Abstract
Rapid adaptation is critical for species persistence in the face of accelerating environmental change, yet the genomic mechanisms underlying the evolution of complex ecotypes remain poorly understood. Natural systems in which similar phenotypes arise repeatedly in parallel provide powerful opportunities to identify the genomic basis of multi-trait evolutionary shifts. In the geographically turbulent freshwater environment of Aotearoa / New Zealand, the facultatively migratory fish Galaxias brevipinnis (kōaro) repeatedly evolves distinct ecotypes following colonisation of lakes formed through natural or anthropogenic isolation. Despite independent origins, these landlocked populations exhibit highly parallel shifts in a number of complex life-history traits over staggeringly rapid ecological timescales. Using genome-wide data from five migratory and eight landlocked kōaro populations across Southern Aotearoa, I aimed to examine population genetic structure and investigate the genomic mechanisms underpinning rapid transitions to a consistent freshwater ecotype in G. brevipinnis. Through construction of a chromosome-level reference genome and analysis of genome-wide SNP data, I uncover a consistent genomic signal associated with parallel life history transitions. Specifically, genome wide scans identified that a majority of outlier loci consistently differentiating landlocked and migratory populations were co-located within a single genomic region, containing several genes implicated in divergent ecotype traits. The tight co-location of outlier loci, together with emerging evidence of elevated linkage disequilibrium in this region suggests freshwater-adaptive alleles may be maintained together as an intact ‘haploblock’. Through this mechanism, modular genomic architecture may circumvent the need for recombination of variation over several generations, allowing rapid evolution. Outlier alleles occur at high frequencies across landlocked populations, but remain rare in migratory stocks consistent with repeated selection on standing variation. Critically, a small number of migratory individuals are widely heterozygous across this outlier region, and may represent ‘jackpot’ individuals carrying intact freshwater-adaptive sequences recessively. Detection of these jackpot carriers within the migratory population indicates this may provide an elegant mechanism allowing the rapid ecotype shifts detected in Galaxias brevipinnis populations isolated by recent catastrophic landslides in Aotearoa. Collectively, these results highlight the crucial role of modular genomic variation in facilitating rapid adaptive change.