Clustering of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies.

Chris D Jiggins,Ian A Warren,Sylvia Fernanda Garza,Stefan Schulz,Pasi M A Rastas,Diana Abondano Almeida,Kelsey J R P Byers,W Owen Mcmillan,Richard M Merrill,Kathy Darragh

doi:10.1002/ece3.6947

Abstract

The degree to which loci promoting reproductive isolation cluster in the genome—that is, the genetic architecture of reproductive isolation—can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male‐transferred antiaphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.

Highlights

The genetic architecture of population differences can profoundly affect the evolution and maintenance of new species, especially in the face of ongoing gene flow
There is considerable interest in finding the genetic basis of traits that contribute to reproductive isolation and understanding both the effect size and distribution of loci across the genome
The genetic basis for traits contributing to reproductive isolation remains poorly studied

Summary

| INTRODUCTION

The genetic architecture of population differences can profoundly affect the evolution and maintenance of new species, especially in the face of ongoing gene flow. Barrier traits can include sex pheromones, chemical signals that mediate intraspecific communication important for mating Due to their critical role in mate attraction, and their ability to convey information about species identity and male quality, pheromones can be important for establishing and maintaining reproductive isolation through relatively simple changes in chemical bouquets (Smadja & Butlin, 2009). In Drosophila, some loci showed pleiotropy of production and perception of pheromones, thought to be rare in Lepidoptera (Haynes, 2016) In combination with their importance in inter- and intraspecific mate choice, such simple genetic control and relatively lower risk of pleiotropy makes them ripe material for adaptation and speciation. We investigated the patterns of QTL distribution across the genome to test for clustering of loci across chromosomes

| METHODS

Findings

| DISCUSSION