ORCID Profile
0000-0002-7518-6159
Current Organisation
University of Queensland
Does something not look right? The information on this page has been harvested from data sources that may not be up to date. We continue to work with information providers to improve coverage and quality. To report an issue, use the Feedback Form.
In Research Link Australia (RLA), "Research Topics" refer to ANZSRC FOR and SEO codes. These topics are either sourced from ANZSRC FOR and SEO codes listed in researchers' related grants or generated by a large language model (LLM) based on their publications.
Zoology | Molecular Evolution | Animal Neurobiology | Behavioural Ecology | Sensory Systems
Expanding Knowledge in the Biological Sciences | Marine Flora, Fauna and Biodiversity |
Publisher: Wiley
Date: 10-12-2018
DOI: 10.1111/JFB.13849
Abstract: Many fishes, both freshwater or marine, have colour vision that may outperform humans. As a result, to understand the behavioural tasks that vision enables including mate choice, feeding, agonistic behaviour and camouflage, we need to see the world through a fish's eye. This includes quantifying the variable light environment underwater and its various influences on vision. As well as rapid loss of light with depth, light attenuation underwater limits visual interaction to metres at most and in many instances, less than a metre. We also need to characterize visual sensitivities, fish colours and behaviours relative to both these factors. An increasingly large set of techniques over the past few years, including improved photography, submersible spectrophotometers and genetic sequencing, have taken us from intelligent guesswork to something closer to sensible hypotheses. This contribution to the special edition on the Ecology of Fish Senses under a shifting environment first reviews our knowledge of fish colour vision and visual ecology, past, present and very recent, and then goes on to examine how climate change may impinge on fish visual capability. The review is limited to mostly colour vision and to mostly reef fishes. This ignores a large body of work, both from other marine environments and freshwater systems, but the reef contains ex les of many of the challenges to vision from the aquatic environment. It is also a concentrate of life, perhaps the most specious and complex on earth, suffering now catastrophically from the consequences of our lack of action on climate change. A clear course of action to prevent destruction of this habitat is the need to spend more time in it, in the study of it and sharing it with those not fortunate enough to see coral reefs first-hand. Sir David Attenborough on The Great Barrier Reef: "Do we really care so little about the Earth upon which we live that we don't wish to protect one of its greatest wonders from the consequences of our behaviours?"
Publisher: American Association for the Advancement of Science (AAAS)
Date: 10-05-2019
Abstract: Vertebrates are typically thought to have a consistent system for processing light, in which multiple cone opsins permit color vision during the day, but a single rod opsin provides only monochrome vision in the dark. Musilova et al. analyzed more than 100 deep-sea fish genomes and found a previously unknown proliferation of rod opsin genes that generate rod opsin photopigments that are tuned to different wavelengths of light. These receptors may allow the fish to perceive bioluminescent signals that pervade their deep-sea environment. These results reveal a previously undescribed visual system that allows for color vision in the dark. Science , this issue p. 588
Publisher: Proceedings of the National Academy of Sciences
Date: 29-12-2014
Abstract: Gene and whole-genome duplications are important evolutionary forces promoting organismal ersification. Teleost fishes, for ex le, possess many gene duplicates responsible for photoreception (opsins), which emerged through gene duplication and allow fishes to adapt to the various light conditions of the aquatic environment. Here, we reevaluate the evolutionary history of the violet-blue–sensitive opsins [short wavelength-sensitive 2 (SWS2)] in modern teleosts using next generation genome sequencing. We uncover a gene duplication event specific to the most erse lineage of vertebrates (the percomorphs) and show that SWS2 evolution was highly dynamic and involved gene loss, pseudogenization, and gene conversion. We, thus, clarify previous discrepancies regarding opsin annotations. Our study highlights the importance of integrative approaches to help us understand how species adapt and ersify.
Publisher: The Company of Biologists
Date: 2019
DOI: 10.1242/JEB.209916
Abstract: Ontogenetic changes of the visual system are often correlated to shifts in habitat and feeding behaviour of animals. Coral reef fishes begin their lives in the pelagic zone and then migrate to the reef. This habitat transition frequently involves a change in diet and light environment as well as major morphological modifications. The spotted unicornfish, Naso brevirostris, is known to shift diet from zooplankton to algae and back to mainly zooplankton when transitioning from larval to juvenile and then to adult stages. Concurrently, N. brevirostris also moves from an open pelagic to a coral-associated habitat before migrating up in the water column when reaching adulthood. Using retinal mapping techniques, we discovered that the distribution and density of ganglion and photoreceptor cells in N. brevirostris mostly changes during the transition from the larval to the juvenile stage, with only minor modifications thereafter. Similarly, visual gene (opsin) expression based on RNA sequencing, although qualitatively similar between stages (all fishes mainly expressed the same three cone opsins SWS2B, RH2B, RH2A), also showed the biggest quantitative difference when transitioning from larvae to juveniles. The juvenile stage in particular seems mismatched with its reef-associated ecology, which may be due to this stage only lasting a fraction of the lifespan of these fishes. Hence, the visual ontogeny found in N. brevirostris is very different from the progressive changes found in other reef fishes calling for a thorough analysis of visual system development of the reef fish community.
Publisher: Annual Reviews
Date: 06-10-2021
DOI: 10.1146/ANNUREV-CELLBIO-120219-024915
Abstract: Visual opsin genes expressed in the rod and cone photoreceptor cells of the retina are core components of the visual sensory system of vertebrates. Here, we provide an overview of the dynamic evolution of visual opsin genes in the most species-rich group of vertebrates, teleost fishes. The examination of the rich genomic resources now available for this group reveals that fish genomes contain more copies of visual opsin genes than are present in the genomes of hibians, reptiles, birds, and mammals. The expansion of opsin genes in fishes is due primarily to a combination of ancestral and lineage-specific gene duplications. Following their duplication, the visual opsin genes of fishes repeatedly ersified at the same key spectral-tuning sites, generating arrays of visual pigments sensitive to the ultraviolet to red spectrum of light. Species-specific opsin gene repertoires correlate strongly with underwater light habitats, ecology, and color-based sexual selection.
Publisher: Wiley
Date: 18-01-2023
DOI: 10.1111/MEC.16831
Abstract: Coral reef fishes are erse in ecology and behaviour and show remarkable colour variability. Investigating the visual pigment gene (opsin) expression in these fishes makes it possible to associate their visual genotype and phenotype (spectral sensitivities) to visual tasks, such as feeding strategy or conspecific detection. By studying all major damselfish clades (Pomacentridae) and representatives from five other coral reef fish families, we show that the long‐wavelength‐sensitive ( lws ) opsin is highly expressed in algivorous and less or not expressed in zooplanktivorous species. Lws is also upregulated in species with orange/red colours (reflectance nm) and expression is highest in orange/red‐coloured algivores. Visual models from the perspective of a typical damselfish indicate that sensitivity to longer wavelengths does enhance the ability to detect the red to far‐red component of algae and orange/red‐coloured conspecifics, possibly enabling social signalling. Character state reconstructions indicate that in the early evolutionary history of damselfishes, there was no lws expression and no orange/red coloration. Omnivory was most often the dominant state. Although herbivory was sometimes dominant, zooplanktivory was never dominant. Sensitivity to long wavelength (increased lws expression) only emerged in association with algivory but never with zooplanktivory. Higher lws expression is also exploited by social signalling in orange/red, which emerged after the transition to algivory. Although the relative timing of traits may deviate by different reconstructions and alternative explanations are possible, our results are consistent with sensory bias whereby social signals evolve as a correlated response to natural selection on sensory system properties in other contexts.
