran Desert Drosophila. Evolution 37: 649 652.
67. Muller, H. J. 1939. Reversibility in evolution from the standpoint of genetics. Biol. Rev. 14: 261 280.
68. Muller, H. J. 1942. Isolating mechanisms, evolution and temperature. Biol. Symp. 6: 71 125.
69. Newby, B. D., and W. J. Etges. 1998. Host preference among populations of Drosophila mojavensis that use different host cacti. J. Insect Behav. 11: 691 712.
70. Olvido, A. E., and T. A. Mousseau. 1995. Effect of rearing environment on calling-song plasticity in the striped ground cricket. Evolution 49: 1271 1277.
71. Ortiz-Barrientos, D., A. S. Chang, and M. A. F. Noor. 2006. A recombinational portrait of the Drosophila pseudoobscura genome. Genet. Res. 87: 23 31.
72. Palumbi, S. R. 1996. Nucleic Acids II: the polymerase chain reaction. Pp. 205 247 in D. M. Hillis, C. Moritz, and B. K. Mable, eds. Molecular systematics. Sinauer Associates, Inc., Sunderland, MA.
73. Pigliucci, M. 2001. Phenotypic plasticity. Beyond nature and nurture. Johns Hopkins Univ. Press, Baltimore, MD.
74. Pomiankowski, A. 1988. The evolution of female mate preferences for male genetic quality. Oxf. Surv. Evol. Biol. 5: 136 184.
75. Ramsey, J., 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.
76. Rantala, M.-J., and R. Kortet. 2003. Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol. J. Linn. Soc. 79: 503 510.
77. Rantala, M. J., R. Kortet, J. S. Kotiaho, A. Vainikka, and J. Suhonen. 2003. Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Funct. Ecol. 17: 534 540.
78. Rieseberg, L. H., A. Widmer, A. M. Arntz, and J. M. Burke. 2002. Directional selection is the primary cause of phenotypic diversification. Proc. Natl. Acad. Sci. USA 99: 12242 12245.
79. Ritchie, M. G. 2000. The inheritance of female preference functions in a mate recognition system. Proc. R. Soc. Lond. B 267: 327 332.
80. Ritchie, M. G., and S. D. F. Phillips. 1998. The genetics of sexual isolation. Pp. 291 308 in D. A. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, Oxford, U.K.
81. Ritchie, M. G., E. J. Halsey, and J. M. Gleason. 1999. Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim. Behav. 58: 649 657.
82. Ritchie, M. G., M. Saarikettu, S. Livingstone, and A. Hoikkala. 2001. Characterization of female preference functions for Drosophila montana courtship song and a test of the temperature coupling hypothesis. Evolution 55: 721 727.
83. Ruiz, A., and W. B. Heed. 1988. Host-plant specificity in the cactophilic Drosophila mulleri species complex. J. Anim. Ecol. 57: 237 249.
84. Ryan, M. J., and A. S. Rand. 1993. Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47: 647 657.
85. SAS Institute. 2004. SAS/STAT 9.1.2. SAS Institute, Inc: Cary, NC.
86. Shaw, K. L. 1996. Polygenic inheritance of a behavioral phenotype: interspecific genetics of song in the Hawaiian cricket genus Laupala. Evolution 50: 256 266.
87. Shaw, K. L., and Y. M. Parsons. 2002. Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am. Nat. 159: S61 S75.
88. Shorey, H. H. 1962. The nature of the sound produced by Drosophila melanogaster during courtship. Science 137: 677 678.
89. Spieth, H. T. 1952. Mating behavior within the genus Drosophila (Diptera). Bull. Am. Mus. Nat. Hist. 99: 395 474.
90. Starmer, W. T. 1982. Analysis of community structure of yeasts associated with the decaying stems of cactus. I. Stenocereus gummosus. Microb. Ecol. 8: 71 81.
91. Starmer, W. T., W. B. Heed, and E. S. Rockwood-Sluss. 1977. Extension of longevity in Drosophila mojavensis by environmental ethanol: differences between subraces. Proc. Natl. Acad. Sci. U S A 74: 387 391.
92. Staten, R., S. Dixon Schully, and M. A. F. Noor. 2004. A microsatellite linkage map of Drosophila mojavensis. BMC Genet. 5: 12.
93. Streelman, J. T., and P. D. Danley. 2003. The stages of vertebrate evolutionary radiation. Trends Ecol. Evol. 18: 126 131.
94. Tomaru, M., and Y. Oguma. 1994. Differences in courtship song in the species of the Drosophila auraria complex. Anim. Behav. 47: 133 140.
95. Via, S. 1990. Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. Annu. Rev. Entomol. 35: 421 446.
96. Via, S., R. Gomulkiewicz, G. D. Jong, S. E. Scheiner, C. D. Schlichting, and P. V. Tienderen. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10: 212 217.
97. Welch, A. M. 2003. Genetic benefits of a female mating preference in gray tree frogs are context dependent. Evolution 57: 883 893.
98. Welch, A. M., R. D. Semlitsch, and H. C. Gerhardt. 1998. Call duration as an indicator of genetic quality in male gray frogs. Science 280: 1928 1930.
99. Williams, M. A., A. G. Blouin, and M. A. F. Noor. 2001. Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences. Heredity 86: 68 77.
100. Zouros, E. 1974. Genic differentiation associated with the early stages of speciation in the mulleri subgroup of Drosophila. Evolution 27: 601 621.
101. Zouros, E., and C. J. d'Entremont. 1974. Sexual isolation among populations of Drosophila mojavensis race B. Drosophila Inf. Serv. 51: 112.
102. Zouros, E., and C. J. d'Entremont. 1980. Sexual isolation among populations of Drosophila mojavensis: response to pressure from a related species. Evolution 34: 421 430.