Fabrizia Ronco

The ability of animals to efficiently track down and digest food is crucial for their survival, and the specialization to different diets is a major driver of diversification in this group^1,2,3. Although the evolution of feeding structures has been studied extensively in this context^4,5,6, the nature and extent of adaptations in the digestive tract remain poorly understood. Here, we examine dietary adaptations in the intestines of one of the largest adaptive radiations in vertebrates, the cichlid fishes of Lake Tanganyika. By generating comprehensive single-cell transcriptomic data for 24 Tanganyikan cichlid species with divergent feeding habits, and integrating this with eco-morphological and genomic information, we uncover that, at the cellular level, dietary adaptations primarily involve anterior enterocytes. In particular, we show that the relative abundances of anterior enterocytes as well as the gene expression profiles in this cell population evolved in response to rapid trophic specializations, and that these diet-related adaptations are driven by fast-evolving, cell-population-specific genes. Overall, our findings show that alterations in intestinal epithelium cell composition and in the cell-type-specific molecular makeup provided the substrate for trophic specializations, demonstrating that ecological adaptations target multiple layers of biological organization.

Understanding population connectivity in the marine realm is crucial for conserving biodiversity, managing fisheries, and predicting species responses to environmental change. This is particularly important in Antarctic waters, where unique evolutionary histories and extreme conditions shape marine biodiversity. The longfin icedevil Aethotaxis mitopteryx is an elusive notothenioid fish endemic to Antarctic waters. To explore population connectivity in A. mitopteryx , we used RAD‐seq to investigate the genetic differentiation of two populations, one from the Eastern Weddell Sea and the other from the Eastern Antarctic Peninsula, two regions of ecological relevance greatly impacted by climate change. Despite spatial separation, analyses revealed no significant genetic differentiation between the two populations, suggesting extensive gene flow. A pronounced genetic distinction was, however, observed between males and females. This differentiation was largely localized to a specific chromosome, implying a genetic sex determination system with males being the heterogametic sex. These findings contribute novel insights into the genetic structure of A. mitopteryx populations and expand our understanding of genetic mechanisms in Antarctic fish. This study provides a foundation for further investigations into the evolutionary and ecological implications of sex chromosome differentiation in extreme environments.

African cichlids comprise more than 1800 species of freshwater fishes, with remarkable adaptive radiations in Lakes Tanganyika, Malawi, and Victoria that have given rise to extraordinary morphological diversity. However, the evolution of the cichlid axial skeleton has been largely overlooked, despite its high variation and functional significance for locomotion. Here, we present the first macroevolutionary study of axial morphology in African cichlids, based on phylogenetic comparative analyses of 4861 individuals from 583 species. Adaptation to demersal, pelagic, and piscivorous niches has led to the evolution of elongate bodies with high vertebral counts in lacustrine cichlids, emphasising the role of the fusiform body shape in ecological adaptation. However, riverine species occupy a broader axial morphospace than lacustrine species, which is partly explained by a higher stochastic rate of vertebral count evolution in riverine lineages. In addition, the occupied axial morphospace broadly correlates with the estimated age of the lacustrine radiations, suggesting that exploration of axial morphospace is a function of divergence time. However, rates of vertebral count evolution are not the same across the lake radiations. Therefore, accumulated variation in vertebral counts (and more broadly axial morphospace) is not solely a function of divergence time. Finally, we show that the common ancestor of African cichlids possessed a distinctly riverine axial morphology, indicating that the exploration of axial morphospace radiated outward from this ancestral riverine form. These findings highlight the importance of a comparative approach to studying cichlid evolution and underscore the value of African cichlids as a model for investigating the evolutionary and developmental dynamics of the teleostean vertebral column.

