Cnidocytes are the explosive stinging cells unique to cnidarians (corals, jellyfish, etc). Specialized for prey capture and defense, cnidocytes comprise a group of over 30 morphologically and functionally distinct cell types. These unusual cells are iconic examples of biological novelty but the developmental mechanisms driving diversity of the stinging apparatus are poorly characterized, making it challenging to understand the evolutionary history of stinging cells. Using CRISPR/Cas9-mediated genome editing in the sea anemone
This content will become publicly available on January 18, 2025
Cnidarians—the phylum including sea anemones, corals, jellyfish, and hydroids—are one of the oldest groups of predatory animals. Nearly all cnidarians are carnivores that use stinging cells called cnidocytes to ensnare and/or envenom their prey. However, there is considerable diversity in cnidocyte form and function. Tracing the evolutionary history of cnidocytes may therefore provide a proxy for early animal feeding strategies. In this study, we generated a time‐calibrated molecular clock of cnidarians and performed ancestral state reconstruction on 12 cnidocyte types to test the hypothesis that the original cnidocyte was involved in prey capture. We conclude that the first cnidarians had only the simplest and least specialized cnidocyte type (the isorhiza) which was just as likely to be used for adhesion and/or defense as the capture of prey. A rapid diversification of specialized cnidocytes occurred through the Ediacaran (~654–574 million years ago), with major subgroups developing unique sets of cnidocytes to match their distinct feeding styles. These results are robust to changes in the molecular clock model, and are consistent with growing evidence for an Ediacaran diversification of animals. Our work also provides insight into the evolution of this complex cell type, suggesting that convergence of forms is rare, with the mastigophore being an interesting counterexample.
more » « less- NSF-PAR ID:
- 10486555
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Evolution & Development
- ISSN:
- 1520-541X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Nematostella vectensis , we show that a single transcription factor (NvSox2 ) acts as a binary switch between two alternative stinging cell fates. Knockout ofNvSox2 causes a transformation of piercing cells into ensnaring cells, which are common in other species of sea anemone but appear to have been silenced inN. vectensis . These results reveal an unusual case of single-cell atavism and expand our understanding of the diversification of cell type identity. -
Cnidocytes (i.e., stinging cells) are an unequivocally novel cell type used by cnidarians (i.e., 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 develop by suppression of neural fate in a subset of neurons expressing RFamide. We further show that a single regulatory gene, a C 2 H 2 -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 report a mechanism by which a truly novel regulatory gene (ZNF845) promotes the development of a truly novel cell type (cnidocyte) through duplication of an ancestral cell lineage (neuron) and inhibition of its ancestral identity (RFamide).more » « less
-
more » « less
Abstract Complex biological traits often originate by integrating previously separate parts, but the organismal functions of these precursors are challenging to infer. If we can understand the ancestral functions of these precursors, it could help explain how they persisted and how they facilitated the origins of complex traits. Animal eyes are some of the best studied complex traits, and they include many parts, such as opsin‐based photoreceptor cells, pigment cells, and lens cells. Eye evolution is understood through conceptual models that argue these parts gradually came together to support increasingly sophisticated visual functions. Despite the well‐accepted logic of these conceptual models, explicit comparative studies to identify organismal functions of eye precursors are lacking. Here, we investigate how precursors functioned before they became part of eyes in Cnidaria, a group formed by sea anemones, corals, and jellyfish. Specifically, we test whether ancestral photoreceptor cells regulated the discharge of cnidocytes, the expensive single‐use cells with various functions including prey capture, locomotion, and protection. Similar to a previous study of
Hydra , we show an additional four distantly related cnidarian groups discharge significantly more cnidocytes when exposed to dim blue light compared with bright blue light. Our comparative analyses support the hypothesis that the cnidarian ancestor was capable of modulating cnidocyte discharge with light, which we speculate uses an opsin‐based phototransduction pathway homologous to that previously described inHydra . Although eye precursors might have had other functions like regulating timing of spawning, our findings are consistent with the hypothesis that photoreceptor cells which mediate cnidocyte discharge predated eyes, perhaps facilitating the prolific origination of eyes in Cnidaria. -
more » « less
Abstract Multisensory integration (MSI) combines information from more than one sensory modality to elicit behaviours distinct from unisensory behaviours. MSI is best understood in animals with complex brains and specialized centres for parsing different modes of sensory information, but dispersive larvae of sessile marine invertebrates utilize multimodal environmental sensory stimuli to base irreversible settlement decisions on, and most lack complex brains. Here, we examined the sensory determinants of settlement in actinula larvae of the hydrozoan
Ectopleura crocea (Cnidaria), which possess a diffuse nerve net. A factorial settlement study revealed that photo‐, chemo‐ and mechanosensory cues each influenced the settlement response in a complex and hierarchical manner that was dependent on specific combinations of cues, an indication of MSI. Additionally, sensory gene expression over development peaked with developmental competence to settle, which in actinulae, requires cnidocyte discharge. Transcriptome analyses also highlighted several deep homological links between cnidarian and bilaterian mechano‐, chemo‐, and photosensory pathways. Fluorescent in situ hybridization studies of candidate transcripts suggested cellular partitioning of sensory function among the few cell types that comprise the actinula nervous system, where ubiquitous polymodal sensory neurons expressing putative chemo‐ and photosensitivity interface with mechanoreceptive cnidocytes. We propose a simple multisensory processing circuit, involving polymodal chemo/photosensory neurons and mechanoreceptive cnidocytes, that is sufficient to explain MSI in actinulae settlement. Our study demonstrates that MSI is not exclusive to complex brains, but likely predated and contextualized their evolution. -
null (Ed.)Abstract Synopsis Siphonophores are free-living predatory colonial hydrozoan cnidarians found in every region of the ocean. Siphonophore tentilla (tentacle side branches) are unique biological structures for prey capture, composed of a complex arrangement of cnidocytes (stinging cells) bearing different types of nematocysts (stinging capsules) and auxiliary structures. Tentilla present an extensive morphological and functional diversity across species. While associations between tentillum form and diet have been reported, the evolutionary history giving rise to this morphological diversity is largely unexplored. Here we examine the evolutionary gains and losses of novel tentillum substructures and nematocyst types on the most recent siphonophore phylogeny. Tentilla have a precisely coordinated high-speed strike mechanism of synchronous unwinding and nematocyst discharge. Here we characterize the kinematic diversity of this prey capture reaction using high-speed video and find relationships with morphological characters. Since tentillum discharge occurs in synchrony across a broad morphological diversity, we evaluate how phenotypic integration is maintaining character correlations across evolutionary time. We found that the tentillum morphospace has low dimensionality, identified instances of heterochrony and morphological convergence, and generated hypotheses on the diets of understudied siphonophore species. Our findings indicate that siphonophore tentilla are phenotypically integrated structures with a complex evolutionary history leading to a phylogenetically-structured diversity of forms that are predictive of kinematic performance and feeding habits.more » « less
