Neuromuscular organization of the freshwater colonial rotifer, Sinantherina socialis, and its implications for understanding the evolution of coloniality in Rotifera

Abstract

Coloniality among rotifers is rare, and while the adaptive signiWcance of the lifestyle has been explored previously, there are few details about how it may have inXuenced the morphology of colony members. In this study, we use confocal laser scanning microscopy combined with cyto-and immunohistochemistry to determine if the colonial rotifer, Sinantherina socialis, diVers in neuromuscular organization relative to other colonial and solitary forms. Our observations indicate that the patterns of serotonergic neurons and somatic muscles in S. socialis are broadly similar to other rotifers. At the neuronal level, the distribution of serotonergic (5HT-IR) neurons in S. socialis is most similar to colony-forming species of Conochilus: (1) paired nerve cords extend the length of the body; (2) the cerebral ganglion innervates the corona with paired neurites that form a neuronal ring; and (3) a single pair of neurites innervates the ventral sensory antennae. Unique to S. socialis is the presence of two additional neuronal rings that supply the corona and may function to modulate ciliary beat. At the muscular level, S. socialis displays a typical pattern of somatic muscle organization similar to other rotifers, but diverges from the pattern in three signiWcant ways: (1) somatic circular muscles form complete rings; (2) circular muscles are distinguishable based on their size and position in the body; and (3) transverse muscles are present within the corona and presumably function to modify its shape for feeding and defensive purposes. These diVerences in neuromuscular organization may be adaptations to the colonial and/or sessile lifestyle, both of which are characteristic of S. socialis.

Serotonin immunoreactivity in the nervous system of the free‐swimming larvae and sessile adult females of Stephanoceros fimbriatus (Rotifera: Gnesiotrocha)

“…According to Montgomery (), who has performed histological research on S. fimbriatus , five sets of neurons project from the cerebral ganglion, three of which innervate sense organs: one pair innervates the dorsal sense organ; one pair innervates the lateral sense organ; and one unpaired median neuron innervates the hypodermis posterior of the dorsal sense organ. Our results could not confirm these observations, but in some respects this is not surprising since serotonergic innervation of sensory organs has only rarely been documented in rotifers (e.g., Hochberg ; Hochberg & Lilley ). Our observations do indicate that at least two of the neurons detected by Montgomery () are likely to correspond to a pair of 5HT‐IR neurites we detected in both larval and adult specimens.…”

“…We focus on immunoreactivity to serotonin in the nervous system for two reasons: (1) serotonin is a modulator of ciliary activity in invertebrates (Weiger ; Hay‐Schmidt ) and (2) the large anatomical differences between the ciliated, larval corona and the ciliated, adult, tentaculate infundibulum would appear to demand a change in innervation. To date, there are few detailed studies of the nervous systems of any gnesiotrochan rotifer (see earlier studies of Vallentin [], Gast [], & Montgomery []; also Hochberg [] & Hochberg & Lilley []), and no knowledge of how the nervous system might be affected by larval metamorphosis.…”

4. Rotifera

“…It consists of a large cerebral ganglion, commonly called brain, located behind the corona dorsally to the mastax, and surrounded by either epithelial or muscular cells. The coronal region with its sensory structures and the dorsal antenna are innervated by a series of paired neurites issuing from the brain that may form neuronal rings (Kotikova 1998, Hochberg & Lilley 2010. The number of cells is constant for each species (e.g., 183 in Epiphanes senta and 249 in Synchaeta tavina).…”

Morphology of the nervous system of monogonont rotiferEpiphanes sentawith focus on sexual dimorphism between feeding females and dwarfed males

“…The serotonin-like immunoreactivity in SNS has been reported for all Ploima species investigated thus far(20, 26), but is apparently absent in all examined Gnesiotrocha(19, 21, 22), a discrepancy that has been stressed as an important difference between those two clades(19). However, we did not detect serotonin-like immunoreactivity in the SNS of E. senta (which is phylogenetically nested within Ploima), which indicates that serotonin-like immunoreactivity in SNS is a homoplastic character in monogonont rotifers similarly to closely related Gnathostomulida(65).…”