Publisher: Wiley
Date: 06-2019
DOI: 10.1111/MEC.15102
Abstract: Animal visual systems adapt to environmental light on various timescales. In scotopic conditions, evolutionary time-scale adaptations include spectral tuning to a narrower light spectrum, loss (or inactivation) of visual genes, and pure-rod or rod-dominated retinas. Some fishes inhabiting shallow coral reefs may show activity during the day and at night. It is unclear whether these fishes show adaptations typical of exclusively nocturnal or deep-sea fishes, or of diurnally active shallow-water species. Here, we investigated visual pigment ersity in cardinalfishes (Apogonidae). Most cardinalfishes are nocturnal foragers, yet they aggregate in multispecies groups in and around coral heads during the day, engaging in social and predator avoidance behaviours. We sequenced retinal transcriptomes of 28 species found on the Great Barrier Reef, assessed the ersity of expressed opsin genes and predicted the spectral sensitivities of resulting photopigments using sequence information. Predictions were combined with microspectrophotometry (MSP) measurements in seven cardinalfish species. Retinal opsin expression was rod opsin (RH1) dominated (>87%), suggesting the importance of scotopic vision. However, all species retained expression of multiple cone opsins also, presumably for colour vision. We found five distinct quantitative expression patterns among cardinalfishes, ranging from short-wavelength-shifted to long-wavelength-shifted. These results indicate that cardinalfishes are both well adapted to dim-light conditions and have retained a sophisticated colour vision sense. Other reef fish families also show both nocturnal and diurnal activity while most are strictly one or the other. It will be interesting to compare these behavioural differences across different phylogenetic groups using the criteria and methods developed here.
Publisher: The Royal Society
Date: 12-2017
DOI: 10.1098/RSOS.171440
Abstract: Humans group components of visual patterns according to their colour, and perceive colours separately from shape. This property of human visual perception is the basis behind the Ishihara test for colour deficiency, where an observer is asked to detect a pattern made up of dots of similar colour with variable lightness against a background of dots made from different colour(s) and lightness. To find out if fish use colour for object segregation in a similar manner to humans, we used stimuli inspired by the Ishihara test. Triggerfish ( Rhinecanthus aculeatus ) were trained to detect a cross constructed from similarly coloured dots against various backgrounds. Fish detected this cross even when it was camouflaged using either achromatic or chromatic noise, but fish relied more on chromatic cues for shape segregation. It remains unknown whether fish may switch to rely primarily on achromatic cues in scenarios where target objects have higher achromatic contrast and lower chromatic contrast. Fish were also able to generalize between stimuli of different colours, suggesting that colour and shape are processed by fish independently.
Publisher: Cold Spring Harbor Laboratory
Date: 05-05-2022
DOI: 10.1101/2022.05.04.490704
Abstract: Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become largely nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used histology and transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well-adapted to photopic conditions with pre-settlement larvae having high cone densities, high cone opsin gene expression, a broad cone opsin gene repertoire (8 genes) and a multibank retina ( i . e ., stacked layers of rods) comprising up to two rod banks. At reef settlement, holocentrids started to invest more in their scotopic visual system and upregulated genes involved in cell differentiation roliferation. By adulthood, they had well-developed scotopic vision with a rod-dominated multibank retina comprising 5-17 rod banks, increased summation of rods onto ganglion cells, high rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems erged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny likely determine the development of the holocentrid visual system. Coral reef fishes in the family Holocentridae remodel their retina at the cellular and molecular levels to adapt to a nocturnal lifestyle during development.
Publisher: The Company of Biologists
Date: 04-2022
DOI: 10.1242/JEB.243907
Abstract: Vision is used by animals to find food and mates, avoid predators, defend resources and navigate through complex habitats. Behavioural experiments are essential for understanding animals' perception but are often challenging and time-consuming therefore, using species that can be trained easily for complex tasks is advantageous. Picasso triggerfish, Rhinecanthus aculeatus, have been used in many behavioural studies investigating vision and navigation. However, little is known about the molecular and anatomical basis of their visual system. We addressed this knowledge gap here and behaviourally tested achromatic and chromatic acuity. In terms of visual opsins, R. aculeatus possessed one rod opsin gene (RH1) and at least nine cone opsins: one violet-sensitive SWS2B gene, seven duplicates of the blue–green-sensitive RH2 gene (RH2A, RH2B, RH2C1-5) and one red-sensitive LWS gene. However, only five cone opsins were expressed: SWS2B expression was consistent, while RH2A, RH2C-1 and RH2C-2 expression varied depending on whether fish were s led from the field or aquaria. Levels of LWS expression were very low. Using fluorescence in situ hybridisation, we found SWS2B was expressed exclusively in single cones, whereas RH2A and RH2Cs were expressed in opposite double cone members. Anatomical resolution estimated from ganglion cell densities was 6.8 cycles per degree (cpd), which was significantly higher than values obtained from behavioural testing for black-and-white achromatic stimuli (3.9 cpd) and chromatic stimuli (1.7–1.8 cpd). These measures were twice as high as previously reported. This detailed information on their visual system will help inform future studies with this emerging focal species.
Publisher: Cold Spring Harbor Laboratory
Date: 22-08-2019
DOI: 10.1101/744011
Abstract: Vertebrates exhibit erse visual systems that vary in terms of morphology, number and distribution of spectrally distinct photoreceptor types, visual opsin genes and gene expression levels. In fish, such adaptations are driven by two main factors: differences in the light environment and behavioural tasks, including foraging, predator avoidance and mate selection. Whether visual systems also adapt to small-scale spectral differences in light, between microhabitats, is less clear. We suggest that differences in microhabitat use by cardinalfishes (Apogonidae) on coral reefs drive morphological and molecular adaptations in their visual systems. To test this, we investigated diurnal microhabitat use in 17 cardinalfish species and assessed whether this correlated with differences in visual opsin gene expression and eye morphology. We found that cardinalfishes display six types of partitioning behaviours during the day, ranging from specialists found exclusively in the water column to species that are always hidden inside the reef matrix. Using data on visual opsin gene expression previously characterized in this family, it was discovered that species in exposed habitats had increased expression of the short-wavelength sensitive violet opsin ( SWS2B ) and decreased expression of the dim-light active rod opsin ( RH1 ). Species of intermediate exposure, on the other hand, expressed opsins that are mostly sensitive to the blue-green central part of the light spectrum ( SWS2As and RH2s ), while fishes entirely hidden in the reef substrate had an increased expression of the long-wavelength sensitive red opsin ( LWS ). We found that eye size relative to body size significantly differed between cardinalfish species, and relative eye size decreased with an increase in habitat exposure. Retinal topography did not show co-adaptation with microhabitat use, but instead with feeding mode. We suggest that, although most cardinalfishes are nocturnal foragers, their visual systems are also adapted to both the light intensity and the light spectrum of their preferred diurnal microhabitat.
