Muscle and nerve net organization in stalked jellyfish (Medusozoa: Staurozoa)

Abstract

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.

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

“…In many species, these muscles are constituted by myocytes completely embedded in the mesoglea, and thus not connected either to the ectoderm or the endoderm epithelia (Widersten, 1966; Werner et al, 1976; Chapman, 1978; Chia et al, 1984; Westlake and Page, 2016). In addition, smooth epitheliomuscular cells are present in the ectoderm of the polyp tentacles (Franc, 1993).…”

Genetic description of Manania handi and Manania gwilliami

“…However, surprisingly we found that all four loci of our M. handi specimen were ≥99.7% identical to M. gwilliami (CA). Since Miranda et al (5) and our study (6), additional COI data from M. gwilliami samples collected in 2018 in Bamfield BC Canada were deposited in GenBank; Bamfield is geographically near our sampling location in Victoria BC Canada. We used this opportunity to confirm these putative identifications of M. handi and M. gwilliami.…”

“…We additionally confirmed our specimen as M. handi using characters described in Larson and Fautin (7) Species-level identifications are difficult for lesser-studied marine invertebrates, particularly uncultivable species like staurozoans. By performing an in-depth description in Westlake and Page (6) and generating supporting sequence data (this study), we provide morphological and genetic support for M. handi and M. gwilliami identification efforts.…”

“…Samples were collected from the intertidal zone adjacent to Chinese Cemetery in Victoria BC, described fully in Westlake and Page (6). DNA was extracted from tissue samples using PrepMan Ultra.…”

“…We recently provided extensive characterization of the neuromusculature for two Staurozoan species: Manania handi and Haliclystus "sanjuanensis" (6). Notably, Miranda et al (5) did not include a M. handi sample in their analyses, using only two Manania species: M. uchidai and M. gwilliami.…”