Multi-Allelic Major Effect Genes Interact with Minor Effect QTLs to Control Adaptive Color Pattern Variation in Heliconius erato

Riccardo Papa,Brian A Counterman,Durrell D Kapan,Tomas Hrbek,Karla Maldonado,Daniel P Lindstrom,Robert D Reed,W Owen Mcmillan,H Frederik Nijhout,Casper Breuker

doi:10.1371/journal.pone.0057033

Abstract

Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato, we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis, to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato. We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change.

Highlights

Butterflies are among the most charismatic insects and their kaleidoscopic color variation has fascinated scientists for centuries
The data suggest that the genetic architecture of wing color pattern variation in H. erato is controlled by few major gene and multiple addictive loci of smaller effect
To determine if there was evidence for multiple loci segregating in our crosses between H. himera and different races of H. erato, we identified Amplified Fragment Length Polymorphisms (AFLPs) fragments tightly linked to the qualitative variation in forewing band shape across our collection of H. himera6H. erato crosses

Summary

Introduction

Butterflies are among the most charismatic insects and their kaleidoscopic color variation has fascinated scientists for centuries. The wing pattern radiations of Heliconius butterflies in particular have become a useful model for understanding the evolution, genetic basis, and development of complex adaptive variation [1,2,3,4,5,6]. With greater than 25 parapatric races, each with a distinctive warning-color pattern, H. erato and H. melpomene represent one of the best example of a parallel radiation [9,10,11]. This patchwork of wing colorpattern races within a species and convergent mimetic matching between H. erato and H. melpomene provides a vivid example of the importance of natural selection in shaping phenotypic variation [12,13]. Recent studies points to a few large-effect loci controlling major phenotypic changes within both species [1,14,15], we still have a limited understanding of the overall number and effect sizes of the loci that control these complex and highly polymorphic color-patterns

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