Sensory‐based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution 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 (Poecilia reticulata). 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 conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically‐relevant colour traits defined by the visual systems of the two selective agents (i.e., guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among‐population variation. In multitrait 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, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool‐sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.

Partial sex linkage and linkage disequilibrium on the guppy sex chromosome

“…Low diversity in upstream populations is consistent with previous studies of polymorphic microsatellite or SNP markers (Barson et al, 2009;Willing et al, 2010).and very high FST values between pairs of samples from upstream populations from different rivers, though previous studies of FST either did not provide nucleotide diversity estimates (Suk & Neff, 2009;Fraser et al, 2015) or did not detect bottlenecks (Willing et al, 2010). FST estimates using the same PoolSeq data as analysed here (Yong et al, 2021 see Supplementary Table S2), support the same pattern, and a recent population genomics study using all site types inferred the occurrence of bottlenecks in several rivers (Whiting et al, 2021). Our analyses of synonymous, probably weakly selected, variants in coding sequences reveals specific loss of rare variants, as expected if upstream populations are recovering after having lost diversity in their recent history.…”

“…Low coverage Illumina sequencing was done for separate male and female pools, each of 20 individuals, for each sample, yielding sequence lengths of 150 bp, and the raw sequence reads from the 24 pools were processed as described previously (Yong, Croft, Troscianko, Ramnarine, & Wilson, 2021). Briefly, reads were trimmed to remove low quality bases and adapter sequences using cutadapt .…”

Revisiting old truths: The evolution of male coloration in guppies as a function of predation

“…Discerning the role of predation on colour pattern evolution requires controlling for differences among drainages. Other studies have found results that are consistent with Endler's original work, although many studies were conducted on the Marianne River drainage (Millar et al 2006;Gotanda & Hendry 2014), where both Yong et al (2021) and Valvo et al (2021) found evidence for large changes in conspicuousness. Multiple transplant studies have found that male coloration changes when predation risk is altered (Endler, 1980;Gordon et al, 2015;Gotanda et al, 2019;Kemp et al, 2018).…”

“…What are we to make of these three separate studies? Do the results of Millar and Hendry (2012), Valvo et al (2021), and Yong et al (2021) invalidate our long‐held assumptions about colour evolution in guppies? Before answering this question, five points deserve consideration.…”

“…Second, one aspect of Yong et al (2021) that gives pause for thought is that the authors modelled the guppy visual system assuming a four‐cone visual system. In reality, guppies have at least five separate cone cells, with lambda max values at ~359, 408, 465, 525–540 and 560 nm (Archer & Lythgoe, 1990; Sandkam et al, 2018; Watson et al, 2011).…”