High complexity of aquatic irradiance may have driven the evolution of four-dimensional colour vision in shallow-water fish

A major goal of sensory ecology is to identify factors that underlie sensory-trait variation. One open question centers on why fishes show the greatest diversity among vertebrates in their capacity to detect color (i.e. spectral sensitivity). Over the past several decades, λ max values (photoreceptor class peak sensitivity) and chromacy (photoreceptor class number) have been cataloged for hundreds of fish species, yet the ecological basis of this diversity and the functional significance of high chromacy levels (e.g. tetra-and pentachromacy) remain unclear. In this study, we examined phylogenetic, physiological and ecological patterns of spectral sensitivity of ray-finned fishes (Actinoptergyii) via a meta-analysis of data compiled from 213 species. Across the fishes sampled, our results indicate that trichromacy is most common, ultraviolet λ max values are not found in monochromatic or dichromatic species, and increasing chromacy, including from tetra-to pentachromacy, significantly increases spectral sensitivity range. In an ecological analysis, multivariate phylogenetic latent liability modeling was performed to analyze correlations between chromacy and five hypothesized predictors (depth, habitat, diet, body coloration, body size). In a model not accounting for phylogenetic relatedness, each predictor with the exception of habitat significantly correlated with chromacy: a positive relationship in body color and negative relationships with body size, diet and depth. However, after phylogenetic correction, the only remaining correlated predictor was depth. The findings of this study indicate that phyletic heritage and depth are important factors in fish spectral sensitivity and impart caution about excluding phylogenetic comparative methods in studies of sensory trait variation.

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Spectral sensitivity in ray-finned fishes: diversity, ecology, and shared descent

Schweikert

Fitak

Caves

et al. 2018

“…The spectrum and intensity of environmental light place constraints on the visual system (Lythgoe, 1968;Lythgoe, 1979;Sabbah et al, 2013a), and influence the success of visual tasks such as mate choice (Sundin et al, 2010) and foraging (Maddocks et al, 2001). 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).…”

Section: Introductionmentioning

confidence: 99%

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

Hornsby

Sabbah

Robertson

et al. 2013

Self Cite

SUMMARYSignal reception and production form the basis of animal visual communication, and are largely constrained by environmental light. However, the role of environmental light in producing variation in either signal reception or production has not been fully investigated. To chart the effect of environmental light on visual sensitivity and body colouration throughout ontogeny, we measured spectral sensitivity, lens transmission and body pattern reflectance from juvenile and adult Nile tilapia held under two environmental light treatments. Spectral sensitivity in juveniles reared under a broad-spectrum light treatment and a red-shifted light treatment differed mostly at short wavelengths, where the irradiance of the two light treatments differed the most. In contrast, adults held under the same two light treatments did not differ in spectral sensitivity. Lens transmission in both juveniles and adults did not differ significantly between environmental light treatments, indicating that differences in spectral sensitivity of juveniles originated in the retina. Juveniles and adults held under the two environmental light treatments differed in spectral reflectance, and adults transferred to a third, white light treatment differed in spectral reflectance from their counterparts held under the two original treatments. These results demonstrate that environmental light plays a crucial role in shaping signal reception in juveniles and signal production throughout ontogeny, reinforcing the notion that environmental light has the capacity to influence animal communication, and suggesting that the characteristics of environmental light should be considered in models of ecological speciation.Key words: ontogenetic variation, visual sensitivity, body colouration, sensory drive, animal communication. (Kocher, 2004), and are a growing presence in laboratory research (El-Sayed, 2006). Cichlid fish show variation in signal reception, as visual pigment complements show a great range of natural variation (Carleton and Kocher, 2001;Parry et al., 2005;Sabbah et al., 2010;O'Quin et al., 2010). Additionally, cichlids are notorious for their variation in signal production, showing myriad behaviours (Barlow, 2000) and body colourations (Kornfield and Smith, 2000), many of which are species specific (Hofmann et al., 2009). When these sources of variation are coupled with changes in the spectral quality of available environmental light, which, for example, occur as water depth varies (e.g. Sabbah et al., 2011), the basic requirements for sensory drive are met. However, the role of environmental light in these sources of variation, particularly signal production, remains somewhat elusive.Nile tilapia have been shown to differentially express seven visual pigments throughout ontogeny: SWS1 (360nm), SWS2b (425nm), SWS2a (456nm), Rh2b (472nm), Rh2aβ (518nm), Rh2aα (528nm) and LWS (561nm) (Spady et al., 2006). Juveniles predominantly express SWS2b, SWS2a, Rh2a (a combination of Rh2aβ and Rh2aα, as their maximum absorbance wavelengt...

“…We suggest that a history of natural selection in spectrally variable shallow waters maintains the expression of at least four spectral classes of opsins in branchiopods, as it does in shallow-water fish (Hofmann et al, 2009). Shallow-water fish in habitats that do not attenuate light as quickly with depth as those hosting branchiopods use four spectral channels for true color vision (Sabbah et al, 2011(Sabbah et al, , 2013. Branchiopods commonly colonize habitats in which there are no fish (Brendonck et al, 2008;Dumont and Negrea, 2002).…”

Section: Neural Substrates For Chromatic and Achromatic Poolingmentioning

confidence: 93%

Multiple spectral channels in branchiopods. I. Vision in dim light and neural correlates

Lessios

Rutowski

Cohen

et al. 2018

Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda+Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here, we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and the optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral freshwater habitats.