Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome-wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.

Automated summary

This study examines the genomic basis of rapid adaptation in the Trinidadian guppy using population genomics. The results show that guppies transplanted from high-predation environments to low-predation environments rapidly evolve towards the phenotypes of naturally colonized low-predation populations. Genome-wide analysis reveals clear signals of population growth and bottlenecks, as well as a region on chromosome 15 under strong selection. These findings provide remarkable insight into the mechanisms underlying rapid adaptation in this species.