Reticulate speciation and barriers to introgression in the anopheles gambiae species complex

Jacob E. Crawford, Michelle M Riehle, Wamdaogo M. Guelbeogo, Awa Gneme, N'fale Sagnon, Kenneth D. Vernick, Rasmus Nielsen, Brian P. Lazzaro

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

Abstract

Speciation as a process remains a central focus of evolutionary biology, but our understanding of the genomic architecture and prevalence of speciation in the face of gene flow remains incomplete. The Anopheles gambiae species complex of malaria mosquitoes is a radiation of ecologically diverse taxa. This complex is well-suited for testing for evidence of a speciation continuum and genomic barriers to introgression because its members exhibit partially overlapping geographic distributions as well as varying levels of divergence and reproductive isolation. We sequenced 20 genomes from wild A. gambiae s.s., Anopheles coluzzii, Anopheles arabiensis, and compared these with 12 genomes from the "GOUNDRY" subgroup of A. gambiae s.l. Amidst a backdrop of strong reproductive isolation, we find strong evidence for a speciation continuum with introgression of autosomal chromosomal regions among species and subgroups. The X chromosome, however, is strongly differentiated among all taxa, pointing to a disproportionately large effect of X chromosome genes in driving speciation among anophelines. Strikingly, we find that autosomal introgression has occurred from contemporary hybridization between A. gambiae and A. arabiensis despite strong divergence (∼5× higher than autosomal divergence) and isolation on the X chromosome. In addition to the X, we find strong evidence that lowly recombining autosomal regions, especially pericentromeric regions, serve as barriers to introgression secondarily to the X. We show that speciation with gene flow results in genomic mosaicism of divergence and introgression. Such a reticulate gene pool connecting vector taxa across the speciation continuum has important implications for malaria control efforts.

Original languageEnglish (US)
Pages (from-to)3116-3131
Number of pages16
JournalGenome biology and evolution
Volume7
Issue number11
DOIs
StatePublished - Nov 1 2015

Bibliographical note

Funding Information:
We thank Matteo Fumagalli, Filipe Vieira, and Tyler Linderoth for assistance with next-generation sequence data analyses and ANGSD. We thank members of the Nielsen group for helpful discussions on various aspects of this work. We also thank Russ Corbett-Detig, Wynn Meyer, and three anonymous reviewers for helpful comments on an earlier version of this manuscript. We are thankful for the use of the Extreme Science and Engineering Discovery Environment, which is supported by National Science Foundation grant number OCI-1053575. This work was supported by National Institutes of Health grant AI062995. This work was also supported by a Cornell Center for Comparative and Population Genomics Graduate Fellowship and the National Institute Of General Medical Sciences of the National Institutes of Health under Award Number F32GM103258 (J.E.C.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Publisher Copyright:
© The Author(s) 2015.

Keywords

  • Anopheles
  • Gene flow
  • Introgression
  • Population genetics
  • Speciation

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