Phenotypic and genomic dissection of colour pattern variation in a reef fish radiation

Abstract

Coral reefs rank among the most diverse species assemblages on Earth. A particularly striking aspect of coral reef communities is the variety of colour patterns displayed by reef fishes. Colour pattern is known to play a central role in the ecology and evolution of reef fishes through, for example, signalling or camouflage. Nevertheless, colour pattern is a complex trait in reef fishes—actually a collection of traits—that is difficult to analyse in a quantitative and standardized way. This is the challenge that we address in this study using the hamlets (Hypoplectrus spp., Serranidae) as a model system. Our approach involves a custom underwater camera system to take orientation‐ and size‐standardized photographs in situ, colour correction, alignment of the fish images with a combination of landmarks and Bézier curves, and principal component analysis on the colour value of each pixel of each aligned fish. This approach identifies the major colour pattern elements that contribute to phenotypic variation in the group. Furthermore, we complement the image analysis with whole‐genome sequencing to run a multivariate genome‐wide association study for colour pattern variation. This second layer of analysis reveals sharp association peaks along the hamlet genome for each colour pattern element and allows to characterize the phenotypic effect of the single nucleotide polymorphisms that are most strongly associated with colour pattern variation at each association peak. Our results suggest that the diversity of colour patterns displayed by the hamlets is generated by a modular genomic and phenotypic architecture.

Diving into the diversity of colour patterns in reef fishes

“…By aiming to identify genes associated with colour diversity in reef fishes, Coulmance et al (2023) introduce a new promising procedure to collect and produce continuous traits associated with colour pattern variation. This method is here illustrated on the acquisition of colours visible by the human eye, but it is well established that reef fishes can also possess colour patterns that contain ultraviolet (UV) components invisible to the human eye (Marshall, 2000;Siebeck, 2004).…”

“…Here are shown (a) a method of quantification by coding the presence/absence of predefined markings in specific body regions as well as (b) a quantitative method through clustering of each pixel based on colour and luminance similarity, hence allowing the estimation of geometric parameters based on the distribution and number of transitions between adjacent clusters (Endler et al, 2018). The procedure introduced by Coulmance et al (2023) relies on the acquisition of standardized photographs obtained in situ and it complements the available toolkits devoted to the characterization of colour patterns in fishes. Outputs of these methods are quantitative traits, which can be summarized in principal components analyses (or similar ordination methods) and then used to test hypotheses in ecology and evolution.…”

“…On the other hand, it has to be admitted that phenotypic characterization would be mainly built on obvious markings, but tenuous information based on colours restricted to few markings could be lacking. Here, Coulmance et al (2023) introduce and describe a very promising procedure to extract colour data by including all the range of colours visible by human eye and quantify colour pattern variation without any a priori definition of markings.…”

“…First, Coulmance al. (2023) applied their innovative protocol on a data set of 13 hamlet species (Hypoplectrus) to characterize the diversification of their colour patterns.…”

“…This method is here illustrated on the acquisition of colours visible by the human eye, but it is well established that reef fishes can also possess colour patterns that contain ultraviolet (UV) components invisible to the human eye (Marshall, 2000;Siebeck, 2004). By associating the protocol of Coulmance et al (2023) with a photographic method to make the UV patterns visible to the human eye (e.g., Siebeck, 2004), it would F I G U R E 1 Overview of different ways to produce traits characterizing colour patterns and associated colours. All the published methods devoted to the quantification of colour patterns are not illustrated.…”