Sensory-based quantification of male colour patterns in Trinidadian guppies reveals nonparallel phenotypic evolution across an ecological transition in multivariate trait space

Abstract

Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy. In guppies, colonisation of low predation habitats is associated with emergence of more colourful phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuity remains strong. Our study differs from previous investigations in three respects. First, we adopt a multivariate phenotyping approach to characterise parallelism in multi-trait space. Second, we use ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e. guppy, predatory cichlid). Third, we estimate population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypyc divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model, but only limited support for the predicted pattern of greater conspicuity at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely non-significant, and explained little among-population variation. In multi-trait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation by female choice, but suggest that this proceeds in (effectively) independent directions of multi-trait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality and/or associations with known colour genes in other species, presenting opportunities for future genetic study.