Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes

Peter A. Moran*, Sonia Pascoal, Timothee Cezard, Judith E. Risse, Michael G. Ritchie, Nathan W. Bailey

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Linking intraspecific and interspecific divergence is an important challenge in speciation research. X chromosomes are expected to evolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16 population transect of two closely related Australian cricket species, Teleogryllus commodus and T. oceanicus, covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane's rule, as hybrid females are sterile. We found no evidence of recent introgression, despite the fact that the species coexist in overlapping habitats in the wild and interbreed in the laboratory. Putative X-linked loci showed greater differentiation between species compared with autosomal loci. However, population differentiation within species was unexpectedly lower on X-linked markers than autosomal markers, and relative X-to-autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex-biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex-linked genes in maintaining species boundaries in this system.

Original languageEnglish
Pages (from-to)3905-3924
Number of pages20
JournalMolecular Ecology
Volume27
Issue number19
DOIs
Publication statusPublished - Oct 2018
Externally publishedYes

Funding

Natural Environment Research Council grants to N.W.B., Grant/Award numbers: NE/G014906/1, NE/L011255/1; Orthopterists’ Society grant to P.A.M. We are grateful to the following people for assistance in the field: K. Holmes, S. Blanksby, M. Higgie, G. Jones, T. Ly, R. Ollerynshaw. S. Vardy, the Chan family and the Westman family generously provided hospitality and assistance in the field and we appreciate their enthusiasm for our research. We would like to thank T. Sneddon for assistance with the DNA extractions and N. Moran for help writing scripts to filter X loci. D. Forbes, A. Grant and M. McGunnigle assisted in the laboratory, and K. Gharbi and Edinburgh Genomics provided excellent support for RAD-sequencing. Funding was provided by NERC grants to N.W.B. (NE/G014906/1, NE/L011255/ 1), and an Orthopterists’ Society grant to P.A.M. is gratefully acknowledged.

FundersFunder number
Orthopterists' Society
Natural Environment Research CouncilNE/G014906/1, NE/L011255/1
National Eye Research Centre

    Keywords

    • faster-X effect
    • hybridization
    • population genomics
    • RAD sequencing
    • sex chromosomes
    • Teleogryllus

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