Fine-scale geographic patterns of gene flow and reproductive character displacement in Drosophila subquinaria and Drosophila recens

Abstract

When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species Drosophila subquinaria and Drosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine-scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. Within D. subquinaria, reinforcement is extremely effective: we find variation in mate discrimination both against D. recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression from D. recens. In D. recens, we do not find evidence for increased mate discrimination in sympatry, even where D. recens is rare, consistent with substantial gene flow throughout the species' range. Finally, we find that introgression between species is asymmetric, with more from D. recens into D. subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement within D. subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations.

Keywords: hybridization; introgression; reproductive character displacement; speciation.

Figure 1.

Map of population locations used in this study and the proportion of each species found at each location. D. recens is indicated by yellow and the color of D. subquinaria is by region, as indicated in the legend. Panel B is the inset of Panel A. Locations are indicated by their abbreviation in Table 1. The region of sympatry between the two species extends east into Manitoba, but we did not sample populations in this province.

Figure 2.

Population differentiation in D. recens. A) Structure analysis with K=2 clusters, and B) scatterplot of individuals on the first two discriminant functions of DAPC. Colors are arranged by geographic region and population, with abbreviations and locations as in Table 1 and Figure 1. Within each geographic region populations are arranged by approximate location west to east.

Figure 3.

Population differentiation in D. subquinaria. A) Structure analysis with K=2 clusters, and B) scatterplot of individuals on the first two discriminant functions of DAPC. Colors are arranged by geographic region and population, with abbreviations and locations as in Table 1 and Figure 1. Within each geographic region populations are arranged by approximate location west to east.

Figure 4.

Population structure using all samples of both D. subquinaria and D. recens. A) Structure analysis with K=2 clusters, and B) scatterplot of individuals on the first two discriminant functions of DAPC. Colors are arranged by species and geographic region, as in Table 1 and Figure 1. Within each geographic region samples are arranged by population location from west to east.

Figure 5.

Mating rate between D. recens females and D. subquinaria males. D. recens strains are listed by geographic region with respect to overlap with D. subquinaria, as in Table 1. Each dot is the proportion of pairs that mated from a single line. The names of the two lines with the highest mating rate are labeled.

Figure 6.

Mating rates of D. subquinaria females by geographic region with A) D. recens males and B) D. subquinaria coastal allopatric males. This figure includes data from this study (sympatric west) and Bewick and Dyer 2014 (allopatric and sympatric east). Each dot is the proportion of pairs that mated from a line, and are arranged by geographic region as described in Table 1. The dotted lines at the top of each panel indicate regions that are significantly different from each other (P < 0.05); see text for details.

Figure 7.

Clines in D. subquinaria inferred using HZAR. The yellow cline indicates the species composition (i.e., the fraction of D. subquinaria collected in a location), the pink cline indicates 1- admixture with D. recens (i.e. the fraction of ‘subquinaria’ from the Structure analysis of both species), the light blue cline indicates admixture among populations of D. subquinaria (i.e., the fraction of the ‘western’ cluster from the Structure analysis with D. subquinaria only), the red cline indicates mating rate with D. recens males, and the dark blue cline indicates mating rate with coastal allopatric D. subquinaria males. The vertical dotted line represents the relative location of the continental divide, and 0 is positioned at the westernmost population of Portland, OR. The shaded region of each cline indicates the 2-unit confidence interval.