Genome-wide analysis of ionotropic receptors provides insight into their evolution in Heliconius butterflies.

Bas Van Schooten,Riccardo Papa,Adriana D Briscoe,Chris D Jiggins

doi:10.1186/s12864-016-2572-y

Abstract

BackgroundIn a world of chemical cues, smell and taste are essential senses for survival. Here we focused on Heliconius, a diverse group of butterflies that exhibit variation in pre- and post-zygotic isolation and chemically-mediated behaviors across their phylogeny. Our study examined the ionotropic receptors, a recently discovered class of receptors that are some of the most ancient chemical receptors.ResultsWe found more ionotropic receptors in Heliconius (31) than in Bombyx mori (25) or in Danaus plexippus (27). Sixteen genes in Lepidoptera were not present in Diptera. Only IR7d4 was exclusively found in butterflies and two expansions of IR60a were exclusive to Heliconius. A genome-wide comparison between 11 Heliconius species revealed instances of pseudogenization, gene gain, and signatures of positive selection across the phylogeny. IR60a2b and IR60a2d are unique to the H. melpomene, H. cydno, and H. timareta clade, a group where chemosensing is likely involved in pre-zygotic isolation. IR60a2b also displayed copy number variations (CNVs) in distinct populations of H. melpomene and was the only gene significantly higher expressed in legs and mouthparts than in antennae, which suggests a gustatory function. dN/dS analysis suggests more frequent positive selection in some intronless IR genes and in particular in the sara/sapho and melpomene/cydno/timareta clades. IR60a1 was the only gene with an elevated dN/dS along a major phylogenetic branch associated with pupal mating. Only IR93a was differentially expressed between sexes.ConclusionsAll together these data make Heliconius butterflies one of the very few insects outside Drosophila where IRs have been characterized in detail. Our work outlines a dynamic pattern of IR gene evolution throughout the Heliconius radiation which could be the result of selective pressure to find potential mates or host-plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2572-y) contains supplementary material, which is available to authorized users.

Highlights

In a world of chemical cues, smell and taste are essential senses for survival
While some ionotropic receptor (IR) map to chromosomes containing major wing color pattern genes, none of these IR genes are tightly linked to color pattern loci (Fig. 2)
Heliconius are best known for their stunning visual signals and vision far into the ultraviolet [77], our work and the recent study of Briscoe et al [37] have shown an elaborate chemosensory system consisting of ~165 chemosensory receptors

Summary

Introduction

In a world of chemical cues, smell and taste are essential senses for survival. Here we focused on Heliconius, a diverse group of butterflies that exhibit variation in pre- and post-zygotic isolation and chemicallymediated behaviors across their phylogeny. Chemosensory receptors (CRs) are the molecular tools that animals have evolved to distinguish a myriad of odors and tastes This complexity in chemical sensing is manifested by the high degree of inter- and intraspecific variation at CR loci which is partly explained by the. IRs are the most primitive class of receptors and are expressed both in olfactory and gustatory tissues [16, 25] Their ability to detect a wide array of solid and volatile molecules probably has to do with their ancestral role in the early protostomes [26], and the necessity to cover functions that during the evolution of chemo-sensation were reassigned to GRs and ORs

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