Signatures of selection in loci governing major colour patterns in Heliconius butterflies and related species

Grace C Wu,Mathieu Joron,Chris D Jiggins

doi:10.1186/1471-2148-10-368

Grace C Wu, Mathieu Joron + Show 1 more

Open Access

https://doi.org/10.1186/1471-2148-10-368

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Abstract

BackgroundProtein-coding change is one possible genetic mechanism underlying the evolution of adaptive wing colour pattern variation in Heliconius butterflies. Here we determine whether 38 putative genes within two major Heliconius patterning loci, HmYb and HmB, show evidence of positive selection. Ratios of nonsynonymous to synonymous nucleotide changes (ω) were used to test for selection, as a means of identifying candidate genes within each locus that control wing pattern.ResultsPreliminary analyses using 454 transcriptome and Bacterial Artificial Chromosome (BAC) sequences from three Heliconius species highlighted a cluster of genes within each region showing relatively higher rates of sequence evolution. Other genes within the region appear to be highly constrained, and no ω estimates exceeded one. Three genes from each locus with the highest average pairwise ω values were amplified from additional Heliconius species and races. Two selected genes, fizzy-like (HmYb) and DALR (HmB), were too divergent for amplification across species and were excluded from further analysis. Amongst the remaining genes, HM00021 and Kinesin possessed the highest background ω values within the HmYb and HmB loci, respectively. After accounting for recombination, these two genes both showed evidence of having codons with a signature of selection, although statistical support for this signal was not strong in any case.ConclusionsTests of selection reveal a cluster of candidate genes in each locus, suggesting that weak directional selection may be occurring within a small region of each locus, but coding changes alone are unlikely to explain the full range of wing pattern diversity. These analyses pinpoint many of the same genes believed to be involved in the control of colour patterning in Heliconius that have been identified through other studies implementing different research methods.

Highlights

Protein-coding change is one possible genetic mechanism underlying the evolution of adaptive wing colour pattern variation in Heliconius butterflies
Frequently cited examples of morphological variation controlled by amino acid changes include repeated involvement of Melanocortin-1 receptor (Mc1r) mutations in mice, birds, and reptiles in adaptive melanic pigmentation [6,7,8]
The theoretical basis for this hypothesis is that every gene possesses a modular arrangement of 5’ cis-regulatory elements (CREs) that control temporal and spatial patterns of expression, and that these regions are less subject to the negative pleiotropic effects constraining coding changes, allowing adaptive evolution to proceed at a higher rate [10]

Summary

Introduction

Protein-coding change is one possible genetic mechanism underlying the evolution of adaptive wing colour pattern variation in Heliconius butterflies. The relative contribution of different mechanisms to adaptive phenotypic variation has been the focus of many recent evolutionary and developmental studies and the subject of much debate [1,2,3,4]. The theoretical basis for this hypothesis is that every gene possesses a modular arrangement of 5’ CREs that control temporal and spatial patterns of expression, and that these regions are less subject to the negative pleiotropic effects constraining coding changes, allowing adaptive evolution to proceed at a higher rate [10]. Oft-cited examples of cis-regulatory change as the molecular basis for phenotypic variation come from

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