Publisher: Wiley
Date: 27-01-2017
DOI: 10.1111/MEC.13968
Abstract: Coral reefs belong to the most erse ecosystems on our planet. The ersity in coloration and lifestyles of coral reef fishes makes them a particularly promising system to study the role of visual communication and adaptation. Here, we investigated the evolution of visual pigment genes (opsins) in damselfish (Pomacentridae) and examined whether structural and expression variation of opsins can be linked to ecology. Using DNA sequence data of a phylogenetically representative set of 31 damselfish species, we show that all but one visual opsin are evolving under positive selection. In addition, selection on opsin tuning sites, including cases of ergent, parallel, convergent and reversed evolution, has been strong throughout the radiation of damselfish, emphasizing the importance of visual tuning for this group. The highest functional variation in opsin protein sequences was observed in the short- followed by the long-wavelength end of the visual spectrum. Comparative gene expression analyses of a subset of the same species revealed that with SWS1, RH2B and RH2A always being expressed, damselfish use an overall short-wavelength shifted expression profile. Interestingly, not only did all species express SWS1 - a UV-sensitive opsin - and possess UV-transmitting lenses, most species also feature UV-reflective body parts. This suggests that damsels might benefit from a close-range UV-based 'private' communication channel, which is likely to be hidden from 'UV-blind' predators. Finally, we found that LWS expression is highly correlated to feeding strategy in damsels with herbivorous feeders having an increased LWS expression, possibly enhancing the detection of benthic algae.
Publisher: American Association for the Advancement of Science (AAAS)
Date: 03-11-2017
Abstract: Deep-sea fishes evolved an unconventional visual system to optimize vision in twilight conditions.
Publisher: Elsevier BV
Date: 03-2015
DOI: 10.1016/J.CUB.2015.02.013
Abstract: Animal communication is often deceptive however, such dishonesty can become ineffective if it is used too often, is used out of context, or is too easy to detect [1-3]. Mimicry is a common form of deception, and most mimics gain the greatest fitness benefits when they are rare compared to their models [3, 4]. If mimics are encountered too frequently or if their model is absent, avoidance learning of noxious models is disrupted (Batesian mimicry [3]), or receivers become more vigilant and learn to avoid perilous mimics (aggressive mimicry [4]). Mimics can moderate this selective constraint by imperfectly resembling multiple models [5], through polymorphisms [6], or by opportunistically deploying mimetic signals [1, 7]. Here we uncover a novel mechanism to escape the constraints of deceptive signaling: phenotypic plasticity allows mimics to deceive targets using multiple guises. Using a combination of behavioral, cell histological, and molecular methods, we show that a coral reef fish, the dusky dottyback (Pseudochromis fuscus), flexibly adapts its body coloration to mimic differently colored reef fishes and in doing so gains multiple fitness benefits. We find that by matching the color of other reef fish, dottybacks increase their success of predation upon juvenile fish prey and are therefore able to deceive their victims by resembling multiple models. Furthermore, we demonstrate that changing color also increases habitat-associated crypsis that decreases the risk of being detected by predators. Hence, when mimics and models share common selective pressures, flexible imitation of models might inherently confer secondary benefits to mimics. Our results show that phenotypic plasticity can act as a mechanism to ease constraints that are typically associated with deception. VIDEO ABSTRACT.
Publisher: The Company of Biologists
Date: 09-2022
DOI: 10.1242/JEB.244513
Abstract: Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well adapted to photopic conditions with pre-settlement larvae having high levels of cone opsin gene expression and a broad cone opsin gene repertoire (8 genes). At reef settlement, holocentrids started to invest more in their scotopic visual system, and compared with adults, showed upregulation of genes involved in cell differentiation roliferation. By adulthood, holocentrids had well developed scotopic vision with high levels of rod opsin gene expression, reduced cone opsin gene expression and repertoire (1–4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems erged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny are likely to determine the development of the holocentrid visual system.
Publisher: Cold Spring Harbor Laboratory
Date: 25-05-2020
DOI: 10.1101/2020.05.24.113811
Abstract: The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual systems of the coral reef fish family Holocentridae (squirrelfish and soldierfish). In addition to their nocturnality, this family is particularly interesting for dim-light vision studies due to its ecological and evolutionary connection to deeper habitats. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae having a slightly more developed photopic visual system than Myripristinae. Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of multibank retina and its potential for dim-light colour vision.
Publisher: Cold Spring Harbor Laboratory
Date: 09-05-2021
DOI: 10.1101/2021.05.08.443214
Abstract: Photopigments, consisting of an opsin protein bound to a light-sensitive chromophore, are at the centre of vertebrate vision. The vertebrate ancestor already possessed four cone opsin classes involved in colour perception during bright-light conditions, which are sensitive from the ultraviolet to the red-wavelengths of light. Teleosts experienced an extra round of whole genome duplication (3R) at their origin, and while most teleosts maintained only one long-wavelength-sensitive opsin gene ( LWS1 ), the second ancestral copy ( LWS2 ) persisted in characins and osteoglossomorphs. Following 3R, teleost opsins have continued to expand and ersify, which is thought to be a consequence of the different light environment fishes inhabit, from clear streams to the relative darkness of the deep-sea. Although many recent and a few ancestral opsin duplicates can be found, none predating the 3R were thought to exist. In this study we report on a second, previously unnoticed ancestral duplication of the red-sensitive opsin ( LWS3 ), which predates the teleost-specific genome duplication and only persists in gobiid fishes. This is surprising, since it implies that LWS3 has been lost at least 19-20 times independently along the teleost phylogeny. Mining 109 teleost genomes we also uncover a third lineage, the elopomorphs, that maintained the LWS2 copy. We identify convergent amino acid changes that green-shift ancestral and recent LWS copies, leading to adaptive differentiation and the functional replacement of the original green-sensitive RH2 opsin. Retinal transcriptomes and in-situ hybridisation show that LWS3 is expressed to various extents in gobies and in the case of the whitebarred goby, Amblygobius phalaena , it occurs in a separate photoreceptor to LWS1 . Our study highlights the importance of comparative studies to comprehend evolution of gene function.
Publisher: Cold Spring Harbor Laboratory
Date: 27-11-2022
DOI: 10.1101/2022.11.27.518067
Abstract: Multibank retinas have rod photoreceptors stacked into multiple layers. They are found in many species of fish that inhabit dim environments and are one of the most common visual adaptations in the deep-sea. Despite its prevalence, the function of multibank retinas remained unknown. Two predominant theories, neither of which has been tested, have emerged: 1) they enhance sensitivity in dim light, and 2) they allow colour vision in dim light. To investigate the sensitivity hypothesis, we performed electrophysiological recordings and compared the rod pigments of three species of nocturnal reef fishes, two with a multibank retina ( Neoniphon sammara and Myripristis violacea ) and a control species with a single rod bank ( Ostorhinchus compressus ). Results indicated that nocturnal reef fishes with a multibank retina have higher temporal resolution of vision, as indicated by electrophysiology, and that their rhodopsin proteins likely also have faster retinal release kinetics, as suggested by amino acid substitutions. Electrophysiology also showed that the multibank retina conferred greater sensitivity to both dim and bright intensities than a single rod bank and this occurred at times when rod-derived signals usually dominate the visual response. This study provides the first functional evidence for enhanced dim-light sensitivity using a multibank retina while also suggesting novel roles for the adaptation in enhancing bright-light sensitivity and the speed of vision. Most vertebrates have one layer of the dim-light active rod photoreceptors however, some species have multiple layers, known as a multibank retina. We used electrophysiology on nocturnal reef fishes with and without multibank retinas to evaluate the sensory advantage of having multiple rod layers. We show that fish with multibank retinas have both faster vision and enhanced sensitivity to bright and dim light intensities. Thus, we resolve for the first time the function of multibank retinas – one of the most common visual adaptations in the deep sea. Our findings highlight an unconventional vertebrate visual system as well as the visual capabilities of fishes from the most vast (deep sea) and vibrant (reefs) ecosystems on the planet.
