Ancient homology underlies adaptive mimetic diversity across butterflies

Abstract

Convergent evolution provides a rare, natural experiment with which to test the predictability of adaptation at the molecular level. Little is known about the molecular basis of convergence over macro-evolutionary timescales. Here we use a combination of positional cloning, population genomic resequencing, association mapping and developmental data to demonstrate that positionally orthologous nucleotide variants in the upstream region of the same gene, WntA, are responsible for parallel mimetic variation in two butterfly lineages that diverged >65 million years ago. Furthermore, characterization of spatial patterns of WntA expression during development suggests that alternative regulatory mechanisms underlie wing pattern variation in each system. Taken together, our results reveal a strikingly predictable molecular basis for phenotypic convergence over deep evolutionary time.

New genomes clarify mimicry evolution

“…This work joins a flurry of recent genomic work on mimicry in P. polytes and other butterflies [2][3][4][5][6] , which together bring us much closer to understanding how mimicry works.…”

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

“…WntA is expressed in the final larval instar where it shows diverse expression patterns associated with black regions in the centre of the forewing (figure 2). Additional evidence for the role of WntA comes from heparin injection into wing tissue of developing Heliconius pupae, which leads to changes in adult wing pattern comparable with genetic effects of Ac [36,37]. Heparin binds Wnt family ligands and promotes their mobility through tissue, and although its effects are not specific to WntA, the combination of genetic mapping, morphogen experiments and expression studies builds a compelling case for the role of WntA in forewing patterning.…”

“…It has also been argued that NGP elements develop independently in each wing cell, with wing veins acting as landmarks during development [61]. However, WntA expression domains are clearly part of a wing-wide patterning system, such as the front-back white stripe of Limenitis [37,59]. Vein information can modulate this underlying whole-wing system to varying degrees, such as repeated patterns of the external symmetry system, where the focal scale cells of eyespots or chevrons are defined by veins.…”

“…WntA is also associated with adaptive pattern variation in Limenitis arthemis [37]. Limenitis and Heliconius diverged about 65 Ma, so the involvement of WntA in patterning implies a shared and relatively ancient role for this gene in nymphalid wing pattern specification.…”

“…WntA was identified as the functional gene at this locus through a combination of genetic linkage mapping using RAD-seq, a population genetic signal of divergence, and differences in expression patterns in developing wings [35][36][37][38]. WntA is expressed in the final larval instar where it shows diverse expression patterns associated with black regions in the centre of the forewing (figure 2).…”