Turbidity drives plasticity in the eyes and brains of an African cichlid.

Natural variation in environmental turbidity correlates with variation in the visual sensory system of many fishes, suggesting that turbidity may act as a strong selective agent on visual systems. Since many aquatic systems experience increased turbidity due to anthropogenic perturbations, it is important to understand the degree to which fish can respond to rapid shifts in their visual environment, and whether such responses can occur within the lifetime of an individual. We examined whether developmental exposure to turbidity (clear, <5 NTU; turbid, ∼9 NTU) influenced the size of morphological structures associated with vision in the African blue-lip cichlid Pseudocrenilabrus multicolor. Parental fish were collected from two sites (clear swamp, turbid river) in western Uganda. F1 broods from each population were split and reared under clear and turbid rearing treatments until maturity. We measured morphological traits associated with the visual sensory system (eye diameter, pupil diameter, axial length, brain mass, optic tectum volume) over the course of development. Age was significant in explaining variation in visual traits even when standardized for body size, suggesting an ontogenetic shift in the relative size of eyes and brains. When age groups were analyzed separately, young fish reared in turbid water grew larger eyes than fish reared in clear conditions. Population was important in the older age category, with swamp-origin fish having relatively larger eyes and optic lobes relative to river-origin fish. Plastic responses during development may be important for coping with a more variable visual environment associated with anthropogenically induced turbidity.

Visual performance impaired by elevated sedimentary and algal turbidity in walleye Sander vitreus and emerald shiner Notropis atherinoides.

The objectives of this study were to determine the effects of different forms of elevated turbidity on the visual acuity of two native Lake Erie fishes and to assess the response of fishes from different trophic levels to elevated turbidity. Additionally, the role of visual morphology (e.g., eye and optic lobe size) on visual acuity was evaluated across visual environments. Reaction distance, a behavioural proxy for measures of visual acuity, was measured for a top predator, walleye Sander vitreus and a forage fish, emerald shiner Notropis atherinoides. In both S. vitreus (n = 27) and N. atherinoides (n = 40) reaction distance across all types of turbidity (sedimentary, algal, sedimentary + algal; 20 NTU) was approximately 50% lower relative to the clear treatment. Reaction distance was further reduced in algal compared with sedimentary turbidity for wild-caught S. vitreus. Eye and brain morphology also influenced reaction distance across turbidity treatments, such that larger relative eye and brain metrics were positively correlated with reaction distance. This study provides evidence for disrupted visual acuity as a potential mechanism underlying fish responses, such as decreased foraging efficiency, to increased turbidity and further indicates that algal turbidity will probably be more detrimental to visual processes than sedimentary turbidity. With the increasing occurrence and severity of harmful algal blooms due to cultural eutrophication globally, this could have significant implications for predator-prey relationships in aquatic systems.

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

Humans use three cone photoreceptor classes for colour vision, yet many birds, reptiles and shallow-water fish are tetrachromatic and use four cone classes. Screening pigments, which narrow the spectrum of photoreceptors in birds and diurnal reptiles, render visual systems with four cone classes more efficient. To date, however, the question of tetrachromacy in shallow-water fish that, like humans, lack screening pigments, is still unsolved. We raise the possibility that tetrachromacy in fish has evolved in response to higher spectral complexity of underwater light. We compared the dimensionality of colour vision in humans and fish by examining the spectral complexity of the colour signal reflected from objects into their eyes. We show that fish require four to six cone classes to reconstruct the colour signal of aquatic objects at the accuracy level achieved by humans viewing terrestrial objects. This is because environmental light, which alters the colour signals, is more complex and contains more spectral fluctuations underwater than on land. We further show that fish cones are better suited than human cones to detect these spectral fluctuations, suggesting that the capability of fish cones to detect high-frequency fluctuations in the colour signal confers an advantage. Taken together, we propose that tetrachromacy in fish has evolved to enhance the reconstruction of complex colour signals in shallow aquatic environments. Of course, shallow-water fish might possess fewer than four cone classes; however, this would come with the inevitable loss in accuracy of signal reconstruction.

Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity.

We identify two processes by which humans increase genetic exchange among groups of individuals: by affecting the distribution of groups and dispersal patterns across a landscape, and by affecting interbreeding among sympatric or parapatric groups. Each of these processes might then have two different effects on biodiversity: changes in the number of taxa through merging or splitting of groups, and the extinction/extirpation of taxa through effects on fitness. We review the various ways in which humans are affecting genetic exchange, and highlight the difficulties in predicting the impacts on biodiversity. Gene flow and hybridization are crucially important evolutionary forces influencing biodiversity. Humans alter natural patterns of genetic exchange in myriad ways, and these anthropogenic effects are likely to influence the genetic integrity of populations and species. We argue that taking a gene-centric view towards conservation will help resolve issues pertaining to conservation and management. Editor's suggested further reading in BioEssays A systemic view of biodiversity and its conservation: Processes, interrelationships, and human culture Abstract.

Gene duplication and divergence of long wavelength-sensitive opsin genes in the guppy, Poecilia reticulata.

