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  • 2020-2024  (9)
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  • 1
    Publication Date: 2023-02-08
    Description: Cichlid fishes’ famous diversity in body coloration is accompanied by a highly diverse and complex visual system. Although cichlids possess an unusually high number of seven cone opsin genes, they express only a subset of these during their ontogeny, accounting for their astonishing interspecific variation in visual sensitivities. Much of this diversity is thought to have been shaped by natural selection as cichlids inhabit a variety of habitats with distinct light environments. Also, sexual selection might have contributed to the observed visual diversity, and sexual dimorphism in coloration potentially co‐evolved with sexual dimorphism in opsin expression. We investigated sex‐specific opsin expression of several cichlids from Africa and the Neotropics and collected and integrated datasets on sex‐specific body coloration, species‐specific visual sensitivities, lens transmission and habitat light properties for some of them. We comparatively analyzed this wide range of molecular and ecological data, illustrating how integrative approaches can address specific questions on the factors and mechanisms driving diversification, and the evolution of cichlid vision in particular. We found that both sexes expressed opsins at the same levels ‐ even in sexually dimorphic cichlid species – which argues against coevolution of sexual dichromatism and differences in sex‐specific visual sensitivity. Rather, a combination of environmental light properties and body coloration shaped the diversity in spectral sensitivities among cichlids. We conclude that although cichlids are particularly colorful and diverse and often sexually dimorphic, it would appear that natural rather than sexual selection is a more powerful force driving visual diversity in this hyper‐diverse lineage.
    Type: Article , PeerReviewed
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  • 2
    Publication Date: 2023-02-08
    Description: Sympatric speciation occurs without geographical barriers and is thought to often be driven by ecological specialization of individuals that eventually diverge genetically and phenotypically. Distinct morphologies between sympatric populations occupying different niches have been interpreted as such differentiating adaptive phenotypes, yet differences in performance and thus likely adaptiveness between them were rarely tested. Here, we investigated if divergent body shapes of two sympatric crater lake cichlid species from Nicaragua, one being a shore‐associated (benthic) species while the other prefers the open water zones (limnetic), affect cruising (Ucrit) and sprinting (Usprint) swimming abilities ‐ performances particularly relevant to their respective lifestyles. Furthermore, we investigated species differences in oxygen consumption (MO2) across different swimming speeds and compare gene expression in gills and white muscle at rest and during exercise. We found a superior cruising ability in the limnetic Amphilophus zaliosus compared to the benthic A. astorquii, while sprinting was not different, suggesting that their distinct morphologies affect swimming performance. Increased cruising swimming ability in A. zaliosus was linked to a higher oxygen demand during activity (but not rest), indicating different metabolic rates during exercise ‐ a hypothesis supported by coinciding gene expression patterns of gill transcriptomes. We identified differentially expressed genes linked to swimming physiology, regulation of swimming behaviour and oxygen intake. A combination of physiological and morphological differences may thus underlie adaptations to these species’ distinct niches. This complex ecological specialization likely resulted in morphological and physiological trade‐offs that contributed to the rapid establishment and maintenance of divergence with gene flow.
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  • 3
    Publication Date: 2023-02-08
    Description: The two toothed jaws of cichlid fishes provide textbook examples of convergent evolution. Tooth phenotypes such as enlarged molar-like teeth used to process hard-shelled molluscs have evolved numerous times independently during cichlid diversification. While the ecological benefit of molar-like teeth to crush prey is known, it is unclear whether the same molecular mechanisms underlie these convergent traits. To identify genes involved in the evolution and development of enlarged cichlid teeth, we performed RNA-seq on the serially homologous toothed oral and pharyngeal jaws as well as the fourth toothless gill arch of Astatoreochromis alluaudi. We identified 27 genes that are highly upregulated on both tooth-bearing jaws compared to the toothless gill arch. Most of these genes have never been reported to play a role in tooth formation. Two of these genes (unk, rpfA) are not found in other vertebrate genomes but are present in all cichlid genomes. They also cluster genomically with two other highly expressed tooth genes (odam, scpp5) that exhibit conserved expression during vertebrate odontogenesis. Unk and rpfA were confirmed via in situ hybridization to be expressed in developing teeth of Astatotilapia burtoni. We then examined expression of the cluster's four genes in six evolutionarily independent and phylogenetically disparate cichlid species pairs each with a large- and a small-toothed species. Odam and unk commonly and scpp5 and rpfA always showed higher expression in larger-toothed cichlid jaws. Convergent trophic adaptations across cichlid diversity are associated with the repeated developmental deployment of this genomic cluster containing conserved and novel cichlid-specific genes.
