Two developmentally temporal quantitative trait loci underlie convergent evolution of increased branchial bone length in sticklebacks

Proc Biol Sci. 2014 Aug 7;281(1788):20140822. doi: 10.1098/rspb.2014.0822.

Abstract

In convergent evolution, similar phenotypes evolve repeatedly in independent populations, often reflecting adaptation to similar environments. Understanding whether convergent evolution proceeds via similar or different genetic and developmental mechanisms offers insight towards the repeatability and predictability of evolution. Oceanic populations of threespine stickleback fish, Gasterosteus aculeatus, have repeatedly colonized countless freshwater lakes and streams, where new diets lead to morphological adaptations related to feeding. Here, we show that heritable increases in branchial bone length have convergently evolved in two independently derived freshwater stickleback populations. In both populations, an increased bone growth rate in juveniles underlies the convergent adult phenotype, and one population also has a longer cartilage template. Using F2 crosses from these two freshwater populations, we show that two quantitative trait loci (QTL) control branchial bone length at distinct points in development. In both populations, a QTL on chromosome 21 controls bone length throughout juvenile development, and a QTL on chromosome 4 controls bone length only in adults. In addition to these similar developmental profiles, these QTL show similar chromosomal locations in both populations. Our results suggest that sticklebacks have convergently evolved longer branchial bones using similar genetic and developmental programmes in two independently derived populations.

Keywords: convergent evolution; endochondral bone; parallel evolution; quantitative trait loci; skeletal development; stickleback.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptation, Biological
  • Animals
  • Biological Evolution
  • Bone Development*
  • British Columbia
  • Female
  • Fresh Water
  • Gills / anatomy & histology
  • Gills / embryology
  • Gills / growth & development*
  • Male
  • Phenotype*
  • Quantitative Trait Loci*
  • Seawater
  • Smegmamorpha / anatomy & histology
  • Smegmamorpha / embryology
  • Smegmamorpha / genetics*
  • Smegmamorpha / growth & development*