Zuzana Musilova

Photopigments, formed by an opsin protein bound to a light‐sensitive chromophore, underlie vertebrate vision. Long‐wavelength–sensitive (LWS) opsins mediate red‐light detection, and most teleosts retain a single functional LWS1. A shorter‐shifted green‐sensitive paralog (LWS2) is found only in a few lineages. By mining teleost genomes and sequencing retinal transcriptomes, we identify elopomorphs as an additional lineage retaining LWS2 (alongside characins and osteoglossomorphs). Surprisingly, we reveal a previously overlooked, shorter‐shifted paralog, LWS3, restricted to gobies (Percomorpha) and arising from an ancestral duplication either in the teleost or in the percomorph ancestor. Structural modelling of twelve LWS opsins reveals convergent evolution at four key amino acid sites (214, 259, 261, 269) in the retinal‐binding pocket, indicating convergent substitutions in human MWS (an old‐world primate‐specific duplicate of the vertebrate LWS1), teleost LWS2, and goby LWS3 relative to red‐sensitive counterparts, consistent with repeated spectral shifts towards greener wavelengths. In several lineages, including characins, mormyrids, gobies, and primates, these shorter‐shifted LWS opsins have at least partially replaced the canonical green‐sensitive RH2‐based visual pigment. Retinal transcriptomes revealed variable lws3 expression across adult gobies, either complementing lws1 in most species, or dominating the visual opsin expression profile as in the sicydiines. In situ hybridisation in the whitebarred goby ( Amblygobius phalaena ; Valenciennes, 1837) showed that lws1 and lws3 are expressed in separate double‐cone members, analogous to rh2 expression in other fish species. Together, these results show that repeated convergence towards shorter LWS sensitivity in vertebrate evolution involves coordinated changes at the molecular, regulatory, and functional levels, providing a striking example of multilevel sensory adaptation.

Hybridisation and whole-genome duplication generate evolutionary novelty by combining and duplicating divergent parental genomes. Yet, how organisms differentially deploy duplicated gene repertoires across development remains poorly understood. The vertebrate visual system provides an excellent model for addressing this question because colour vision depends on the tightly regulated expression of opsin genes, which often undergo pronounced ontogenetic changes. Here, using comparative transcriptomics, we show that the allopolyploid common barbel ( Barbus barbus ) has evolved coordinated developmental partitioning of duplicated cone opsin genes. During ontogeny, the short-wavelength-sensitive opsins SWS1 and SWS2 switch expression between parental-subgenome ohnologs, while the middle-wavelength-sensitive RH2 switches between tandem paralogs, with all three transitions being synchronised. In contrast, the long-wavelength-sensitive LWS ohnologs from both parental genomes remain co-expressed throughout development. Single-nucleus RNA sequencing further revealed a strongly rod-dominated retina and largely conserved expression of phototransduction genes across recent ohnologs. The retention of all 14 visual opsin genes and their differential developmental deployment in common barbel highlights the value of independently evolved allopolyploid lineages for investigating the evolutionary consequences of genome duplication. More broadly, our findings show how hybridisation and genome duplication can enable divergent expression of parental gene copies, potentially contributing to sensory adaptation over evolutionary timescales.

Deep-water habitats have been colonized repeatedly by fishes, driving the evolution of visual systems under extremely low-light conditions. Here, we investigated visual adaptation in cichlids from the Barombi Mbo crater lake by comparing shallow- and deep-water species using retinal single-cell transcriptomics and analyses of retinal specializations. The shallow-water species Pungu maclareni expressed a broader repertoire of visual opsins across distinct populations of short-(SWS), medium-(RH2), and long-wavelength-sensitive (LWS) cone photoreceptors. In contrast, the deep-water species Myaka myaka lacked a distinct LWS cone population and instead relied predominantly on RH2Aα/β -expressing, green-sensitive photoreceptors. To assess whether these deep-water RH2 cones corresponded to canonical RH2 or LWS programmes, we compared conserved photoreceptor markers. Deep-water RH2 cones retained elements of both RH2- and LWS-associated transcriptional programmes, revealing a mixed profile lacking a clear canonical cone-type signature. LWS-associated transcriptional regulators also differed between species, with tbx2a absent from M. myaka cones, consistent with the loss of LWS opsin expression, whereas thrb persisted in M. myaka RH2 cones. We further examined retinal specialization across eight species from the radiation and found that retinal topography also differed in photoreceptor distributions and ganglion cell-based acuity centers in association with habitat depth but also with trophic ecology of the species. Together, our findings show that visual adaptation in a young adaptive radiation involves coordinated changes in visual opsin expression, cone-associated transcriptional programmes, and retinal organization, highlighting how sensory systems can quickly evolve through changes at multiple biological levels in response to ecological conditions.

