Staurozoan cnidarians display an unusual combination of polyp and medusa characteristics and their morphology may be informative about the evolutionary origin of medusae. We studied neuromuscular morphology of two staurozoans, Haliclystus 'sanjuanensis' and Manania handi, using whole mount immunohistochemistry with antibodies against FMRFamide and α-tubulin to label neurons and phalloidin to label muscles. All muscles appeared to lack striations. Longitudinal interradial muscles are probable homologues of stalk muscles in scyphopolyps, but in adult staurozoans they are elaborated to inwardly flex marginal lobes of the calyx during prey capture; these muscles are pennate in M. handi. Manubrial perradial muscles, like the manubrium itself, are an innovation shared with pelagic medusae and manubrial interradial muscles are shared with scyphozoan ephyra. Marginal muscles of M. handi displayed occasional synchronous contraction reminiscent of a medusa swim pulse, but contractions were not repetitive. The nerve net in both species showed regional variation in density and orientation of neurons. Some areas labeled predominantly by α-tubulin antibodies (exumbrellar epidermis), other areas labeled exclusively by FMRFamide antibodies (dense plexus of neurites surrounding the base of secondary tentacles, neuronal concentration at the base of transformed primary tentacles; gastrodermal nerve net), but most areas showed a mix of neurons labeled by these two antibodies and frequent co-labeling of neurons. Transformed primary tentacles had a concentration of FMRFamide-immunoreactive neurons at their base that was associated with a pigment spot in M. handi; this is consistent with their homology with rhopalia of medusae, which are also derived from primary tentacles. The muscular system of these staurozoans embodies characteristics of both scyphopolyps and pelagic medusae. However, their nerve net is more polyp-like, although marginal concentrations of the net associated with primary and secondary tentacles may facilitate the richer behavioral repertoire of staurozoans relative to polyps of other medusozoans. J. Morphol. 278:29-49, 2017. ©© 2016 Wiley Periodicals,Inc.
Rhogocytes, terminal cells of protonephridia, and podocytes of metanephridial systems share an architectural feature that creates an apparent sieving device. The sieve serves to ultrafilter body fluid during the excretion and osmoregulation process carried out by nephridial systems, but its function in rhogocytes is unclear. Rhogocytes are molluscan hemocoelic cells that appear to have various functions related to metabolism of metal ions, including synthesis of hemocyanin in some gastropods and metal detoxification in pteriomorph bivalves. A hypothesis that proposed developmental and possibly evolutionary conversion between protonephridial terminal cells and rhogocytes has never been further explored; indeed, information on the occurrence of rhogocytes in molluscan developmental stages is meager. We used transmission electron microscopy to show that rhogocytes are present within larvae of eight species of gastropods sampled from the three major gastropod clades with a feeding larval stage in the life history. In larvae of a heterobranch gastropod, a rhogocyte was located next to each terminal cell of a pair of protonephridia that flanked the foregut, whereas all six species of caenogastropod larvae and a neritimorph larva that we examined had rhogocytes, but no protonephridia, in this location. We did not find ringshaped profiles of hemocyanin decamers within rhogocytes of larvae or pre-hatch embryos. Rhogocytes in newly released larvae of Nerita melanotragus contained orderly bundles of cylinders, but the diameter of the cylinders was only 70% of the diameter typical of hemocyanin multidecamers. By examining embryos of the caenogastropod Nassarius mendicus at four successive developmental time points that bracketed the occurrence of larval hatching, we found that terminal cells from non-functional protonephridia in pre-hatch embryos transformed into rhogocytes around the time of hatching. This empirical evidence of ontogenetic transformation of protonephridial terminal cells into rhogocytes might be interpreted as developmental recapitulation of an evolutionary transition that occurred early in molluscan history.
Staurozoa is an intriguing lineage of cnidarians bearing both polypoid and medusoid characters in the adult body plan. Miranda et al. (2016) provided a massive descriptive effort of specimen collection, sequencing, and character evolution. We also recently described the neuromusculature of two staurozoan species: Manania handi and Haliclystus "sanjuanensis." We found that our M. handi samples genetically matched Manania gwilliami samples used in Miranda et al. (2016). Taking advantage of newly-deposited M. gwilliami sequence data, we confirm the identity of our M. handi samples, and provide additional sequence data for M. handi and H. sanjuanensis for future staurozoan identification efforts.
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