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Indermaur, A.

Publications and source records attributed to Indermaur, A..

10 recordsLinked to original sources

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↗

Social and environmental cues mask circadian activity patterns in a highly social shell-dwelling cichlid fish

Species exhibit variation in their circadian activity rhythms, including being active during the day (diurnal), the night (nocturnal), or the twilight periods (crepuscular). While the influence of environmental factors such as light on entraining and controlling activity patterns is well known, it is unclear how social and abiotic factors affect circadian behaviors. The daily activity patterns of Lake Tanganyikan cichlid fish are diverse, and may be associated with species diversification. Intriguingly, some shell-dwelling cichlid species, which anecdotal observation suggests are diurnal, displayed strong nocturnal activity when assayed in a "common garden" lab setup. Here, by integrating field and lab-based studies, we provide three lines of evidence that social and environmental cues mask underlying circadian rhythms in shell-dwelling cichlids. First, we demonstrate that shell-dwelling cichlids are diurnal in their natural habitat, but convert to nocturnal activity when assayed alone in a common garden. Second, we identify that in the presence of a shell and conspecifics the highly social N. multifasciatus becomes diurnal. In contrast, the circadian activity pattern of a closely related, but sub-social species, N. brevis, is masked only by a shell, and unaffected by the presence of conspecifics. Third, we demonstrate that the masking effect of shells and conspecifics is circadian and continues in the absence of light. Fourth, we identify that the response to these cues is influenced by sex, with greater effects in female fish, and by pedigree, with stronger effects in individuals bred and raised in captivity compared to those captured in the wild. Together, these experiments reveal new relationships between circadian rhythms and sociality in these fishes, offering broader insights into the ecological and evolutionary drivers of these behaviours.

animal behavior and cognition↗

Genomic evidence for facultative selfing in the cichlid fish Cyphotilapia frontosa

Organisms have evolved a remarkable diversity of reproductive strategies in response to environmental variations and selective pressures. Although most vertebrates do reproduce biparentally, rare alternative modes such as selfing (self-fertilization) and different forms of parthenogenesis exist, but remain poorly characterized. Here, we investigated an unusual reproductive event in the normally biparental cichlid fish Cyphotilapia frontosa, in which a female produced offspring in the absence of a male. Using whole-genome sequencing data, we analyzed whether reproduction occurred via selfing or parthenogenesis by comparing patterns of heterozygosity with those from a wild, genetically diverse C. frontosa family collected in Lake Tanganyika and a closely related inbred Ctenochromis benthicola family. The uniparental family exhibited reduced genetic diversity, elevated relatedness, and genome-wide patterns of homozygosity distinct from those expected under parthenogenesis or inbreeding, but consistent with self-fertilization. Our study provides rare genomic evidence of selfing in a vertebrate and suggests that such alternative reproductive modes may be overlooked rather than truly absent. These findings contribute to a broader understanding of how alternative reproductive strategies evolve in vertebrate lineages. SignificanceThe overwhelming majority of vertebrates reproduce sexually, requiring a male and a female to produce genetically distinct offspring. Yet, rare alternative modes involving only a single parent such as asexual parthenogenesis ("virgin birth") or self-fertilization challenge this paradigm. Among these, selfing is exceptionally uncommon and poorly studied in vertebrates. Here, we unveiled - based on genomic analyses - the reproductive strategy of a member of the extraordinarily diverse cichlid fish radiation in Lake Tanganyika that reproduced in captivity in the absence of a male. By comparing patterns of genome-wide heterozygosity with both wild and inbred reference families, we identified a rare case of selfing. This finding adds to the limited records of selfing in vertebrates and expands current understanding of reproductive diversity, highlighting the power of whole-genome sequencing to distinguish among alternative reproductive mechanisms.

evolutionary biology↗

Evolution of chromatin accessibility associated with traits of cichlid phenotypic diversity

