The processes that underlie mate choice have long fascinated biologists. With the advent of increasingly refined genetic tools, we are now beginning to understand the genetic basis of how males and females discriminate among potential mates. One aspect of mate discrimination of particular interest is that which isolates one species from another. As behavioral isolation is thought to be the first step in speciation, and females are choosy more often than males in this regard, identifying the genetic variants that influence interspecies female mate choice can enhance our understanding of the process of speciation. Here, we review the literature on female mate choice in the most widely used model system for studies of species isolation Drosophila. Although females appear to use the same traits for both within- and between-species female mate choice, there seems to be a different genetic basis underlying these choices. Interestingly, most genomic regions that cause females to reject heterospecific males fall within areas of low recombination. Likely, candidate genes are those that act within the auditory or olfactory system, or within areas of the brain that process these systems. 1. Introduction Sex has long been a popular topic of research among evolutionary biologists. Our personal fascination with the subject is related to the variation that is seen in sexual behavior. This includes the different roles that make up mating rituals, such as courtship traits or preference for the traits, and the variation of these behaviors observed both within and between species. Understanding the biological basis of mating behavior is not only interesting, it is also important for our understanding of evolution as it can shed light on how species boundaries are formed and maintained. Different mating behaviors of closely related species can act as an isolating barrier that stops gene flow between two interbreeding populations. This usually results from closely related species having diverse mating signals: one or both of the sexes fail to identify the other as a suitable mate [1–4]. For example, males of some species court conspecific females more often or with more vigor than heterospecific females [5] and females mate more readily with conspecific than heterospecific males [6, 7]. The impact of Drosophila in this area of research has been pronounced primarily because many obstacles can be bypassed in this system. First, the stereotypical mating behavior observed in this genus is relatively easy to score [8–10], there are genetic tools available to allow manipulation
References
[1]
M. W. Blows and R. A. Allan, “Levels of mate recognition within and between two Drosophila species and their hybrids,” American Naturalist, vol. 152, no. 6, pp. 826–837, 1998.
[2]
J. A. Coyne, “Genetics of sexual isolation in females of the Drosophila simulans species complex,” Genetical Research, vol. 60, no. 1, pp. 25–31, 1992.
[3]
M. Doi, M. Matsuda, M. Tomaru, H. Matsubayashi, and Y. Oguma, “A locus for female discrimination behavior causing sexual isolation in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 12, pp. 6714–6719, 2001.
[4]
B. Moulin, T. Aubin, and J. M. Jallon, “Why there is a one-way crossability between D. melanogaster and D. simulans? An ontogenic explanation,” Genetica, vol. 120, no. 1–3, pp. 285–292, 2004.
[5]
D. Nickel and A. Civetta, “An X chromosome effect responsible for asymmetric reproductive isolation between male Drosophila virilis and heterospecific females,” Genome, vol. 52, no. 1, pp. 49–56, 2009.
[6]
A. J. Moehring, J. Li, M. D. Schug et al., “Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana,” Genetics, vol. 167, no. 3, pp. 1265–1274, 2004.
[7]
A. J. Moehring, A. Llopart, S. Elwyn, J. A. Coyne, and T. F. C. Mackay, “The genetic basis of prezygotic reproductive isolation between Drosophila santomea and D. yakuba due to mating preference,” Genetics, vol. 173, no. 1, pp. 215–223, 2006.
[8]
J. C. Hall, “The mating of a fly,” Science, vol. 264, no. 5166, pp. 1702–1714, 1994.
[9]
R. J. Greenspan, “Understanding the genetic construction of behavior,” Scientific American, vol. 272, no. 4, pp. 74–79, 1995.
[10]
R. J. Greenspan and J. F. Ferveur, “Courtship in Drosophila,” Annual Review of Genetics, vol. 34, pp. 205–232, 2000.
[11]
K. A. Matthews, T. C. Kaufman, and W. M. Gelbart, “Research resources for Drosophila: the expanding universe,” Nature Reviews Genetics, vol. 6, no. 3, pp. 179–193, 2005.
