Genome annotation of Apeltes quadracus

Chromosomal fusions have been 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 stickleback genome to a
de novo assembly of the fourspine stickleback (Apeltes quadracus) and an
outgroup species, we find two chromosomal fusion events have occurred in
the threespine stickleback lineage. On these fused chromosomes, 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. Surprisingly, we find elevated
genetic diversity within regions under selection in the freshwater
population. However, these results are consistent with a recent simulation
study showing that gene flow can increase diversity in genomic regions
associated with local adaptation. Our demographic models provide evidence
for gene flow between the marine and freshwater populations. By combining
our results with those of 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.

染色体融合被假设为通过两种方式促进生物对不同环境的适应：一是将先前未连锁的适应性等位基因聚集在一起，二是形成低重组区域以促进适应性等位基因的连锁。然而，目前缺乏实证证据支持这一假设。在此，我们通过研究三刺鱼（Gasterosteus aculeatus）来填补这一知识空白——其祖先海水鱼在北半球范围内反复适应了淡水环境。通过将三刺鱼基因组与四刺鱼（Apeltes quadracus）的从头组装基因组及一个外群物种进行比较，我们发现三刺鱼谱系中发生过两次染色体融合事件。在这些融合染色体上，我们观察到与海水-淡水适应相关性状的数量性状位点（QTL）存在富集。此外，通过比较淡水和海水三刺鱼种群的全基因组序列，我们还发现这两条融合染色体上存在歧化选择区域的富集。令人惊讶的是，我们发现淡水种群中选择区域内的遗传多样性有所升高。不过，这一结果与近期一项模拟研究一致，该研究表明基因流可增加与局部适应相关基因组区域的多样性。我们的种群统计模型为海水与淡水种群之间的基因流提供了证据。结合现有研究结果，我们提出：这些融合事件形成了低重组区域，促成了适应性簇的形成，从而在海水与淡水三刺鱼之间反复发生基因流的情况下促进了淡水适应。