title: A combination of sexual and ecological divergence contributes to rearrangement spread during initial stages of speciation.
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 the dynamics of rearrangement evolution by studying how a rearrangement covaries with 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 more than 39% of the Z chromosome (encompassing up to ~10 megabases and ~300 genes) resides within a nonrecombining unit, including pheromone olfactory receptor genes and a major quantitative trait locus that contributes to ecotype differences (Pdd). Combining direct and indirect estimates of recombination suppression, we found that the rearrangement was occasionally present between sexually isolated strains (E vs. Z) and between divergent ecotypes (univoltine vs. bivoltine). However, it was only consistently present when populations differed in both sexual and ecological traits. Our results suggest that independent of the forces that drove the initial establishment of the rearrangement, a combination of sexual and ecological divergence is required for rearrangement spread during speciation.
authors.affiliation: Department of Biology, Tufts University, 200 Boston Ave. Ste. 4700, Medford, MA, 02155, USA.
authors.forename: Genevieve M
authors.identifier: http://orcid.org/0000-0001-6413-1403
authors.initials: GM
authors.lastname: Kozak
authors.affiliation: Department of Biology, Tufts University, 200 Boston Ave. Ste. 4700, Medford, MA, 02155, USA.|Harvard TH Chan School of Public Health, 677 Huntington Ave., Boston, MA, 02115, USA.
authors.forename: Crista B
authors.initials: CB
authors.lastname: Wadsworth
authors.affiliation: Department of Biology, Tufts University, 200 Boston Ave. Ste. 4700, Medford, MA, 02155, USA.
authors.forename: Shoshanna C
authors.initials: SC
authors.lastname: Kahne
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, 215 Tower Road, Ithaca, NY, 14853, USA.
authors.forename: Steven M
authors.initials: SM
authors.lastname: Bogdanowicz
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, 215 Tower Road, Ithaca, NY, 14853, USA.
authors.forename: Richard G
authors.initials: RG
authors.lastname: Harrison
authors.affiliation: Corn Insects and Crop Genetics Research Unit, USDA-ARS, Iowa State University, 103 Genetics Laboratory, Ames, IA, 50011, USA.
authors.forename: Brad S
authors.initials: BS
authors.lastname: Coates
authors.affiliation: Department of Biology, Tufts University, 200 Boston Ave. Ste. 4700, Medford, MA, 02155, USA.
authors.forename: Erik B
authors.initials: EB
authors.lastname: Dopman
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D002874:Chromosome Mapping; D060146:Ecotype; D005260:Female; D015321:Gene Rearrangement; D049810:Genetic Speciation; D005828:Genetics, Population; D008297:Male; D009036:Moths / Q000235:genetics*; D009656:North America; D010375:Pedigree; D040641:Quantitative Trait Loci; D011995:Recombination, Genetic; D012621:Seasons; D012724:Sex Attractants / Q000235:genetics; D061350:Sympatry
chemical_list: D012724:Sex Attractants
keywords: assortative mating; chromosomal rearrangements; ecological speciation; inversions; pheromone; reproductive isolation