Asymmetrical sexual isolation but no postmating isolation between the closely related species Drosophila suboccidentalis and Drosophila occidentalis

Abstract

Background: During the speciation process several types of isolating barriers can arise that limit gene flow between diverging populations. Studying recently isolated species can inform our understanding of how and when these barriers arise, and which barriers may be most important to limiting gene flow. Here we focus on Drosophila suboccidentalis and D. occidentalis, which are closely related mushroom-feeding species that inhabit western North America and are not known to overlap in geographic range. We investigate patterns of reproductive isolation between these species, including premating, postmating prezygotic, and postzygotic barriers to gene flow.

Results: Using flies that originate from a single population of each species, we find that the strength of premating sexual isolation between these species is asymmetric: while D. occidentalis females mate with D. suboccidentalis males at a reduced but moderate rate, D. suboccidentalis females discriminate strongly against mating with D. occidentalis males. Female hybrids will mate at high rates with males of either species, indicating that this discrimination has a recessive genetic basis. Hybrid males are accepted by females of both species. We do not find evidence for postmating prezygotic or postzygotic isolating barriers, as females use the sperm of heterospecific males and both male and female hybrids are fully fertile.

Conclusions: Premating isolation is substantial but incomplete, and appears to be the primary form of reproductive isolation between these species. If these species do hybridize, the lack of postzygotic barriers may allow for gene flow between them. Given that these species are recently diverged and are not known to be sympatric, the level of premating isolation is relatively strong given the lack of intrinsic postzygotic isolation. Further work is necessary to characterize the geographic and genetic variation in reproductive isolating barriers, as well as to determine the factors that drive reproductive isolation and the consequences that isolating barriers as well as geographic isolation have had on patterns of gene flow between these species.

Figure 1

Pure species mating rates. Mating rates within and between species in no-choice trials. Error bars indicate the binomial 95% confidence intervals. “Subo” refers to D. suboccidentalis and “Occ” refers to D. occidentalis. Ninety-fine trials were completed for each type.

Figure 2

Mating rates of crosses involving hybrids. Mating rates of hybrids relative to pure species crosses in no-choice mate trials. Error bars are the 95% binomial confidence intervals, and the sample size is indicated within each bar. “Subo” refers to D. suboccidentalis, “Occ” refers to D. occidentalis, “F1(OxS)” are F1 hybrids from a D. occidentalis female, and “F1(SxO)” are F1 hybrids from a D. suboccidentalis female.

Figure 3

Female egg production. Female egg production after mating with conspecific or heterospecific males. Error bars represent standard errors, and the sample size of each type is shown within bar. “Subo” refers to D. suboccidentalis, “Occ” refers to D. occidentalis, and F1 hybrids combine the results from both reciprocal crosses.

Figure 4

Female progeny production. Number of progeny produced by pure species females after conspecific or heterospecific matings. Bars indicate standard errors, and numbers within the bars are sample sizes. “Subo” refers to a D. suboccidentalis and “Occ” refers to D. occidentalis.

Figure 5

Male progeny production. Offspring production of hybrid males relative to pure species and heterospecific crosses. Error bars indicate standard errors, and the numbers within the bars are the sample sizes. “Subo” refers to D. suboccidentalis, “Occ” refers to D. occidentalis, “F1(SxO)” are F1 hybrids from a D. suboccidentalis female, and “F1(OxS)” are F1 hybrids from a D. occidentalis female.