Conserved Sensory-Neurosecretory Cell Types in Annelid and Fish Forebrain: Insights into Hypothalamus Evolution

Abstract

Neurosecretory control centers form part of the forebrain in many animal phyla, including vertebrates, insects, and annelids. The evolutionary origin of these centers is largely unknown. To identify conserved, and thus phylogenetically ancient, components of neurosecretory brain centers, we characterize and compare neurons that express the prohormone vasotocin (vasopressin/oxytocin)-neurophysin in the developing forebrain of the annelid Platynereis dumerilii and of the zebrafish. These neurons express the same tissue-restricted microRNA, miR-7, and conserved, cell-type-specific combinations of transcription factors (nk2.1, rx, and otp) that specify their identity, as evidenced by the specific requirement of zebrafish rx3 for vasotocin-neurophysin expression. MiR-7 also labels another shared population of neurons containing RFamides. Since the vasotocinergic and RFamidergic neurons appear to be directly sensory in annelid and fish, we propose that cell types with dual sensory-neurosecretory properties were the starting point for the evolution of neurosecretory brain centers in Bilateria.

The saccus vasculosus of fish is a sensor of seasonal changes in day length

“…However, during the course of evolution, the mammalian pinealocyte has lost the photoreceptive and pacemaker functions and acts primarily as an endocrine organ that secretes melatonin. It has been proposed that multifunctionality (for example, sensory and neurosecretory functions) is a general feature of ancient cell types (Vigh's protoneuron concept) [32][33][34] . Over the course of evolution, these multiple functions were then inherited in a complementary manner by sister cell types with increasing specialization.…”

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

“…S3A) showed that the axonal projections of these cells terminate in the apical nerve plexus ( Fig. 2 E and F), a region of strong neurosecretory activity (18,19). By using the Platynereis MIP antibody or an antibody against the conserved C-amidated dipeptide VWamide that is strongly conserved in mollusks and annelids (Figs.…”

“…We scanned, registered, and averaged at least five individual larvae per gene from whole-mount in situ hybridization samples. We analyzed the neurosecretory marker prohormone convertase prohormone convertase 2 (phc2) and the neuroendocrine transcription factors orthopedia (otp) (18) and dimmed (dimm) (Fig. S4 A-D).…”

“…Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11)(12)(13)(14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17)(18)(19)(20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22)(23)(24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.…”

Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

“…Over the past decade, the annelid P. dumerilii has become a valuable model for evolutionary developmental biology studies, especially regarding the development of its nervous system that resembles that of vertebrates in many aspects. Studies in Platynereis shed light on several ancestral features of the CNS in bilaterians 13 , including the molecular regionalization of the neurectoderm along the mediolateral axis 14 , the presence of conserved brain neurosecretory cells 15 , and the common ancestry of the vertebrate pallium and the protostome corpora pedunculata 16 .…”