Abstract
The virilis group of Drosophila represents a relatively unexplored but potentially useful model to investigate the genetics of speciation. Good resolution of phylogenetic relationships and the ability to obtain fertile hybrid offspring make the group especially promising for analysis of genetic changes underlying reproductive isolation separate from hybrid sterility and inviability. Phylogenetic analyses reveal a close relationship between the sister species, Drosophila americana and D. novamexicana, yet excepting their contemporary allopatric distributions, factors that contribute to reproductive isolation between this species pair remain uncharacterized. A previous report has shown reduced progeny numbers in laboratory crosses between the two species, especially when female D. novamexicana are crossed with male D. americana. We show that the hatch rate of eggs produced from heterospecific matings is reduced relative to conspecific matings. Failure of eggs to hatch, and consequent reduction in hybrid progeny number, is caused by low fertilization success of heterospecific sperm, thus representing a postmating, prezygotic incompatibility. Following insemination, storage and motility of heterospecific sperm is visibly compromised in female D. novamexicana. Our results provide evidence for a mechanism of reproductive isolation that is seldom reported for Drosophila species, and indicate the rapid evolution of postmating, prezygotic reproductive barriers in allopatry.
Highlights
One of the main goals in recent studies of speciation has been to identify the underlying genetic components of reproductive isolation and the evolutionary forces that cause their divergence [1]
Consistent with results previously reported by Patterson and Stone [10], progeny numbers are reduced in interspecies crosses between D. americana and D. novamexicana relative to crosses within species (Table 1)
The number of progeny produced by female D. novamexicana mated to heterospecific males is only about 2% of the number produced by female D. novamexicana mated to conspecific males (Table 1; t = 20.0, d.f. = 48, P < 0.001)
Summary
One of the main goals in recent studies of speciation has been to identify the underlying genetic components of reproductive isolation and the evolutionary forces that cause their divergence [1]. In contrast to the ancestral arrangement of chromosome arms maintained by D. novamexicana, several derived inversions have been fixed, yet in each case both the ancestral and derived arrangements continue to segregate in D. americana [29] These chromosomal rearrangements with their associated sequence variants have the potential to influence patterns of genetic differentiation locally throughout the genomes of these species. Genomic regions are variably related between species, with shared chromosomal rearrangements having localized affects on relationships, but phylogenetic analysis of combined data from multiple genes successfully resolves reciprocally monophyletic clades of the sister species [25] Overall, these observations are consistent with a scenario wherein, following the initial peripatric split within the D. americana-D. novamexicana ancestral population, a much smaller population of D. novamexicana persisted west of the Rocky Mountains compared with the broadly distributed populations of D. americana to the east. Noncompetitive gametic isolation is the primary reproductive barrier that has evolved between these species
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