Publisher: Cold Spring Harbor Laboratory
Date: 21-12-2018
DOI: 10.1101/503516
Abstract: Evolutionary adaptations to life on land include changes to the physiology, morphology and behaviour of an animal in response to physical differences between water and air. The visual systems of hibious species show pronounced morphological adaptations yet, whether molecular changes also occur remains largely unknown. Here, we investigated the molecular evolution of visual pigment genes (opsins) in hibious and terrestrial fishes belonging to the Salariini ision of blennies (Blenniidae). We hypothesized that when conquering land, blenny opsins adapt, in terms of sequence variation and/or gene expression, to match both higher light intensities as well as the broader light spectrum. Using retinal transcriptomes in six species ranging from fully aquatic to fully terrestrial, we found very little variation in opsin gene sequences or gene expression between species. All blennies expressed a single rod opsin gene as well as two cone opsin genes sensitive to longer-wavelengths of light: RH2A-1 (green-sensitive) and LWS (red-sensitive). They also expressed one or two short-wavelength-sensitive cone opsin genes (SWS2Aα, SWS2Aβ blue-sensitive) in a phylogenetically inert manner. However, based on amino acid predictions, both SWS2A proteins confer similar peak spectral sensitivities and differential expression is therefore unlikely to be ecologically significant. Red-sensitivity is likely beneficial for feeding on algae and detritus, the main food source of Salariini blennies, and could be co-adapted to perceive visual displays in terrestrial species, which often use red dorsal fins to signal during aggressive disputes and courtship. Our data suggests that on the molecular level, the visual systems that evolved in aquatic blennies have been retained in species that have transitioned onto land.
Publisher: Wiley
Date: 11-11-2022
DOI: 10.1111/MEC.16744
Abstract: The visual capabilities of fish are optimized for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e.g. , ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short‐term changes in the light environment, e.g., algal blooms and light pollution. In this study, we investigated the effect of short‐term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in juvenile and adult diurnal reef fish (convict surgeonfish Acanthurus triostegus ). Results revealed phenotypic plasticity in the retina across ontogeny, particularly during development. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light and simulated artificial light at night had a lesser effect. Under dim light, juveniles and adults increased absolute expression of the cone opsin genes, sws2a, rh2c and lws, within a few days and juveniles also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes potentially enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species' natural light environment, i.e., a diurnal fish in “constant night”. Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 h. Overall, our study showed rapid, reversible light‐induced changes in the retina of A. triostegus , demonstrating phenotypic plasticity in the visual system of a reef fish throughout life.
Publisher: Wiley
Date: 16-02-2020
Publisher: Wiley
Date: 15-02-2021
Publisher: Elsevier BV
Date: 05-2023
Publisher: The Company of Biologists
Date: 2020
DOI: 10.1242/JEB.233098
Abstract: The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual system of the nocturnal reef fish family Holocentridae. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae (squirrelfish) having a slightly more developed photopic visual system than Myripristinae (soldierfish). Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of the multibank retina and its potential for dim-light colour vision.
Publisher: Elsevier BV
Date: 10-2020
Publisher: The Company of Biologists
Date: 09-2022
DOI: 10.1242/JEB.244740
Abstract: Ontogenetic changes in the habitats and lifestyles of animals are often reflected in their visual systems. Coral reef fishes start life in the shallow open ocean but inhabit the reef as juveniles and adults. Alongside this change in habitat, some species also change lifestyles and become nocturnal. However, it is not fully understood how the visual systems of nocturnal reef fishes develop and adapt to these significant ecological shifts over their lives. Therefore, we used a histological approach to examine visual development in the nocturnal coral reef fish family, Holocentridae. We examined 7 representative species spanning both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes). Pre-settlement larvae showed strong adaptation for photopic vision with high cone densities and had also started to develop a multibank retina (i.e. multiple rod layers), with up to two rod banks present. At reef settlement, holocentrids showed greater adaptation for scotopic vision, with higher rod densities and higher summation of rods onto the ganglion cell layer. By adulthood, they had well-developed scotopic vision with a highly rod-dominated multibank retina comprising 5–17 rod banks and enhanced summation of rods onto the ganglion cell layer. Although the ecological demands of the two subfamilies were similar throughout their lives, their visual systems differed after settlement, with Myripristinae showing more pronounced adaptation for scotopic vision than Holocentrinae. Thus, it is likely that both ecology and phylogeny contribute to the development of the holocentrid visual system.
Publisher: Cold Spring Harbor Laboratory
Date: 10-07-2022
DOI: 10.1101/2022.07.08.499304
Abstract: The contribution of hybridisation in the generation of global species ersity has long been controversial among evolutionary biologists. However, it is now increasingly accepted that hybridisation has many impacts on the process of speciation. Notably, it is an important mechanism fostering adaptive radiation since it can generate new phenotypic combinations enabling the occupancy of new niches. Here, we focused on clownfish (Pomacentridae), a clade of 28 coral reef fishes displaying a mutualistic interaction with sea anemones. This behaviour is the key innovation that triggered adaptive radiation of clownfishes, as each species is able to occupy a different combination of host anemone species and habitat. Previous work suggested that hybridisation might be responsible for the extant ersity of clownfish species. To test this hypothesis, we analysed whole-genome datasets for each clownfish species. First, we reconstructed the phylogeny of the clade based on topology weighting methods, which enables the visualisation of the relationships between taxa across the genome. Then, we highlighted possible ancient hybridisation events based on a comparative genomic framework for detecting introgression in genomes. The resulting phylogeny is consistent with previous works based on a few mitochondrial and nuclear genes, and shallow nodes are now well supported in contrast to past studies. Furthermore, we detected multiple past hybridisation events throughout the evolutionary history of clownfishes, corroborating the potential role of hybridisation in the clownfish adaptive radiation. This study adds to the growing number of studies investigating the genomic mechanisms behind species ersification, drawing us closer to understanding how Earth bio ersity is generated.