Diet specialisation is a main driver of diversification in many adaptive radiations. Therefore, identifying diet items is essential to characterise trophic specialisations and to understand the dynamics of dietary adaptations. In this study, we explored the trophic niches of 56 species from the adaptive radiation of cichlid fishes in Lake Tanganyika, encompassing all major phylogenetic lineages and feeding specialisations. We employed a metagenomic sequencing approach to identify the food sources of the investigated species at high taxonomic resolution, sequencing over 400 digestive content samples from wild‐caught individuals at around 50 million paired‐end read depth per sample. Our analyses revealed Arthropoda, Chordata (fishes), Bacillariophyta and Streptophyta as the primary diet phyla of the Tanganyikan cichlids. Moreover, we confirmed the presence of other food sources and identified taxa not previously documented to be part of the cichlids' diet. Based on their dietary compositions, the Tanganyikan cichlids can be grouped into herbivores, invertivores, piscivores and mixed feeders. Further, we showed that trophic disparity in the radiation is shaped by rapid divergence and documented cases of dietary niche convergence. Diet composition correlated with carbon and nitrogen stable isotope values, gut length, and body morphology. Differences in diet—such as the consumption of diatoms, streptophytes and chlorophytes versus fish and arthropods—were associated with changes in body, upper oral jaw and lower pharyngeal jaw shape. Collectively, this study presents a comprehensive and detailed diet classification of the Tanganyikan cichlids, highlighting the power of metagenomic approaches in delineating dietary adaptations.

The lamprologine cichlid genus Telmatochromis was long considered primarily lacustrine and endemic to Lake Tanganyika until an undescribed Telmatochromis species was reported from the Lufubu River (Lake Tanganyika drainage, Zambia). A phylogenomic study in 2021 confirmed the association of Telmatochromis sp. “lufubu” with Telmatochromis along with another riverine species, Neolamprologus devosi (Malagarasi drainage, Tanzania). Here, we quantify the morphological diversity of the genus Telmatochromis and the two associated riverine species using a multivariate dataset combining geometric and classical morphometrics, as well as meristics. We identify three distinct morphological clusters: the “Telmatochromis vittatus complex” with highly elongated bodies and short heads, the “Telmatochromis temporalis complex” with deeper bodies, and the two riverine species with intermediate body elongation and large heads. Further, we formally describe the species endemic to the lower Lufubu River as Telmatochromis salzburgeri sp. nov. and reassign N. devosi to Telmatochromis. Telmatochromis devosi comb. nov. differs from all congeners by the absence of bi‐ and tricuspid teeth in the inner tooth rows of the oral dentition. T. salzburgeri sp. nov. can be distinguished from all other Telmatochromis species by a prominent orange stripe along the base of the dorsal fin and from T. devosi comb. nov. by the relatively smaller size of the lower pharyngeal jaw. Both riverine species differ from all lacustrine Telmatochromis by a lower number of dorsal‐fin spines. Additionally, the riverine species can be distinguished from the T. vittatus complex by having larger heads and longer oral jaws, and from the T. temporalis complex by their lower relative body depth. With the inclusion of new riverine members, the genus Telmatochromis is revealed to be more morphologically and ecologically diverse than previously recognized.

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.

Aim: Quantify the contribution of environmental factors (water temperature, salinity and depth) and evolutionary history to varied skeletal mineralogy in calcifying marine organisms.Location: Global Ocean.Time period: Present.Major taxa studied: Order: Cheilostomatida; Phylum: Bryozoa.Methods: We employed X‐ray diffraction (XRD) to analyse the skeletal mineral composition of 872 individual colonies, representing 437 bryozoan species, in terms of calcite/aragonite ratios. We integrated these data with equivalent published data, thus reaching 981 species, and applied linear models (LMs), generalized linear models (GLMs) and phylogenetic generalized least squares models (PGLSs) to investigate the influences of temperature, salinity, depth and phylogenetic history on the mineralogy of nearly 1000 cheilostome bryozoan species.Results: Cheilostome bryozoans vary considerably in their skeletal mineral composition: in our dataset 65% of the species possess purely calcite skeletons, 15% exclusively employ aragonite and 20% exhibit mixed (i.e. calcite and aragonite) mineralogies. Temperature is the predominant measured environmental factor influencing bryozoan skeletal mineralogy, accounting for 20% of its variability across species, when phylogenetic relatedness is unaccounted for. Bryozoans in lower latitudes, characterized by higher seawater temperatures, have higher aragonite concentrations. By accounting for phylogenetic structure using a subset of 87 species for which we have topological information, 40% of the observed mineralogical variability could be attributed to present‐day temperature. In contrast, depth and salinity played minor roles, explaining less than 1% of the mineralogical variation each.Main conclusions: This study emphasizes the influence of evolutionary history on the mineralogical variability of calcifying organisms, even when it can be shown that a single environmental factor (temperature) explains a substantial amount of this variability. When confronted with changing temperature, calcifiers such as bryozoans are likely to respond in diverse ways, depending on the species, given their phylogenetic relatedness and the external conditions they meet.

