Abstract

In nature, closely related species may hybridize while still retaining their distinctive identities. Chromosomal regions that experience reduced recombination in hybrids, such as within inversions, have been hypothesized to contribute to the maintenance of species integrity. Here, we examine genomic sequences from closely related fruit fly taxa of the Drosophila pseudoobscura subgroup to reconstruct their evolutionary histories and past patterns of genic exchange. Partial genomic assemblies were generated from two subspecies of Drosophila pseudoobscura (D. ps.) and an outgroup species, D. miranda. These new assemblies were compared to available assemblies of D. ps. pseudoobscura and D. persimilis, two species with overlapping ranges in western North America. Within inverted regions, nucleotide divergence among each pair of the three species is comparable, whereas divergence between D. ps. pseudoobscura and D. persimilis in non-inverted regions is much lower and closer to levels of intraspecific variation. Using molecular markers flanking each of the major chromosomal inversions, we identify strong crossover suppression in F1 hybrids extending over 2 megabase pairs (Mbp) beyond the inversion breakpoints. These regions of crossover suppression also exhibit the high nucleotide divergence associated with inverted regions. Finally, by comparison to a geographically isolated subspecies, D. ps. bogotana, our results suggest that autosomal gene exchange between the North American species, D. ps. pseudoobscura and D. persimilis, occurred since the split of the subspecies, likely within the last 200,000 years. We conclude that chromosomal rearrangements have been vital to the ongoing persistence of these species despite recent hybridization. Our study serves as a proof-of-principle on how whole genome sequencing can be applied to formulate and test hypotheses about species formation in lesser-known non-model systems.

Highlights

  • One of the most significant empirical insights in evolutionary biology is that a large number of species naturally hybridize with close relatives [see reviews in 1,2], and these species pairs often exchange genetic material (‘‘introgression’’)

  • We only scored positions for which aligned sequences were available for all four taxa (Table S2), eliminating the possibility that a particular region of high or low divergence would be represented in some estimates but not others

  • Nucleotide polymorphism estimated within D. ps. pseudoobscura was confirmed to be in the same range as that observed in polymorphism studies of focal genomic regions of this species [18]

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Summary

Introduction

One of the most significant empirical insights in evolutionary biology is that a large number of species naturally hybridize with close relatives [see reviews in 1,2], and these species pairs often exchange genetic material (‘‘introgression’’). While introgression may homogenize parts of genomes, regions of low recombination in hybrids, such as those within chromosomal inversions, maintain their distinction despite the influx of foreign alleles in collinear regions. This pattern of localized differentiation should be strong if regions of low recombination harbor loci with divergently selected alleles or alleles conferring reproductive isolation. This hypothesis has been difficult to test rigorously on a genome-wide scale

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