[12]
P. G. Byrne and W. R. Rice, “Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster,” Proceedings of the Royal Society B, vol. 273, no. 1589, pp. 917–922, 2006.
[13]
J. A. Coyne, “Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 14, pp. 5464–5468, 1989.
[14]
T. Sakai and N. Ishida, “Circadian rhythms of female mating activity governed by clock genes in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 16, pp. 9221–9225, 2001.
[15]
T. Dobzhansky, “Speciation as a stage in evolutionary divergence,” American Naturalist, vol. 74, no. 753, pp. 312–321, 1940.
[16]
J. C. Uyeda, S. J. Arnold, P. A. Hohenlohe, and L. S. Mead, “Drift promotes speciation by sexual selection,” Evolution, vol. 63, no. 3, pp. 583–594, 2009.
[17]
P. Nanda and B. N. Singh, “Origin of sexual isolation in Drosophila ananassae due to founder effects,” Genetica, vol. 139, no. 6, pp. 779–787, 2011.
[18]
M. Turelli, N. H. Barton, and J. A. Coyne, “Theory and speciation,” Trends in Ecology and Evolution, vol. 16, no. 7, pp. 330–343, 2001.
[19]
J. A. Coyne and A. Orr, Speciation, Sinauer and Associates, Sunderland, UK, 2004.
[20]
J. M. Sobel, G. F. Chen, L. R. Watt, and D. W. Schemske, “The biology of speciation,” Evolution, vol. 64, no. 2, pp. 295–315, 2010.
[21]
P. Nanda and B. N. Singh, “Behavioural reproductive isolation and speciation in Drosophila,” Journal of Biosciences, vol. 37, no. 2, pp. 359–374, 2012.
[22]
M. A. Noor, “Speciation driven by natural selection in Drosophila,” Nature, vol. 375, no. 6533, pp. 674–675, 1995.
[23]
E. Zouros and C. J. d'Entremont, “Sexual isolation among populations of Drosophila mojavensis: response to pressure from a related species,” Evolution, vol. 34, no. 3, pp. 421–430, 1980.
[24]
A. R. Templeton, “Mechanisms of speciation—a population genetic approach,” Annual Review of Ecology, Evolution, and Systematics, vol. 12, pp. 23–48, 1981.
[25]
M. A. F. Noor, “Reinforcement and other consequences of sympatry,” Heredity, vol. 83, no. 5, pp. 503–508, 1999.
[26]
J. H. Jennings and W. J. Etges, “Species hybrids in the laboratory but not in nature: a reanalysis of premating isolation between Drosophila arizonae and D. mojavensis,” Evolution, vol. 64, no. 2, pp. 587–598, 2010.
[27]
H. D. Rundle, S. F. Chenoweth, P. Doughty, and M. W. Blows, “Divergent selection and the evolution of signal traits and mating preferences,” PLoS Biology, vol. 3, no. 11, article e368, 2005.
[28]
D. R. Matute, “Reinforcement can overcome gene flow during speciation in Drosophila,” Current Biology, vol. 20, no. 24, pp. 2229–2233, 2010.
[29]
E. M. Myers and W. A. Frankino, “Time in a bottle: the evolutionary fate of species discrimination in sibling Drosophila species,” PLoS ONE, vol. 7, no. 2, Article ID e31759, 2012.
[30]
R. Yukilevich, “Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila,” Evolution, vol. 66, no. 5, pp. 1430–1446, 2012.
[31]
R. J. Ayala, “Relative fitness of populations of Drosophila serrata and Drosophila birchii,” Genetics, vol. 51, pp. 527–544, 1965.
[32]
M. C. Carracedo, L. García-Florez, and E. San Miguel, “Sexual maturation in Drosophila melanogaster females and hybridization with D. simulans males: a study of inheritance modes,” Journal of Heredity, vol. 80, no. 2, pp. 157–158, 1989.
