Rapid neo-sex chromosome evolution and incipient speciation in a major forest pest

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Abstract

Genome evolution is predicted to be rapid following the establishment of new (neo) sex chromosomes, but it is not known if neo-sex chromosome evolution plays an important role in speciation. Here we combine extensive crossing experiments with population and functional genomic data to examine neo-XY chromosome evolution and incipient speciation in the mountain pine beetle. We find a broad continuum of intrinsic incompatibilities in hybrid males that increase in strength with geographic distance between reproductively isolated populations. This striking progression of reproductive isolation is coupled with extensive gene specialization, natural selection, and elevated genetic differentiation on both sex chromosomes. Closely related populations isolated by hybrid male sterility also show fixation of alternative neo-Y haplotypes that differ in structure and male-specific gene content. Our results suggest that neo-sex chromosome evolution can drive rapid functional divergence between closely related populations irrespective of ecological drivers of divergence.

Original languageEnglish
Article number1593
JournalNature Communications
Volume8
Issue number1
DOIs
StatePublished - Dec 1 2017

Funding

This research was supported by USDA AFRI NIFA (grant no. 2013–67011–21113), the Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD073439; J.M.G.), and through instrumentation in the University of Montana Genomics Core funded by the M.J. Murdock Charitable Trust. We thank Jim Vandygriff, Greta Schen-Langenheim and Joseph Dysthe for help collecting data. We also thank the Good lab and the Evolutionary Genetics and Genomics community at the University of Montana for helpful discussions. We thank Lila Fishman, Doug Emlen, Dan Matute, and Matt Hahn for providing helpful comments on earlier drafts of this manuscript.

Funder number
2013–67011–21113
R01HD073439

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