Abstract
Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are “hotspots” for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by ∼100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.
Highlights
One of the central outstanding questions in evolutionary biology concerns the predictability of evolution
Can we predict the number and effect size of genes involved in evolution, and the types of genetic changes that underlie particular kinds of evolution? Striking empirical examples of repeated use of the same genes in similar evolutionary changes suggest that common patterns may emerge even across distantly related taxa [1,2]
A direct comparison of gene order was not possible, as several H. erato BAC clones are not yet fully assembled, a single copy of all 24 predicted H. melpomene HmB genes was identified in H. erato, and a similar pattern is seen at HmYb where sequence is available for H. erato
Summary
One of the central outstanding questions in evolutionary biology concerns the predictability of evolution. A few loci of major phenotypic effect are commonly involved in adaptation, and second, the same genes can be involved repeatedly across divergent lineages [2]. Both cis-regulatory, structural and null mutations can play a role in adaptation, intriguingly there is a suggestion that cisregulatory change may be more important in inter-specific versus intra-specific adaptation [7]. To date, these patterns are inferred from just a handful of well-studied examples
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
