Visual mate preference evolution during butterfly speciation is linked to neural processing genes

Matteo Rossi,Timothy J. Thurman,W. Owen McMillan,Richard M. Merrill,Chris D. Jiggins,Alexander E. Hausmann,Stephen H. Montgomery,Riccardo Papa

doi:10.1038/s41467-020-18609-z

Abstract

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they “choose” not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspecifics. Here, we couple QTL for divergence in visual preference behaviours with population genomic and gene expression analyses of neural tissue (central brain, optic lobes and ommatidia) across development in two sympatric Heliconius species. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences. Three of these have previously been implicated in key components of neural signalling (specifically an ionotropic glutamate receptor and two regucalcins), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. This would allow preference evolution without altering perception of the wider environment.

Highlights

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they “choose” not to mate
Backcrosses-to-cydno males heterozygous at the best supported Quantitative trait locus (QTL) from our previous analysis[19] initiated courtship towards H. melpomene females more frequently than males homozygous for the H. cydno allele (Fig. 1, bottom left; n = 139, ΔELPD: −10.9 (S.E. ± 5.1), i.e., a change of 2.14 SE units)
Together with previous evidence that male hybrids bearing H. melpomene alleles at optix prefer to court the artificial models of H. melpomene females over those of H. cydno[25], these results suggest that the QTL on chromosome 18 harbours genes for visual attraction behaviours towards females with the red pattern

Summary

Introduction

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they “choose” not to mate. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences Three of these have previously been implicated in key components of neural signalling ( an ionotropic glutamate receptor and two regucalcins), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. The closely related species Heliconius melpomene and Heliconius cydno differ in warning patterns, which are both under disruptive selection due to mimicry[14] and are important mating cues[15] As a result, these divergent patterns couple ecological and behavioural components of reproductive isolation, which (as predicted by so-called “magic trait” models16) is expected to facilitate speciation in the face of gene flow. This QTL, and its associated candidate region, contain hundreds of genes, and the exact genes responsible for differences in preference behaviour are not known

Methods

Results

Conclusion