Search bioRxiv⌕ Search

Biology subjects

Musilova, Z.

Publications and source records attributed to Musilova, Z..

11 recordsLinked to original sources

Synchronised developmental partitioning of visual opsins across parental subgenomes in allopolyploid Barbus barbus

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.

evolutionary biology↗

Rapid evolution of cone identity and retinal topography in deep-water crater lake cichlids

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 RH2A/{beta}-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.

evolutionary biology↗

Seeing in the deep: evolution of the opsin gene expression in Bermin crater lake cichlids

Cichlid visual systems can evolve rapidly during adaptive radiations. This study investigates the Bermin crater lake species flock in Cameroon, comprising thirteen (nine valid and four undescribed) Coptodon species, to explore the effects of deep-water light environments on visual evolution. We analyzed visual opsin genes and their expression using 109 retina transcriptomes, focusing on differences among species at varying depths, and seasonal changes in the visual system of a seasonally migrating species. All species exhibit a multichromatic system with at least five cone opsins. While opsin sequence variability among species was minimal due to the flocks evolutionary youth, opsin expression patterns varied significantly. Deep-water species showed reduced SWS1 and SWS2B expression, consistent with diminished UV-to-violet light in deeper waters. Unexpectedly, we observed increased proportional expression of the red-sensitive LWS opsin gene, contrary to trends seen in other lacustrine fishes. Additionally, in the seasonally deep-dwelling species Coptodon imbriferna, opsin expression varied plastically between the rainy (shallow) and dry (deep) seasons, with reduced SWS2B expression when the fish reside in the deeper habitats. To add context of other cichlid systems and to explore shared patterns of molecular adaptation, we compared Bermin cichlids to the deep-water species of the Barombi Mbo crater lake. Both cases exemplify independent evolution of deep-water species, yet their visual systems adapted similarly in the single cones (less UV- and violet-sensitive and more blue-sensitive cones), whereas differently in the long-wavelength sensitive double cones (LWS expression lost in Barombi while increased in Bermin). Overall, our study focuses on an evolutionarily young example of cichlid adaptive radiation, providing a unique opportunity to examine the initial phases of molecular adaptation in visual systems.

evolutionary biology↗

Hemoglobin gene repertoire in teleost and cichlid fishes shaped by gene duplications and genome rearrangements

Hemoglobin is a crucial element of the oxygen transport system in vertebrates. It exhibits remarkable gene diversity across teleost fishes, reflecting their evolutionary adaptations for thriving in various aquatic environments. In this study, we present the dynamic evolution of hemoglobin subunit genes based on a comparison of high quality long-read genome assemblies of 24 vertebrate species, including 16 teleosts (of which six are cichlids). Our findings indicate that teleost genomes contain between five (fugu) and 43 (salmon) hemoglobin genes, representing the largest hemoglobin gene repertoire among vertebrates. We find evidence that the ancestor of teleosts had at least four Hb and three or four Hb{beta} subunit genes, and that the current gene diversity emerged during subsequent teleost radiation, driven primarily by (tandem) gene duplications, genome compaction, and rearrangement dynamics. We provide insights into the genomic organization of hemoglobin clusters, revealing the parallel origin of multiple clusters in tetrapods and in teleosts. Importantly, we show that the presence of paralogous rhbdf1 genes flanking both teleost hemoglobin clusters (LA and MN) supports the hypothesis for the origin of the LA cluster by rearrangement within teleosts, rather than by the teleost specific whole-genome duplication. We specifically focus on cichlid fishes, where adaptation to low oxygen environments has been shown to play roles in species diversification. Our analysis of six cichlid genomes, including the Pungu maclareni from crater lake Barombi Mbo, for which we sequenced the representative genome, reveals 18 to 31 copies of the Hb genes, and elevated rates of non- synonymous substitutions compared to other teleosts. Overall, this work facilitates a deeper understanding of how hemoglobin genes contribute to the adaptive and diversification potential of teleosts.

evolutionary biology↗

Trophic niche differentiation in the African elephant fish community (Mormyridae) from the Sanaga River in Cameroon

Multiple species of the elephant fishes (Mormyridae) commonly coexist in sympatry in most African tropical rivers and lakes. In this study, we investigated the trophic ecology and potential trophic niche partitioning of eleven mormyrid fish species from the Sanaga River system (Cameroon) using the stable isotopes of carbon and nitrogen of muscles and of trophic prey samples. Albeit mormyrids mainly feed on invertebrates, we found differences in isotope signals and the trophic niche partitioning in the studied species. We further show that species with elongated snout tend to show higher carbon and nitrogen isotope signals, suggesting a potential role of snout shape in their trophic preferences. Furthermore, we found significant differences in isotopic signatures within the Mormyrus genus, highlighting ecological niche diversification among three closely related species. We also report on different isotopic signals between seasons of the year in four species, possibly caused by species migration and/or anthropogenic agricultural activities. Overall, our research presents robust evidence of the trophic niche partitioning within the entire mormyrid species community, shedding light on the enigmatic evolutionary history of these fascinating African fishes.

