Rapid genome-wide purging following tsunami-induced hybridization in a stickleback population

Abstract

Speciation is the process by which barriers to gene flow evolve between populations. As speciation approaches completion, genome-wide divergence can be maintained in the face of hybridization. Because real-time observations of genomic changes following hybridization in natural populations remain rare, little is known about the processes and mechanisms by which introgressed genomes are purged in nature. Here we report a 9-year genomic monitoring of a tsunami-induced hybrid stickleback population, revealing rapid genome-wide purging within only a few generations. On 11 March 2011, a devastating tsunami struck the Tohoku Region, Japan, creating new stickleback habitats and inducing hybridization between freshwater Gasterosteus aculeatus and marine Gasterosteus nipponicus. Within the first few generations, G. nipponicus alleles were purged at major loci responsible for reproductive isolation, including ancestral-X and neo-X chromosomes. These loci are involved in freshwater survival, migratory divergence associated with habitat choice, sexual isolation and hybrid sterility. Subsequently, G. nipponicus alleles were purged across the genome except at several loci. We provide direct evidence from a natural population that rapid genome-wide purging allows species identity to persist even after extensive introgression. Elucidating the genetic mechanisms underlying genome-wide purging is crucial for understanding the factors that drive progress towards speciation completion. Species persistence following hybridization in nature requires the purging of introgressed alleles. Genomic monitoring of a tsunami-induced hybrid stickleback population in Japan reveals rapid genome-wide purging including of loci involved in reproductive isolation.