Diversity in the Development of the Neuromuscular System of Nemertean Larvae (Nemertea, Spiralia)

Abstract

In studies on the development of nervous systems and musculature, fluorescent labeling of neuroactive substances and filamentous actin (f-actin) of muscle cells and the subsequent analysis with confocal laser scanning microscopy (CLSM), has led to a broad comparative data set for the majority of the clades of the superphylum Spiralia. However, a number of clades remain understudied, which results in gaps in our knowledge that drastically hamper the formulation of broad-scale hypotheses on the evolutionary developmental biology (EvoDevo) of the structures in question. Regarding comparative data on the development of the peptidergic nervous system and the musculature of species belonging to the spiralian clade Nemertea (ribbon worms), such considerable knowledge gaps are manifest. This paper presents first findings on fluorescent labeling of the FMRFamide-like component of the nervous system and contributes additional data on the muscle development in the presently still underrepresented larvae of palaeo- and hoplonemertean species. Whereas the architecture of the FMRFamide-like nervous system is comparably uniform between the studied representatives, the formation of the musculature differs considerably, exhibiting developmental modes yet undescribed for any spiralian species. The presented results fill a significant gap in the spiralian EvoDevo data set and thus allow for further elaboration of hypotheses on the ancestral pattern of the musculature and a prominent component of the nervous system in Nemertea. However, with respect to the variety observed, it is expected that the true diversity of the developmental pathways is still to be discovered when more detailed data on other nemertean species will be available.

Postembryonic development and lifestyle shift in the commensal ribbon worm

“…In Malacobdella , unique morphological characteristics, such as the presence of a terminal sucker and the loss of sensory organs (apical/cerebral organs), formed in postembryonic stages. This finding aligns with a recent comparative study on embryonic/postembryonic development in Nemertea, which suggests that most of the within-clade morphological diversity in the phylum has resulted from postembryonic development [ 53 ]. Molecular phylogenetic analyses have shown that Malacobdella is robustly nested within the Amphiporiina and forms a clade with the land-dwelling monostiliferans Geonemertes , although the relationship is not well supported.…”

Comparative development of the serotonin- and FMRFamide-immunoreactive components of the nervous system in two distantly related ribbon worm species (Nemertea, Spiralia)

“…Currently, data on the development of the nervous system by means of immunohistochemistry against serotonin and FMRFamide combined with analysis by confocal laser scanning microscopy are available for a handful of species from all three high-ranking clades of Nemertea (Hay-Schmidt, 1990;Chernyshev and Magarlamov, 2010;Maslakova, 2010a;Hindinger et al, 2013;Hiebert and Maslakova, 2015;von Döhren, 2016bvon Döhren, , 2021. However, both antibodies have so far only been studied in two species, Lineus albocinctus (Heteronemertea) (Hindinger et al, 2013) and Carinina ochracea (Carinomiformes) (von Döhren, 2016b).…”

“…In the developing juvenile of Pilidiophora inside the pilidial envelope, the developing proboscis also displays 5HT-lir neurite processes (Hay-Schmidt, 1990;Maslakova, 2010a). A dorsal nerve that is present in the larvae of C. ochracea and Tubulanus polymorphus (Tubulaniformes), is absent from the larva of C. rufifrons, although it is present in adults (Beckers et al, 2013;von Döhren, 2016bvon Döhren, , 2021. In Carinoma species (Carinomiformes), the dorsal nerve is also present in adults but has not yet formed in the investigated larval stages (Beckers et al, 2013;von Döhren, 2021).…”

“…In all palaeonemertean species studied so far, immunoreactivity against serotonin, FMRFamide, and synapsin is not detectable until after hatching (Figure 9C;von Döhren, 2016bvon Döhren, , 2021. In all investigated hoplonemertean species, however, the timing of the development of the nervous system components relative to hatching is different (Chernyshev and Magarlamov, 2010;Hiebert and Maslakova, 2015;von Döhren, 2021). Whereas larvae of Carcinonemertes carcinophila (Monostilifera) and Amphiporus sp.…”

“…The sequence of nervous system formation in Palaeonemertea and Hoplonemertea shows only minor differences that are congruent with general developmental characteristics Development of the respective nervous system components in C. rufifrons and E. gracile is largely similar to their relatives within Palaeonemertea and Hoplonemertea, respectively. Generally, the main components, i.e., the ring-shaped brain and the paired longitudinal nerve cords, develop in a frontal to caudal progression in all investigated paleonemertean and hoplonemertean species (Figure 9C; Chernyshev and Magarlamov, 2010;Hiebert and Maslakova, 2015;von Döhren, 2016bvon Döhren, , 2021. Whereas the 5HTlir signals in the peripheral epidermal plexus of C. rufifrons and E. gracile are seen almost as early as the onset of brain development, the RFa-lir signals in this part of the nervous system are seen much later, after the brain and the longitudinal nerve cords have already progressed considerably in their development (Figure 9C).…”