Comparative Analysis of Japanese Three-Spined Stickleback Clades Reveals the Pacific Ocean Lineage Has Adapted to Freshwater Environments While the Japan Sea Has Not

PLoS One. 2014 Dec 2;9(12):e112404. doi: 10.1371/journal.pone.0112404. eCollection 2014.

Abstract

Divergent selection and adaptive divergence can increase phenotypic diversification amongst populations and lineages. Yet adaptive divergence between different environments, habitats or niches does not occur in all lineages. For example, the colonization of freshwater environments by ancestral marine species has triggered adaptive radiation and phenotypic diversification in some taxa but not in others. Studying closely related lineages differing in their ability to diversify is an excellent means of understanding the factors promoting and constraining adaptive evolution. A well-known example of the evolution of increased phenotypic diversification following freshwater colonization is the three-spined stickleback. Two closely related stickleback lineages, the Pacific Ocean and the Japan Sea occur in Japan. However, Japanese freshwater stickleback populations are derived from the Pacific Ocean lineage only, suggesting the Japan Sea lineage is unable to colonize freshwater. Using stable isotope data and trophic morphology, we first show higher rates of phenotypic and ecological diversification between marine and freshwater populations within the Pacific Ocean lineage, confirming adaptive divergence has occurred between the two lineages and within the Pacific Ocean lineage but not in the Japan Sea lineage. We further identified consistent divergence in diet and foraging behaviour between marine forms from each lineage, confirming Pacific Ocean marine sticklebacks, from which all Japanese freshwater populations are derived, are better adapted to freshwater environments than Japan Sea sticklebacks. We suggest adaptive divergence between ancestral marine populations may have played a role in constraining phenotypic diversification and adaptive evolution in Japanese sticklebacks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Biological / genetics*
  • Animals
  • Biological Evolution
  • Environment
  • Feeding Behavior
  • Fresh Water*
  • Geography
  • Japan
  • Lakes
  • Oceans and Seas
  • Pacific Ocean
  • Phenotype
  • Phylogeny
  • Smegmamorpha / genetics
  • Smegmamorpha / physiology*
  • Species Specificity

Grant support

This research was supported by the Japan Science and Technology Agency PRESTO program, Center for the Promotion of Integrated Sciences (CPIS) of Sokendai, and Grant-in-Aid for Scientific Research on Innovative Areas (23113007 and 23113001) from the Ministry of Education, Science, Sports, and Culture to JK. MR was kindly funded by the Japanese Society for the Promotion of Science on a Short-term Postdoctoral Fellowship and the NIG Collaborative Research Program (2013-A33 and A34). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.