A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies

Abstract

We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Müllerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius melpomene, maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a “supergene”, determining multiple sympatric morphs in a third species, H. numata. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic “supergene” polymorphism without intermediates. Although we cannot at this stage confirm the homology of the loci segregating in the three species, our results imply that a conserved yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions.

Mapping and recombination analysis of two moth colour mutations, Black moth and Wild wing spot, in the silkworm Bombyx mori

“…Therefore, recombination between both genes occurred in none of the individuals. Moreover, we found that the candidate regions of both genes shared correspondence with a region associated with wing-and body-colour variations in different lepidopteran species, that is, B. betularia, Heliconius cydno, Heliconius erato, Heliconius melpomene and Heliconius numata (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011). These results strongly suggest that the same genes and/or regulatory elements responsible for wing and body colour in Bombyx, Bm and Ws, may underlie these variants in different Lepidoptera.…”

“…The genetic and genomic analysis demonstrated the following: (i) the candidate regions of the Bm and Ws genes are located in~2-Mb-long and 100-kb-long regions on the same scaffold Bm_scaf33 of chromosome 17; (ii) chromosome 17 of Bm mutation harbours inversion within a compartment corresponding to Bm_scaf33; and (iii) the Bm and Ws regions share synteny with a region associated with wing-and body-colour variations in different lepidopteran species (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011). Based on our results, we hypothesise that this common region may control wingand body-colour variations in lepidopteran insects.…”

“…Comparative genomic analysis of the Bm and Ws regions, and other lepidopteran genomes Based on the comparative genomic analysis, we found that the Bm and Ws regions shared synteny with a region associated with wing-and body-colour variations in different lepidopteran species of B. betularia and Heliconius butterflies (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011 (Figure 4). Both of these causal genes determine wing colour variations in H. melpomene (Ferguson et al, 2010 Table 1 for details of the BAC probe information.…”

Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

“…In terms of camouflage, the EUB Dark phenotype is also likely to be a poor combination, as a distinctly dark apex on an otherwise white shell is conspicuous. Whatever the exact mechanism is, the rarity of the EUB Dark combination contrasts with the highly flexible combinations of colour and banding in the supergene of C. nemoralis (Cook, 2005), but parallels similar rarities in other land snails (for example, Murray and Clarke, 1976a,b;Asami and Asami, 2008) and mimetic butterflies (for example, Clarke and Sheppard, 1969;Joron et al, 2006). By contrast, the other three morphs have potential advantages.…”

Stripes, sex and sparrows: what processes underlie heteromorphic chromosome evolution?

“…Indeed, the extent of sequence divergence and LD between the ZAL2 forms, revealing the suppression of recombination and their long-term coexistence, suggests that both functional haplotypes are actively maintained, and it was suggested that they might encode coadapted combinations of multiple traits (Falls and Kopachena, 1994;Romanov et al, 2009)-a form of giant supergene combining behavioural as well as plumage variation (Mather, 1950;Clarke et al, 1968;Joron et al, 2006). One remarkable finding is indeed the sheer number of genes locked into very large non-recombining units maintained by balancing selection.…”