Biology subjects

Babonis, L. S.

Publications and source records attributed to Babonis, L. S..

11 recordsLinked to original sources

bioRxiv2026

Extreme conservation of cnidarian stinging cell identity despite 600 million years of evolution

Understanding how cells specialize is essential for reconstructing the diversification of life on earth. Cnidocytes (stinging cells) have a single origin in the stem cnidarian ([~]800mya) and have since specialized into extremes in morphology and function. Using single-cell RNA sequencing and transcriptional lineage reconstruction in a coral and a sea anemone, we show that a single gene (FoxL2) controls a critical switch point in the evolution of cnidocyte diversity: the decision to be a piercing cell (nematocyte) or an ensnaring cell (spirocyte). Nematocytes are lowly conserved between species and express younger genes, reflecting the continued diversification of this cell lineage. Surprisingly, ensnaring cells are one of the most highly conserved differentiated cell types and express older genes than nematocytes. This suggests spirocytes reached an adaptive peak early and have changed little during the 600 million years since corals and sea anemones last shared a common ancestor, making them living fossil cells.

evolutionary biology↗

bioRxiv2026

Novel cell and tissue dynamics drive the unusual biology of the catch tentacle, an inducible organ of aggression found in the sea anemone Metridium senile

Metridium senile is a clonal anemone that engages in fighting interactions to defend its territory from non-clonemates utilizing an inducible fighting organ, the catch tentacle. Upon contact with a non-clonemate, the catch tentacle tip detaches onto the non-clonal individual, resulting in necrosis where the tip attaches to the non-clone. The incapacitating function of the catch tentacle is driven by a unique type of cnidocyte, the holotrich, which is not found elsewhere in M. senile, including the feeding tentacles from which catch tentacles develop. Metridium farcimen, the sister species to M. senile, never develops catch tentacles despite their close phylogenetic relationship, as exemplified by their ability to hybridize. Here, we compare the feeding tentacles of both species to the catch tentacles in M. senile to determine how catch tentacles achieve their unusual function. We found that the feeding tentacles of M. senile and M. farcimen house similar types of cnidocytes that develop from proliferative cells distributed throughout the tentacle. By contrast, catch tentacles house distinct cnidocyte types from feeding tentacles and restrict proliferative cells to the base of the tentacle. This suggests immature cnidocytes migrate from base to tip to replace lost cells after an aggressive interaction in the catch tentacle. Additionally, we observed two morphologically and chemically distinct types of holotrichs in the catch tentacles that appear to use different cues to induce firing. Together, our data suggests that the novelty of catch tentacle aggression is mediated by distinct cell and tissue dynamics.

evolutionary biology↗

bioRxiv2026

Morphological and functional characterization of the ptychocyte, a stingless stinging cell

Cnidocytes (stinging cells), unique to cnidarians (corals, anemones, jellyfish), have diversified into distinct types with variable forms and functions. Nematocytes, cnidocytes found in all cnidarians, are used for prey capture and defense. When triggered, a pressurized capsule inside the nematocyte releases a harpoon-like structure attached to a hollow tubule that pierces prey and delivers venom. Ptychocytes, a cnidocyte unique to tube anemones (sister to corals and sea anemones) discharge a long spineless tubule used exclusively to build the tube in which the animal lives. Given that nematocytes and ptychocytes are specialized for different functions, we hypothesized that they might respond to firing cues in different ways. To test this, we examined the morphology, function, and distribution of nematocytes and ptychocytes in the North American Tube Anemone, Ceriantheopsis americana. We determined that ptychocytes have apical sensory structures like the cones previously described on nematocytes. Surprisingly, the body wall has a dense population of multiciliated cells that appear to function in tube formation. To determine how divergent selection pressures may have affected firing dynamics, we compared the discharge kinematics of cnidocytes from C. americana and the model sea anemone, Nematostella vectensis. Both nematocytes and ptychocytes from C. americana fired slower than nematocytes from N. vectensis, suggesting the rapid discharge speed of sea anemone nematocytes resulted from modification to these cells after sea anemones and tube anemones diverged from their common ancestor. By comparing the morphology and function of different cnidocytes, we can reconstruct the steps that gave rise to cnidocyte diversity.