Behavior is critical for animal survival and reproduction, and possibly for diversification and evolutionary radiation. However, the genetics behind adaptive variation in behavior are poorly understood. In this work, we examined a fundamental and widespread behavioral trait, exploratory behavior, in one of the largest adaptive radiations on Earth, the cichlid fishes of Lake Tanganyika. By integrating quantitative behavioral data from 57 cichlid species (702 wild-caught individuals) with high-resolution ecomorphological and genomic information, we show that exploratory behavior is linked to macrohabitat niche adaptations in Tanganyikan cichlids. Furthermore, we uncovered a correlation between the genotypes at a single-nucleotide polymorphism upstream of the AMPA glutamate-receptor regulatory gene cacng5b and variation in exploratory tendency. We validated this association using behavioral predictions with a neural network approach and CRISPR-Cas9 genome editing.

Fish biologists have long assumed a link between intestinal length and diet, and relative gut length or Zihler’s index are often used to classify species into trophic groups. This has been done for specific fish taxa or specific ecosystems, but not for a global fish dataset. Here, we assess these relationships across a dataset of 468 fish species (254 marine, 191 freshwater, and 23 that occupy both habitats) in relation to body mass and fish length. Herbivores had significantly relatively stouter bodies and longer intestines than omni- and faunivores. Among faunivores, corallivores had longer intestines than invertivores, with piscivores having the shortest. There were no detectable differences between herbivore groups, possibly due to insufficient understanding of herbivorous fish diets. We propose that reasons for long intestines in fish include (i) difficult-to-digest items that require a symbiotic microbiome, and (ii) the dilution of easily digestible compounds with indigestible material (e.g., sand, wood, exoskeleton). Intestinal indices differed significantly between dietary groups, but there was substantial group overlap. Counter-intuitively, in the largest dataset, marine species had significantly shorter intestines than freshwater fish. These results put fish together with mammals as vertebrate taxa with clear convergence in intestine length in association with trophic level, in contrast to reptiles and birds, even if the peculiar feeding ecology of herbivorous fish is probably more varied than that of mammalian herbivores.

The cichlid species flock from Lake Tanganyika is a well-studied system for evolutionary biology research because its species assemblage shows a high degree of endemism and is a product of adaptive radiation. While our understanding of the evolutionary history of Lake Tanganyika cichlids has advanced tremendously over the past decades, their taxonomy received considerably less attention, despite numerous taxonomic misplacements (e.g., polyphyletic genera and species) that have been revealed by phylogenetic studies. One prominent example of a polyphyletic genus is Gnathochromis, which includes two distantly related species, belonging to two different tribes. To resolve this issue, here we present a taxonomic revision based on an extensive morphological dataset obtained from a comprehensive taxon sampling including 587 specimens from 63 taxa. We introduce a new monotypic genus, Jabarichromis gen. nov. for ‘Gnathochromis’ pfefferi, a member of the tribe Tropheini, thereby separating it from the type species of Gnathochromis, G. permaxillaris. As a result, the genus Gnathochromis, which belongs to the tribe Limnochromini, is rendered monophyletic. Further, we provide an additional character to distinguish the recently described genus Shuja, which also belongs to the Tropheini, from its former mostly riverine congeners.