Abstract
Understanding the role of chromosomal inversions in speciation is a fundamental problem in evolutionary genetics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in Drosophila persimilis and D. pseudoobscura. We provide a solution to the puzzling origins of the selfish Sex-Ratio arrangement in D. persimilis and uncover surprising patterns of phylogenetic discordance on this chromosome. These patterns show that, contrary to widely held views, all fixed chromosomal inversions between D. persimilis and D. pseudoobscura were already present in their ancestral population long before the species split. Our results suggest that patterns of higher genomic divergence and an association of reproductive isolation genes with chromosomal inversions may be a direct consequence of incomplete lineage sorting of ancestral polymorphisms. These findings force a reconsideration of the role of chromosomal inversions in speciation, not as protectors of existing hybrid incompatibilities, but as fertile grounds for their formation.
Highlights
Chromosomal inversions are structural rearrangements where the linear gene order is reversed
Studies on chromosomal inversions and reproductive isolation between Drosophila persimilis and D. pseudoobscura have played a profound role in shaping our understanding of inversions, speciation and selfish chromosomes
We reconstruct the evolutionary histories of chromosomal inversions in D. persimilis and D. pseudoobscura to show that, contrary to widely accepted ideas, these inversions existed as polymorphisms in the ancestor of both species before their initial split
Summary
Chromosomal inversions are structural rearrangements where the linear gene order is reversed. In crosses between two species that differ by one or more inversions, the resulting hybrids can experience meiotic chromosome pairing problems and may, become sterile. In a number of plant species, direct experimental evidence has cemented the role of chromosomal rearrangements in the evolution of reproductive isolation through the reduced fertility in heterokaryotic hybrids [1,4,5,6]. Classic studies in hybrids between Drosophila persimilis and D. pseudoobscura have shown that chromosomal inversions do not play a direct role in causing hybrid sterility in animal species [2,4]. There is clear evidence for genic incompatibilities as the cause hybrid sterility in many cases, and the idea that chromosomal inversions may play a role in animal speciation fell out of favor [2,4]. Two new empirical observations regarding the patterns of reproductive isolation and genetic divergence in D. persimilis and D. pseudoobscura are key to these developments: i) the fixed chromosomal inversions between these species display higher genetic divergence than collinear regions of the genome, and ii) most genes that contribute to reproductive isolation between these species are located among the fixed chromosomal inversion differences [7,8,9,10,11,12]
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