Genetic coupling of signal and preference facilitates sexual isolation during rapid speciation

Mingzi Xu, Kerry L. Shaw

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

Abstract

The divergence of sexual signals is ultimately a coevolutionary process: while signals and preferences diverge between lineages, they must remain coordinated within lineages for matings to occur. Divergence in sexual signals makes a major contribution to evolving species barriers. Therefore, the genetic architecture underlying signal-preference coevolution is essential to understanding speciation but remains largely unknown. In Laupala crickets where male song pulse rate and female pulse rate preferences have coevolved repeatedly and rapidly, we tested two contrasting hypotheses for the genetic architecture underlying signal-preference coevolution: linkage disequilibrium between unlinked loci and genetic coupling (linkage disequilibrium resulting from pleiotropy of a shared locus or tight physical linkage). Through selective introgression and quantitative trait locus (QTL) fine mapping, we estimated the location of QTL underlying interspecific variation in both female preference and male pulse rate from the same mapping populations. Remarkably, map estimates of the pulse rate and preference loci are as close as 0.06 cM apart, the strongest evidence to date for genetic coupling between signal and preference loci. As the second pair of colocalizing signal and preference loci in the Laupala genome, our finding supports an intriguing pattern, pointing to a major role for genetic coupling in the quantitative evolution of a reproductive barrier and rapid speciation in Laupala. Owing to its effect on suppressing recombination, a coupled, quantitative genetic architecture offers a powerful and parsimonious genetic mechanism for signal-preference coevolution and the establishment of positive genetic covariance on which the Fisherian runaway process of sexual selection relies.

Original languageEnglish (US)
Article number20191607
JournalProceedings of the Royal Society B: Biological Sciences
Volume286
Issue number1913
DOIs
StatePublished - Oct 23 2019
Externally publishedYes

Bibliographical note

Funding Information:
This project is funded by the National Science Foundation (grant no. 1257682) to K.L.S.

Publisher Copyright:
© 2019 The Author(s) Published by the Royal Society. All rights reserved.

Keywords

  • Behavioural barrier
  • Genetic architecture
  • Laupala
  • Mating preference
  • Pleiotropy
  • Reproductive isolation

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