Publisher: Cold Spring Harbor Laboratory
Date: 22-10-2023
Publisher: Wiley
Date: 02-07-2016
DOI: 10.1111/MEC.13712
Abstract: Phenotypic plasticity plays an important role in adapting the visual capability of many animal species to changing sensory requirements. Such variability may be driven by developmental change or may result from environmental changes in light habitat, thereby improving performance in different photic environments. In this study, we examined inter- and intraspecific plasticity of visual sensitivities in seven damselfish species, part of the species-rich and colourful fish fauna of the Great Barrier Reef in Australia. Our goal was to test whether the visual systems of damselfish were tuned to the prevailing light environment in different habitats and/or other aspects of their lifestyle. More specifically, we compared the opsin gene expression levels from in iduals living in different photic habitats. We found that all species expressed rod opsin (RH1) used for dim-light vision, and primarily three cone opsins (SWS1, RH2B and RH2A) used for colour vision. While RH1 levels changed exclusively following a diurnal cycle, cone opsin expression varied with depth in four of the seven species. Estimates of visual pigment performance imply that changes in opsin expression adjust visual sensitivities to the dominant photic regime. However, we also discovered that some species show a more stable opsin expression profile. Further, we found indication that seasonal changes, possibly linked to changes in the photic environment, might also trigger opsin expression. These findings suggest that plasticity in opsin gene expression of damselfish is highly species-specific, possibly due to ecological differences in visual tasks or, alternatively, under phylogenetic constraints.
Publisher: Springer Science and Business Media LLC
Date: 11-11-2019
DOI: 10.1038/S41598-019-52297-0
Abstract: Vision plays a major role in the life of most teleosts, and is assumingly well adapted to each species ecology and behaviour. Using a multidisciplinary approach, we scrutinised several aspects of the visual system and ecology of the Great Barrier Reef anemonefish, Amphiprion akindynos , including its orange with white patterning, retinal anatomy and molecular biology, its symbiosis with anemones and sequential hermaphroditism. Amphiprion akindynos possesses spectrally distinct visual pigments and opsins: one rod opsin, RH1 (498 nm), and five cone opsins, SWS1 (370 nm), SWS2B (408 nm), RH2B (498 nm), RH2A (520 nm), and LWS (554 nm). Cones were arranged in a regular mosaic with each single cone surrounded by four double cones. Double cones mainly expressed RH2B (53%) in one member and RH2A (46%) in the other, matching the prevailing light. Single cones expressed SWS1 (89%), which may serve to detect zooplankton, conspecifics and the host anemone. Moreover, a segregated small fraction of single cones coexpressed SWS1 with SWS2B (11%). This novel visual specialisation falls within the region of highest acuity and is suggested to increase the chromatic contrast of Amphiprion akindynos colour patterns, which might improve detection of conspecifics.
Publisher: The Company of Biologists
Date: 15-04-2020
DOI: 10.1242/JEB.193334
Abstract: Among vertebrates, teleost eye ersity exceeds that found in all other groups. Their spectral sensitivities range from ultraviolet to red, and the number of visual pigments varies from 1 to over 40. This variation is correlated with the different ecologies and life histories of fish species, including their variable aquatic habitats: murky lakes, clear oceans, deep seas and turbulent rivers. These ecotopes often change with the season, but fish may also migrate between ecotopes diurnally, seasonally or ontogenetically. To survive in these variable light habitats, fish visual systems have evolved a suite of mechanisms that modulate spectral sensitivities on a range of timescales. These mechanisms include: (1) optical media that filter light, (2) variations in photoreceptor type and size to vary absorbance and sensitivity, and (3) changes in photoreceptor visual pigments to optimize peak sensitivity. The visual pigment changes can result from changes in chromophore or changes to the opsin. Opsin variation results from changes in opsin sequence, opsin expression or co-expression, and opsin gene duplications and losses. Here, we review visual ersity in a number of teleost groups where the structural and molecular mechanisms underlying their spectral sensitivities have been relatively well determined. Although we document considerable variability, this alone does not imply functional difference per se. We therefore highlight the need for more studies that examine species with known sensitivity differences, emphasizing behavioral experiments to test whether such differences actually matter in the execution of visual tasks that are relevant to the fish.
Publisher: Wiley
Date: 02-02-2017
DOI: 10.1111/EVO.13166
Abstract: Male secondary sexual traits are targets of inter- and/or intrasexual selection, but can vary due to a correlation with life-history traits or as by-product of adaptation to distinct environments. Trade-offs contributing to this variation may comprise conspicuousness toward conspecifics versus inconspicuousness toward predators, or between allocating resources into coloration versus the immune system. Here, we examine variation in expression of a carotenoid-based visual signal, anal-fin egg-spots, along a replicate environmental gradient in the haplochromine cichlid fish Astatotilapia burtoni. We quantified egg-spot number, area, and coloration applied visual models to estimate the trait's conspicuousness when perceived against the surrounding tissue under natural conditions and used the lymphocyte ratio as a measure for immune activity. We find that (1) males possess larger and more conspicuous egg-spots than females, which is likely explained by their function in sexual selection (2) riverine fish generally feature fewer but larger and/or more intensely colored egg-spots, which is probably to maintain signal efficiency in intraspecific interactions in long wavelength shifted riverine light conditions and (3) egg-spot number and relative area correlate with immune defense, suggesting a trade-off in the allocation of carotenoids. Taken together, haplochromine egg-spots feature the potential to adapt to the respective underwater light environment, and are traded off with investment into the immune system.
Publisher: Cold Spring Harbor Laboratory
Date: 02-12-2022
DOI: 10.1101/2022.12.01.518784
Abstract: In many animals, ultraviolet (UV) vision guides navigation, foraging, and communication, but few studies have addressed the contribution of UV vision to color discrimination, or behaviorally assessed UV discrimination thresholds. Here, we tested UV-color vision in an anemonefish ( Amphiprion ocellaris ) using a novel five-channel (RGB-V-UV) LED display designed to test UV perception. We first determined that the maximal sensitivity of the A. ocellaris UV cone was at ∼386 nm using microspectrophotometry. Three additional cone spectral sensitivities had maxima at ∼497, 515, and ∼535 nm, which together informed the modelling of the fish’s color vision. Anemonefish behavioral discrimination thresholds for nine sets of colors were determined from their ability to distinguish a colored target pixel from grey distractor pixels of varying intensity. We found that A. ocellaris used all four cones to process color information and is therefore tetrachromatic, and fish were better at discriminating colors (i.e., color discrimination thresholds were lower, or more acute) when targets had UV chromatic contrast elicited by greater stimulation of the UV cone relative to other cone types. These findings imply that a UV component of color signals and cues improves their detectability, that likely increases the salience of anemonefish body patterns used in communication and the silhouette of zooplankton prey.
Publisher: Cold Spring Harbor Laboratory
Date: 10-06-2020
DOI: 10.1101/2020.06.09.139766
Abstract: Many animals can see ultraviolet (UV) light (shorter than 400 nm) undetectable to human vision. UV vision may have functional importance in many taxa including for foraging and communication in birds, reptiles, insects and teleost fishes. Shallow coral reefs transmit a broad spectrum of light and are rich in UV driving the evolution of erse spectral sensitivities in teleost reef fishes, including UV-sensitivity. However, the identities and sites of the specific visual genes that underly vision in reef fishes remain elusive and are useful in determining how molecular evolution has tuned vision to meet the ecological demands of life on the reef. We investigated the visual systems of eleven anemonefish (Amphiprioninae) species, specifically probing for the molecular pathways that facilitate UV-sensitivity. Searching the genomes of anemonefishes, we identified a total of seven functional visual genes from all five vertebrate opsin gene subfamilies. We found rare instances of UV-sensitive SWS1 opsin gene duplications, that produced two functional paralogs ( SWS1α and SWS1β ) and a pseudogene. We also found separate RH2A opsin gene duplicates not yet reported in the family Pomacentridae. Finally, we report on both qualitative and quantitative aspects of opsin gene expression found in the adult retina of the false clown anemonefish ( Amphiprion ocellaris ), and their photoreceptor spectral sensitivities measured using microspectrophotometry.