Female preference for male orange coloration in the genus Poecilia suggests a role for duplicated long wavelength-sensitive (LWS) opsin genes in facilitating behaviors related to mate choice in these species. Previous work has shown that LWS gene duplication in this genus has resulted in expansion of long wavelength visual capacity as determined by microspectrophotometry (MSP). However, the relationship between LWS genomic repertoires and expression of LWS retinal cone classes within a given species is unclear. Our previous study in the related species, Xiphophorus helleri, was the first characterization of the complete LWS opsin genomic repertoire in conjunction with MSP expression data in the family Poeciliidae, and revealed the presence of four LWS loci and two distinct LWS cone classes. In this study we characterized the genomic organization of LWS opsin genes by BAC clone sequencing, and described the full range of cone cell types in the retina of the colorful Cumaná guppy, Poecilia reticulata. In contrast to X. helleri, MSP data from the Cumaná guppy revealed three LWS cone classes. Comparisons of LWS genomic organization described here for Cumaná to that of X. helleri indicate that gene divergence and not duplication was responsible for the evolution of a novel LWS haplotype in the Cumaná guppy. This lineage-specific divergence is likely responsible for a third additional retinal cone class not present in X. helleri, and may have facilitated the strong sexual selection driven by female preference for orange color patterns associated with the genus Poecilia.

The underwater photic environment of Cape Maclear, Lake Malawi: comparison between rock- and sand-bottom habitats and implications for cichlid fish vision.

Lake Malawi boasts the highest diversity of freshwater fishes in the world. Nearshore sites are categorized according to their bottom substrate, rock or sand, and these habitats host divergent assemblages of cichlid fishes. Sexual selection driven by mate choice in cichlids led to spectacular diversification in male nuptial coloration. This suggests that the spectral radiance contrast of fish, the main determinant of visibility under water, plays a crucial role in cichlid visual communication. This study provides the first detailed description of underwater irradiance, radiance and beam attenuation at selected sites representing two major habitats in Lake Malawi. These quantities are essential for estimating radiance contrast and, thus, the constraints imposed on fish body coloration. Irradiance spectra in the sand habitat were shifted to longer wavelengths compared with those in the rock habitat. Beam attenuation in the sand habitat was higher than in the rock habitat. The effects of water depth, bottom depth and proximity to the lake bottom on radiometric quantities are discussed. The radiance contrast of targets exhibiting diffused and spectrally uniform reflectance depended on habitat type in deep water but not in shallow water. In deep water, radiance contrast of such targets was maximal at long wavelengths in the sand habitat and at short wavelengths in the rock habitat. Thus, to achieve conspicuousness, color patterns of rock- and sand-dwelling cichlids would be restricted to short and long wavelengths, respectively. This study provides a useful platform for the examination of cichlid visual communication.

Functional diversity in the color vision of cichlid fishes.

BACKGROUND: Color vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed. RESULTS: To examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes. CONCLUSIONS: Our study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.

Striving for population-level conservation: integrating physiology across the biological hierarchy.

The field of conservation physiology strives to achieve conservation goals by revealing physiological mechanisms that drive population declines in the face of human-induced rapid environmental change (HIREC) and has informed many successful conservation actions. However, many studies still struggle to explicitly link individual physiological measures to impacts across the biological hierarchy (to population and ecosystem levels) and instead rely on a 'black box' of assumptions to scale up results for conservation implications. Here, we highlight some examples of studies that were successful in scaling beyond the individual level, including two case studies of well-researched species, and using other studies we highlight challenges and future opportunities to increase the impact of research by scaling up the biological hierarchy. We first examine studies that use individual physiological measures to scale up to population-level impacts and discuss several emerging fields that have made significant steps toward addressing the gap between individual-based and demographic studies, such as macrophysiology and landscape physiology. Next, we examine how future studies can scale from population or species-level to community- and ecosystem-level impacts and discuss avenues of research that can lead to conservation implications at the ecosystem level, such as abiotic gradients and interspecific interactions. In the process, we review methods that researchers can use to make links across the biological hierarchy, including crossing disciplinary boundaries, collaboration and data sharing, spatial modelling and incorporating multiple markers (e.g. physiological, behavioural or demographic) into their research. We recommend future studies incorporating tools that consider the diversity of 'landscapes' experienced by animals at higher levels of the biological hierarchy, will make more effective contributions to conservation and management decisions.

Behavioral differences within and among populations of an African cichlid found in divergent and extreme environments.