zoology↗

Expanded olfactory system in fishes capable of terrestrial exploration

Smell abilities differ greatly among vertebrate species, as reflected by the exceptional size variability of gene families and brain regions involved in odour detection. However, key environmental factors shaping the molecular and phenotypic evolution of the olfactory sensory system remain mostly unknown. Here, we investigate the association between diverse ecological traits and the number of olfactory chemoreceptors in the genomes of more than two hundred ray-finned fishes. We found independent expansions producing large gene repertoires in nocturnal amphibious fishes, generally able to perform active terrestrial exploration. Furthermore, we reinforced this finding with an additional analysis of a clariid species (Channallabes apus), a fish lineage with chemosensory-based aerial orientation. Importantly, we also detected an augmented information-processing capacity in the olfactory bulb of examined nocturnal amphibious species. Overall, we report a convergent magnification of the olfactory system in amphibious fishes potentially enhancing terrestrial orientation, revealing the likelihood of an analogous event in tetrapod ancestors during the water-to-land transition.

evolutionary biology↗

Developmental changes of opsin gene expression in ray-finned fishes (Actinopterygii)

Fish often change their habitat and trophic preferences during development. Dramatic functional differences between embryos, larvae, juveniles and adults also concern sensory systems, including vision. Here we focus on the photoreceptors (rod and cone cells) in the retina and their gene expression profiles during the development. Using comparative transcriptomics on 63 species, belonging to 23 actinopterygian orders, we report general developmental patterns of opsin expression, mostly suggesting an increased importance of the rod opsin (RH1) gene and the long-wavelength sensitive (LWS) cone opsin, and a decreasing importance of the shorter wavelength sensitive cone opsin throughout development. Furthermore, we investigate in detail ontogenetic changes in 14 selected species (from Polypteriformes, Acipenseriformes, Cypriniformes, Aulopiformes and Cichliformes), and we report examples of expanded cone opsin repertoires, cone opsin switches (mostly within RH2) and increasing rod:cone ratio as evidenced by the opsin and phototransduction cascade genes. Our findings provide molecular support for developmental stage-specific visual palettes of ray-finned fishes and shifts between, which most likely arose in response to ecological, behavioural and physiological factors.

evolutionary biology↗

Multiple ancestral and a plethora of recent gene duplications during the evolution of the green sensitive opsin genes (RH2) in teleost fishes

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 todays RH2 diversity 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.

evolutionary biology↗

Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies

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), and we reveal a previously overlooked shorter-shifted paralog, LWS3, restricted to gobies (Percomorpha) and arising from an ancient duplication. Structural modeling 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, teleost LWS2, and goby LWS3 relative to red-sensitive counterparts, consistent with repeated spectral shifts toward green wavelengths. In several lineages--including characins, mormyrids, gobies, and primates--these shorter-shifted LWS opsins have functionally replaced the canonical green-sensitive RH2 opsin. Retinal transcriptomes and in situ hybridization demonstrate variable lws3 expression across gobies, with localization to a distinct double-cone member in Amblygobius phalaena, analogous to rh2 expression in other fish species. Together, these results show that repeated convergent evolution toward green sensitivity over 500 million years involves coordinated changes at the molecular, regulatory, and functional levels, providing a striking example of multilevel sensory adaptation. Significance statementVertebrate vision depends on opsins, which detect specific wavelengths of light. Most teleosts retain a single long-wavelength-sensitive opsin (LWS1), while a green-sensitive paralog (LWS2) occurs only in a few lineages. We identify a previously overlooked green-shifted opsin, LWS3, which is restricted to gobies, and show that LWS2 and LWS3 have repeatedly evolved green sensitivity through convergent amino acid changes. In parallel to the primate MWS/LWS evolution, these shorter-shifted opsins have functionally replaced the canonical green-sensitive RH2 opsin in multiple teleost lineages. By integrating genomic, structural, and expression data, we reveal how multilevel convergent evolution--from molecular tuning to photoreceptor specialization--has repeatedly shaped green-light vision over the past 500 million years of evolution, illustrating the remarkable flexibility of vertebrate visual systems.

evolutionary biology↗

Opsin gene expression in larval and adult deep-sea fishes supports a conserved cone-to-rod pathway in teleost visual development

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 diverse 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.

evolutionary biology↗

Vision using multiple distinct rod opsins in deep-sea fishes

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 ({lambda}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.\n\nSHORT ABSTRACTContrary to the single rod opsin used by most vertebrates, some fishes use multiple rod opsins for vision in the dimly lit deep-sea.

evolutionary biology↗