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

Jörn Von Döhren

doi:10.3389/fevo.2021.654846

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.

Highlights

Bilaterian animals are currently grouped into three major superphyla, Ecdysozoa, Deuterostomia, and Spiralia (Halanych et al, 1995; Aguinaldo et al, 1997; Giribet, 2002, 2016; Dunn et al, 2008, 2014; Hejnol et al, 2009; Edgecombe et al, 2011)
This study aims at a comparative description of the development of the body wall musculature and of the FMRFamide immunoreactive component, a subset of the peptidergic nervous system in several non-pilidiophoran representatives that possess the type of development that has traditionally been termed as “direct.” Both hoplo- and palaeonemertean representatives were investigated
In the majority of specimens observed, gastrulation is completed after 1 day of development and the epidermal cells are adorned with a dense coat of epidermal cilia visualized by acetylated α-tubulin-like immunoreactivity (Figure 1A: α-tub-lir at 2-dpf)

Summary

Introduction

Bilaterian animals are currently grouped into three major superphyla, Ecdysozoa, Deuterostomia, and Spiralia (Halanych et al, 1995; Aguinaldo et al, 1997; Giribet, 2002, 2016; Dunn et al, 2008, 2014; Hejnol et al, 2009; Edgecombe et al, 2011). No other metazoan superphylum shows such an enormous diversity of morphologies as Spiralia and as a consequence, body wall musculature and nervous systems are highly diverse (Wanninger, 2015) This diversity in morphologies and the body wall muscles and nervous systems is somewhat puzzling, since most members of Spiralia share a stereotypic, spiral cleavage (Boyer and Henry, 1998; Lambert, 2010; Nielsen, 2010; Martín-Durán and Marlétaz, 2020). It is characterized by a spiral arrangement of the blastomeres, with quartets of cells in a helicoidal arrangement above each other, that each have a determined fate in the future morphology of the species. The solution to this paradox may be that the majority of the morphological diversity observed in adult spiralian lineages results from diversification of post-embryonic development

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