[33]
R. Pineiro, M. C. Carracedo, J. I. Izquierdo, and P. Casares, “Bidirectional selection for female receptivity in Drosophila melanogaster,” Behavior Genetics, vol. 23, no. 1, pp. 77–83, 1993.
[34]
J. I. Izquierdo, M. C. Carracedo, R. Pineiro, and P. Casares, “Response to selection for increased hybridization between Drosophila melanogaster females and D. simulans males,” Journal of Heredity, vol. 83, no. 2, pp. 100–104, 1992.
[35]
M. Laturney and A. J. Moehring, “Fine-scale genetic analysis of species-specific female preference in Drosophila simulans,” Journal of Evolutionary Biology, vol. 25, pp. 1718–1731, 2012.
[36]
K. Y. Kaneshiro, “Ethological isolation and phylogeny in the Planitibia subgroup of Hawaiian Drosophila,” Evolution, vol. 30, no. 4, pp. 740–745, 1976.
[37]
K. Y. Kaneshiro, “Sexual selection and direction of evolution in the biosystematics of Hawaiian Drosophilidae,” Annual Review of Entomology, vol. 28, pp. 161–178, 1983.
[38]
Y. K. Kim, M. Ruiz-Garcia, D. Alvarez, D. R. Phillips, and W. W. Anderson, “Sexual isolation between North American and Bogota strains of Drosophila pseudoobscura,” Behavior Genetics, vol. 42, no. 3, pp. 472–482, 2012.
[39]
J. Ringo, G. Sharon, and D. Segal, “Bacteria-induced sexual isolation in Drosophila,” Fly, vol. 5, no. 4, pp. 310–315, 2011.
[40]
J. A. Coyne and H. A. Orr, “Patterns of speciation in Drosophila revisited,” Evolution, vol. 51, no. 1, pp. 295–303, 1997.
[41]
A. J. Moehring and T. F. C. Mackay, “The quantitative genetic basis of male mating behavior in Drosophila melanogaster,” Genetics, vol. 167, no. 3, pp. 1249–1263, 2004.
[42]
R. R. H. Anholt and T. F. C. Mackay, “Quantitative genetic analyses of complex behaviours in Drosophila,” Nature Reviews Genetics, vol. 5, no. 11, pp. 838–849, 2004.
[43]
U. Klahre, A. Gurba, K. Hermann et al., “Pollinator choice in Petunia depends on two major genetic loci for floral scent production,” Current Biology, vol. 21, no. 9, pp. 730–739, 2011.
[44]
N. I. Morehouse and R. L. Rutowski, “In the eyes of the beholders: female choice and avian predation risk associated with an exaggerated male butterfly color,” American Naturalist, vol. 176, no. 6, pp. 768–784, 2010.
[45]
M. R. Kronforst, L. G. Young, D. D. Kapan, C. McNeely, R. J. O'Neill, and L. E. Gilbert, “Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 17, pp. 6575–6580, 2006.
[46]
M. E. Maan, O. Seehausen, L. S？derberg et al., “Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei,” Proceedings of the Royal Society B, vol. 271, no. 1556, pp. 2445–2452, 2004.
[47]
M. P. Haesler and O. Seehausen, “Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation,” Proceedings of the Royal Society B, vol. 272, no. 1560, pp. 237–245, 2005.
[48]
G. E. Carney, “A rapid genome-wide response to Drosophila melanogaster social interactions,” BMC Genomics, vol. 8, article 288, 2007.
[49]
E. A. Ruedi and K. A. Hughes, “Age, but not experience, affects courtship gene expression in male Drosophila melanogaster,” PLoS ONE, vol. 4, no. 7, Article ID e6150, 2009.
[50]
M. K. N. Lawniczak and D. J. Begun, “A genome-wide analysis of courting and mating responses in Drosophila melanogaster females,” Genome, vol. 47, no. 5, pp. 900–910, 2004.
