Genomic analysis of complex speciation in Heliconius

Lead Research Organisation: University College London
Department Name: Genetics Evolution and Environment


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.

Technical Summary

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.


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Description This research investigated the possibility that species occasionally share genomic information, and that this variation may
sometimes be employed in adaptive evolution.

Since the mid 20th Century, species have been inferred to be "reproductively isolated." It was assumed that genes cannot
usually be transferred among members of different species. It has long been known that species occasionally hybridize,
and that their progeny, while often suffering from sterility and other problems, may produce at least some fertile offspring.
The problems of hybrids led to the belief that the possibility of gene transfer was remote. Indeed, the very fact of hybrid
sterility and hybrid inviability suggested that hybridization was rarely successful over the long term.

Newer DNA sequencing technologies became available late in the first decade of the 21st Century, long after these views
had been crystallized. Genomic resequencing methods provide the possibility for definitive tests that species share
genomic regions via hybridization. We adapted new molecular methods and applied them to Passionflower Butterflies
(genus Heliconius) of the Amazon basin.

In the course of this work, the investigators on this BBSRC project brought to fruition the first complete, annotated and
chromosomally mapped genome project in a butterfly, Heliconius melpomene.

Heliconius are warningly coloured and protected from predators by unpleasant taste. Many species also show "Mullerian
mimicry" with other species: this consists of copying a signal (such as a colourful warning pattern) of one species by
another that is also unpalatable. Because naïve predators must attack unpalatable prey in order to learn that the warning
colour advertises distastefulness, both mimic and model benefit from reduced attacks due to faster predator learning of the
same rather than different colour patterns.

Using the latest resequencing methods, we showed that sequences from across the genome are indeed shared between
closely related species that occasionally hybridize. Although hybridization is rare and often unsuccessful, the continual
trickle of hybridization among species provides sufficient gene flow to have a powerful effect over the long term. In our
most recent estimate (in Panama), different species that occurred together have exchanged 40% or more of their genome
with related species in the same area. Furthermore, we were able to show that gene exchange has occurred over a long
period during the history of both species, dating back to near the time when the two species initially diverged. We have
also shown that some of this admixed sequence is used in adaptive evolution: regions that determine colour pattern
switching are included among the regions that have been exchanged.

We have also shown that occasional hybridization may occasionally lead to the origin of new species. We discovered
during the course of this work that the widespread butterfly Heliconius elevatus may be an example of the origin of new
species triggered by hybridization.
Exploitation Route Our methods are quite general, and could be employed for many other studies of introgression, or indeed population and
linkage-mapping studies of any kind, including organisms of commercial or health importance such as pests or carriers of
pathogenic microbes.

Versions of our low-cost genome sequencing and assembly strategy has been now used by other groups working on other non-model organisms, and these strategies is revolutionising evolutionary biology as well as agriculture and healthcare. Closer to home, a revised strategy of our group has now led to an extremely impressive Heliconius erato genome with an N50 score of 11 Mb. We are currently working on a 20-genome Heliconius project using similar methods in order to exploit comparative methods in genomics.
Sectors Agriculture, Food and Drink,Environment,Healthcare

Description A number of our findings have made the news, and we've all had quite a lot of publicity because of our somewhat counter-intuitive findings that a number of different adaptations have been exchanged, via occasional hybridization, between "good" species in nature. This work has importance in understanding problems of human health, particularly in vector biology, since a number of cryptic species of African Anopheles (which carry malaria) and Simulium damnosum complex species (which carry river blindness) also show similar signs of gene exchange. Similar findings have also been found in many complexes of insect pests of agriculture. In addition, our work is contributing to a better understanding of species, in particular for conservation in endangered species. Occasional hybridization and reticulation among rapidly evolving species in adaptive radiations is increasingly recognized as important and has adaptive consequences, with our own work in Heliconius butterflies providing a particularly clear example of such adaptation-sharing.
First Year Of Impact 2011
Sector Creative Economy,Education,Environment,Healthcare
Impact Types Cultural,Societal,Economic,Policy & public services