The radiations of cichlid fishes in East African Lakes Victoria, Malawi, and Tanganyika showcase a remarkable example of rapid adaptive speciation, with over 2000 species evolving diverse morphological and ecological adaptations within the last few million years. Understanding the molecular basis of this phenotypic diversity remains a key challenge. Building on prior evidence of gene regulatory network (GRN) rewiring underpinning adaptive traits, we profiled chromatin accessibility (ATAC-seq) and matched transcriptomes across forebrain, retina, liver, and testis tissues in five representative cichlid species using optimised protocols. We show extensive divergence in chromatin accessibility corresponding to phylogenetic lineages and tissue identity, with many regulatory regions exhibiting accelerated nucleotide evolution. Transcription factor binding site (TFBS) variation correlates with both chromatin accessibility and differential gene expression, particularly in genes linked to sensory systems. Building on this, we reconstructed tissue- and species-specific GRNs and show that motif-supported network inference reveals pervasive but tissue-dependent rewiring, with the strongest candidate edges concentrated among accessible, highly expressed genes linked to adaptive traits. By integrating TF footprinting with regulatory motif turnover analyses, we demonstrate that dynamic nucleotide changes are associated with GRN rewiring, concordant with ecological niche and lineage-specific adaptations. Our findings highlight that regulatory variation at conserved and novel TFBSs associates with genes linked to phenotypic innovation across radiating and non-radiating East African cichlids. This study provides foundational epigenomic evidence linking GRN divergence to key mechanisms facilitating rapid adaptive diversification in this iconic vertebrate radiation.

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↗

Adaptive cellular evolution in the intestinal tracts of hyperdiverse African cichlid fishes

Adaptations related to how nutrients are acquired and processed play a central role in the colonization of novel ecological niches and, therefore, in organismal diversification. While the evolution of feeding structures has been studied extensively in this context, the nature of dietary adaptations in the digestive tract remains largely unexplored. Here, we investigate the cellular and molecular basis of dietary adaptations in the massive radiation of cichlid fishes in Lake Tanganyika using comprehensive single-cell transcriptomic data derived from the intestines of 24 endemic cichlid species with distinct habitats and diets. We show that, at the cellular level, dietary adaptations are primarily driven by anterior enterocytes, and that both the relative abundance and gene expression profiles of these cells have evolved in response to rapid dietary specializations. These dietary adaptations are driven by rapidly evolving cell population-specific genes, suggesting that alterations in epithelial cell specification programs and molecular makeup promote ecological diversification.

evolutionary biology↗

Widespread temporal niche partitioning in an adaptive radiation of cichlid fishes

The partitioning of ecological niches is a fundamental component of species diversification in adaptive radiations. However, it is presently unknown if and how such bursts of organismal diversity are influenced by temporal niche partitioning, wherein species avoid competition by being active during different time windows. Here, we address this question through profiling temporal activity patterns in the exceptionally diverse fauna of cichlid fishes from African Lake Tanganyika. By integrating week-long longitudinal behavioural recordings of over 500 individuals from 60 species with eco-morphological and genomic information, we provide two lines of evidence that temporal niche partitioning facilitated this massive adaptive radiation. First, Tanganyikan cichlids exhibit all known circadian temporal activity patterns (diurnal, nocturnal, crepuscular, and cathemeral) and display substantial inter-specific variation in daily amounts of locomotion. Second, many species with similar habitat and diet niches occupy distinct temporal niches. Moreover, our results suggest that shifts between diurnal and nocturnal activity patterns are facilitated by a crepuscular intermediate state. In addition, genome-wide association studies indicate that the genetics underlying activity patterns is complex, with different clades associated with different combinations of variants. The identified variants were not associated with core circadian clock genes but with genes implicated in synapse function. These observations indicate that temporal niche partitioning contributed to adaptive radiation in cichlids and that many genes are associated with the diversity and evolution of temporal activity patterns.

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↗

Structural manipulations of a shelter resource reveal underlying preference functions in a shell-dwelling cichlid fish

Many animals can modify the environments in which they live, thereby changing the selection pressures they experience. A common example of such niche-construction is the use, creation, or modification of environmental resources for use as nests or shelters. Because these resources often have correlated structural elements, it can be difficult to disentangle the relative contribution of these elements to resource choice, and the preference functions underlying niche-construction behaviour remain hidden. Here, we present an experimental paradigm that uses 3D-scanning, -modelling, and -printing to create replicas of structures that differ with respect to key structural attributes. We show that a niche-constructing, shelldwelling cichlid fish, Neolamprologus multifasciatus, has strong open-ended preference functions for exaggerated shell replicas. Fish preferred shells that were fully intact and either enlarged, lengthened, or had widened apertures. Shell intactness was the most important structural attribute, followed by shell length, then aperture width. We disentangle the relative roles of different shell attributes, which are tightly correlated in the wild, but nevertheless differentially influence shelter choice and therefore niche construction in this species. We highlight the broad utility of our approach when compared to more traditional methods (e.g. two-choice tasks) for studying animal decision-making in a range of contexts.

evolutionary biology↗