Meningeal‐like organization of neural tissues in calanoid copepods (Crustacea)

Abstract

Meninges, the connective tissue of the vertebrate central nervous system (CNS), have not been recognized in invertebrates. We describe the ultrastructure of the adult brain, antennules, and cord in five marine copepods: Calanus finmarchicus, Gaussia princeps, Bestiolina similis, Labidocera madurae, and Euchaeta rimana. In all of these locations we identified cell types with characteristics of the typical cells of vertebrate meninges and of their peripheral nervous system (PNS) connective tissue counterpart: fibroblasts, having flattened twisting processes with labyrinthine cavities communicating with the extracellular space, and macrophages, containing prominent lysosomes, well-developed endoplasmic reticulum, Golgi apparatus, and indented heterochromatin. The vertebrate distinction between electron-dense cells in the most external connective tissues (dura mater and epineurium) versus electron-lucent cells in the more internal connective tissues (pia-arachnoid and endoneurium-perineurium) was also found in the copepod CNS and PNS. Similar to the vertebrate organization, electron-dense cell networks penetrated from the outer layer (subcuticle) to surround inner substructures of the copepod nervous systems, and electron-lucent networks penetrated deeply from the brain and nerve surfaces to form intertwined associations with neural cells. Moreover, the association of these cells with basement membranes, glycocalyx, and fibrils of collagen in copepods conforms to a meningeal organization. The primary deviation from the vertebrate ultrastructural organization was the often tight investment of axons by the meningeal-like cells, with an intercalated basement membrane. Together, these data suggest that the tissues investing the copepod nervous system possess an organization that is analogous in many respects to that of vertebrate meninges.