Résumé
Understanding the genetic architecture of adaptive traits has been at the
centre of modern evolutionary biology since Fisher; however, evaluating
how the genetic architecture of ecologically important traits influences
their diversification has been hampered by the scarcity of empirical data.
Now, high-throughput genomics facilitates the detailed exploration of
variation in the genome-to-phenotype map among closely related taxa. Here,
we investigate the evolution of wing pattern diversity in Heliconius, a
clade of neotropical butterflies that have undergone an adaptive radiation
for wing-pattern mimicry and are influenced by distinct selection regimes.
Using crosses between natural wing-pattern variants, we used genome-wide
restriction site-associated DNA (RAD) genotyping, traditional linkage
mapping and multivariate image analysis to study the evolution of the
architecture of adaptive variation in two closely related species:
Heliconius hecale and H. ismenius. We implemented a new morphometric
procedure for the analysis of whole-wing pattern variation, which allows
visualising spatial heatmaps of genotype-to-phenotype association for each
quantitative trait locus separately. We used the H. melpomene reference
genome to fine-map variation for each major wing-patterning region
uncovered, evaluated the role of candidate genes and compared genetic
architectures across the genus. Our results show that, although the loci
responding to mimicry selection are highly conserved between species,
their effect size and phenotypic action vary throughout the clade.
Multilocus architecture is ancestral and maintained across species under
directional selection, whereas the single-locus (supergene) inheritance
controlling polymorphism in H. numata appears to have evolved only once.
Nevertheless, the conservatism in the wing-patterning toolkit found
throughout the genus does not appear to constrain phenotypic evolution
towards local adaptive optima.