Biology subjects

Naumann, B.

Publications and source records attributed to Naumann, B..

9 recordsLinked to original sources

bioRxiv2025

The 3D architecture of the ctenophore aboral organ and the evolution of complex integrative centers in animals

The ability to sense and respond to environmental cues is fundamental to animal behavior and survival. In ctenophores - early-branching marine animals - a syncytial nerve net underlies complex behaviors such as geotaxis, feeding, and escape. At the center of this system is the aboral organ (AO), a dense sensory hub that detects motion, light, and pressure and coordinates ciliary movement. However, the AOs cellular architecture and its integration with the nerve net remain poorly understood. Here, using volume electron microscopy in Mnemiopsis leidyi, we reveal that the syncytial nerve net converges and condenses around the AO, forming synaptic connections with diverse effector cells. We annotated 17 distinct cell types, including candidate light and pressure sensors, novel ciliated and secretory cells, and non-synaptic vesicle-rich cells likely involved in volume transmission. Our data shows that signal processing within the AO relies on both synaptic and non-synaptic communication. Gene expression profiling of conserved transcription factors indicates that the AO is a functionally convergent, evolutionarily distinct sensory structure that retains minimal homology. Our findings redefine the ctenophore AO as a highly integrated, multilayered sensory system critical for behavioral regulation.

evolutionary biology↗

bioRxiv2025

Skin development and metamorphic re-arrangement in Arthroleptella villiersi Hewitt, 1935 reveals distinct heterochronic patterns in anurans with different life histories

BackgroundThe evolvability of ontogenetic trajectories, driven by modular developmental processes and their evolutionary repatterning, plays a crucial role in the diversity of animal diversity. Anurans offer a model for exploring how developmental repatterning, including the loss of larval features and heterochronic shifts of metamorphic processes lead to the diversity of, often terrestrialized, life histories. Ancestrally, anurans exhibit an aquatic larva (tadpoles) that differs tremendously from their semi-terrestrial adult forms. The transition from this tadpole to the adult is a thyroid hormone-dependent metamorphosis that results in the rearrangement of almost all organ systems. One of the organ systems that experiences the most extensive rearrangements is the skin. Is the ancestral pattern of metamorphic skin rearrangement altered in anurans with a completely terrestrial tadpole phase? ResultsSkin development and metamorphic rearrangement in the terrestrial tadpole of Arthroleptella villiersi is investigated based on histological sections. It follows the major pattern observed in anurans with an aquatic tadpole phase and correlates with thyroid gland maturation. Neuromasts develop and are present during a short developmental time. Both, metamorphic skin rearrangement and neuromast degeneration correlate with histological thyroid gland maturation. A few minor heterochronic shifts are detectable compared to aquatic indirect and terrestrial direct developing anurans. ConclusionSkin development and metamorphic rearrangement in anurans with different reproductive modes is very similar and correlates with thyroid gland maturation indicating that skin development in anurans might be constrained by thyroid hormone activity. Neuromasts are the major exception being present in aquatic and terrestrial indirect developing species but not in terrestrial direct developing anurans. Heterochronic shifts detected during skin development indicate that at least the differentiation of multicellular gland complexes might represent a developmental module similar to neuromasts.

zoology↗

bioRxiv2025

Developmental stages of Arthroleptella villiersi (Pyxicephalidae)

Terrestrialization in anurans is associated with the evolution of endotrophy. It is hypothesized that heterochrony, or changes in the time or rate of developmental events, is associated with the development in endotrophic species. To analyse the developmental heterochrony, we investigated and revised the description of the development in Arthroleptella villierisi, a small frog species of the family Pyxicephalidae, found in the Cape fold mountain region of the Western Cape, South Africa. We also compared the developmental stages of A. villiersi to the heterochronic patterns of taxa with endotrophic terrestrial indirect and direct development using heterochrony plots to identify heterochronic shifts during development. As a result, we found that the terrestrial endotrophic larva of A. villiersi shares external similarities with exotrophic, aquatic larvae in having a long muscularized tail with a fin, a lateral line system and an opercular fold that completely covers the forelimbs. However, other developmental events like the reduction of larval mouthparts and the pre-displaced fore- and hindlimb development is comparatively similar to direct developing taxa. The results of our study show that the timing of early developmental events can be shifted profoundly, while the timing of later events seem to be more conserved in anuran development. We interpret that some of these heterochronic shifts might be consequences of functional and developmental constraints underlying the establishment of the adult body plan.

