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

Abstract

It is now accepted that phenotypic evolution can occur quickly but the genetic 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 mimic naturally-colonised LP populations phenotypically in as few as 8 generations. The new phenotypes persist in subsequent generations in lab environments, indicating their high heritability. Here, we compared whole genome variation in four populations recently introduced into LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography, and uncovered signatures of selection with a combination of genome scans and a novel multivariate approach based on allele frequency change vectors. We were able to identify a limited number of candidate loci for convergent evolution across the genome. In particular, we found a region on chromosome 15 under strong selection in three of the four populations, 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. IMPACT STATEMENTThe genetic basis of rapid adaptation to new environments is largely unknown. Here we take advantage of a unique replicated experiment in the wild, where guppies from a high predation source were introduced into four low predation localities. Previous reports document census size fluctuations and rapid phenotypic evolution in these populations. We used genome-wide sequencing to understand past demography and selection. We detected clear signals of population growth and bottlenecks at the genome-wide level matching known census population data changes. We then identified candidate regions of selection across the genome, some of which were shared between populations. In particular, using a novel multivariate method, we identified parallel allele frequency change at a strong candidate locus for adaptation to low predation. These results and methods will be of use to those studying evolution at a recent, ecological timescale.