Animals are increasingly faced with human-induced stressors that vary in space and time, thus we can expect population-level divergence in behaviors that help animals to cope with environmental change. However, empirical evidence of behavioral trait divergence across environmental extremes is lacking. We tested for variation in behavioral traits among 2 populations of an African cichlid fish (Pseudocrenilabrus multicolor victoriae Seegers, 1990) that experience extremes of dissolved oxygen (DO) and turbidity and are known to vary in a number of physiological and life history traits associated with these stressors. Using a common garden rearing experiment, F1 progeny from wild-caught parents originating from a swamp (low DO, clear) and a river (high DO, turbid) were reared in high DO, clear water. Predator simulation assays were conducted to test for (1) variation in boldness, general activity, and foraging activity between populations, (2) differences in correlations between behaviors within and across populations, and (3) repeatability of behaviors. There was strong evidence for divergence between populations, with swamp fish being more bold (i.e., leaving refuge sooner after a simulated predator attack) and active (i.e., spent more time out of refuge) than river fish. Across populations there were positive correlations between foraging activity and both boldness and general activity; however, within populations, there was only a strong positive relationship between foraging activity and boldness in the river population. Here, we have demonstrated that populations that originate from drastically different environments can produce progeny that exhibit measurable differences in behaviors and their correlated relationships even when reared under common conditions.

Environment-contingent sexual selection in a colour polymorphic fish.

Sexual selection could be a driving force in the maintenance of intraspecific variation, but supporting observations from nature are limited. Here, we test the hypothesis that spatial heterogeneity of the visual environment can influence sexual selection on colourful male secondary traits such that selective advantage is environment contingent. Using a small fish endemic to Sulawesi, Indonesia (Telmatherina sarasinorum) that has five male colour morphs varying in frequency between two visually distinct mating habitats, we used direct behavioural observations to test the environment-contingent selection hypothesis. These observations were combined with measurements of the visual environment, fish coloration and the sensitivity of visual photopigments to determine whether differential morph conspicuousness was associated with reproductive success across habitats. We found that blue and yellow males are most conspicuous in different habitats, where they also have the highest reproductive fitness. A less conspicuous grey morph also gained high reproductive success in both habitats, raising the possibility that alternative behaviours may also contribute to reproductive success. In a comprehensive analysis, conspicuousness was strongly correlated with reproductive success across morphs and environments. Our results suggest an important role for spatially heterogeneous environments in the maintenance of male colour polymorphism.

Visual detection thresholds in two trophically distinct fishes are compromised in algal compared to sedimentary turbidity.

Increasing anthropogenic turbidity is among the most prevalent disturbances in freshwater ecosystems, through increases in sedimentary deposition as well as the rise of nutrient-induced algal blooms. Changes to the amount and color of light underwater as a result of elevated turbidity are likely to disrupt the visual ecology of fishes that rely on vision to survive and reproduce; however, our knowledge of the mechanisms underlying visual responses to turbidity is lacking. First, we aimed to determine the visual detection threshold, a measure of visual sensitivity, of two ecologically and economically important Lake Erie fishes, the planktivorous forage fish, emerald shiner (Notropis atherinoides), and a primary predator, the piscivorous walleye (Sander vitreus), under sedimentary and algal turbidity. Secondly, we aimed to determine if these trophically distinct species are differentially impacted by increased turbidity. We used the innate optomotor response to determine the turbidity levels at which individual fish could no longer detect a difference between a stimulus and the background (i.e. visual detection threshold). Detection thresholds were significantly higher in sedimentary compared to algal turbidity for both emerald shiner (meansediment ± SE = 79.66 ± 5.51 NTU, meanalgal ± SE = 34.41 ± 3.19 NTU) and walleye (meansediment ± SE = 99.98 ± 5.31 NTU, meanalgal ± SE = 40.35 ± 2.44 NTU). Our results suggest that across trophic levels, the visual response of fishes will be compromised under algal compared to sedimentary turbidity. The influence of altered visual environments on the ability of fish to find food and detect predators could potentially be large, leading to population- and community-level changes within the Lake Erie ecosystem.

Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases.

Perceived certainty of paternity is expected to influence a male's behavior toward his offspring: if he is uncertain of his reproductive success with a current brood due to the presence of cuckolders, it may benefit him to invest instead in future reproduction. A decrease in perceived certainty of paternity incites filial cannibalism (the eating of one's own offspring) in some teleost fishes that provide parental care; however, no work has demonstrated that cannibalism increases proportionately with increased levels of cuckoldry. Here we show for the first time in a fish with no parental care that as the number of cuckolders at a spawning event increases, so does the probability that a male will cannibalize eggs. In field observations of Telmatherina sarasinorum, a small fish endemic to Sulawesi, Indonesia, males increased filial cannibalism behavior threefold in the presence of one cuckolder and nearly sixfold in the presence of two or more cuckolders. This suggests that males may use detection of cuckolders as an indication that the paternity of current offspring has been compromised.

Linking color polymorphism maintenance and speciation.

Here, we review the recently burgeoning literature on color polymorphisms, seeking to integrate studies of the maintenance of genetic variation and the evolution of reproductive isolation. Our survey reveals that several mechanisms, some operating between populations and others within them, can contribute to both color polymorphism persistence and speciation. As expected, divergent selection clearly can couple with gene flow to maintain color polymorphism and mediate speciation. More surprisingly, recent evidence suggests that diverse forms of within-population sexual selection can generate negative frequency dependence and initiate reproductive isolation. These findings deserve additional study, particularly concerning the roles of heterogeneous visual environments and correlational selection. Finally, comparative studies and more comprehensive approaches are required to elucidate when color polymorphism evolves, persists, or leads to speciation.