Publisher: The Company of Biologists
Date: 2016
DOI: 10.1242/JEB.139501
Abstract: Animals often change their habitat throughout ontogeny yet, the triggers for habitat transitions and how these correlate with developmental changes – e.g. physiological, morphological, and behavioural – remain largely unknown. Here, we investigated how ontogenetic changes in body colouration and of the visual system relate to habitat transitions in a coral-reef fish. Adult dusky dottybacks, Pseudochromis fuscus, are aggressive mimics that change colour to imitate various fishes in their surroundings however, little is known about the early life stages of this fish. Using a developmental time-series in combination with the examination of wild caught specimens we uncover that dottybacks change colour twice during development: (i) nearly translucent cryptic pelagic larvae change to a grey camouflage colouration when settling on coral reefs and (ii) juveniles change to mimic yellow or brown coloured fishes when reaching a size capable of consuming juvenile fish prey. Moreover, microspectrophotometric (MSP) and quantitative real time PCR (qRT-PCR) experiments show developmental changes of the dottyback visual system, including the use of a novel adult specific visual gene (RH2 opsin). This gene is likely to be coexpressed with other visual pigments to form broad spectral sensitivities that cover the medium-wavelength part of the visible spectrum. Surprisingly, the visual modifications precede changes in habitat and colour, possibly because dottybacks need to first acquire the appropriate visual performance before transitioning into novel life stages.
Publisher: Public Library of Science (PLoS)
Date: 15-12-2021
DOI: 10.1371/JOURNAL.PONE.0261331
Abstract: Genomic manipulation is a useful approach for elucidating the molecular pathways underlying aspects of development, physiology, and behaviour. However, a lack of gene-editing tools appropriated for use in reef fishes has meant the genetic underpinnings for many of their unique traits remain to be investigated. One iconic group of reef fishes ideal for applying this technique are anemonefishes (Amphiprioninae) as they are widely studied for their symbiosis with anemones, sequential hermaphroditism, complex social hierarchies, skin pattern development, and vision, and are raised relatively easily in aquaria. In this study, we developed a gene-editing protocol for applying the CRISPR/Cas9 system in the false clown anemonefish, Amphiprion ocellaris . Microinjection of zygotes was used to demonstrate the successful use of our CRISPR/Cas9 approach at two separate target sites: the rhodopsin-like 2B opsin encoding gene ( RH2B ) involved in vision, and Tyrosinase-producing gene ( tyr ) involved in the production of melanin. Analysis of the sequenced target gene regions in A . ocellaris embryos showed that uptake was as high as 73.3% of injected embryos. Further analysis of the subcloned mutant gene sequences combined with licon shotgun sequencing revealed that our approach had a 75% to 100% efficiency in producing biallelic mutations in F0 A . ocellaris embryos. Moreover, we clearly show a loss-of-function in tyr mutant embryos which exhibited typical hypomelanistic phenotypes. This protocol is intended as a useful starting point to further explore the potential application of CRISPR/Cas9 in A . ocellaris , as a platform for studying gene function in anemonefishes and other reef fishes.
Publisher: Wiley
Date: 26-05-2010
DOI: 10.1111/J.1420-9101.2010.02018.X
Abstract: Aposematism is defined as the use of conspicuous colouration to warn predators that an in idual is chemically or otherwise defended. Mechanisms that drive the evolution of aposematism are complex. Theoretical and empirical studies show that conspicuousness can be either positively or negatively correlated with toxicity as once aposematism is established, species can allocate resources into becoming more conspicuous and/or increase secondary defences. Here, we investigated the evolution of conspicuousness and toxicity in marine opisthobranchs. Conspicuousness of colour signals was assessed using spectral reflectance measurements and theoretical vision models from the perspective of two reef fish signal receivers. The relative toxicity of chemicals extracted from each opisthobranch species was then determined using toxicity assays. Using a phylogenetic comparative analysis, we found a significant correlation between conspicuousness and toxicity, indicating that conspicuousness acts as an honest signal when signifying level of defence and provides evidence for aposematism in opisthobranchs.
Publisher: Oxford University Press (OUP)
Date: 11-2017
DOI: 10.1002/EVL3.24
Abstract: Our understanding of animal communication has been largely driven by advances in theory since empirical evidence has been difficult to obtain. Costly signaling theory became the dominant paradigm explaining the evolution of honest signals, according to which communication reliability relies on differential costs imposed on signalers to distinguish animals of different quality. On the other hand, mathematical models disagree on the source of costs at the communication equilibrium. Here, we present an empirical framework to study the evolution of honest signals that generates predictions on the form, function, and sources of reliability of visual signals. We test these predictions on the facial color patterns of the cooperatively breeding Princess of Burundi cichlid, Neol rologus brichardi. Using theoretical visual models and behavioral experiments we show that these patterns possess stable chromatic properties for efficient transmission in the aquatic environment, while dynamic changes in signal luminance are used by the fish to communicate switches in aggressive intent. By manipulating signal into out-of-equilibrium expression and simulating a cheater invasion, we demonstrate that social costs (receiver retaliation) promote the honesty of this dynamic conventional signal. By directly probing the sender of a signal in real time, social selection is likely to be the mechanism of choice shaping the evolution of inexpensive, yet reliable context-dependent social signals in general.
Publisher: Oxford University Press (OUP)
Date: 25-09-2021
Abstract: Vertebrates use cone cells in the retina for color vision and rod cells to see in dim light. Many deep-sea fishes have adapted to their environment to have only rod cells in the retina, while both rod and cone genes are still preserved in their genomes. As deep-sea fish larvae start their lives in the shallow, and only later submerge to the depth, they have to cope with erse environmental conditions during ontogeny. Using a comparative transcriptomic approach in 20 deep-sea fish species from eight teleost orders, we report on a developmental cone-to-rod switch. While adults mostly rely on rod opsin (RH1) for vision in dim light, larvae almost exclusively express middle-wavelength-sensitive (“green”) cone opsins (RH2) in their retinas. The phototransduction cascade genes follow a similar ontogenetic pattern of cone—followed by rod-specific gene expression in most species, except for the pearleye and sabretooth (Aulopiformes), in which the cone cascade remains dominant throughout development, casting doubts on the photoreceptor cell identity. By inspecting the whole genomes of five deep-sea species (four of them sequenced within this study: Idiacanthus fasciola, Chauliodus sloani Stomiiformes Coccorella atlantica, and Scopelarchus michaelsarsi Aulopiformes), we found that they possess one or two copies of the rod RH1 opsin gene, and up to seven copies of the cone RH2 opsin genes in their genomes, while other cone opsin classes have been mostly lost. Our findings hence provide molecular evidence for a limited opsin gene repertoire in deep-sea fishes and a conserved vertebrate pattern whereby cone photoreceptors develop first and rod photoreceptors are added only at later developmental stages.
