Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the Heliconius melpomene Clade

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.

Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

“…Turner et al (14) argued, using allozyme data, that markers unlinked to color pattern exhibit a different history to color-pattern loci and are poor indicators of the evolutionary history of these phenotypic races. This notion is supported by recent association data showing that only loci tightly linked to the adaptive color patterns have restricted gene flow at racial hybrid zones within both H. erato and H. melpomene (15)(16)(17). Phylogenetic data from the genomic regions near color-pattern loci should provide a more accurate picture of the history of these phenotypes.…”

“…The genomic interval controlling red pattern variation (Fig. 1) has recently been localized to a homologous region in both comimics (16,17,21). Further population genetic and comparative gene-expression work on this region has identified a gene, optix, that controls red color-pattern variation in both H. erato and H. melpomene (22).…”

“…Further population genetic and comparative gene-expression work on this region has identified a gene, optix, that controls red color-pattern variation in both H. erato and H. melpomene (22). Although no other genes show the pattern-specific expression of optix, other genes in this interval have shown significant genotype-by-phenotype associations (16,17,23) and expression differences between divergent color-pattern races (16,17,24).…”

Influences of geographic differentiation in the forewing warning signal of the wood tiger moth in Alaska

“…Such patterns of predation are observed in Heliconius butterflies (Mallet & Barton 1989, Kapan 2001, Langham 2004) and poison frogs (Noonan & Comeault 2009, Chouteau & Angers 2011, Chouteau & Angers 2012. The effects of selective predation can be seen even at the genomic level where differentiation between Heliconius melpomene morphs is greater at loci coding for coloration than neutral loci (Baxter et al 2010). Overall, forewings appear to be warning signals and the geographic differences seen in Alaska is in part due to predation and likely helped by some restricted gene flow from physical barriers, or both.…”

“…Studies in the field (Mallet & Barton 1989, Kapan 2001 and in the lab with local predators (Langham 2004) have found that predators from areas with local predominant morphs are more likely to attack foreign than local morphs. Indeed, even at a broader genomic level differentiation across hybrid zones is greater at loci directly responsible for coloration than at neutral loci (Baxter et al 2010).…”