Elucidating theories of sex chromosome evolution requires approaches that allow fine scale delimitations of sex-determining regions within a phylogenetic context. This can address whether shared sex chromosomes across related species are due to shared ancestry, or whether genetic sex-determining regions have repeatedly evolved. Haplochromine cichlids, as one of the most successful fish lineages on Earth, have been a focal study system of sex chromosome research, both because of their rapid rate of sex chromosome turnover and the repeated emergence of certain sex chromosomes across the lineage. Here, we newly describe sex chromosomes in members of the earliest branch of the modern haplochromines, the Tropheini, based on whole-genome sequencing data, using a combination of SNP- and kmers-based methods. We show that despite the repeated co-options of ancestral chromosomes LG5 and LG7 in these species, the origins of these sex chromosomes are independent. Investigation of gene functions, allele differences, and sex-biased gene expression within the discovered sex-linked regions provides no evidence that sexual antagonism has driven the repeated evolution of a region on LG5 that overlaps between four of these species. By comparing the sex-determining regions on LG5 and LG7 across haplochromines, we show that a common origin is unlikely, and that while sex chromosomes themselves may be shared between several Haplochromini, the sex-determining genes or mechanism likely differ. This study paves the way to explore newly emerging theories of sex chromosome evolution, such as the role of chromosomal fusion or recombination patterns across the genome.

Evolutionary adaptations to life on land include changes to an animal's physiology, morphology and behaviour. The visual systems of amphibious fishes show pronounced morphological adaptations; however, whether molecular changes also occur remains largely unknown. Here, we investigated the molecular evolution of visual opsin genes in blennies (Blenniidae), with a primary focus on the amphibious and terrestrial Salariini. Using retinal transcriptomes and amino acid comparisons in nine species from fully aquatic to terrestrial, we found limited sequence changes and no correlation between habitat and cone opsin gene expression. The ‘red-sensitive’ lws, the ‘green-sensitive’ rh2a, and two ‘blue-sensitive’ sws2aα and sws2aβ paralogs were expressed in all species, with the latter two showing pronounced phylogenetic inertia. Long-wavelength-dominated vision is likely beneficial for feeding on algae and detritus, the primary food source of most study species, and may be co-adapted to perceive red-coloured displays in terrestrial blennies. Conversely, a lack of ‘ultraviolet-sensitive’ sws1 expression coincides with UV-absorbing lenses in blennies, which likely evolved to protect the retina from the damaging effects of short-wavelength radiation, independent of habitat. Our data suggest that, at the molecular level, the visual systems that evolved in aquatic blennies have been retained in species that have progressively transitioned onto land.

Animal selection of foraging grounds is a trade‐off among available feeding resources, intra and interspecific competition, disturbance and predation risks. The present study was carried out at Kadalundi‐Vallikkunnu Community Reserve on the West coast of Kerala (India) in the Central Asian Flyway. The Reserve hosts different coastal habitats, including mudflats, mangroves and sand beaches, and although 31 species of shorebirds are commonly present, it is heavily impacted by human activities. The findings highlight the necessity of robust management of anthropogenic waste and reveal the detrimental impacts of human activities on species communities of conservation concern. We investigated how the densities and intake rates of nine migratory shorebird species responded spatially and temporally (9 years) to a complex situation where different levels of disturbance, prey density, densities of predators and shorebirds were found among three habitats. Human activities, specifically waste disposal, acted as a continuous over time anthropogenic resource subsidy and significantly affected predator density, resulting in overabundant predator density and high attack rates. The densities of all shorebirds were positively regulated by shorebirds and prey densities and affected by habitat type and year. The density of predators and attack rates negatively affected the densities of shorebirds. Despite this, all species continued to concentrate to feed at the beach, the habitat with the second highest density of predators but also of prey. It is hypothesized that the high predator density and attack rates were above a natural upper threshold, making the three habitats equally dangerous. Most of the intake rates of the different shorebird species were positively regulated by the density of shorebirds and affected by habitat type, season, and year. Nearly half of the shorebirds' intake rates were negatively affected by the density of predators or predator's attack rates. Our results showed that non‐lethal effects (reduction of energy intake) were at play in a situation where a continuous anthropogenic resource subsidy resulted in overabundant predator density and high attack rates. Practical implication : In the context of overabundant predation pressure and disturbance, shorebirds used public information and habitat structure/cues to congregate in the habitat that was signalled as the best feeding and safest habitat, the beach. In a system where a clear situation of anthropogenic resource subsidies to predators exists resulting in overabundant predator density and high attack rates and with signs of non‐lethal effects (reduction of energy intake), it is urgent to upgrade significantly the waste management plan in order to decrease overabundant predators and improve habitat quality for migratory shorebirds. Under the situation where shorebirds use public information and habitat cues to concentrate in specific feeding grounds, they can be attracted to areas that can act as ecological traps. And migratory species that are under high energetic demands and depend on few high‐quality habitats scattered along their migratory routes are particularly at risk.