Publisher: Cold Spring Harbor Laboratory
Date: 11-02-2016
DOI: 10.1101/039552
Abstract: How honest signals evolve is a question that has been hotly debated by animal communication theoreticians and for which empirical evidence has been difficult to obtain. Theory predicts that, due to strong conflicts of interest, communication in aggressive contexts should be under strong selection for clear and reliable signaling. On the other hand, context-dependent signaling increases cheating opportunities, depending on how senders and receivers use, acquire and process signal information. Using animal signaling theory, theoretical visual models and behavioral experimentation, we characterize and determine proximate honesty mechanisms of the facial coloration in the Princess of Burundi cichlid, Neol rologus brichardi, a species with complex social interactions. We show that this facial color pattern evolved stable chromatic conspicuousness for efficient transmission in the aquatic environment, while context-dependent plasticity in luminance of the horizontal black stripe element is used to signal switches in aggressive intent. Importantly, using experimental signal manipulation we demonstrate that social selection by receiver retaliation is the mechanism responsible for maintaining signal honesty. We suggest that by affecting the evolution of pigmentation patterns in sexually monochromatic cichlid species, social selection can have potential impacts on ersification dynamics.
Publisher: Cold Spring Harbor Laboratory
Date: 04-06-2022
DOI: 10.1101/2022.06.02.494615
Abstract: The visual capabilities of fish are optimised for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e . g ., ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short-term changes in the light environment, e . g ., algal blooms and light pollution. In this study, we investigated the effect of short-term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in larval and adult diurnal reef fish (convict surgeonfish Acanthurus triostegus ). Results revealed phenotypic plasticity in the retina across ontogeny, particularly in the larvae. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light or simulated artificial light at night had a lesser effect. Under dim light, larvae and adults increased expression of the cone opsin genes, sws2a, rh2c and lws , within a few days and larvae also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes likely enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species’ natural light environment, i . e ., a diurnal fish in ‘constant night’. Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 hours. Overall, our study showed rapid, reversible light-induced changes in the retina of A. triostegus , demonstrating phenotypic plasticity in the visual system of a reef fish throughout life.
Publisher: Cold Spring Harbor Laboratory
Date: 24-10-2023
Publisher: SPIE
Date: 03-10-2022
DOI: 10.1117/12.2646127
Publisher: CRC Press
Date: 03-11-2022
Publisher: Cold Spring Harbor Laboratory
Date: 27-05-2020
DOI: 10.1101/2020.05.25.114991
Abstract: Vertebrates use cone cells in the retina for colour vision and rod cells to see in dim light. Many deep-sea fishes have adapted to their environment to have only rod cells in the retina, while both rod and cone genes are still preserved in their genomes. As deep-sea fish larvae start their lives in the shallow, and only later submerge to the depth, they have to cope with erse environmental conditions during ontogeny. Using a comparative transcriptomic approach in 20 deep-sea fish species from eight teleost orders, we report on a developmental cone-to-rod switch. While adults mostly rely on rod opsin ( RH1 ) for vision in dim light, larvae almost exclusively express middle-wavelength-sensitive (“green”) cone opsins ( RH2 ) in their retinas. The phototransduction cascade genes follow a similar ontogenetic pattern of cone-followed by rod-specific gene expression in most species, except for the pearleye and sabretooth (Aulopiformes), in which the cone cascade remains dominant throughout development. By inspecting the whole genomes of five deep-sea species (four of them sequenced within this study: Idiacanthus fasciola, Chauliodus sloani Stomiiformes Coccorella atlantica, and Scopelarchus michaelsarsi Aulopiformes), we found that deep-sea fish possess one or two copies of the rod RH1 opsin gene, and up to seven copies of the cone RH2 opsin genes in their genomes, while other cone opsin classes have been mostly lost. Our findings hence provide molecular evidence for a limited opsin gene repertoire and a conserved vertebrate pattern whereby cone photoreceptors develop first and rod photoreceptors are added only at later developmental stages.
Publisher: Oxford University Press (OUP)
Date: 09-06-2017
Publisher: Oxford University Press (OUP)
Date: 10-08-2021
DOI: 10.1093/GBE/EVAB184
Abstract: Many animals including birds, reptiles, insects, and teleost fishes can see ultraviolet (UV) light (shorter than 400 nm), which has functional importance for foraging and communication. For coral reef fishes, shallow reef environments transmit a broad spectrum of light, rich in UV, driving the evolution of erse spectral sensitivities. However, the identities and sites of the specific visual genes that underly vision in reef fishes remain elusive and are useful in determining how evolution has tuned vision to suit life on the reef. We investigated the visual systems of 11 anemonefish (Amphiprioninae) species, specifically probing for the molecular pathways that facilitate UV-sensitivity. Searching the genomes of anemonefishes, we identified a total of eight functional opsin genes from all five vertebrate visual opsin subfamilies. We found rare instances of teleost UV-sensitive SWS1 opsin gene duplications that produced two functionally coding paralogs (SWS1α and SWS1β) and a pseudogene. We also found separate green sensitive RH2A opsin gene duplicates not yet reported in the family Pomacentridae. Transcriptome analysis revealed false clown anemonefish (Amphiprion ocellaris) expressed one rod opsin (RH1) and six cone opsins (SWS1β, SWS2B, RH2B, RH2A-1, RH2A-2, LWS) in the retina. Fluorescent in situ hybridization highlighted the (co-)expression of SWS1β with SWS2B in single cones, and either RH2B, RH2A, or RH2A together with LWS in different members of double cone photoreceptors (two single cones fused together). Our study provides the first in-depth characterization of visual opsin genes found in anemonefishes and provides a useful basis for the further study of UV-vision in reef fishes.
Publisher: Elsevier BV
Date: 10-2020
Publisher: Cold Spring Harbor Laboratory
Date: 23-09-2018
DOI: 10.1101/424895
Abstract: Vertebrate vision is accomplished through a set of light-sensitive photopigments, which are located in the photoreceptors of the retina and consist of a visual opsin protein bound to a chromophore. In dim-light, vertebrates generally rely upon a single rod opsin (RH1) for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Amongst these, the silver spinyfin ( Diretmus argenteus Johnson 1863) stands out as having the highest number of visual opsins known for animals to date (2 cone and 38 rod opsins). Spinyfins simultaneously express up to 14 RH1s encoding for photopigments with different peak spectral sensitivities (λ max =448-513 nm) that cover the range of the residual daylight, as well as the bioluminescence spectrum present in the deep-sea. Our findings present novel molecular and functional evidence for the recurrent evolution of multiple rod opsin-based vision in vertebrates. Contrary to the single rod opsin used by most vertebrates, some fishes use multiple rod opsins for vision in the dimly lit deep-sea.
