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.

Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies

“…This replicated downstream/HP and upstream/LP habitat has produced convergent HP-LP guppy phenotypes; LP guppies produce fewer, larger, offspring per brood [ 40 , 41 ], differ in shoaling behaviour [ 42 , 43 ], swimming performance [ 44 ] and predator evasion [ 45 ], and exhibit brighter sexual ornamentation [ 46 ]. However, whilst LP guppies evolve brighter colouration, the repeatability of specific colour patterns is limited and can be non-parallel [ 47 , 48 ]. Rearing second generation HP-LP guppies in a laboratory setting with controlled rearing conditions confirms that observed differences in life history have a genetic basis [ 49 ], and additional work has further demonstrated heritability for colour [ 50 , 51 ] and behaviour [ 52 ].…”

Dimensionality and modularity of adaptive variation: Divergence in threespine stickleback from diverse environments

“…The implications of these findings are important to consider when attempting to assess the repeatability and predictability of evolution in nature, one of the central themes of evolutionary biology. The possibility of adaptation in a high-dimensional space certainly makes predicting the evolutionary effect of an environmental condition in any particular instance difficult, even with high-quality data about multiple aspects of the environment and when the relatedness among populations is known (Stuart et al 2017; Yong et al 2020). However, the potential to adapt along a number of axes may increase resilience to environmental changes, allowing a population to adapt to the change in the context of its specific habitat conditions (Reisch et al 2015), rather constraining it to a single axis that may be perpendicular to the direction of selection.…”