[51]
T. F. C. Mackay, S. L. Heinsohn, R. F. Lyman, A. J. Moehring, T. J. Morgan, and S. M. Rollmann, “Genetics and genomics of Drosophila mating behavior,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 1, pp. 6622–6629, 2005.
[52]
R. Butlin and M. G. Ritchie, “Evolutionary biology: searching for speciation genes,” Nature, vol. 412, no. 6842, pp. 31–33, 2001.
[53]
C. P. Kyriacou, “Single gene mutations in Drosophila: what can they tell us about the evolution of sexual behaviour?” Genetica, vol. 116, no. 2-3, pp. 197–203, 2002.
[54]
D. Yamamoto and Y. Nakano, “Sexual behavior mutants revisited: molecular and cellular basis of Drosophila mating,” Cellular and Molecular Life Sciences, vol. 56, no. 7-8, pp. 634–646, 1999.
[55]
M. Tomaru, H. Yamada, and Y. Oguma, “Female mate recognition and sexual isolation depending on courtship song in Drosophila sechellia and its siblings,” Genes and Genetic Systems, vol. 79, no. 3, pp. 145–150, 2004.
[56]
J. M. Gleason, J. M. Jallon, J. D. Rouault, and M. G. Ritchie, “Quantitative trait loci for cuticular hydrocarbons associated with sexual isolation between Drosophila simulans and D. sechellia,” Genetics, vol. 171, no. 4, pp. 1789–1798, 2005.
[57]
D. A. Wheeler, C. P. Kyriacou, M. L. Greenacre et al., “Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster,” Science, vol. 251, no. 4997, pp. 1082–1085, 1991.
[58]
B. J. Dickson, “Wired for sex: the neurobiology of Drosophila mating decisions,” Science, vol. 322, no. 5903, pp. 904–909, 2008.
[59]
A. Civetta and E. J. F. Cantor, “The genetics of mating recognition between Drosophila simulans and D. sechellia,” Genetical Research, vol. 82, no. 2, pp. 117–126, 2003.
[60]
R. L. Davis, “Traces of Drosophila memeory,” Neuron, vol. 14, no. 1, pp. 8–19, 2011.
[61]
J. S. de Belle and M. Heisenberg, “Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies,” Science, vol. 263, no. 5147, pp. 692–695, 1994.
[62]
M. Balakireva, R. F. Stocker, N. Gendre, and J. F. Ferveur, “Voila, a new Drosophila courtship variant that affects the nervous system: behavioral, neural, and genetic characterization,” Journal of Neuroscience, vol. 18, no. 11, pp. 4335–4343, 1998.
[63]
K. M. C. O'Dell, J. D. Armstrong, M. Y. Yang, and K. Kalser, “Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments,” Neuron, vol. 15, no. 1, pp. 55–61, 1995.
[64]
W. S. Neckameyer, “Dopamine modulates female sexual receptivity in Drosophila melanogaster,” Journal of Neurogenetics, vol. 12, no. 2, pp. 101–114, 1998.
[65]
J. M. Gleason, “Mutations and natural genetic variation in the courtship song of Drosophila,” Behavior Genetics, vol. 35, no. 3, pp. 265–277, 2005.
[66]
C. P. Kyriacou and J. C. Hall, “Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 11 I, pp. 6729–6733, 1980.
[67]
M. G. Ritchie and C. P. Kyriacou, “Reproductive isolation and the period gene of Drosophila,” Molecular Ecology, vol. 3, no. 6, pp. 595–599, 1994.
[68]
T. Sakai and N. Ishida, “Time, love and species,” Neuroendocrinology Letters, vol. 22, no. 4, pp. 222–228, 2001.
[69]
J. D. Rouault, C. Marican, C. Wicker-Thomas, and J. M. Jallon, “Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans,” Genetica, vol. 120, no. 1–3, pp. 195–212, 2004.
[70]
J. F. Ferveur, “Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication,” Behavior Genetics, vol. 35, no. 3, pp. 279–295, 2005.
