Divergence Between the Drosophila pseudoobscura and D. persimilis Genome Sequences in Relation to Chromosomal Inversions

Abstract

As whole-genome sequence assemblies accumulate, a challenge is to determine how these can be used to address fundamental evolutionary questions, such as inferring the process of speciation. Here, we use the sequence assemblies of Drosophila pseudoobscura and D. persimilis to test hypotheses regarding divergence with gene flow. We observe low differentiation between the two genome sequences in pericentromeric and peritelomeric regions. We interpret this result as primarily a remnant of the correlation between levels of variation and local recombination rate observed within populations. However, we also observe lower differentiation far from the fixed chromosomal inversions distinguishing these species and greater differentiation within and near these inversions. This finding is consistent with models suggesting that chromosomal inversions facilitate species divergence despite interspecies gene flow. We also document heterogeneity among the inverted regions in their degree of differentiation, suggesting temporal differences in the origin of each inverted region consistent with the inversions arising during a process of divergence with gene flow. While this study provides insights into the speciation process using two singlegenome sequences, it was informed by lower throughput but more rigorous examinations of polymorphism and divergence. This reliance highlights the need for complementary genomic and population genetic approaches for tackling fundamental evolutionary questions such as speciation.

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

“…2011), and because they are a parallel case to that of D. pseudoobscura and D. persimilis , where inversions do appear to maintain the species barrier (Noor et al. 2007). Comparisons between sympatric and allopatric populations of the two Heliconius species have shown that almost a third of the genome is admixed in sympatry and that hybridization has been ongoing for a long time (Martin et al.…”

“…2007; Noor et al. 2007), where major fixed inversions occur on most chromosomes. Although H. melpomene and H. cydno have similarly divergent genomes overall compared to the Drosophila species pair, we do not find evidence for a similar role for inversions in maintaining the species barrier.…”

“…2007; Noor et al. 2007), genome differentiation is greater within and near inversions (Noor et al. 2007; McGaugh and Noor 2012) and sterility factors are associated with inversions in a sympatric species pair, but with collinear regions in an allopatric pair (Brown et al.…”

Genomic impacts of chromosomal inversions in parapatricDrosophilaspecies

“…Chromosomal rearrangements such as inversions (an orientation reversal of a piece of DNA within a single chromosome) impact species divergence by reducing recombination in heterokaryotypes [2,[4][5][6]. For paracentric inversions, which do not span a centromere, a single meiotic recombination event between heterokaryotypes results in acentric and dicentric products-both of which do not produce viable gametes (electronic supplementary material, figure S1).…”

“…This suppressed effective recombination between heterokaryotypes of paracentric inversions may facilitate speciation by protecting locally adapted alleles inside the inversions from gene flow with other populations, allowing further divergence between two karyotypes (reviewed in earlier studies [9,10]). While theoretical [11 -14] and empirical [15 -21] support for this hypothesis exists, the maintenance of genomic divergence-within inversions over long time periods (many hundreds of thousands of generations), and the shape of elevated divergence-within inversions have been less explored empirically (but see [2][3][4][5]). …”