Final Report Summary - MIMEVOL (Balancing selection and the molecular evolution of mimicry supergenes)
Colour pattern polymorphism in Heliconius numata is controlled by a supergene (P), a cluster of tightly-linked genetic elements working together as a single unit. Each morph in H. numata is a close mimic of another toxic butterfly in the community, bringing strong benefits in survival.
We discovered chromosomal rearrangements at the supergene implying segments were inverted during evolution. At this locus, 3 types of chromosomal structures coexist in the population. We described the breakpoints of inversions, and developed a molecular test for each of them. We found a tight association between chromosome structures and wing patterns in H. numata. Each inverted chromosomal segment was DNA-sequenced and genes were annotated. Genes underlying morphological differences were identified by association study, although the way they control wing pattern is still unclear. A reference genome sequence was assembled fully by chromosome, the first such reference for the butterflies. This reference is useful for population genomics studies in those butterflies, and the publication made important impact.
Inversions cause suppression of crossing-over during meiosis, and reduce the mixing of genes around them throughout population history. We found strong suppression of recombination across the supergene. Our findings showed that the supergene had evolved through the inversion of key segments at this locus on the chromosome, causing genes around those inversions to be locked together and inherited as a single block, preserving good (mimetic) combinations of traits. This was the first molecular dissection of a supergene in nature and the publication made considerable impact.
Comparing the DNA sequence of each inverted segment showed that the alleles have an ancient origin, and have been maintained through long evolutionary time. In contrast, the rest of the genome show signals of recent exponential growth. Behavioral assays revealed that those butterflies show negative assortative mate choice, a very peculiar finding which, together with other experimental results on survival in nature, may contribute to long-term maintenance of wing pattern diversity.
Allelic dominance between supergene alleles was investigated using novel tools developed in our team for colour pattern analysis. Distinct mechanisms of dominance were revealed, associated with the chromosomal rearrangements. We showed dominance had responded to selection for local mimicry.
Colour-pattern loci were sequenced in multiple morphs of H. numata and 8 other closely-related species in the clade, revealing a unique origin of inversions in the clade, common to H. pardalinus and H. numata, perhaps involving introgression. Hybridization was also studied in the pair of species H. timareta and H. melpomene, from genomic and phenotypic data in natural populations. This allowed benchmarking hybrid detection, and revealed adaptive sharing of mimicry alleles, flowing between species. Crosses between colour-pattern races of Heliconius ismenius and H. hecale, closely related to H. numata, revealed a multi-locus architecture of pattern variation, demonstrating that genetic architecture evolved in the clade and that the supergene is restricted to the H. numata lineage.
A new morphometric pipeline was developed to quantify all phenotypes in the project. This was a major methodological breakthrough applicable to many other cases of colour pattern variation outside butterflies.
Overall our project investigated the molecular and ecological underpinnings of the maintenance of adaptive variation in a highly diverse group of tropical insects. Very novel results were found which will make a lasting contribution to evolutionary biology and our understanding of the rules of diversification in the natural world.
We discovered chromosomal rearrangements at the supergene implying segments were inverted during evolution. At this locus, 3 types of chromosomal structures coexist in the population. We described the breakpoints of inversions, and developed a molecular test for each of them. We found a tight association between chromosome structures and wing patterns in H. numata. Each inverted chromosomal segment was DNA-sequenced and genes were annotated. Genes underlying morphological differences were identified by association study, although the way they control wing pattern is still unclear. A reference genome sequence was assembled fully by chromosome, the first such reference for the butterflies. This reference is useful for population genomics studies in those butterflies, and the publication made important impact.
Inversions cause suppression of crossing-over during meiosis, and reduce the mixing of genes around them throughout population history. We found strong suppression of recombination across the supergene. Our findings showed that the supergene had evolved through the inversion of key segments at this locus on the chromosome, causing genes around those inversions to be locked together and inherited as a single block, preserving good (mimetic) combinations of traits. This was the first molecular dissection of a supergene in nature and the publication made considerable impact.
Comparing the DNA sequence of each inverted segment showed that the alleles have an ancient origin, and have been maintained through long evolutionary time. In contrast, the rest of the genome show signals of recent exponential growth. Behavioral assays revealed that those butterflies show negative assortative mate choice, a very peculiar finding which, together with other experimental results on survival in nature, may contribute to long-term maintenance of wing pattern diversity.
Allelic dominance between supergene alleles was investigated using novel tools developed in our team for colour pattern analysis. Distinct mechanisms of dominance were revealed, associated with the chromosomal rearrangements. We showed dominance had responded to selection for local mimicry.
Colour-pattern loci were sequenced in multiple morphs of H. numata and 8 other closely-related species in the clade, revealing a unique origin of inversions in the clade, common to H. pardalinus and H. numata, perhaps involving introgression. Hybridization was also studied in the pair of species H. timareta and H. melpomene, from genomic and phenotypic data in natural populations. This allowed benchmarking hybrid detection, and revealed adaptive sharing of mimicry alleles, flowing between species. Crosses between colour-pattern races of Heliconius ismenius and H. hecale, closely related to H. numata, revealed a multi-locus architecture of pattern variation, demonstrating that genetic architecture evolved in the clade and that the supergene is restricted to the H. numata lineage.
A new morphometric pipeline was developed to quantify all phenotypes in the project. This was a major methodological breakthrough applicable to many other cases of colour pattern variation outside butterflies.
Overall our project investigated the molecular and ecological underpinnings of the maintenance of adaptive variation in a highly diverse group of tropical insects. Very novel results were found which will make a lasting contribution to evolutionary biology and our understanding of the rules of diversification in the natural world.