[71]
J. C. Billeter, J. Atallah, J. J. Krupp, J. G. Millar, and J. D. Levine, “Specialized cells tag sexual and species identity in Drosophila melanogaster,” Nature, vol. 461, no. 7266, pp. 987–991, 2009.
[72]
D. Scott, “Genetic variation for female mate discrimination in Drosophila melanogaster,” Evolution, vol. 48, no. 1, pp. 112–121, 1994.
[73]
M. D. Sharma, J. Hunt, and D. J. Hosken, “Antagonistic responses to natural and sexual selection and the sex-specific evolution of cuticular hydrocarbons in Drosophila simulans,” Evolution, vol. 66, no. 3, pp. 665–677, 2012.
[74]
J. M. Gleason, R. A. James, C. Wicker-Thomas, and M. G. Ritchie, “Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females,” Heredity, vol. 103, no. 5, pp. 416–424, 2009.
[75]
J. F. Ferveur, M. Cobb, H. Boukella, and J. M. Jallon, “World-wide variation in Drosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences,” Genetica, vol. 97, no. 1, pp. 73–80, 1996.
[76]
R. Dallerac, C. Labeur, J. M. Jallon, D. C. Knipple, W. L. Roelofs, and C. Wicker-Thomas, “A δ9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 17, pp. 9449–9454, 2000.
[77]
C. Wicker-Thomas and J. M. Jallon, “Control of female pheromones in Drosophila melanogaster by homeotic genes,” Genetical Research, vol. 78, no. 3, pp. 235–242, 2001.
[78]
C. Marican, L. Duportets, S. Birman, and J. M. Jallon, “Female-specific regulation of cuticular hydrocarbon biosynthesis by dopamine in Drosophila melanogaster,” Insect Biochemistry and Molecular Biology, vol. 34, no. 8, pp. 823–830, 2004.
[79]
J. F. Ferveur and J. M. Jallon, “Nerd, a locus on chromosome III, affects male reproductive behavior in Drosophila melanogaster,” Naturwissenschaften, vol. 80, no. 10, pp. 474–475, 1993.
[80]
J. F. Ferveur and J. M. Jallon, “Genetic control of male cuticular hydrocarbons in Drosophila melanogaster,” Genetical Research, vol. 67, no. 3, pp. 211–218, 1996.
[81]
J. M. Jallon, G. Lauge, L. Orssaud, and C. Antony, “Female pheromones in Drosophila melanogaster are controlled by the doublesex locus,” Genetics Research, vol. 51, no. 1, pp. 17–22, 1988.
[82]
J. A. Coyne, C. Wicker-Thomas, and J. M. Jallon, “A gene responsible for a cuticular hydrocarbon polymorphism in Drosophila melanogaster,” Genetical Research, vol. 73, no. 3, pp. 189–203, 1999.
[83]
M. G. Ritchie and M. A. Noor, “Evolutionary genetics: gene replacement and the genetics of speciation,” Heredity, vol. 93, no. 1, pp. 1–2, 2004.
[84]
M. A. F. Noor, K. L. Gratos, L. A. Bertucci, and J. Reiland, “Chromosomal inversions and the reproductive isolation of species,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 21, pp. 12084–12088, 2001.
[85]
M. C. Carracedo, R. Pineiro, and P. Casares, “Chromosomal substitution analysis of receptivity and sexual isolation in Drosophila melanogaster females,” Heredity, vol. 75, no. 5, pp. 541–546, 1995.
[86]
M. C. Carracedo, A. Suarez, A. Asenjo, and P. Casares, “Genetics of hybridization between Drosophila simulans females and D. melanogaster males,” Heredity, vol. 80, no. 1, pp. 17–24, 1998.
[87]
T. Uenoyama and Y. Inoue, “Genetic studies on premating isolation in Drosophila simulans. I. A D. simulans line highly crossable with D. melanogaster,” Japanese Journal of Genetics, vol. 70, no. 3, pp. 365–371, 1995.
