Evolution of flatworm central nervous systems: Insights from polyclads

Abstract

The nervous systems of flatworms have diversified extensively as a consequence of the broad range of adaptations in the group. Here we examined the central nervous system (CNS) of 12 species of polyclad flatworms belonging to 11 different families by morphological and histological studies. These comparisons revealed that the overall organization and architecture of polyclad central nervous systems can be classified into three categories (I, II, and III) based on the presence of globuli cell masses -ganglion cells of granular appearance-, the cross-sectional shape of the main nerve cords, and the tissue type surrounding the nerve cords. In addition, four different cell types were identified in polyclad brains based on location and size. We also characterize the serotonergic and FMRFamidergic nervous systems in the cotylean Boninia divae by immunocytochemistry. Although both neurotransmitters were broadly expressed, expression of serotonin was particularly strong in the sucker, whereas FMRFamide was particularly strong in the pharynx. Finally, we test some of the major hypothesized trends during the evolution of the CNS in the phylum by a character state reconstruction based on current understanding of the nervous system across different species of Platyhelminthes and on up-to-date molecular phylogenies.

Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution

“…The 'microturbellarian' catenulid and macrostomid nervous systems are relatively similar and the comparison with other members of the group allows the reconstruction of the ground plan for the Platyhelminthes [185][186][187]. This ground pattern comprises a pair of main neurite bundles, which are located laterally in the slightly orthogonal nervous system [188]. These main neurite bundles are partly lined by perikarya and thus can be described as a medullary cord, while some of the dorsal and lateral neurite bundles lack neural cell bodies and are usually referred to as 'minor cords' [187,189].…”

The serotonergic nervous system of prolecithophorans shows a closer similarity to fecampiids than to triclads (Platyhelminthes)

“…However, the neuropil of C. fingalianum and A. dioicum is broader than that of V. auriculatum . In triclads and polyclads, a correlation of the shape and position of the cephalic ganglion and the body shape, especially the shape of the head, has been noticed (Lang, 1884; Quiroga et al, 2015; Sluys, 1989). C. fingalianum and A. dioicum have a droplet‐shaped body while P. koreni and V. auriculatum have more oblong bodies.…”

“…However, in macrostomorphans, polyclads, proseriates, rhabdocoels, as well as in prolecithophorans a transverse commissure is completely missing, and the two halves of the brain are fused together. The brain has an incision at the anterior and posterior part that indicates the division (Joffe & Reuter, 1993; Kotikova et al, 2002; Kotikova & Timoshkin, 1987; Ladurner et al, 2005; Quiroga et al, 2015; von Graff, 1882). Our results agree with these observations, as they do not show a clear separation of the brain halves either.…”

Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye–brain-independent movement and arousal

“…Intriguingly, we find that the opsin-expressing cells are juxtaposed with the body-wide nerve net that runs across the worm. Flatworms are unique in having evolved a more centralized (cephalized) nervous system comprising a brain and a pair of ventral cords, while still retaining a more diffuse nerve net reminiscent of that seen in Cnidarians (62)(63)(64)(65)(66). The planarian nerve net has also been described as a subepidermal and submuscular plexus and eventually connects to the pair of ventral nerve cords (64)(65)(66).…”