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The genomic architecture of speciation in tropical butterflies

Final Report Summary - SPECIATIONGENETICS (The genomic architecture of speciation in tropical butterflies)

Speciation is the evolutionary process that gives rise to biodiversity, and as such is fundamental to our understanding of evolution and of the world around us. These are exciting times for speciation research with a wealth of recent theoretical and empirical advances, but there is much we still do not understand. The Heliconius butterflies offer an excellent opportunity to gain novel insights into the genetic architecture of speciation and its genomic consequences, by integrating genomic data with the well-studied ecological and behavioural processes that underlie speciation in this group. Here we are bringing together two lines of recent research in speciation, a) the evolution of genetic architectures, such as clustering of barrier genes, that facilitate divergence in the face of gene flow and b) the genomic patterns of divergence.
First, we have greatly improved the genome sequence for Heliconius melpomene, generating a near-complete chromosomal assembly of the genome of this species. We have then applied large-scale whole genome resequencing to study patterns of divergence and exchange between the species. This has demonstrated widespread evidence for genetic exchange between these species, despite the fact that they hybridise only rarely. The patterns of exchange between the species offer insight into this process.
Second, we have investigated the genetic basis for traits that differentiate the two species, using a genome-wide quantitative trait analysis of reproductive isolation in two hybridizing species pairs. This has demonstrated the existence of major loci underlying behavioural isolation between the species, suggesting a relatively simple genetic basis for mating preferences. We can also map hybrid sterility in our crosses which seems to similarly be affected by a single large-effect locus on the X-chromosome. We have identified a novel terpene synthase gene responsible for pheromone difference between the species. We also explored patterns of introgression and selection on wing patterning genes across the radiation, demonstrating signatures of adaptive introgression and widespread selection.
Third, we have investigated the role of chromosomal rearrangements in reducing between-species recombination rate where species hybridize. Despite widespread interest in this topic among speciation biologists, we have found no evidence for genomic rearrangements that differentiate the closely related hybridizing species that we have studied. The genomes of these species are highly conserved in their gene order and chromosome level organization. We also showed that introgression is regulated by rates of recombination across the genome.
Overall, the project integrates information on the distribution of genes controlling ecological, behavioural and genetic differences between species with patterns of recombination, in order to understand the process of genome divergence and adaptive radiation. This work has offered new insights into speciation, a process fundamental to evolution and biodiversity, but also has wider implications for our understanding of the processes that drive genome evolution.