A combination of sexual and ecological divergence contributes to the spread of a chromosomal rearrangement during initial stages of speciation

Authors: KOZAK, GENNY - Tufts University; WADSWORTH, CHRISTA - Harvard University; KAHNE, SHOSHANNA - Tufts University; BOGDANOWICZ, STEVEN - Cornell University; HARRISON, RICHARD - Cornell University; Coates, Brad; DOPMAN, ERIK - Tufts University

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/10/2017
Publication Date: 4/17/2017
Citation: Kozak, G.M., Wadsworth, C.B., Kahne, S.C., Bogdanowicz, S.M., Harrison, R.G., Coates, B.S., Dopman, E. 2017. A combination of sexual and ecological divergence contributes to the spread of a chromosomal rearrangement during initial stages of speciation. Molecular Ecology. 26(9):2331-2347. doi:10.1111/mec.14036.

Interpretive Summary: The genetic basis by which pest insect populations adapt new environmental conditions, or changes the way in which they mate and reproduce remain largely unknown. An ARS scientist in collaboration with university collaborators identified a large chromosomal region of the European corn borer (ECB) that shows an inverted arrangement of genes, and that this inversion is at higher frequency among ECB populations that differ in both the number of mating generations per year and the pheromone used in attraction of mates. Since the inversion is at high frequency prior to speciation, the results of this study show that major chromosomal changes can contribute to local adaptations and may influence the eventual formation of unique species. These data are important for government and university researchers interested in defining cryptic species and understanding genome-level changes that contribute to the formation of species.

Technical Abstract: Chromosomal rearrangements between sympatric species often contain multiple loci contributing to assortative mating, local adaptation, and hybrid sterility. When and how these associations arise during the process of speciation remains a subject of debate. Here, we address the relative roles of local adaptation and assortative mating on evolution of a species by studying the covariance between chromosomal rearrangements and sexual and ecological trait divergence within a species. Previously, a chromosomal rearrangement that suppresses recombination on the Z (sex) chromosome was identified in European corn borer moths (Ostrinia nubilalis). We further characterize this recombination suppressor and explore its association with variation in sex pheromone communication and seasonal ecological adaptation in pairs of populations that are divergent in one or both of these characteristics. Direct estimates of recombination suppression in pedigree mapping families indicated that at least 47% of the Z chromosome (~10 megabases and ~ 300 genes) resides within a non-recombining unit, including pheromone olfactory receptor (OR) genes, as well as a major quantitative trait locus (QTL) that contributes to ecotype differences (Pdd). Combining pedigree data with indirect estimates of recombination suppression from population genomic data, we found that the rearrangement was present in all populations but at highest frequency when populations differed in both pheromone preference and ecotype. Our results suggest that sexual or ecological divergence alone does not drive the persistence of chromosomal rearrangements, but instead a combination of both factors appear influence the selection for an increase in the frequency of the rearrangement spread during the initial stages of species formation.