Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia

Abstract

Background 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). 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. Results In 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. Conclusions The 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.

Distinct patterns of gene expression during regeneration and asexual reproduction in the annelid Pristina leidyi

“…Conversely, anteriorly regenerating worms lack most of the anterior structures and therefore the genes herein expressed may explain the high number of downregulated genes in this regeneration condition, and thus it would be reasonable to find several anterior identities and head markers downregulated in this condition. However, we have found no differential expression of several anterior neural markers previously reported in adult and larval annelids and other invertebrates as aristaless-related homeobox, dachshund, empty spiracles homeobox, forebrain zinc-finger, orthopedia, paired box 3/6, retinal homeobox, six 3/6 homeobox, or synaptotagmin 1 (Gąsiorowski et al, 2021;Kerbl et al, 2016;Santagata et al, 2012).…”

“…However, none of the genes previously reported (Gąsiorowski et al, 2021;Kerbl et al, 2016;Santagata et al, 2012) has been found to be significantly differentially expressed in this condition.…”

“…As anteriorly regenerating worms lack most of the anterior tissues and structures, as well as the anterior brain, the downregulation of different anterior identity markers is to be expected. However, none of the genes previously reported (Gąsiorowski et al, 2021 ; Kerbl et al, 2016 ; Santagata et al, 2012 ) has been found to be significantly differentially expressed in this condition. However, among the 529 genes downregulated during anterior regeneration (Supporting Information: Table S5 ), 14 of them were identified as regeneration‐related genes previously reported in other species (reviewed by Zhao et al, 2016 ).…”

The localization of Toll and Imd pathway and complement system components and their response to Vibrio infection in the nemertean Lineus ruber

“…As with all nemerteans, Lineus ruber have an eversible proboscis used to catch prey [64]. Lineus ruber's nervous system is formed by a brain and two lateral and dorsal nerve cords, as well as cephalic nerves that emerge from the brain and extend to the anterior area of the head, innervating the frontal sensory organ and eyes [64][65][66][67]. Furthermore, this species possesses a closed circulatory system that consists of two lateral and dorsal blood vessels that run parallel to the lateral and the dorsal nerve cords [64].…”

The Toll and Imd pathway, the complement system and lectins during immune response of the nemertean Lineus ruber

“…As all nemerteans, Lineus ruber have an eversible proboscis used to catch prey (59). Lineus ruber nervous system is formed by a brain and two lateral and a dorsal nerve cords, as well as cephalic nerves that emerge from the brain and extend to the anterior area of the head, innervating the frontal sensory organ and eyes (59)(60)(61)(62). Furthermore, this species possesses a closed circulatory system that consists of two lateral and a dorsal blood vessels that run parallel to the lateral and the dorsal nerve cords (59).…”