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Abstract

High- (HP) and low-predation (LP) Trinidadian guppies are a textbook example of convergent evolution. LP guppies have repeatedly evolved from HP sources to be more colourful and have longer life histories, but, despite a plethora of phenotypic data, whether this process involves the same genes is unknown. Here, we present results from whole-genome sequencing data from five HP-LP river pairs to address this question, highlighting constraints that are predicted to reduce the likelihood of genetic convergence. We first analyse the distribution and structuring of genetic variation across our rivers, observing strict drainage-structuring, recurrent LP bottlenecks, and some limited between-river introgression. These results imply constraints on shared adaptive variation among LP populations. Selection scans across all river pairs highlight limited overlapping regions under selection, but genes of similar function are under selection in all five rivers, suggesting limited functional redundancy. Finally, we explore a large candidate haplotype fixed in three LP populations from the same drainage. We explore this region by reconstructing its hylogenetic history and using a novel multivariate method involving allele frequency (AF) vectors. Phylogenetics suggest these three LP populations have fixed a common ancestral haplotype, but further analysis of subtle AF changes hints all five rivers may be experiencing parallel and non-parallel selection at a TE-rich region within the haplotype. Combined, these results present the guppy as a compelling system in which convergent phenotypes are derived by convergent and nonconvergent changes at the genome level, and points towards important limitations in governing this phenomenon.