evolutionary biology↗

bioRxiv2026

Regression of juvenile tentacles is driven by loss of cell proliferation in Haliclystus sanjuanensis, a cnidarian with limited metamorphosis

Medusozoan cnidarians (e.g., jellyfish) metamorphose from a benthic juvenile polyp into a pelagic adult medusa, providing a well-known example of a clade that uses tissue remodeling to create distinct juvenile and adult body plans. Staurozoans (i.e., stalked jellyfish) are an atypical lineage of medusozoans that have lost their medusa stage; thus, their juvenile and adult body plans look remarkably alike. Their limited metamorphosis is characterized by the regression of primary (juvenile) tentacles and the development of secondary (adult) tentacles. In some staurozoan lineages, metamorphosis also involves development of novel adhesive structures (anchors), which are built on top of the regressing primary tentacles. Understanding how cells are partitioned from making juvenile tissues to making adult tissues is important for understanding how animals can make adult structures in the absence of complete metamorphosis. We compared the abundance and distribution of proliferative cells in tissues undergoing regression (primary tentacles) and development (secondary tentacles and anchors) during the juvenile to adult transition in the San Juan Island stalked jellyfish, Haliclystus sanjuanensis. We show that proliferative cells are lost in regressing primary tentacles but are gained in anchors, consistent with a shift in investment from juvenile to adult tissue. Prior to regression, primary and secondary tentacles show similar patterns in their proliferative cell distribution and in the identity of their cnidocytes (stinging cells), indicating that adult tentacles are made by re-deploying a juvenile tentacle program. Finally, we demonstrate that unlike secondary tentacles, primary tentacles cannot regenerate, illustrating that the temporary investment in this tissue is tied to their loss of proliferative cells. Thus, we propose that continued investment in a population of proliferating cells is an important mechanism for segregating temporary tissues (primary tentacles) from long-term tissues (secondary tentacles). These observations of cell dynamics in H. sanjuanensis suggest that temporary investment into juvenile structures may be used to pattern novel adult tissues, providing an important mechanism for diversifying adult body plans.

evolutionary biology↗

bioRxiv2026

Evolutionary rewiring of the endomesoderm gene regulatory networks specify skeleton secreting cells in stony corals.

Stony corals are the eponymous keystone organisms for the most diverse marine ecosystems on earth: coral reefs. Despite their importance, little is known about the developmental genetic programs that drive their embryonic development and subsequent emergence of coral-specific traits. Like all developmental processes, coral development is governed by a series of genetic interactions collectively termed a gene regulatory network. Evolutionary changes in these gene regulatory networks are key sources of biological innovation, but how these networks operate in corals and how they have changed over time remains poorly understood. Here, we integrate chromatin profiling and transcriptomics to define the cis-regulatory architecture of early development in stony corals using the emerging model, Astrangia poculata. We find that key elements of the deeply conserved cnidarian endomesoderm gene regulatory network have been co-opted into a novel subnetwork that specifies secretory cells in corals. Using transgenic reporter assays, we found that a proximal cis-regulatory element of the endomesodermal gene Brachyury is sufficient to drive coral-specific expression patterns in the sea anemone Nematostella vectensis, demonstrating these elements as a key evolvable unit in stony corals. Collectively these findings establish a gene-regulatory framework for coral development and cell specification and suggest that evolutionary rewiring of ancestral developmental programs is a key driver in the evolution and diversification of stony corals.

developmental biology↗

bioRxiv2023

Microinjection, gene knockdown, and CRISPR-mediated gene knock-in in the hard coral, Astrangia poculata

