Department of Biological Sciences, University of Bergen, Bergen, Norway.
Biological Faculty, M.V. Lomonosov Moscow State University, Moscow, Russia.
BMC Biol. 2021 Aug 27;19(1):175. doi: 10.1186/s12915-021-01113-1.
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.
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.
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.
螺旋动物门的脑解剖结构从简单的、连合的脑（例如，腹毛类、轮虫）到相当复杂的、分隔的结构（例如，头足类和环节动物）都有。复杂的大脑是如何以及在哪些谱系中进化的仍然不清楚。纽形动物是一类蠕虫状的螺旋动物，它们拥有复杂的中枢神经系统（CNS），其中包括一个显著的大脑和复杂的化学感觉和神经分泌脑器官，这些器官以前被认为是环节动物蘑菇体的同源物。为了了解纽形动物和一般螺旋动物复杂大脑的发育和进化起源，我们研究了纽形动物 Lineus ruber 幼虫的脑和脑器官的神经解剖和基因表达的细节。
在幼虫中，CNS 已经由成年动物中存在的所有主要元素组成，包括大脑、成对的纵向侧神经索和不成对的背神经索，这表明进一步的神经发育主要与大小的增加有关，而不是与复杂性有关。幼虫脑器官的超微结构显示，它由几种在成年动物中也存在的不同细胞类型组成。在两侧对称动物中常用的 12 种转录因子作为脑细胞类型标记，在纽形动物大脑中表现出区域特异性表达，并将整个器官分为几个分子上不同的区域，与形态学隔室部分重叠。此外，几个蘑菇体特异性基因在发育中的脑器官中表达。
L. ruber 和环节动物 Platynereis dumerilii 之间的分子脑标记物的不同表达表明，这两个物种的复杂大脑是通过其最后共同祖先中简单大脑的非同源区域的独立扩展而趋同进化的。尽管相同的基因在蘑菇体和脑器官中表达，但它们在器官内的空间表达在环节动物和纽形动物之间存在明显差异，这表明相同基因被趋同招募到非同源器官的模式形成中，或者暗示了一个更复杂的进化过程，其中保守和新的细胞类型有助于非同源结构的形成。