developmental biology↗

bioRxiv2023

Development of the branchial musculature of the Siberian sturgeon (Acipenser baerii) reveals a heterochronic shift during the evolution of acipenseriform cranial muscles

Heterochronic shifts are regarded one of the major evolutionary changes acting on developmental modules and underlying the origin of morphological disparity. Conserved characters, rarely subject to heterochronic shifts during the curse of evolution, in contrast could indicate underlying developmental or functional constraints. Here we use the development of the cranial musculature Siberian sturgeon (Acipenser baerii) as a model to investigate the role of heterochrony during the evolution of the craniofacial system of Actinopterygii. Using histology, fluorescent antibody staining and fast propagation-based phase contrast imaging in combination with 3D-reconstruction we describe the development of the branchial and hypobranchial musculature. We show that the development of the first branchial arch is accelerated compared to other basal-branching actinopterygians leading to a more synchronous development with the hyoid arch. A pattern that could relate to the derived migratory behaviour of the neural crest cells in sturgeons. In contrast, the developmental timing of the more posterior branchial musculature, including the cucullaris muscle in the Siberian sturgeon, appears to be highly conserved compared to other Actinopterygii and even Osteognathostomata. This could indicate the presence of functional or developmental constraints underlying the evolution of the muscles at the head/trunk interface.

zoology↗

bioRxiv2022

In flagranti - Functional morphology of copulatory organs of odontopygid millipedes (Diplopoda: Juliformia: Spirostreptida)

The copulatory organs of many animal groups exhibit a high degree of morphological complexity and diversity that is thought to have evolved on the basis of different selective mechanisms including lock- and-key mechanism, pleiotropy, sperm competition, internal courtship and female choice. Identifying the effects of these different selective mechanisms on copulatory organs one of the central topics of the study of sexual selection. To tackle this challenge, knowledge of the functions of all parts of the copulatory organs is indispensable. Here we study the functional morphology of the gonopods (male copulatory organs) and vulvae (female copulatory organs) in the odontopygid millipede Spinotarsus (Diplopoda, Spirostreptida, Odontopygidae). While the vulvae of female odontopygids are rather simple, male gonopods are complex, walking leg-derived copulatory organs that exhibit many movable sub-parts. Using CT-based 3D reconstruction, confocal laser scanning microscopy and mating observations we revise the functional morphology of odontopygid gonopods, propose biological roles and evaluate the possible involvement of different selective mechanisms underlying their evolution.

zoology↗

bioRxiv2022

Syncytial nerve net in a ctenophore sheds new light on the early evolution of nervous systems

A fundamental breakthrough in neurobiology has been the formulation of the neuron doctrine by Santiago Ramon y Cajal, which states that the nervous system is composed of discrete individual cells. Electron microscopy later confirmed the doctrine and allowed the identification of synaptic connections. Here we use volume electron microscopy and 3D reconstructions to characterize the nerve net of a cydippid-phase ctenophore, belonging to one of the earliest-branching animal lineages. We found that neurons of its subepithelial nerve net do not follow Cajals neuron doctrine but instead show a continuous plasma membrane forming a syncytium. This is more similar to the reticulate theory of the nervous system put forward by Camillo Golgi. Additionally, we were able to identify new sensory cell types and describe simple neuro-sensory circuits for cydippid-phase ctenophores. Together with the ctenophore-specific synaptic architecture and the presence of an extensive repertoire of lineage-specific neuropeptides our morphological data provide substantial evidence for the independent evolution of the nervous system of ctenophores and the remaining animals.

evolutionary biology↗

bioRxiv2021

The unique neuronal structure and neuropeptide repertoire in the ctenophore Mnemiopsis leidyi shed light on the evolution of animal nervous systems