Cnidarians have become valuable models for understanding many aspects of developmental biology including the evolution of body plan diversity, novel cell type specification, and regeneration. Most of our understanding of gene function during early development in cnidarians comes from a small number of experimental systems including the sea anemone, Nematostella vectensis. Few molecular tools have been developed for use in hard corals, limiting our understanding of this diverse and ecologically important clade. Here, we report the development of a suite of tools for manipulating and analyzing gene expression during early development in the northern star coral, Astrangia poculata. We present methods for gene knockdown using short hairpin RNAs, gene overexpression using exogenous mRNAs, and endogenous gene tagging using CRISPR-mediated gene knock-in. Combined with our ability to control spawning in the laboratory, these tools make A. poculata a tractable experimental system for investigative studies of coral development. Further application of these tools will enable functional analyses of embryonic patterning and morphogenesis across Anthozoa and open new frontiers in coral biology research. Summary StatementThis study reports the development of the first transgenic knock-in coral, providing the opportunity to track the behavior of various cell types during early coral development.

developmental biology↗

bioRxiv2023

Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia

BackgroundOpsins are the primary proteins responsible for light detection in animals. Cnidarians (jellyfish, sea anemones, corals) have diverse visual systems that have evolved in parallel with bilaterians (squid, flies, fish) for hundreds of millions of years. Medusozoans (e.g. jellyfish, hydroids) have evolved eyes multiple times, each time independently incorporating distinct opsin orthologs. Anthozoans (e.g. corals, sea anemones,) have diverse light-mediated behaviors and, despite being eyeless, exhibit more extensive opsin duplications than medusozoans. To better understand the evolution of photosensitivity in animals without eyes we increased anthozoan representation in the phylogeny of animal opsins and investigated the large but poorly characterized opsin family in the sea anemone Nematostella vectensis. ResultsWe analyzed genomic and transcriptomic data from 16 species of cnidarians to generate a large opsin phylogeny (708 sequences) with the largest sampling of anthozoan sequences to date. We identified 29 opsins from N. vectensis (NvOpsins) with high confidence, using transcriptomic and genomic datasets. We found that lineage-specific opsin duplications are common across Cnidaria, with anthozoan lineages exhibiting among the highest numbers of opsins in animals. To establish putative photosensory function of NvOpsins, we identified canonically conserved protein domains and amino acid sequences essential for opsin function in other animal species. We show high sequence diversity among NvOpsins at sites important for photoreception and transduction, suggesting potentially diverse functions. We further examined the spatiotemporal expression of NvOpsins and found both dynamic expression of opsins during embryonic development and sexually dimorphic opsin expression in adults. ConclusionsThese data show that lineage-specific duplication and divergence has led to expansive diversity of opsins in eyeless cnidarians, suggesting opsins from these animals may exhibit novel biochemical functions. The variable expression patterns of opsins in N. vectensis suggest opsin gene duplications allowed for a radiation of unique sensory cell types with tissue-and stage-specific functions. This diffuse network of distinct sensory cell types could be an adaptive solution for varied sensory tasks experienced in distinct life history stages in Anthozoans.

evolutionary biology↗

bioRxiv2022

Independent innexin radiation shaped signaling in ctenophores.

Innexins facilitate cell-cell communication by forming gap junctions or non-junctional hemichannels, which play important roles in metabolic, chemical, ionic, and electrical coupling. The lack of knowledge regarding the evolution and role of these channels in ctenophores (comb jellies), the likely sister group to the rest of animals, represents a substantial gap in our understanding of the evolution of intercellular communication in animals. Here we identify and phylogenetically characterize the complete set of innexins of four ctenophores: Mnemiopsis leidyi, Hormiphora californensis, Pleurobrachia bachei, and Beroe ovata. Our phylogenetic analyses suggest that ctenophore innexins diversified independently from those of other animals and were established early in the emergence of ctenophores. We identified a four-innexin genomic cluster, which was present in the last common ancestor of these four species and has been largely maintained in these lineages. Evidence from correlated spatial and temporal gene expression of the M. leidyi innexin cluster suggest that this cluster has been maintained due to constraints related to gene regulation. We describe basic electrophysiological properties of putative ctenophore hemichannels from muscle cells using intracellular recording techniques, showing substantial overlap with the properties of bilaterian innexin channels. Together, our results suggest that the last common ancestor of animals had gap junctional channels also capable of forming functional innexin hemichannels, and that innexin genes have independently evolved in major lineages throughout Metazoa.

