The development of early pioneer neurons in the annelid Malacoceros fuliginosus

Abstract

Background Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus. Results We performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 h postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d221), which after 7 cleavages starts expressing Neurogenin, Acheate-Scute and NeuroD. Conclusions We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. We suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.

Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis

“…Besides larval specific neurons and gland cells, we also noted a significant difference in the spatial distribution of neuropeptide transcripts along the oral-aboral axis in Nematostella (Fig 8A). Along with the previously identified Nv-RPamide III neuropeptide [22], we also detected distribution are also identified in a range of marine phyletic taxa including sponge [27,28,49,50] and eumetazoan larvae [12][13][14], signifying a deeply conserved larval sensory/secretory system.…”

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

“…Our study demonstrates that the first cilia to appear in O. fusiformis are those in the apical tuft and the prototroch, followed by the neurotroch, and lastly the metatroch (Fig 10a). As observed in other annelid studies with enough temporal resolution, the prototroch and apical tuft develop quicker, presumably providing the early larvae with a way to move and sense the environment (Fischer et al, 2010; Kumar et al, 2020; McDougall et al, 2006), while the metatroch differentiates soon after, in preparation for feeding. Unlike the definitive prototrochal cells of other annelid and spiralian larvae (Bird, 2012; Emlet and Strathmann, 1994; Özpolat et al, 2017), ciliated cells in Owenids are monociliated (Gardiner, 1978; Smart and Von Dassow, 2009), and thus can continue dividing once differentiated and integrated in the ciliated band, as previously observed in O. collaris (Bird, 2012; Smart and Von Dassow, 2009) and our study shows for O. fusiformis (Fig.…”

“…However, most other annelid trochophore-like larvae display more complex nervous systems at the moment of hatching (Marlow et al, 2014; Verasztó et al, 2020; Vergara et al, 2017), thus suggesting that the early mitraria larva emerges with a rudimentary nervous system that matures as the larva grows. To test this scenario, we identified and analysed the embryonic expression of the pan-neural marker gene elav1 (Carrillo-Baltodano et al, 2019; Denes et al, 2007; Koushika et al, 1996; Kumar et al, 2020; Meyer and Seaver, 2009) and the mature neuron marker synaptotagmin1 ( syt1 ) (Carrillo-Baltodano et al, 2019; Kerbl et al, 2016a; Kumar et al, 2020; Meyer et al, 2015; Rizo and Rosenmun, 2008; Santagata et al, 2012; Simionato et al, 2008) (Fig. 6).…”

“…In some members of Sedentaria (e.g. Spirobranchus lamarcki (McDougall et al, 2006) and Malacoceros fuliginosus (Kumar et al, 2020)) and Errantia (e.g. Platynereis dumerilii (Starunov et al, 2017) and Phyllodoce maculata (Voronezhskaya et al, 2003)), neurogenesis starts with a dual anterior and posterior differentiation of pioneer neurons, which has been proposed as the ancestral condition to Pleistoannelida or even Annelida as a whole (Kumar et al, 2020).…”

“…Spirobranchus lamarcki (McDougall et al, 2006) and Malacoceros fuliginosus (Kumar et al, 2020)) and Errantia (e.g. Platynereis dumerilii (Starunov et al, 2017) and Phyllodoce maculata (Voronezhskaya et al, 2003)), neurogenesis starts with a dual anterior and posterior differentiation of pioneer neurons, which has been proposed as the ancestral condition to Pleistoannelida or even Annelida as a whole (Kumar et al, 2020). However, our findings in O. fusiformis are in agreement with observations in sipunculans (Carrillo-Baltodano et al, 2019; Kristof and Maiorova, 2015; Kristof et al, 2008) and dinophilids (Kerbl et al, 2016a; Kerbl et al, 2016b), thus suggesting that an initial anterior/apical specification of neurons and pioneer neurons is common in groups outside Pleistoannelida.…”