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Fogg, L. G.

Publications and source records attributed to Fogg, L. G..

7 recordsLinked to original sources

Evolutionary dynamics of the vertebrate Wnt gene repertoire

The Wnt gene family plays a central role in vertebrate development, yet its evolutionary dynamics across lineages remain largely unexplored. Here, we present the most comprehensive analysis of Wnt gene evolution in vertebrates to date, leveraging a large-scale comparative genomics approach of 38,886 Wnt gene sequences mined from 1,961 species. We first investigate overall patterns of gene retention, duplication, and loss, and then focus specifically on the impact of whole-genome duplications (WGDs). We uncover striking variation in Wnt gene repertoire sizes, with ray-finned fishes (Actinopterygii) exhibiting the largest repertoires - even after excluding taxa with recent WGDs. Notably, we identify extreme expansions in polyploid cyprinids, including an octoploid hybrid harbouring 99 Wnt genes, the highest number observed. Unexpectedly elevated Wnt copy numbers in diploid species, such as the Antarctic lanternfish (Electrona antarctica) and the brook lamprey (Lethenteron reissneri), point to lineage-specific expansions with potential adaptive significance. Evolutionary rate analyses reveal that certain Wnt clades - especially Wnt8 and Wnt16 - exhibit elevated dN/dS ratios and high birth-death rates, indicative of repeated episodes of relaxed constraint or adaptive diversification. Contrary to our expectations, there was no relationship between developmental expression timing and evolutionary rates, suggesting pleiotropic regulation and functional redundancy of Wnt genes. Altogether, our findings reveal pervasive, lineage-specific remodelling of Wnt gene repertoires, shaped by both genome duplication history and divergent evolutionary trajectories. This work provides a high-resolution framework for understanding the molecular evolution of a key developmental toolkit and highlights candidate genes for future studies of vertebrate eco-morphological diversity.

evolutionary biology↗

The visual system of the longest-living vertebrate, the Greenland shark

The Greenland shark (Somniosus microcephalus) is the longest-living vertebrate and inhabits the extremely dim and cold waters of the Arctic deep sea. This has led to speculations that it may have lost functional vision. Here, we present genomic, transcriptomic, histological and functional evidence that the Greenland shark retains an intact visual system well-adapted for life in dim light. Histology and in vitro opsin expression revealed visual adaptations typical of deep-sea species, including densely packed, elongated rods and a short-wavelength shift in rod visual pigment sensitivity. RNAscope confirmed the presence of essential visual cell types, such as rods, Muller glia, and bipolar, amacrine, and ganglion cells. Moreover, despite being centuries old, the examined specimens showed no signs of retinal degeneration. Using whole genome and retinal RNA-sequencing, we further show that dim-light (rod-based) vision genes are intact and robustly expressed, while many bright-light (cone-based) vision genes have become pseudogenized and/or are no longer expressed. Finally, our data suggest that efficient DNA repair mechanisms may contribute to the long-term preservation of retinal function over centuries in the Greenland shark.

evolutionary biology↗

Deep-sea fish reveal alternative pathway for vertebrate visual development

Vertebrate vision is accomplished by two phenotypically distinct types of photoreceptors in the retina: the saturation-resistant cones for the detection of bright light and the highly sensitive rods for dim light conditions [1]. The current dogma is that, during development, all vertebrates initially feature a cone-dominated retina, and rods are added later [2, 3]. By studying the ontogeny of vision in three species of deep-sea fishes, we show that their larvae express cone-specific genes in photoreceptors with rod-like morphologies. Through development, these fishes either retain this rod-like cone retina (Maurolicus mucronatus) or switch to a retina with true rod photoreceptors with expression of rod-specific genes and transcription factors (Vinciguerria mabahiss and Benthosema pterotum). In contrast to the larvae of most marine fishes, which inhabit the bright upper layer of the open ocean, the larvae of deep-sea fishes occur deeper, exposing them to a dimmer light environment [4-7]. Spectral maxima predictions from molecular dynamics simulations and environmental light estimations suggest that using transmuted photoreceptors that combine the characteristics of both cones and rods maximises visual performance in these dimmer light conditions. Our findings provide molecular, morphological, and functional evidence for the evolution of an alternative developmental pathway for vertebrate vision.

evolutionary biology↗

Evolution of the non-visual and visual opsin gene repertoire in ray-finned fishes

Photoreception - the detection of light for image formation (vision) as well as for non-image-forming purposes (circadian regulation, DNA repair) - is critical to the survival of most animals. In vertebrates, photoreception is mediated by opsin proteins, which are classified, according to their function, into visual and non-visual opsins. Here, we provide the most comprehensive study to date on the evolution of the opsin gene family in the largest class of vertebrate, fishes, with a particular focus on the understudied non-visual opsins. Based on an in-depth analysis of 535 high-quality genomes, we document great variation in gene numbers in the different opsin gene subfamilies across ray-finned fishes and show that visual opsins are more prone to duplications and losses than non-visual opsins. We provide compelling evidence that visual and non-visual opsins co-evolve in ray-finned fishes, both in terms of copy numbers and selective pressures acting on their coding sequences, probably in response to the different photic environments they inhabit. Species that live in dim light or all in the dark (such as in caves or the deep sea) convergently reduced their visual and non-visual opsin gene repertoires, while polar species feature accelerated evolution in both. Fishes that rely on electroreception show a reduction in the number of visual and non-visual opsin genes and accelerated evolution of the remaining genes. We further found that genes of the phototransduction cascade co-evolve with opsins. Finally, that non-visual opsins are mainly expressed in testes and ovaries (next to the eyes) supports a function in gamete biology.

evolutionary biology↗

Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes

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. SignificanceMost 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.

zoology↗

Developing and adult reef fish show rapid, reversible light-induced plasticity in their visual system

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.

developmental biology↗

Development of dim-light vision in the nocturnal coral reef fish family, Holocentridae

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/proliferation. 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 diverged 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. Summary statementCoral reef fishes in the family Holocentridae remodel their retina at the cellular and molecular levels to adapt to a nocturnal lifestyle during development.

developmental biology↗