Many studies have demonstrated the rapid diversification of reproductive genes that function after mating but before fertilization. This process might lead to the evolution of postmating, prezygotic barriers between species. Here, I investigate the phenotypic and genetic basis of postmating, prezygotic isolation between two closely related species of Drosophila,
Drosophila virilis and
D. americana. I show that a strong barrier to interspecific fertilization results in a 99% reduction in progeny production. A genetic interaction among maternal and paternal alleles at only a few loci prevents the fertilization of
D. virilis females by
D. americana males. These loci are autosomal and isolation acts recessively; the fertilization incompatibility is caused by at least two loci in the maternal
D. virilis parent in combination with at least three loci in the paternal
D. americana parent. These findings, together with results from classical experiments, suggest that male–female coevolution within
D. americana may have driven postmating, prezygotic isolation between species.AN understanding of speciation requires insight into the origins and mechanisms of reproductive isolation. Divergent selection on traits that facilitate mating or fertilization might eventually lead to incompatibilities between males and females of incipient species. In animals, it has long been recognized that sexual selection can promote the evolution of specialized courtship rituals or elaborate phenotypic displays to attract mates (
Darwin 1871). Similarly, sexual selection can be a powerful evolutionary force during or after mating by affecting the many biochemical, physiological, and morphological mechanisms involved in fertilization (
Eberhard 1996). Postmating reproductive traits might also be subject to sexually antagonistic coevolution, whereby a difference in the reproductive interests of males and females leads to an evolutionary arms race between the sexes (
Rice 1996). Just as divergent sexual selection on mate signals and preferences might give rise to premating (sexual) isolation (reviewed in
Ritchie 2007), postcopulatory sexual selection and sexual conflict might promote the evolution of postmating barriers to fertilization or hybrid incompatibilities (
Howard 1999;
Wu and Davis 1993). Indeed, these evolutionary forces have apparently led to competitive gametic isolation (
Price 1997;
Price et al. 2000;
Fishman et al. 2008) and sperm–egg incompatibilities (
Galindo et al. 2003). Moreover, because sexual selection and antagonistic coevolution can act rapidly (
Fisher 1930;
Rice 1996), they might be particularly important in the early stages of speciation.In diverse animal taxa, sexual selection and/or sexual conflict are thought to drive rapid evolution of a variety of postmating reproductive traits, including male genital morphology (
Eberhard 1996), length of sperm and female sperm-storage organs (
Pitnick et al. 1997;
Miller and Pitnick 2002), ejaculate composition (
e.g.,
Swanson et al. 2001a;
Dorus et al. 2004), female reproductive tract proteins (
e.g.,
Lawniczak and Begun 2007;
Kelleher et al. 2007), and gamete recognition molecules (
e.g.,
Wyckoff et al. 2000;
Swanson et al. 2001b). In recent years, many studies have also documented strong signatures of positive selection in the rapid evolution of reproductive genes (
e.g.,
Haerty et al. 2007;
Turner et al. 2008; reviewed in
Swanson and Vacquier 2002;
Clark et al. 2006). For internally fertilizing species, coevolution between the female reproductive tract and the male ejaculate is particularly dynamic (
Pitnick et al. 2007). For example, in Drosophila, hundreds of nonsperm seminal fluid proteins are transferred during mating, including many fast-evolving accessory gland proteins (ACPs) (
Swanson et al. 2001a;
Wagstaff and Begun 2005). As expected, there is evidence for coordinated evolution of female reproductive tract genes, which also show elevated rates of evolution in Drosophila (
Panhuis and Swanson 2006;
Prokupek et al. 2008). But what are the consequences of such rapid rates of diversification? How many of these fast-evolving reproductive genes contribute to isolating barriers? Major progress toward addressing these questions would require identifying and characterizing individual loci that cause postmating, prezygotic isolation.A large body of classical work suggests that the
Drosophila virilis species group might represent an ideal model for studying the genetics of reproductive isolation (
Patterson and Stone 1952); and importantly, the
D. virilis genome sequence is now available. There is also evidence that postmating, prezygotic isolation may be significant among
D. virilis and the closely related North American species,
D. americana and
D. novamexicana.
Patterson et al. (1942) describe reproductive isolation due to “gamete mortality” in reciprocal crosses between
D. virilis and
D. americana. In later studies, these authors discovered that very few eggs from interspecific crosses become fertilized or hatch and speculate that sperm become “immobilized in the reproductive tract of the alien female” (
Patterson and Stone 1952). Moreover, a recent study has found a similar problem with fertilization in crosses between
D. americana and
D. novamexicana (Y. A
hmed and B. M
cA
llister, personal communication). Consistent with the evolution of these interspecific barriers, male and female reproductive tract proteins have been shown to evolve rapidly in the
D. virilis species group (
Civetta and Singh 1995;
Haerty et al. 2007). In addition, females of both
D. virilis and
D. americana produce a large opaque vaginal mass in response to mating (the “insemination reaction”;
Wheeler 1947), which almost certainly reflects an evolutionary history of interaction between the female reproductive tract and male ejaculate (
Knowles and Markow 2001).Despite the potential importance of postmating, prezygotic isolation in
D. virilis group divergence, almost nothing is known about its genetic architecture. On the basis of the results from their crosses between
D. virilis and
D. americana,
Patterson et al. (1942) infer that postmating isolation involves recessive autosomal genes. However, their experiments often cannot distinguish between the effects of the apparent fertilization incompatibility and premating isolation, the latter also being strong between
D. americana females and
D. virilis males (
Stalker 1942). Their genetic mapping studies were also crude.In this study, I have two main objectives. First, I characterize the phenotypic basis of postmating isolation between
D. virilis and
D. americana. To do so, I perform a series of crosses within and between species. I find that low F
1 hybrid production between
D. virilis and
D. americana is due primarily to a reduction in interspecific fertilization; females presented with heterospecific males almost always become inseminated, but very few eggs are fertilized. Second, I perform a detailed genetic analysis of the fertilization incompatibility between
D. virilis females and
D. americana males. Using the
D. virilis genome assembly, I developed molecular markers targeted to genomic regions of interest for high-resolution genetic mapping of both the maternal and paternal components of isolation. This study is a first step toward understanding the genetic and evolutionary mechanisms of postmating, prezygotic reproductive isolation in Drosophila.
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