Rapid sexual and genomic isolation in sympatricDrosophilawithout reproductive character displacement

Abstract

The rapid evolution of sexual isolation in sympatry has long been associated with reinforcement (i.e., selection to avoid maladaptive hybridization). However, there are many species pairs in sympatry that have evolved rapid sexual isolation without known costs to hybridization. A major unresolved question is what evolutionary processes are involved in driving rapid speciation in such cases. Here, we focus on one such system; the Drosophila athabasca species complex, which is composed of three partially sympatric and interfertile semispecies: WN, EA, and EB. To study speciation in this species complex, we assayed sexual and genomic isolation within and between these semispecies in both sympatric and allopatric populations. First, we found no evidence of reproductive character displacement (RCD) in sympatric zones compared to distant allopatry. Instead, semispecies were virtually completely sexually isolated from each other across their entire ranges. Moreover, using spatial approaches and coalescent demographic simulations, we detected either zero or only weak heterospecific gene flow in sympatry. In contrast, within each semispecies we found only random mating and little population genetic structure, except between highly geographically distant populations. Finally, we determined that speciation in this system is at least an order of magnitude older than previously assumed, with WN diverging first, around 200K years ago, and EA and EB diverging 100K years ago. In total, these results suggest that these semispecies should be given full species status and we adopt new nomenclature: WN—D. athabasca, EA—D. mahican, and EB—D. lenape. While the lack of RCD in sympatry and interfertility do not support reinforcement, we discuss what additional evidence is needed to further decipher the mechanisms that caused rapid speciation in this species complex.

The evolution of male and female mating preferences inDrosophilaspeciation*

“…We did not use "choice tests" that have a female with two different types of males, as this would have increased the difficulty of the study. However, when both no-choice and female-choice tests were performed on the same system, they have shown consistent results, as exemplified in the D. melanogaster subgroup (Wood and Ringo 1980;Robertson 1988;Wu et al 1995) and in the D. athabasca species complex (Yukilevich et al 2016(Yukilevich et al , 2018. This supports the conclusions of a recent metanalysis that found no difference in mating preferences between interspecific no-choice versus choice designs across diverse taxa, including Drosophila (Dougherty and Shuker 2014).…”

“…) and in the D. athabasca species complex (Yukilevich et al. , ). This supports the conclusions of a recent metanalysis that found no difference in mating preferences between interspecific no‐choice versus choice designs across diverse taxa, including Drosophila (Dougherty and Shuker ).…”

Divergence of a speciation trait through artificial selection: Insights into constraints, by‐product effects and sexual isolation

“…Our results also showed that selecting on IPI had no effect on morphology, copulation duration, courtship intensity and courtship latency or fecundity. This is especially interesting because species in the D. athabasca complex have diverged in many of these traits (Chang & Miller, 1978;Miller, 1958;Miller et al, 1975;Patty, 1975;Yukilevich et al, 2016Yukilevich et al, , 2018. For instance, D. athabasca (WN) have much longer copulation durations and are on average larger and darker compared with D. mahican (EA).…”

“…To understand the mechanisms of diversification of secondary sexual characteristics, it is advantageous to study young species pairs. Here, we focused on the rapidly evolving Drosophila athabasca species complex, which is a member of the affinis subgroup in the obscura group (Miller, 1958), composed of three incipient species, recently renamed as D. athabasca (WN), D. mahican (EA) and D. lenape (EB; Yukilevich et al, 2018). The latest estimates suggest that D. athabasca diverged about 200 000 years ago, whereas D. mahican and D. lenape diverged only 100 000 years ago (Yukilevich et al, 2018; but see Ford & Aquadro, 1996; Wong‐Miller et al, 2017 for much younger divergence times).…”

“…Based on their different geographical ranges, they appear to have adapted to different climatic environments, but still produce fertile and viable hybrids (Miller & Westphal, 1967; R. Yukilevich unpublished data). These incipient species have also diverged in body pigment, copulation duration, cuticular hydrocarbons, chromosomal inversions, female mating preferences and male courtship songs, resulting in near‐complete sexual isolation (Chang & Miller, 1978; Miller, 1958; Miller et al, 1975; Novitski, 1946; Yukilevich et al, 2016, 2018). Because females primarily target divergent male courtship songs in sexual discrimination between D. athabasca and D. mahican , male courtship songs represent a veritable ‘speciation phenotype’ (Yukilevich et al, 2016).…”