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

Ryan R Bracewell,Brian T Sullivan,Barbara J Bentz,Jeffrey M Good

doi:10.1038/s41467-017-01761-4

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.

Highlights

Genome evolution is predicted to be rapid following the establishment of new sex chromosomes, but it is not known if neo-sex chromosome evolution plays an important role in speciation
Genes involved in reproductive isolation have been linked to recently established neo-sex chromosomes in threespine sticklebacks[19] and butterflies[20], but it is unclear if or how these hybrid incompatibilities relate to neo-sex chromosome evolutionary dynamics per se
Our results reveal that extensive genic specialization and structural degeneration on the neo-sex chromosomes can be sufficiently rapid to drive intrinsic functional differentiation between closely related populations, which may in turn play an important role in incipient speciation

Summary

Introduction

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. A century of research has established that hybrid incompatibilities usually manifest in the heterogametic (male) sex first (i.e., Haldane’s Rule1) and that the early stages of hybrid male sterility (HMS) and inviability (HMI) are almost always asymmetric in reciprocal genetic crosses[2, 3] These patterns reflect the fundamental role that heteromorphic sex chromosomes play in the evolution of deleterious epistatic interactions underlying intrinsic reproductive isolation[4,5,6], but the importance of these processes to the early stages of speciation has been debated[7]. It is well established that older, highly heteromorphic sex chromosomes often play a disproportionately large role in speciation through the exposure of recessive genetic incompatibilities in hybrid males (i.e., dominance theory)[4] and various evolutionary dynamics (e.g., faster-X, meiotic drive) that can drive rapid sex-linked divergence[5, 6]. Previous studies have found that populations at the southern reaches of the beetle’s range (southern California and Arizona) are the most genetically divergent and genetic variation follows an isolation-by-distance pattern around the Great Basin

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Results

Conclusion