Abstract

BackgroundThe brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a clade of worm-like spiralians, which possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been previously suggested as homologs to the annelid mushroom bodies. To understand the developmental and evolutionary origins of the complex brain in nemerteans and spiralians in general, we investigated details of the neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber.ResultsIn the juveniles, the CNS is already composed of all major elements present in the adults, including the brain, paired longitudinal lateral nerve cords, and an unpaired dorsal nerve cord, which suggests that further neural development is mostly related with increase in the size but not in complexity. The ultrastructure of the juvenile cerebral organ revealed that it is composed of several distinct cell types present also in the adults. The 12 transcription factors commonly used as brain cell type markers in bilaterians show region-specific expression in the nemertean brain and divide the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, several of the mushroom body-specific genes are expressed in the developing cerebral organs.ConclusionsThe dissimilar expression of molecular brain markers between L. ruber and the annelid Platynereis dumerilii indicates that the complex brains present in those two species evolved convergently by independent expansions of non-homologous regions of a simpler brain present in their last common ancestor. Although the same genes are expressed in mushroom bodies and cerebral organs, their spatial expression within organs shows apparent differences between annelids and nemerteans, indicating convergent recruitment of the same genes into patterning of non-homologous organs or hint toward a more complicated evolutionary process, in which conserved and novel cell types contribute to the non-homologous structures.

Highlights

  • The brain anatomy in the clade Spiralia can vary from simple, commissural brains to rather complex, partitioned structures

  • We visualized the nervous system of the juveniles by applying antibody staining against tyrosinated tubulin, FMRF-amide, and serotonin (5-HT), as well as Sytox green nuclear staining and fluorescent in situ mRNA hybridization of the choline acetyltransferase (ChAT), a genetic marker of the cholinergic neurons [55]

  • This indicates that even though the general morphology of the brain is already established at the moment of hatching, the following growth of the brain is purely quantitative, and new cell types are added in certain brain regions or some of the neurons change their immunoreactivity during further development

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Summary

Introduction

The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). Most nemerteans are active predators, which hunt for their invertebrate prey using a specialized eversible proboscis, a morphological apomorphy of the clade [1, 14,15,16,17,18] This active lifestyle is accompanied by a relatively complex nervous system, which is coupled with an extensive complement of neuropeptides [19,20,21] and includes a large, multilobed brain (with two ventral and two dorsal lobes), a pair of lateral medullary nerve cords, vast peripheral network, and multiple specialized sensory organs [17, 18, 21,22,23,24,25,26,27,28,29,30,31]. The cerebral organs show some structural and functional similarities with the mushroom bodies of annelids [22] and both organs share high expression levels of proteins with the alleged function in memory and learning [42]

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