Genetic dissection of assortative mating behavior

PLoS Biol. 2019 Feb 7;17(2):e2005902. doi: 10.1371/journal.pbio.2005902. eCollection 2019 Feb.

Abstract

The evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution or more generally about the genetic basis for assortative mating behaviors. Both tight physical linkage and the existence of large-effect preference loci will strengthen genetic associations between behavioral and ecological barriers, promoting the evolution of assortative mating. The warning patterns of Heliconius melpomene and H. cydno are under disruptive selection due to increased predation of nonmimetic hybrids and are used during mate recognition. We carried out a genome-wide quantitative trait locus (QTL) analysis of preference behaviors between these species and showed that divergent male preference has a simple genetic basis. We identify three QTLs that together explain a large proportion (approximately 60%) of the difference in preference behavior observed between the parental species. One of these QTLs is just 1.2 (0-4.8) centiMorgans (cM) from the major color pattern gene optix, and, individually, all three have a large effect on the preference phenotype. Genomic divergence between H. cydno and H. melpomene is high but broadly heterogenous, and admixture is reduced at the preference-optix color pattern locus but not the other preference QTLs. The simple genetic architecture we reveal will facilitate the evolution and maintenance of new species despite ongoing gene flow by coupling behavioral and ecological aspects of reproductive isolation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Butterflies / genetics*
  • Butterflies / physiology*
  • Chromosomes, Insect / genetics
  • Courtship
  • Female
  • Male
  • Mating Preference, Animal / physiology
  • Quantitative Trait Loci / genetics*
  • Sexual Behavior, Animal / physiology*
  • Species Specificity
  • Sympatry / genetics

Associated data

  • Dryad/10.5061/dryad.4b240j4

Grants and funding

ERC https://erc.europa.eu (grant number 339873). Grant to CDJ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. DFG http://www.dfg.de/en/research_funding/programmes/individual/emmy_noether/index.html (grant number GZ: ME 4845/1-1). Emmy Noether fellowship and DFG grant to RMM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. King's College (grant number). Junior Research Fellowship to RMM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. University of Cambridge (grant number). Herschel Smith Postdoctoral Fellowship awarded to JD. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. St John's, Cambridge (grant number). Junior Research Fellowship awarded to SHM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.