A distributed genomic architecture of repeated thermal adaptation in a low-dispersal marine invader

Abstract

The repeatability of the genomic basis of adaptation depends on both genetic architecture and demographic history. Understanding this repeatability, and therefore the predictability of evolution, is increasingly important under global environmental change. Biological invasions are themselves a major component of global change and provide natural experiments for testing rapid adaptation and genomic parallelism across independently invaded ranges. The colonial ascidian Botryllus schlosseri is a widespread marine invader characterized by restricted larval dispersal and strong population structure. We used low-coverage whole-genome sequencing of 532 B. schlosseri individuals from 24 populations across North America to test for repeated thermal adaptation across the Atlantic and Pacific coasts. Genotype-environment association analyses identified thousands of loci associated with temperature in divergent lineages on either coast. Although most significant SNPs, genomic windows, and genes were lineage-specific, cross-lineage overlap exceeded null expectations, revealing a modest but detectable repeated component of putative thermal adaptation. Temperature-associated variation was broadly distributed across the genome. Regions with distinctive local population structure, potentially reflecting linked haplotypic structure or reduced recombination, showed modest enrichment for genotype-environment associations, particularly in the Pacific lineage, but did not disproportionately contain the parallel component of the response. Together, these results suggest that rapid thermal adaptation in B. schlosseri is partially repeatable despite deep divergence, but is largely distributed across the genome rather than concentrated within a few tightly linked regions. Restricted migration may therefore permit locally adaptive variants to evolve more independently across the genome, reducing the importance of concentrated genomic architectures favored under stronger migration-selection conflict.