Relative LWS cone opsin expression determines optomotor thresholds in Malawi cichlid fish

Abstract

Associating quantitative genetic traits with quantitative behaviors is a relatively unexplored region of sensory neurobiology. The visual system is an ideal place to test models associating these levels of sensory perception. In this study, we reared cichlid fish from Lake Malawi in different ambient light environments. We then tested the visual sensitivities of these fish using the optomotor response (OMR) behavioral paradigm and measured the relative expression of cone opsin genes. We found that the light environment experienced by fish during development can alter gene expression, particularly as it applies to the long wavelength-sensitive (LWS) opsin gene. Also, fish from different rearing conditions exhibited different behavioral sensitivities. We combined these data with predictions of opsin pigment absorption by the different OMR stimuli to determine which cone types are most likely to influence the OMR behavior. While we hypothesized that this behavior would be controlled by a random-wiring model reflecting the expression of both medium wavelength-sensitive (MWS) and LWS opsins, our models suggest that only the LWS pigment is required to predict behavior. Furthermore, analyses show that LWS expression variation accounts for ∼20% of the observed behavioral variance. This work confirms that sensory gene expression influences behavior in a predictable fashion. It also suggests that the neural wiring of basal visual pathways in cichlid fish may differ from that observed in mammals and zebrafish, but is similar to that described in goldfish. This finding has important implications for the evolution of the magnocellular neural pathway in teleosts.

Modulation of environmental light alters reception and production of visual signals in Nile tilapia

“…Reflectance spectra correlated with each other, and each spectrum comprised a large number of data points. Therefore, we used principal component analysis (PCA) to reduce the redundancy in the reflectance dataset (Smith, 2002). For each life stage, PCA was performed on the whole spectral reflectance dataset that included all fish from all light treatments, and the loadings of the various principal components (PCs) were obtained.…”

“…Nonetheless, while there is some evidence that environmental light can drive variation in signal reception (Shand et al, 2008;Fuller and Claricoates, 2011;Smith et al, 2012), evidence for the ability of environmental light to drive variation in signal production is scant (but see Imanpoor and Abdollahi, 2011;Kelley et al, 2012).…”

Differential Survival between Visual Environments Supports a Role of Divergent Sensory Drive in Cichlid Fish Speciation

“…Fish visual systems have been shown to respond plastically to environmental variation (Fuller et al 2005;Shand et al 2008), influencing visually guided behaviors such as foraging and mate choice . Also in cichlids, the expression of retinal pigments and different photoreceptors changes in response to the light conditions during development (Van der Meer 1993;Smith et al 2012), but some species show stronger responses than others . The data presented here suggest that Pundamilia may express limited plasticity and/or that the plastic response is not sufficient to compensate for the genetically determined species differences in visual development.…”

Evolution of bower building in Lake Malawi cichlid fish: phylogeny, morphology, and behavior

“…The nature of this relationship is largely determined by the visual environment, as determined by factors such as depth. This has apparently played an important role in the variable distribution of male coloration and photoreceptor opsins properties amongst Lake Malawi cichlids, and is putatively shaped by sexual selection (Smith et al, 2012).…”