Speciation driven by ancestrally polymorphic chromosomal inversions

Abstract

AbstractChromosomal inversions may play a central role in speciation given their ability to reduce recombination and therefore genetic exchange at parts of the genome between diverging populations. We analysed long- and short-read whole-genome data from sympatric and allopatric populations of twoDrosophila virilisgroup species,D. montanaandD. flavomontana, to understand how inversions have contributed to their divergence. We identified three large alternatively fixed inversions on the X chromosome and one on each of the autosomes 4 and 5. A comparison of demographic models estimated for inverted and non-inverted (colinear) chromosomal regions suggest that these inversions arose before the time of the species split. We detected low rate of interspecific gene flow (introgression) fromD. montanatoD. flavomontana, which was further reduced inside inversions and was lower in allopatric than in sympatric populations. Together, these results suggest that the inversions were already present in the common ancestral population, and that gene exchange between the sister taxa was reduced within inversions both before and after the onset of species divergence. Such ancestrally polymorphic inversions may act as drivers of speciation by allowing the accumulation of genetic divergence and incompatibilities inside inversions, while gene exchange at colinear regions continues until the evolving reproductive barriers complete speciation. The overlapping X inversions are particularly good candidates for driving the speciation process ofD. montanaandD. flavomontana, since the strongest genetic incompatibilities detected in a study of experimental introgression reside within these inversions and prevent introgression between the species.