Abstract
Chromosomal fusions are hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles; but, there is little empirical evidence to support this hypothesis. Here, we address this knowledge gap by studying threespine stickleback (Gasterosteus aculeatus), in which ancestral marine fish have repeatedly adapted to freshwater across the northern hemisphere. By comparing the threespine and ninespine stickleback (Pungitius pungitius) genomes to a de novo assembly of the fourspine stickleback (Apeltes quadracus) and an outgroup species, we find two chromosomal fusion events involving the same chromosomes have occurred independently in the threespine and ninespine stickleback lineages. On the fused chromosomes in threespine stickleback, we find an enrichment of quantitative trait loci underlying traits that contribute to marine versus freshwater adaptation. By comparing whole-genome sequences of freshwater and marine threespine stickleback populations, we also find an enrichment of regions under divergent selection on these two fused chromosomes. There is elevated genetic diversity within regions under selection in the freshwater population, consistent with a simulation study showing that gene flow can increase diversity in genomic regions associated with local adaptation and our demographic models showing gene flow between the marine and freshwater populations. Integrating our results with previous studies, we propose that these fusions created regions of low recombination that enabled the formation of adaptative clusters, thereby facilitating freshwater adaptation in the face of recurrent gene flow between marine and freshwater threespine sticklebacks.
Highlights
Chromosomal fusions are hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles
On the fused chromosomes in threespine stickleback, we find an enrichment of quantitative trait loci (QTL) underlying traits that contribute to marine versus freshwater adaptation
There is elevated genetic diversity within regions under selection in the freshwater population, consistent with a simulation study showing that gene flow can increase diversity in genomic regions associated with local adaptation and our demographic models showing gene flow between the marine and freshwater populations
Summary
Chromosomal fusions are hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles. A study incorporating both analytical models and individual-based simulations suggested that genomic clusters are more likely to form through genomic rearrangements that bring together adaptive loci than through the establishment of an adaptive mutation near another locally adapted mutation (Yeaman 2013) Consistent with this finding, empirical studies have often found that such genomic clusters are often associated with chromosomal rearrangements, such as inversions (Kirkpatrick and Barton 2006; Schwander et al 2014; Thompson and Jiggins 2014; Wellenreuther and Bernatchez 2018). Unlike chromosome inversions, which can only create clusters by reducing recombination between loci that are already physically linked, chromosomal fusions have been predicted to facilitate adaption both by bringing together previously unlinked loci and by changing the recombination landscape to create a new region of reduced recombination (Guerrero and Kirkpatrick 2014)
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