Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

Abstract

In deep‐water animals, the visual sensory system is often challenged by the dim‐light environment. Here, we focus on the molecular mechanisms involved in rapid deep‐water adaptations. We examined visual system evolution in a small‐scale yet phenotypically and ecologically diverse adaptive radiation, the species flock of cichlid fishes in deep crater lake Barombi Mbo in Cameroon, West Africa. We show that rapid adaptations of the visual system to the novel deep‐water habitat primarily occurred at the level of gene expression changes rather than through nucleotide mutations, which is compatible with the young age of the radiation. Based on retinal bulk RNA sequencing of all eleven species, we found that the opsin gene expression pattern was substantially different for the deep‐water species. The nine shallow‐water species feature an opsin palette dominated by the red‐sensitive (LWS) opsin, whereas the two unrelated deep‐water species lack expression of LWS and the violet‐sensitive (SWS2B) opsin, thereby shifting the cone sensitivity to the centre of the light spectrum. Deep‐water species further predominantly express the green‐sensitive RH2Aα over RH2Aβ. We identified one amino acid substitution in the RH2Aα opsin specific to the deep‐water species. We finally performed a comparative gene expression analysis in retinal tissue of deep‐ vs. shallow‐water species. We thus identified 46 differentially expressed genes, many of which are associated with functions in vision, hypoxia management or circadian clock regulation, with some of them being associated with human eye diseases.

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

“…Similarly, opsin expression in guppies varies between different watershed populations (Sandkam et al, 2015b) and even between populations with high versus low predation (Sandkam et al, 2015a). Opsin expression is also known to vary among fishes living in different small lakes and streams, presumably matching changes in the light environment (Musilova et al, 2019b;Veen et al, 2017).…”

Adaptive Radiation from a Chromosomal Perspective: Evidence of Chromosome Set Stability in Cichlid Fishes (Cichlidae: Teleostei) from the Barombi Mbo Lake, Cameroon

“…This flock is evolutionary quite recent, sharing a most recent common ancestor with the riverine species Sarotherodon galilaeus between 1 and 2.5 million years ago [28,35]. Most of the species in the lake have evolved probably by adaptive ecological speciation [33,34] triggered by the ecological differentiation. For example, deep-water specialists have evolved twice independently within the lake ( Konia dikume , Myaka myaka ; [34,60,61]), a mechanism also recently described from the onset of speciation in Massoko crater lake cichlids [62].…”

“…Most of the species in the lake have evolved probably by adaptive ecological speciation [33,34] triggered by the ecological differentiation. For example, deep-water specialists have evolved twice independently within the lake ( Konia dikume , Myaka myaka ; [34,60,61]), a mechanism also recently described from the onset of speciation in Massoko crater lake cichlids [62]. Further, different trophic strategies have been established within the flock, which includes predators, planktivores, insectivores, pure herbivores, and spongivores [33,34,60,61].…”

“…Despite the size of the lake not exceeding 7 km 2 [31], it harbors an endemic monophyletic radiation of 11 cichlid species. This monophyletic species flock has most likely radiated in situ, via sympatric ecological speciation [32,33,34] from the common ancestor, probably Sarotherodon galilaeus (Oreochromini), which colonized the lake no earlier than one million years ago [17,18,35] when the last substantial geological activity was detected [36,37]. Cichlids from the Barombi Mbo Lake are classified in five genera, four of which are endemic to the lake (i.e., Konia , Myaka , Pungu , and Stomatepia ), and one genus ( Sarotherodon ) is widely used also for other African mostly riverine cichlids [32,38].…”

Visual adaptation could aid sympatric speciation in a deep crater lake

“…In this issue, Musilova et al () have taken a candidate gene approach to understand the diversification of sensory systems in the Barombi Mbo flock. They used quantitative PCR, retinal transcriptomes, and in situ hybridization to study the expression of the opsin genes that determine visual sensitivity.…”