    Type: Article , PeerReviewed
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  • 4
    Publication Date: 2024-02-07
    Description: PUBLIC SUMMARY: Endothermy has evolved multiple times not only in mammals and birds but also in fishes (teleosts and chondrichthyans) A chromosome-level genome sequence of the whole-body endothermic opah was generated, explaining genetic changes in heat production, sensory, and adaptive immune system Convergent evolution in endothermic vertebrate lineages was investigated, and genes essential for heart function and metabolic heat production were screened Analyses of the unique pectoral muscle of opah revealed that numerous proteins were co-opted from dorsal swimming muscles for thermogenesis and oxidative phosphorylation ABSTRACT: Few fishes have evolved elevated body temperatures compared to ambient temperatures and only in opah (Lampris spp) is the entire body affected. To understand the molecular basis of endothermy, we analyzed the opah genome and identified 23 genes with convergent amino acid substitutions across fish, birds, and mammals, including slc8b1, which encodes the mitochondrial Na+/Ca2+ exchanger and is essential for heart function and metabolic heat production. Among endothermic fishes, 44 convergent genes with suggestive metabolic functions were identified, such as glrx3, encoding a crucial protein for hemoglobin maturation. Numerous genes involved in the production and retention of metabolic heat were also found to be under positive selection. Analyses of opah’s unique inner heat-producing pectoral muscle layer, an evolutionary key-innovation, revealed that many proteins were co-opted from dorsal swimming muscles for thermogenesis and oxidative phosphorylation. Thus, the opah genome provides valuable resources and opportunities to uncover the genetic basis of thermal adaptations in fish.
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  • 5
    Publication Date: 2024-02-07
    Description: Seahorses have a circum-global distribution in tropical to temperate coastal waters. Yet, seahorses show many adaptations for a sedentary, cryptic lifestyle: they require specific habitats, such as seagrass, kelp or coral reefs, lack pelvic and caudal fins, and give birth to directly developed offspring without pronounced pelagic larval stage, rendering long-range dispersal by conventional means inefficient. Here we investigate seahorses’ worldwide dispersal and biogeographic patterns based on a de novo genome assembly of Hippocampus erectus as well as 358 re-sequenced genomes from 21 species. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleo-temporal seaway openings. Furthermore, the genetic basis of the recurring “bony spines” adaptive phenotype is linked to independent substitutions in a key developmental gene. Analyses thus suggest that rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats.
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  • 6
    Publication Date: 2024-02-07
    Description: Background: Syngnathids are a highly derived and diverse fish clade comprising the pipefishes, pipe-horses, and seahorses. They are characterized by a plethora of iconic traits that increasingly capture the attention of biologists, including geneticists, ecologists, and developmental biologists. The current understanding of the origins of their derived body plan is, however, hampered by incomplete and limited descriptions of the early syngnathid ontogeny. Results: We provide a comprehensive description of the development of Nerophis ophidion, Syngnathus typhle, and Hippocampus erectus from early cleavage stages to release from the male brooding organ and beyond, including juvenile development. We comparatively describe skeletogenesis with a particular focus on dermal bony plates, the snout-like jaw morphology, and appendages. Conclusions: This most comprehensive and detailed account of syngnathid development to date suggests that convergent phenotypes (e.g., reduction and loss of the caudal fins), likely arose by distinct ontogenetic means in pipefishes and seahorses. Comparison of the ontogenetic trajectories of S. typhle and H. erectus provides indications that characteristic features of the seahorse body plan result from developmental truncation. Altogether, this work provides a valuable resource and framework for future research to understand the evolution of the outlandish syngnathid morphology from a developmental perspective.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
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  • 7
    Publication Date: 2024-02-07