evolutionary biology↗

bioRxiv2021

Knockout of a single Sox gene resurrects an ancestral cell type in the sea anemone Nematostella vectensis

Cnidocytes are the explosive stinging cells found only in cnidarians (corals, jellyfish, etc). Specialized for prey capture and defense, cnidocytes are morphologically complex and vary widely in form and function across taxa; how such diversity evolved is unknown. Using CRISPR/Cas9-mediated genome editing in the burrowing sea anemone Nematostella vectensis, we show that a single transcription factor (NvSox2) acts as a binary switch between two alternative cnidocyte fates. Knockout of NvSox2 caused a complete transformation of nematocytes (piercing cells) into spirocytes (ensnaring cells). The type of spirocyte induced by NvSox2 knockout (robust spirocyte) is not normally found in N. vectensis but is common in sea anemones from other habitats. Homeotic control of cell fate provides a mechanistic explanation for the discontinuous distribution of cnidocyte types across cnidarians and demonstrates how simple counts of cell types can underestimate biodiversity.

evolutionary biology↗

bioRxiv2021

A novel regulatory gene promotes novel cell fate by suppressing ancestral fate in the sea anemone Nematostella vectensis

Cnidocytes ("stinging cells") are an unequivocally novel cell type used by cnidarians (corals, jellyfish, and their kin) to immobilize prey. Although they are known to share a common evolutionary origin with neurons, the developmental program that promoted the emergence of cnidocyte fate is not known. Using functional genomics in the sea anemone, Nematostella vectensis, we show that cnidocytes evolved by suppression of neural fate in a subset of neurons expressing RFamide. We further show that a single regulatory gene, a C2H2-type zinc finger transcription factor (ZNF845), coordinates both the gain of novel (cnidocyte-specific) traits and the inhibition of ancestral (neural) traits during cnidocyte development and that this gene arose by domain shuffling in the stem cnidarian. Thus, we uncover a mechanism by which a truly novel regulatory gene (ZNF845) promoted the origin of a truly novel cell type (cnidocyte) through duplication of an ancestral cell lineage (neuron) and inhibition of its ancestral identity (RFamide). SignificanceIn this study, we demonstrate how new cell types can arise in animals through duplication of an ancestral (old) cell type followed by functional divergence of the new daughter cell. Specifically, we show that stinging cells in cnidarians (jellyfish and corals) evolved by duplication of an ancestral neuron followed by inhibition of the RFamide neuropeptide it once secreted. This is the first evidence that stinging cells evolved from a specific subtype of neurons and suggests some neurons may be easier to co-opt for novel functions than others.

developmental biology↗

bioRxiv2019

Evolutionary dynamics of the trypsin superfamily and the origins of novel secretory cell function in the internalized ectoderm of the sea anemone Nematostella vectensis

Understanding the drivers of morphological diversity is a persistent challenge in evolutionary biology. Here, we investigate functional diversification of secretory cells in the sea anemone Nematostella vectensis to understand the mechanisms promoting cellular specialization across animals. We demonstrate regionalized expression of gland cell subtypes in the internal ectoderm of N. vectensis and show that adult gland cell identity is acquired very early in development. A phylogenetic survey of trypsins across animals suggests this gene family has undergone numerous expansions. We reveal unexpected diversity in trypsin protein structure and show that trypsin diversity arose through independent acquisitions of non-trypsin domains. Finally, we show that trypsin diversification in N. vectensis was effected through a combination of tandem duplication, exon shuffling, and retrotransposition. Together we reveal that numerous evolutionary mechanisms drove trypsin duplication and divergence during the morphological specialization of cell types and suggest the secretory cell phenotype is highly adaptable as a vehicle for novel secretory products.

evolutionary biology↗