[88]
Drosophila 12 Genomes Consortium, “Evolution of genes and genomes on the Drosophila phylogeny,” Nature, vol. 450, no. 7167, pp. 203–218, 2007.
[89]
S. Holtzman, D. Miller, R. Eisman, H. Kuwayama, T. Niimi, and T. Kaufman, “Transgenic tools for members of the genus Drosophila with sequenced genomes,” Fly, vol. 4, no. 4, pp. 349–362, 2010.
[90]
C. I. Wu, H. Hollocher, D. J. Begun, C. F. Aquadro, Y. Xu, and M. L. Wu, “Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 7, pp. 2519–2523, 1995.
[91]
H. Hollocher, C. T. Ting, M. L. Wu, and C. I. Wu, “Incipient speciation by sexual isolation in Drosophila melanogaster: extensive genetic divergence without reinforcement,” Genetics, vol. 147, no. 3, pp. 1191–1201, 1997.
[92]
C. T. Ting, A. Takahashi, and C. I. Wu, “Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 12, pp. 6709–6713, 2001.
[93]
R. I. Bailey, P. Innocenti, E. H. Morrow, U. Friberg, and A. Qvarnstr？m, “Female Drosophila melanogaster gene expression and mate choice: the X chromosome harbours candidate genes underlying sexual isolation,” PLoS ONE, vol. 6, no. 2, Article ID e17358, 2011.
[94]
A. Takahashi, S. C. Tsaur, J. A. Coyne, and C. I. Wu, “The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 7, pp. 3920–3925, 2001.
[95]
J. A. Coyne, “Genetics of differences in pheromonal hydrocarbons between Drosophila melanogaster and D. simulans,” Genetics, vol. 143, no. 1, pp. 353–364, 1996.
[96]
S. J. Macdonald and D. B. Goldstein, “A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia,” Genetics, vol. 153, no. 4, pp. 1683–1699, 1999.
[97]
J. A. Coyne, A. P. Crittenden, and K. Mah, “Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila,” Science, vol. 265, no. 5177, pp. 1461–1464, 1994.
[98]
J. A. Coyne, “Genetics of a difference in male cuticular hydrocarbons between two sibling species, Drosophila simulans and D. sechellia,” Genetics, vol. 143, no. 4, pp. 1689–1698, 1996.
[99]
J. M. Gleason and M. G. Ritchie, “Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes for intraspecific QTL?” Genetics, vol. 166, no. 3, pp. 1303–1311, 2004.
[100]
J. A. Coyne, “The genetics of an isolating mechanism between two sibling species of Drosophila,” Evolution, vol. 47, no. 3, pp. 778–788, 1993.
[101]
J. R. True, J. Liu, L. F. Stam, Z. B. Zeng, and C. C. Laurie, “Quantitative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana,” Evolution, vol. 51, no. 3, pp. 816–832, 1997.
[102]
Z. B. Zeng, J. Liu, L. F. Stam, C. H. Kao, J. M. Mercer, and C. C. Laurie, “Genetic architecture of a morphological shape difference between two Drosophila species,” Genetics, vol. 154, no. 1, pp. 299–310, 2000.
[103]
J. A. Coyne, “Genetics of sexual isolation in male hybrids of Drosophila simulans and D. mauritiana,” Genetical Research, vol. 68, no. 3, pp. 211–220, 1996.
[104]
J. A. Coyne and B. Charlesworth, “Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia,” Genetics, vol. 145, no. 4, pp. 1015–1030, 1997.
[105]
W. J. Etges, C. C. de Oliveira, E. Gragg, D. Ortíz-Barrientos, M. A. F. Noor, and M. G. Ritchie, “Genetics of incipient speciation in Drosophila mojavensis. I. Male courtship song, mating success, and genotype X environment interactions,” Evolution, vol. 61, no. 5, pp. 1106–1119, 2007.
