Testing sensory drive speciation in cichlid fish: Linking light conditions to opsin expression, opsin genotype and female mate preference

Abstract

Ecological speciation is facilitated when divergent adaptation has direct effects on selective mating. Divergent sensory adaptation could generate such direct effects, by mediating both ecological performance and mate selection. In aquatic environments, light attenuation creates distinct photic environments, generating divergent selection on visual systems. Consequently, divergent sensory drive has been implicated in the diversification of several fish species. Here, we experimentally test whether divergent visual adaptation explains the divergence of mate preferences in Haplochromine cichlids. Blue and red Pundamilia co‐occur across south‐eastern Lake Victoria. They inhabit different photic conditions and have distinct visual system properties. Previously, we documented that rearing fish under different light conditions influences female preference for blue versus red males. Here, we examine to what extent variation in female mate preference can be explained by variation in visual system properties, testing the causal link between visual perception and preference. We find that our experimental light manipulations influence opsin expression, suggesting a potential role for phenotypic plasticity in optimizing visual performance. However, variation in opsin expression does not explain species differences in female preference. Instead, female preference covaries with allelic variation in the long‐wavelength‐sensitive opsin gene (LWS), when assessed under broad‐spectrum light. Taken together, our study presents evidence for environmental plasticity in opsin expression and confirms the important role of colour perception in shaping female mate preferences in Pundamilia. However, it does not constitute unequivocal evidence for the direct effects of visual adaptation on assortative mating.

Contribution of opsins and chromophores to cone pigment variation across populations of Lake Victoria cichlids

“…Such plasticity may enhance population persistence and thereby provide a starting point for evolutionary change (Fusco and Minelli 2010;Price et al 2003,West-Eberhard 2003. Several cichlid species have been shown to change opsin gene expression levels over development and in response to different light regimes (Härer et al 2019;Nandamuri et al 2018;Wright et al 2020), suggesting a potential role of phenotypic plasticity in optimizing visual performance. Also in Pundamilia, expression levels of long-wavelength-sensitive (LWS) and short-wavelength-sensitive (SWS2a) opsins can be influenced by light manipulations (Wright et al 2020).…”

Visual adaptation and microhabitat choice in Lake Victoria cichlid fish

“…To explore this and to assess the causal relationship between visual sensitivity and habitat preference, we manipulate visual development by raising the fish under different light conditions. We have previously shown that these light treatments induce changes in opsin expression in Pundamilia [15]. We therefore predict that the light regime during development influences visual habitat preference as well.…”

Light induced changes in starry flounder (Platichthys stellatus) opsin expression and its influence on vision estimated from a camouflage-based behavioural assay.

“…In addition Sakai et al (2016) found that Lws-3 expression increased in guppies grown in orange light and that fish with higher levels of Lws-3 expression had higher visual sensitivity to nm light (11). Conversely, Wright et al (2020) found colour perception plays an important role in female cichlid mate preference but opsin expression was only weakly correlated and a direct causal link between expression and behaviour was lacking (12).…”