The Genomic Landscape at a Late Stage of Stickleback Speciation: High Genomic Divergence Interspersed by Small Localized Regions of Introgression

PLoS Genet. 2018 May 23;14(5):e1007358. doi: 10.1371/journal.pgen.1007358. eCollection 2018 May.


Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little knowledge of the genomic signatures of divergence and introgression in older stickleback systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian Computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atlantic Ocean
  • Bayes Theorem
  • Datasets as Topic
  • Female
  • Gene Flow / genetics*
  • Genetic Speciation*
  • Genome
  • Genomics / methods
  • Hybridization, Genetic / genetics*
  • Japan
  • Male
  • Pacific Ocean
  • Recombination, Genetic / genetics
  • Smegmamorpha / genetics*
  • Sympatry / genetics*

Associated data

  • Dryad/10.5061/dryad.104g3d0

Grant support

MR and KY were supported by a Standard Postdoctoral Research Fellowship for Research in Japan and a Postdoctoral Research Fellowship for Young Scientists PD from JSPS, respectively. This research was supported by NIG collaborative grant –I (98I2017) to MR, Grant-in-Aid for Scientific Research on Innovative Areas “Gene Correlative System” (23113007 and 23113001) to JK, “Genome Science” (221S0002) to AT and AF, and JSPS KAKENHI (15H02418) to JK, NIBB Collaborative Research Program (10-337, 11-311) to JK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.