What can we learn about adaptation from the wing pattern genetics of heliconius butterflies?

Abstract

Heliconius wing patterns are an adaptive trait under strong selection in the wild. They are also amenable to genetic studies and have been the focus of evolutionary genetic analysis for many years. Early genetic studies characterised a large number of Mendelian loci with large effects on wing pattern elements in crossing experiments. The recent application of molecular genetic markers has consolidated these studies and led to recognition that a huge range of allelic variation at just a few major loci controls patterns across most of the Heliconius radiation. Some of these loci consist of tightly linked components that control different aspects of the phenotype and can be separated by occasional recombination. More recent quantitative analyses have also identified minor-effect loci that influence the expression of these major loci. Studies of a single locus polymorphism in Heliconius numata provide an example of a 'supergene', in which a single major locus controls segregation of a variable phenotype. This supports 'Turner's Sieve' hypothesis for the evolution of supergenes, whereby sequential linked mutations arise at the same locus. In addition, inversion polymorphisms are associated with wing pattern variation in wild populations, which reduce recombination across the supergene locus. This provides direct evidence that the architecture and organisation of genomes can be shaped by natural selection. There is also evidence that patterns of dominance of the alleles at this locus have also been shaped by natural selection. Mimicry therefore provides a case study of how natural selection shapes the genetic control of adaptive variation.