[106]
E. Zouros, “The chromosomal basis of sexual isolation in two sibling species of Drosophila: D. arizonensis and D. mojavensis,” Genetics, vol. 97, no. 3-4, pp. 703–718, 1981.
[107]
A. R. Templeton, “Analysis of head shape differences between two interfertile species of Hawaiian Drosophila,” Evolution, vol. 31, no. 3, pp. 630–641, 1977.
[108]
F. C. Val, “Genetic analysis of the morphological differences between two interfertile species of Hawaiian Drosophila,” Evolution, vol. 31, no. 3, pp. 611–629, 1977.
[109]
D. Ortiz-Barrientos, B. A. Counterman, and M. A. F. Noor, “The genetics of speciation by reinforcement,” PLoS Biology, vol. 2, no. 12, article e416, 2004.
[110]
D. Ortíz-Barrientos and M. A. F. Noor, “Evolution: evidence for a one-allele assortative mating locus,” Science, vol. 310, no. 5753, article 1467, 2005.
[111]
M. A. F. Noor, “Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis,” Evolution, vol. 51, no. 3, pp. 809–815, 1997.
[112]
M. A. F. Noor, K. L. Grams, L. A. Bertucci, Y. Almendarez, J. Reiland, and K. R. Smith, “The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. Persimilis via backcross hybrid males,” Evolution, vol. 55, no. 3, pp. 512–521, 2001.
[113]
M. A. Williams, A. G. Blouin, and M. A. F. Noor, “Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences,” Heredity, vol. 86, no. 1, pp. 68–77, 2001.
[114]
M. A. F. Noor and J. A. Coyne, “Genetics of a difference in cuticular hydrocarbons between Drosophila pseudoobscura and D. persimilis,” Genetical Research, vol. 68, no. 2, pp. 117–123, 1996.
[115]
A. Hoikkala, S. P？？llysaho, J. Aspi, and J. Lumme, “Localization of genes affecting species differences in male courtship song between Drosophila virilis and D. littoralis,” Genetical Research, vol. 75, no. 1, pp. 37–45, 2000.
[116]
A. Hoikkala and J. Lumme, “Genetic control of the difference in male courtship sound between Drosophila virilis and D. lummei,” Behavior Genetics, vol. 14, no. 3, pp. 257–268, 1984.
[117]
J. O. Liimatainen and J. M. Jallon, “Genetic analysis of cuticular hydrocarbons and their effect on courtship in Drosophila virilis and D. lummei,” Behavior Genetics, vol. 37, no. 5, pp. 713–725, 2007.
[118]
T. R. Shirangi, H. D. Dufour, T. M. Williams, and S. B. Carroll, “Rapid evolution of sex pheromone-producing enzyme expression in Drosophila,” PLoS Biology, vol. 7, no. 8, Article ID e1000168, 2009.
[119]
W. J. Etges, C. C. de Oliveira, M. A. F. Noor, and M. G. Ritchie, “Genetics of incipient speciation in Drosophila mojavensis. III. Life-history divergence in allopatry and reproductive isolation,” Evolution, vol. 64, no. 12, pp. 3549–3569, 2010.
[120]
P. Nanda and B. N. Singh, “Effect of chromosome arrangements on mate recognition system leading to behavioral isolation in Drosophila ananassae,” Genetica, vol. 139, no. 2, pp. 273–279, 2011.
[121]
K. Sawamura, H. Zhi, K. Setoguchi et al., “Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines,” Genetica, vol. 133, no. 2, pp. 179–185, 2008.
[122]
H. Yamada, M. Matsuda, and Y. Oguma, “Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa,” Genetica, vol. 116, no. 2-3, pp. 225–237, 2002.
[123]
S. E. McGaugh and M. A. Noor, “Genomic impacts of chromosomal inversions in parapatric Drosophila species,” Philosophical Transactions of the Royal Society B, vol. 367, no. 1587, pp. 422–429, 2012.
