Genomic analysis of complex speciation in Heliconius

Recent ideas suggest that evolution of new species (speciation) may be complex, whereby different parts of the genome separate at different times rather than a simple process consisting of a single split. Even our own species has been suggested to result from hybridization with chimpanzee lineages a few million years ago, although this conclusion is contested. Recent high-throughput genomics technologies now permit detailed investigation of complex speciation in likely non-model organism candidates, such as Heliconius butterflies. Heliconius are conspicuous warningly coloured tropical butterflies distasteful to birds. The patterns of most species also mimic those of other Heliconius or ithomiine butterflies. Some species show remarkable divergence in colour patterns between geographical races or species, but others share suspiciously similar patterns with closely related species, which they could have acquired via hybridization long after speciation. Hybridization is common: 35% of species are involved. In the melpomene/silvaniform group, almost all species are known to hybridize and backcross in both lab and in nature. This fascinating system provides an excellent test group for studying recent ideas about complex speciation. In this project, we will determine the extent to which four species (Heliconius melpomene, H. numata, H. elevatus and H. timareta) have recently exchanged parts of their genomes. This project brings together British and overseas knowledge of Heliconius butterfly biology and the latest genomic technologies to understand the genetic mechanisms that lead to the origin and maintenance of species. We propose to combine new high-throughput genomic technologies (454 and Solexa sequencing, and Illumina genotyping array chips) to map genomic regions in two focal species, H. melpomene and H. numata from Peru. Next generation sequencing technology will be used to obtain large amounts of genomic sequence data from the two species to identify thousands of genetic markers (single nucleotide polymorphisms, or SNPs). Subsequently, we will use these SNPs to produce high resolution genetic maps of each species. We will then genotype wild-caught specimens of H. melpomene, H. numata, H. elevatus and H. timareta. If complex speciation is occurring, we expect to find regions of shared polymorphism (indicating regions of recent exchange) and 'genomic islands' of fixed differences (indicating regions of older divergence probably surrounding sites of divergently selected genes such as those affecting mimicry, genomic incompatibility, mate choice, and ecological adaptations). A number of Eastern Andean taxa have recently been discovered that are close to H. melpomene, yet remain distinct from that species. The species contain some gene markers more similar to another species, H. cydno, but unlike that species they often share the local mimicry colour pattern of H. melpomene. We predict that these forms acquired their colour pattern via hybridization, which is a relatively common phenomenon in Heliconius. Using SNPs concentrated around these genes we will investigate the possibility that H. melpomene genes have been transferred to these segregate forms via hybridization, leading to the formation of new hybrid species. These SNPs will also allow investigation of colour pattern polymorphism in races of H. melpomene and H. numata The proposed research is a collaboration between Heliconius experts at a number of UK universities, The Gene Pool (Edinburgh), and the Centre for Microarray Resources (Cambridge). Further laboratory/bioinformatics support will be provided by the Max Planck Institute for Chemical Ecology (Germany). Up to now, whole-genome studies have been restricted to a few model organisms such as fruit flies and mice. Our proposal outlines a means of enabling ground breaking whole-genome understanding of evolution and speciation in a wild tropical organism for the first time.

Recent studies suggest that speciation may be complex, such that different parts of the genome separate at different times, rather than in a simple, single-split process. Even our own species has been suggested to have acquired a chimpanzee X chromosome a few million years ago, although this conclusion is contentious. Few studies have investigated this possibility in any detail in likely candidate species. New genomics technologies now permit detailed investigations of complex speciation in non-model organisms such as the butterflies employed here. We will determine the extent to which four tropical American species (Heliconius melpomene, H. numata, H. elevatus and H. timareta) have recently exchanged parts of their genomes. We propose to combine high-throughput technologies (454/Solexa sequencing and Illumina SNP arrays) to produce high-resolution genomic maps of two main species, H. melpomene and H. numata from Peru; with existing BAC-end sequences these will act as scaffolds for ongoing genomics work by the Heliconius Consortium. We will genotype wild-caught specimens of the four species. If complex speciation is occurring, we expect to find regions of shared polymorphism (indicating regions of recent exchange) and 'genomic islands' of fixed differences (indicating regions of older divergence, in part protected by species isolating traits or regions of divergent selection). Higher resolution SNP maps near two colour pattern determining genes will also allow investigation of colour pattern polymorphism in races of H. melpomene and H. numata, as well as the possibility of transfer of colour pattern genes in East Andean species H. elevatus and H. timareta that share patterns with H. melpomene and are likely to have obtained them via hybridization.