Chromosomal Fusions Facilitate Adaptation to Divergent Environments in Threespine Stickleback

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 (QTL) 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.

Local Adaptation and the Evolution of Genome Architecture in Threespine Stickleback

“…This is particularly noteworthy given that in both threespine and ninespine stickleback, chromosome IV has likely been created by fusions of the same ancestral chromosomes, which would be very unlikely to happen by chance. These patterns are consistent with another analysis of macro-rearrangements using a de novo assembly of the fourspine stickleback ( Liu, Chen, et al 2021 ; Liu, Roesti, et al 2022 ), and strongly suggest an adaptive mechanism driving macro-rearrangements in stickleback. Finding macro-rearrangements associated with local adaptation is consistent with population genetic predictions: if two locally adapted loci experience selection of s a and s b and are separated by recombination at rate r , then they will experience an advantage due to linkage whenever r < s a s b / m , where m is the migration rate ( Yeaman et al 2016 ).…”

Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots

“…Breakpoints of inter-chromosomal rearrangements. We next asked whether the chromosomal fusions were adaptive 72,73 , and whether fissions occurred at random positions. To evaluate whether the newly joined chromatins have established frequent interactions due to new cis-regulation across the fusion sites, we examined the fusion sites for insulation scores (ISs).…”

Chromosomal inversions can limit adaptation to new environments

“…The here-described idea of how inversions may limit rapid adaptation to changing ecological conditions seems compatible with observations in nature. For instance, QTL underlying trait variation that is important for adaptive divergence across a major habitat transition have been mapped to chromosomal inversions in populations of threespine stickleback fish and littorina snails (stickleback: Peichel & Marques 2017; Liu et al 2021; littorina: Koch et al 2021). However, both of these species have recently been exposed to new niches imposing novel selection pressures, possibly favoring novel combinations of these inversion-linked QTL (stickleback: e.g., Bell & Foster 1994; Reid et al 2021; littorina: Morales et al 2019).…”

“…transition have been mapped to chromosomal inversions in populations of threespine stickleback fish and littorina snails (stickleback:Peichel & Marques 2017;Liu et al 2021; littorina: Koch et al 2021). However, both of these species have recently been exposed to new niches imposing novel selection pressures, possibly favoring novel combinations of these inversion-linked QTL (stickleback: e.g.,Bell & Foster 1994;Reid et al 2021; littorina: Morales et al 2019).…”