    Description: Evolutionary novelties—derived traits without clear homology found in the ancestors of a lineage—may promote ecological specialization and facilitate adaptive radiations. Examples for such novelties include the wings of bats, pharyngeal jaws of cichlids and flowers of angiosperms. Belonoid fishes (flying fishes, halfbeaks and needlefishes) feature an astonishing diversity of extremely elongated jaw phenotypes with undetermined evolutionary origins. We investigate the development of elongated jaws in a halfbeak (Dermogenys pusilla) and a needlefish (Xenentodon cancila) using morphometrics, transcriptomics and in situ hybridization. We confirm that these fishes' elongated jaws are composed of distinct base and novel ‘extension’ portions. These extensions are morphologically unique to belonoids, and we describe the growth dynamics of both bases and extensions throughout early development in both studied species. From transcriptomic profiling, we deduce that jaw extension outgrowth is guided by populations of multipotent cells originating from the anterior tip of the dentary. These cells are shielded from differentiation, but proliferate and migrate anteriorly during the extension's allometric growth phase. Cells left behind at the tip leave the shielded zone and undergo differentiation into osteoblast-like cells, which deposit extracellular matrix with both bone and cartilage characteristics that mineralizes and thereby provides rigidity. Such bone has characteristics akin to histological observations on the elongated ‘kype’ process on lower jaws of male salmon, which may hint at common conserved regulatory underpinnings. Future studies will evaluate the molecular pathways that govern the anterior migration and proliferation of these multipotent cells underlying the belonoids' evolutionary novel jaw extensions.
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  • 8
    Publication Date: 2024-02-07
    Description: With over 18,000 species, the Acanthomorpha, or spiny-rayed fishes, form the largest and arguably most diverse radiation of vertebrates. One of the key novelties that contributed to their evolutionary success are the spiny rays in their fins that serve as a defense mechanism. We investigated the patterning mechanisms underlying the differentiation of median fin Anlagen into discrete spiny and soft rayed domains during the ontogeny of the direct-developing cichlid fish Astatotilapia burtoni. Distinct transcription factor signatures characterize these two fin domains, whereby mutually exclusive expression of hoxa13a/b with alx4a/b and tbx2b marks the spine to soft-ray boundary. The soft-ray domain is established by BMP inhibition via gremlin1b, which synergizes in the posterior fin with shh secreted from a zone of polarizing activity. Modulation of BMP signaling by chemical inhibition or gremlin1b CRISPR/Cas9 knockout induces homeotic transformations of spines into soft rays and vice versa. The expression of spine and soft-ray genes in nonacanthomorph fins indicates that a combination of exaptation and posterior expansion of an ancestral developmental program for the anterior fin margin allowed the evolution of robustly individuated spiny and soft-rayed domains. We propose that a repeated exaptation of such pattern might underly the convergent evolution of anterior spiny fin elements across fishes.
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  • 9
    Publication Date: 2024-02-07
    Description: The unique male pregnancy in pipefishes and seahorses ranges from basic attachment (pouch-less species: Nerophinae) of maternal eggs to specialized internal gestation in pouched species (e.g. Syngnathus and Hippocampus) with many transitions in between. Due to this diversity, male pregnancy offers a unique platform for assessing physiological and molecular adaptations in pregnancy evolution. These insights will contribute to answering long-standing questions of why and how pregnancy evolved convergently in so many vertebrate systems. To understand the molecular congruencies and disparities in male pregnancy evolution, we compared transcriptome-wide differentially expressed genes in four syngnathid species, at four pregnancy stages (nonpregnant, early, late and parturition). Across all species and pregnancy forms, metabolic processes and immune dynamics defined pregnancy stages, especially pouched species shared expression features akin to female pregnancy. The observed downregulation of adaptive immune genes in early-stage pregnancy and its reversed upregulation during late/parturition in pouched species, most notably in Hippocampus, combined with directionless expression in the pouch-less species, suggests immune modulation to be restricted to pouched species that evolved placenta-like systems. We propose that increased foeto-paternal intimacy in pouched syngnathids commands immune suppression processes in early gestation, and that the elevated immune response during parturition coincides with pouch opening and reduced progeny reliance. Immune response regulation in pouched species supports the recently described functional MHC II pathway loss as critical in male pregnancy evolution. The independent co-option of similar genes and pathways both in male and female pregnancy highlights immune modulation as crucial for the evolutionary establishment of pregnancy.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
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