Genomic analysis of complex speciation in Heliconius

Lead Research Organisation: University of Cambridge
Department Name: Zoology

Abstract

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.
 
Description 1) The most significant achievement of the grant was demonstration of adaptive introgression between Heliconius species, recently published in Nature. We contributed to this discovery by designing and applying the SureSelect targeted sequence capture that generated this data, and collaborating with Kanchon Dasmahapatra on analysis pipelines used for these data.

2) The grant contributed to generation of a genome sequence for Heliconius melpomene, and in particular in mapping of the genome scaffolds to chromosomes. My group raised mapping families, constructed RAD libraries and carried out linkage analysis in collaboration with John Davey at GenePool to achieve this goal. This provides a model for the analysis of genomes in non-model species.

3) Comparative analysis of islands of speciation. The grant also demonstrated evidence for the hypothesis that islands of divergence gradually enlarge during speciation, through comparison between H. melpomene races and more distant species H. timareta and H. hecale.
Exploitation Route Further research in this area. Comparative insect genomics analysis using the genome sequence, including potential uses for analysis of crop pests.
Sectors Agriculture, Food and Drink,Education,Environment

URL http://www.heliconius.org
 
Description The work has played an important role in promoting the idea of adaptive introgression and the importance of hybridisation in evolution. The project led to publication of the Heliconius genome which has been a resource for comparative insect genomics and has made Heliconius one of the high quality insect genomes available for population genomic analysis. In addition the project contributed towards our Royal Society Summer Science Exhibition at which more than 14,000 members of the public saw our exhibit and learnt about the evolution of butterfly wing patterns and hybridisation.
First Year Of Impact 2012
Sector Education,Environment
Impact Types Cultural,Societal

 
Description BBSRC BBR Fund
Amount £534,491 (GBP)
Funding ID BB/K020161/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 11/2013 
End 06/2017
 
Description ERC Advanced Grant
Amount € 2,500,000 (EUR)
Funding ID SpeciationGenetics 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 06/2014 
End 06/2019
 
Title Heliconius genome sequence 
Description ENSEMBL database of the Heliconius genome 
Type Of Material Database/Collection of data 
Year Produced 2012 
Provided To Others? Yes  
Impact Widely used in genomic research 
URL http://metazoa.ensembl.org/Heliconius_melpomene/Info/Index
 
Title LepBase 
Description LepBase is a community resource providing lepidopteran genome sequences in a genome browser based on the ENSEMBL format. This provides tools for comparative genome analysis. This database is the first community level database to use the ENSEMBL genome browser established outside the EBI and as such provides a model for future community genomics databases 
Type Of Material Database/Collection of data 
Year Produced 2015 
Provided To Others? Yes  
Impact The resource is being widely used by the lepidopteran genome community for functional and research applications 
URL http://ensembl.lepbase.org/index.html
 
Description Heliconius Genome Consortium 
Organisation Baylor College of Medicine
Department Human Genome Sequencing Centre
Country United States 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Description Heliconius Genome Consortium 
Organisation Cornell University
Country United States 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Description Heliconius Genome Consortium 
Organisation Harvard University
Country United States 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Description Heliconius Genome Consortium 
Organisation National Museum of Natural History
Country United States 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Description Heliconius Genome Consortium 
Organisation Smithsonian Institution
Department Smithsonian Tropical Research Institute
Country Panama 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Description Heliconius Genome Consortium 
Organisation University of the Andes, Chile
Country Chile 
Sector Academic/University 
PI Contribution I led establishment of the Heliconius Genome Consortium which sequenced the first butterfly genome
Collaborator Contribution Many skills in genomic analysis and Heliconius biology
Impact Genome sequenced and published
Start Year 2010
 
Title Lepbase Genome Database 
Description A web database for interrogation of genome sequences across the Lepidoptera (moths and butterflies), a large group of insects that includes many pest species 
Type Of Technology Webtool/Application 
Year Produced 2015 
Impact This is now a widely used resource for the genomics community in our field 
URL http://ensembl.lepbase.org/index.html