[124]
C. V. Barnwell and M. A. F. Noor, “Failure to replicate two mate preference QTLs across multiple strains of Drosophila pseudoobscura,” Journal of Heredity, vol. 99, no. 6, pp. 653–656, 2008.
[125]
M. R. Servedio and M. A. F. Noor, “The role of reinforcement in speciation: theory and data,” Annual Review of Ecology, Evolution, and Systematics, vol. 34, pp. 339–364, 2003.
[126]
A. Llopart, S. Elwyn, D. Lachaise, and J. A. Coyne, “Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea,” Evolution, vol. 56, no. 11, pp. 2262–2277, 2002.
[127]
D. Lachaise, M. Harry, M. Solignac, F. Lemeunier, V. Benassi, and M. L. Cariou, “Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from S？o Tomé,” Proceedings of the Royal Society B, vol. 267, no. 1452, pp. 1487–1495, 2000.
[128]
J. A. Coyne, S. Y. Kim, A. S. Chang, D. Lachaise, and S. Elwyn, “Sexual isolation between two sibling species with overlapping ranges: Drosophila santomea and Drosophila yakuba,” Evolution, vol. 56, no. 12, pp. 2424–2434, 2002.
[129]
R. M. Kliman, P. Andolfatto, J. A. Coyne et al., “The population genetics of the origin and divergence of the Drosophila simulans complex species,” Genetics, vol. 156, no. 4, pp. 1913–1931, 2000.
[130]
L. Tsacas and J. David, “Drosophila mauritiana n. sp. du groupe melanogaster de l'ile Maurice,” Bulletin de la Societe Entomologique de France, vol. 79, pp. 42–46, 1974.
[131]
D. Wood, J. M. Ringo, and L. L. Johnson, “Analysis of courtship sequences of the hybrids between Drosophila melanogaster and Drosophila simulans,” Behavior Genetics, vol. 10, no. 5, pp. 459–466, 1980.
[132]
M. C. Carracedo, A. Asenjo, and P. Casares, “Genetics of Drosophila simulans male mating discrimination in crosses with D. melanogaster,” Heredity, vol. 91, no. 3, pp. 202–207, 2003.
[133]
M. C. Carracedo, A. Asenjo, and P. Casares, “Inheritance mode of Drosophila simulans female mating propensity with D. melanogaster males,” Journal of Heredity, vol. 89, no. 1, pp. 102–104, 1998.
[134]
J. A. Jamart, M. C. Carracedo, and P. Casares, “Sexual isolation between Drosophila melanogaster females and D. simulans males. Male mating propensities versus success in hybridization,” Experientia, vol. 49, no. 6-7, pp. 596–598, 1993.
[135]
M. C. Carracedo, C. Suarez, and P. Casares, “Sexual isolation between Drosophila melanogaster, D. simulans and D. mauritiana: sex and species specific discrimination,” Genetica, vol. 108, no. 2, pp. 155–162, 2000.
[136]
M. Kreitman and M. Aguade, “Genetic uniformity in two populations of Drosophila melanogaster as revealed by filter hybridization of four-nucleotide-recognizing restriction enzyme digests,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 10, pp. 3562–3566, 1986.
[137]
D. J. Begun and C. F. Aquadro, “African and North American populations of Drosophila melanogaster are very different at the DNA level,” Nature, vol. 365, no. 6446, pp. 548–550, 1993.
[138]
L. S. Stevison, K. B. Hoehn, and M. A. Noor, “Effects of inversions on within- and between-species recombination and divergence,” Genome Biology and Evolution, vol. 3, pp. 830–841, 2011.
[139]
J. L. Feder, R. Gejji, T. H. Q. Powell, and P. Nosil, “Adaptive chromosomal divergence driven by mixed geographic mode of evolution,” Evolution, vol. 65, no. 8, pp. 2157–2170, 2011.
[140]
D. B. Lowry and J. H. Willis, “A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation,” PLoS Biology, vol. 8, no. 9, Article ID e1000500, 2010.