Cichlid visual systems can evolve rapidly during adaptive radiations. The Bermin crater lake species flock in Cameroon, comprising 13 (nine valid and four undescribed) Coptodon species, offers an ideal model to investigate visual adaptation to the deep-water light environments. Here, we examine visual opsin genes sequences and expression using 109 retina transcriptomes, focusing on interspecific variation with habitat depth, as well as on seasonal changes in the migratory species between depths. All species possess a multichromatic system with at least five cone opsins. While opsin coding sequences show limited divergence—consistent with the flock's recent origin—opsin expression profiles vary substantially. Deep-water species showed reduced sws1 and sws2b expression, in line with lower UV and violet light availability in deeper waters. Unexpectedly, proportional expression of the red-sensitive lws opsin gene increases with depth, contrasting with patterns in other lacustrine cichlids. In the seasonally migrating species Coptodon imbrifernus, opsin expression is plastic, with decreased sws2b levels in deeper-dwelling dry-season individuals. To contextualize our findings, we compared Bermin cichlids to the older Barombi Mbo crater lake radiation. While single cone adaptations to the depth were convergent (loss of UV/violet sensitivity, enhanced blue sensitivity), double cone response diverged: lws expression was lost in Barombi Mbo while increased in Bermin deep-water species. Our findings suggest that plasticity in opsin expression plays a crucial role at the onset of sensory evolution, potentially paving the way for future genetic change. This study underscores the power of young systems like Bermin for uncovering the mechanisms driving early visual system diversification.

Sensory systems are under constant pressure from environmental changes, and vision offers a particularly rich lens to study adaptation. In this Special Feature, we present a collection of contributions that explore the roles of visual systems in extreme or dynamic environments. Too little light—In habitats ranging from caves to the deep sea, vision either becomes redundant and is lost, or undergoes striking morphological and molecular adaptations to maximize photon capture. The persistence of vision in dark deep‐sea ecosystems underscores the ecological role of bioluminescence as an alternative light source. Too much light—Excessive illumination, glare and UV radiation during the polar summer, in desert or snow‐covered habitats, drive the evolution of protective mechanisms, from UV‐filtering ocular media to behavioural strategies. Polar animals, such as reindeer, face the added challenge of coping with extreme seasonal variability in light conditions. Changing is challenging—While capable of remarkable plasticity, vision is vulnerable to abrupt or anthropogenic changes. Light pollution, turbidity and habitat alteration can disrupt communication, orientation and species boundaries, with cascading ecological effects. Coral reef fishes illustrate both the potential and limits of plasticity, while pigment functions reveal that visual systems are shaped by both visual and non‐visual demands, highlighting the need for integrative approaches to understand how changes may reshape visual ecology.

The endostyle is an endodermal organ unique to nonvertebrate chordates except for lamprey larvae, where it serves as forerunner to the adult thyroid. Here, we examine whether the acquisition of neural crest in the vertebrate lineage played a role in the elaboration of the endostyle. CM-DiI lineage tracing reveals a neural crest contribution to the endostyle, and CRISPR-Cas9 mutagenesis of key neural crest genes causes endostyle defects including formation of a single rather than bilobed structure. RNA sequencing reveals gene profiles characteristic of embryonic neural crest cells and Schwann cell precursors in the developing endostyle. Contrasting with the prevailing view that the endostyle is an endoderm-derived organ, we propose that the acquisition of the neural crest played a critical step in promoting thyroid evolution from chordate endostyle.

In the evolution of vision, changes in the number of visual opsin genes, gene conversion, amino acid sequence mutations, and gene expression levels are common molecular mechanisms in how teleost fishes adapt to different aquatic (light) environments. Visual evolution in challenging environments like the deep sea often pushes this to the extreme. Many adaptations to the visual systems of deep‐sea fishes have evolved multiple times convergently or in parallel in different species, for example, morphologically tubular eyes and rod‐only retinas, and molecularly rhodopsin duplications. Others are unique to this extreme environment, such as 38 rhodopsins in spinyfins or far‐red vision in dragon fishes using a visual pigment plus photosensitizer (bacteriochlorophyll) complex. This illustrates the strength of the selective pressures, including low‐light conditions, cold temperatures, and extreme pressure, which act to shape vision at depth. Rod and cone cell identity (and dichotomy) is unclear in some deep‐sea fishes, as evidenced by the molecular mismatch with the photoreceptor morphology or among the expressed visual genes (e.g. opsin vs. phototransduction cascade genes). Rod‐like cones are found in some deep‐sea fishes (e.g. in pearlsides) and are thought to result from cell transmutation, a process in which the gross morphology of the cell resembles rods, but the molecular machinery is typical of cones. In other fish species (e.g. Aulopiformes), there is a mismatch between the expression of opsins and phototransduction cascade genes. The mechanism is unknown but may be caused by transmuted rod‐like cones, which have, in addition, co‐opted the rod opsin (to replace its cone opsin). Comparative‐omic and imaging approaches have the power to detect and evolutionarily explain such intermediate photoreceptor cell types. Leveraging recent advances in the ‐omics and imaging fields, such as spatial single‐cell multi‐omics approaches will significantly increase the depth and breadth of the species studied. This dramatically enhances the comparative power of deep‐sea fish visual exploration, enabling us to address century‐old and newly emerging questions in this exciting field. Read the free Plain Language Summary for this article on the Journal blog.