Publisher: Cold Spring Harbor Laboratory
Date: 08-10-2020
DOI: 10.1101/2020.10.07.330746
Abstract: Genomic manipulation is a useful approach for elucidating the molecular pathways underlying aspects of development, physiology, and behaviour. However, a lack of gene-editing tools appropriated for use in reef fishes has meant the genetic underpinnings for many of their unique traits remain to be investigated. One iconic group of reef fishes ideal for applying this technique are anemonefishes (Amphiprioninae) as they are widely studied for their symbiosis with anemones, sequential hermaphroditism, complex social hierarchies, skin pattern development, and vision, and are raised relatively easily in aquaria. In this study, we developed a gene-editing protocol for applying the CRISPR/Cas9 system in the false clown anemonefish, Amphiprion ocellaris . Microinjection of eggs at the one-cell stage was used to demonstrate the successful use of our CRISPR/Cas9 approach at two separate target sites: the rhodopsin-like 2B opsin encoding gene ( RH2B ) involved in vision, and Tyrosinase-producing gene ( tyr ) involved in the production of melanin. Analysis of the sequenced target gene regions in A. ocellaris embryos showed that uptake was as high as 50% of injected eggs. Further analysis of the subcloned mutant gene sequences revealed that our approach had a 75% to 100% efficiency in producing biallelic mutations in G0 A. ocellaris embryos. Moreover, we clearly show a loss-of-function in tyr mutant embryos which exhibited typical hypomelanistic phenotypes. This protocol is intended as a useful resource for future experimental studies that aim to elucidate gene function in anemonefishes and reef fishes in general.
Publisher: Cold Spring Harbor Laboratory
Date: 12-05-2021
DOI: 10.1101/2021.05.11.443711
Abstract: Vertebrates have four visual cone opsin classes that, together with a light-sensitive chromophore, provide sensitivity from the ultraviolet to the red wavelengths of light. The rhodopsin-like 2 (RH2) opsin is sensitive to the centre blue-green part of the spectrum, which is the most prevalent light underwater. While various vertebrate groups such as mammals and sharks have lost the RH2 gene, in teleost fishes this opsin has continued to proliferate. By investigating the genomes of 115 teleost species, we find that RH2 shows an extremely dynamic evolutionary history with repeated gene duplications, gene losses and gene conversion affecting entire orders, families and species. At least four ancestral duplications provided the substrate for today’s RH2 ersity with duplications occurring in the common ancestors of Clupeocephala, Neoteleostei, and Acanthopterygii. Following these events, RH2 has continued to duplicate both in tandem and during lineage specific genome duplications. However, it has also been lost many times over so that in the genomes of extant teleosts, we find between zero to eight RH2 copies. Using retinal transcriptomes in a phylogenetic representative dataset of 30 species, we show that RH2 is expressed as the dominant green-sensitive opsin in almost all fish lineages. The exceptions are the Osteoglossomorpha (bony tongues and mooneyes) and several characin species that have lost RH2 , and tarpons, other characins and gobies which do not or only lowly express the gene. These fishes instead express a green-shifted long-wavelength-sensitive LWS opsin. Our study highlights the strength of using modern genomic tools within a comparative framework to elucidate the detailed evolutionary history of gene families.
Publisher: CRC Press
Date: 03-11-2022
Publisher: The Royal Society
Date: 09-2015
Abstract: Aggressive mimicry is an adaptive tactic of parasitic or predatory species that closely resemble inoffensive models in order to increase fitness via predatory gains. Although similarity of distantly related species is often intuitively implicated with mimicry, the exact mechanisms and evolutionary causes remain elusive in many cases. Here, we report a complex aggressive mimicry strategy in Plecodus straeleni , a scale-eating cichlid fish from Lake Tanganyika, which imitates two other cichlid species. Employing targeted sequencing on ingested scales, we show that P. straeleni does not preferentially parasitize its models but—contrary to prevailing assumptions—targets a variety of co-occurring dissimilar looking fish species . Combined with tests for visual resemblance and visual modelling from a prey perspective, our results suggest that complex interactions among different cichlid species are involved in this mimicry system.
Publisher: Oxford University Press (OUP)
Date: 11-2022
Abstract: Ultraviolet (UV) vision is widespread among teleost fishes, of which many exhibit UV skin colors for communication. However, aside from its role in mate selection, few studies have examined the information UV signaling conveys in other socio-behavioral contexts. Anemonefishes (subfamily, Amphiprioninae) live in a fascinating dominance hierarchy, in which a large female and male dominate over non-breeding subordinates, and body size is the primary cue for dominance. The iconic orange and white bars of anemonefishes are highly UV-reflective, and their color vision is well tuned to perceive the chromatic contrast of skin, which we show here decreases in the amount of UV reflectance with increasing social rank. To test the function of their UV-skin signals, we compared the outcomes of staged contests over dominance between size-matched Barrier Reef anemonefish (Amphiprion akindynos) in aquarium chambers viewed under different UV-absorbing filters. Fish under UV-blocking filters were more likely to win contests, where fish under no-filter or neutral-density filter were more likely to submit. For contests between fish in no-filter and neutral density filter treatments, light treatment had no effect on contest outcome (win/lose). We also show that sub-adults were more aggressive toward smaller juveniles placed under a UV filter than a neutral density filter. Taken together, our results show that UV reflectance or UV contrast in anemonefish can modulate aggression and encode dominant and submissive cues, when changes in overall intensity are controlled for.
Publisher: Cold Spring Harbor Laboratory
Date: 03-07-2019
DOI: 10.1101/691774
Abstract: Ontogenetic changes of the visual system are often correlated to shifts in habitat and feeding behaviour of animals. Coral reef fishes begin their lives in the pelagic zone and then migrate to the reef. This transition of habitat frequently involves a change in diet and light environment as well as major morphological modifications. The spotted unicornfish, Naso brevirostris , is known to shift diet from zooplankton to algae and back to zooplankton when transitioning from larval to juvenile and then to adult stages. Concurrently, N. brevirostris also moves from an open pelagic to a coral-associated habitat before migrating up in the water column when reaching adulthood. Using retinal mapping techniques, we discovered that the distribution and density of ganglion and photoreceptor cells in N. brevirostris do not change with the habitat or the feeding habits of each developmental stage. Instead, fishes showed a neotenic development with a slight change from larval to juvenile stages and not many modifications thereafter. Visual gene expression based on RNA sequencing mirrored this pattern independent of stage, fishes mainly expressed three cone opsin genes ( SWS2B, RH2B, RH2A ), with a quantitative difference in the expression of the green opsin genes ( RH2A and RH2B ) when transitioning from larvae to juveniles. Hence, contrary to the ontogenetic changes found in many animals, the visual system is fixed early on in N. brevirostris development calling for a thorough analysis of visual system development of the reef fish community.
Start Date: 2020
End Date: 2020
Funder: Society for Molecular Biology and Evolution
View Funded ActivityStart Date: 2020
End Date: 2022
Funder: Australian Research Council
View Funded ActivityStart Date: 2016
End Date: 2017
Funder: Sea World Research and Rescue Foundation
View Funded ActivityStart Date: 2018
End Date: 2021
Funder: Australian Research Council
View Funded ActivityStart Date: 2018
End Date: 2019
Funder: Sea World Research and Rescue Foundation
View Funded ActivityStart Date: 2014
End Date: 2014
Funder: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
View Funded ActivityStart Date: 2016
End Date: 2017
Funder: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
View Funded ActivityStart Date: 2013
End Date: 2014
Funder: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
View Funded ActivityStart Date: 03-2018
End Date: 12-2021
Amount: $550,496.00
Funder: Australian Research Council
View Funded ActivityStart Date: 01-2020
End Date: 12-2023
Amount: $424,856.00
Funder: Australian Research Council
View Funded Activity