Patterns of genetic variation around a locus under strong selection in wild Heliconius populations

Lead Research Organisation: University of Cambridge
Department Name: Zoology

Abstract

Wild populations of all plants and animals vary in many traits that are controlled by genetic variation. Finding the genes that control natural variation in wild populations is a major challenge, important in both applied and basic science. Evolutionary biologists are interested to know what the genes are that control diversity and adaptation in animals and plants, while applied biologists would like to identify genes involved in economically important traits such as disease resistance in crops or insecticide resistance in pests and their relatives. Here we will study a classic system in evolutionary biology, the mimetic wing patterns of tropical Heliconius butterflies. We will use modern molecular techniques to investigate a genetic locus that controls a geographic variation in mimetic pattern in the butterfly Heliconius melpomene and a within-population mimetic polymorphism in the closely-related species Heliconius numata. Mimicry, by which different chemically-defended prey share warning colours, is an ecologically well-understood adaptive trait with selection for convergence within the local prey community. Mimicry alleles vary between and within populations of the same species and are involved in speciation. The P locus in H. numata is found in the same genome region as the N-Yb-Sb locus in H. melpomene. Markers will be generated within all genes present across the region containing the mimicry locus. Variation will then be screened in wild populations of H. numata in order to search for variants that are associated with the pattern phenotype of the butterflies. For example, if a polymorphism occurs between an A and a G at a particular locus, we will investigate whether there is a tendency for the butterflies with a particular wing pattern to have either A or G at a higher frequency than expected at random. We will use high throughput, cost-effective genetic techniques that accurately estimate the association of each variable marker with colour pattern. This work will further localize the region, and possibly identify the gene, that is responsible for dramatic morphological variation and adaptation to local prey communities. In H. melpomene, where all individuals in any particular locality have the same wing pattern, we will investigate whether there is a region that shows reduced variation or a high frequency of rare variants, both of which are suggestive of the recent action of natural selection on a locus. The range margins of H. melpomene races change rapidly, so our work will provide insight into the effect of rapid adaptive range expansion on associated genetic variation.
 
Description This grant aimed to study a classic system in evolutionary biology, the mimetic wing patterns of tropical Heliconius butterflies and investigate a genetic locus that controls both geographic variation in mimetic pattern in the butterfly Heliconius melpomene and a within-population mimetic polymorphism in Heliconius numata. Mimicry, by which different chemically-defended prey share warning colours, is an ecologically well-understood adaptive trait with selection for convergence within the local prey community. The work has been carried out in close collaboration with Mathieu Joron who has been funded by an EMBO fellowship and latterly a Royal Society University Research Fellowship at the University of Edinburgh.

The P locus in H. numata was already known to be in the same genome region as the N-Yb-Sb locus in H. melpomene. During this grant, the region was first cloned in H. melpomene and the candidate region mapped (Fig. 1). Next markers were taken and used to map the homologous region in H. numata, clearly demonstrating concordance of the region in the two species. However subsequently, we have discovered a large genomic rearrangement in H. numata relative to H. melpomene which has considerably complicated the initial view that the two regions were entirely homologous. This result is exciting as it is concordant with the hypothesis that genomic rearrangement has reduced recombination in the 'supergene' architecture of H. numata, but it has significantly complicated the process of obtaining population data for all the genes in the candidate region which was the primary aim of this proposal.

In H. melpomene, where all individuals in any particular locality have the same wing pattern, we aimed to investigate whether there is a region that shows either reduced variation or a high frequency of rare variants, or fixed differences between colour pattern races, which might be indicative of the recent action of natural selection. Despite obtaining a large data set of sequence for 11 gene regions, we have found no clear signal of selection either in terms of reduced variation or differentiation between races (Fig. 2). This implies that the region with a signal of selection is very small relative to the current candidate region. This has implications for genomic scans of loci under selection in wild populations, which may be very challenging if this pattern is common. In contrast, in H. numata there is a clear signal of genetic variation associated with phenotypic variation across a large region of around 50kb.
Exploitation Route Further research on animal patterning and evolution
Sectors Education,Environment

URL http://www.heliconius.org
 
Description Our work on wing patterning has been widely cited in textbooks and in evolutionary biology undergraduate courses. We also presented our work at the Royal Society Summer Science Exhibition 2014 to an audience of 15,000 members of the public
First Year Of Impact 2010
Sector Environment
Impact Types Societal