Ashleigh Iwikau, Jason Augspurger, Marc Bailie, Graham A. McCulloch, Mitra M. Darestani, Tania M. King, Gerard P. Closs, Travis Ingram, P. Mark Lokman, Bruce Deagle, Christopher P. Burridge, Ludovic Dutoit, Jonathan M. Waters
Adaptation is considered essential for species facing environmental change, but our understanding of the evolution of complex ecotypes remains limited. We show that a substantial genomic cluster of co-adapted alleles has repeatedly fuelled complex life-history shifts in fishes. Specifically, the majority of strong outlier loci underpinning repeated landlocking of formerly marine-migratory Galaxias lineages are co-located on a single chromosome. Phenotypic, behavioural and genomic comparisons reveal a strong parallel basis for multi-trait ecotype shifts (osmoregulation; musculature; locomotion; reproduction) across eight independently landlocked populations. Critically, migratory populations house 'jackpot' individuals carrying intact sequences essential for rapid multi-trait life-history switches. The observed high frequencies of these migratory jackpot carriers explain the rapid ecotype shifts detected in Galaxias populations isolated by recent catastrophic landslides in New Zealand. These findings represent a complete example of complex ecotype evolution, highlighting the key role of modular genomic variation in facilitating rapid adaptive change.