Rare Jackpot Individuals Drive Rapid Adaptation in Threespine Stickleback

Abstract

Recombination has long been considered the primary mechanism to bring beneficial alleles together, which can increase the speed of adaptation from standing genetic variation. Recombination is fundamental to the transporter hypothesis proposed to explain precise parallel adaptation in Threespine Stickleback. We studied an instance of freshwater adaptation in the Threespine Stickleback system using whole genomic data from an evolutionary time series to observe the genomic dynamics underlying rapid parallel adaptation. Our experiment showed that rapid adaptation to a freshwater environment depended on a few individuals with large haploblocks of freshwater-adaptive alleles (jackpot carriers) present among the anadromous (i.e., sea-run) founders at low frequencies. Biological kinship analyses indicate that mating among jackpot carriers and between jackpot carriers and non-jackpot individuals led to a rapid increase in freshwater-adaptive alleles within the first few generations. This process allowed the population to overcome a substantial bottleneck likely caused by the low fitness of first-generation stickleback with a few freshwater-adaptive alleles born in the lake. Additionally, we found evidence that the genetic load that emerged from population growth after the bottleneck may have been reduced through an increase in homozygosity by inbreeding, ultimately purging deleterious alleles. Recombination likely played a limited role in this case of very rapid adaptation.