The ctenophore nerve net represents one of the earliest evolved nervous system of animals. Due to the uncertainties of their phylogenetic placement of ctenophores and the absence of several key bilaterian neuronal genes, it has been hypothesized that their neurons have evolved independently. Whether this is indeed the case remains unclear, and thus the evolutionary history of neurons is still contentious. Here, we have characterized the neuropeptide repertoire of the ctenophore Mnemiopsis leidyi. Using the machine learning NeuroPID tool1 129 new putative neuropeptide precursors were predicted. Sixteen of them are detected in the subepithelial nerve net (SNN), aboral organ (AO) and epithelial sensory cells (ESC) of early cydippid-stage M. leidyi by in situ hybridization (ISH) and immunohistochemistry (IHC). Four of these neuropeptides increase the animals swimming velocity in a behavioral essay. The new neuropeptides were used as markers to identify neuronal cell types in single cell transcriptomic data2. To unravel the neuronal architecture, we 3D reconstructed the SNN underlying the comb plates using serial block-face scanning electron microscopy (SBF-SEM). For the first time, we confirm a more than 100 years old hypothesis about anastomoses between neurites of the same cell in ctenophores and reveal that they occur through a continuous membrane. Our findings reveal the unique neuronal structure and neuropeptide repertoire of ctenophores and are important for reconstructing the evolutionary origin of animal neurons and nervous systems.

evolutionary biology↗

bioRxiv2020

Parallel evolution of direct development in frogs - Skin and thyroid gland development in African Squeaker Frogs (Anura: Arthroleptidae: Arthroleptis)

Cases of parallel evolution offer the possibility to identify adaptive traits and to uncover developmental constraints on the evolutionary trajectories of these traits. The independent evolution of direct development, from the ancestral biphasic life history in frogs is such a case of parallel evolution. In frogs, aquatic larvae (tadpoles) differ profoundly from their adult forms and exhibit a stunning diversity regarding their habitats, morphology and feeding behaviors. The transition from the tadpole to the adult is a climactic, thyroid hormone (TH)-dependent process of profound and fast morphological rearrangement called metamorphosis. One of the organ systems that experiences the most comprehensive metamorphic rearrangements is the skin. Direct-developing frogs lack a free-swimming tadpole and hatch from terrestrial eggs as fully formed froglets. In the few species examined, development is characterized by the condensed and transient formation of some tadpole-specific features and the early formation of adult-specific features during a "cryptic" metamorphosis. In this study we show that skin in direct-developing African squeaker frogs (Arthroleptis) is also repatterned from a tadpole-like to an adult-like histology during a cryptic metamorphosis. This repatterning correlates with an increase of thyroid gland activity. A comparison with data from the Puerto Rican coqui (Eleutherodactylus coqui) reveals that direct development might have evolved in parallel in these frogs by a comparable heterochronic shift of thyroid gland activity. This suggests that the development of many adult-features is still constrained by the ancestral dependency on thyroid hormone signaling.

developmental biology↗

bioRxiv2019

Spatial cell disparity in the colonial choanoflagellate Salpingoeca rosetta

Choanoflagellates are the closest unicellular relatives of animals (Metazoa). These tiny protists display complex life histories that include sessile as well as different pelagic stages. Some choanoflagellates have the ability to form colonies as well. Up until recently, these colonies have been described to consist of mostly identical cells showing no spatial cell differentiation, which supported the traditional view that spatial cell differentiation, leading to specific cell types in animals, evolved after the split of the last common ancestor of the Choanoflagellata and Metazoa. The recent discovery of single cells in colonies of the choanoflagellate Salpingoeca rosetta that exhibit unique cell morphologies challenges this traditional view. We have now reanalyzed TEM serial sections, aiming to determine the degree of similarity of S. rosetta cells within a rosette colony. We investigated cell morphologies and nuclear, mitochondrial and food vacuole volumes of 40 individual cells from four different S. rosetta rosette colonies and compared our findings to previously published data on sponge choanocytes. Our analysis show that cells in a choanoflagellate colony differ from each other in respect to cell morphology and content ratios of nuclei, mitochondria and food vacuoles. Furthermore, cell disparity within S. rosetta colonies is higher compared to cell disparity within sponge choanocytes. Moreover, we discovered the presence of plasma membrane contacts between colonial cells in addition to already described intercellular bridges and filo-/pseudopodial contacts. Our findings indicate that the last common ancestor of Choanoflagellata and Metazoa might have possessed plasma membrane contacts and spatial cell disparity during colonial life history stages.

evolutionary biology↗