The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications

Abstract

IntroductionAcoels are microscopic marine worms that have become the focus of renewed debate and research due to their placement at the base of the Bilateria by molecular phylogenies. To date, Isodiametra pulchra is the most promising “model acoel” as it can be cultured and gene knockdown can be performed with double-stranded RNA. Despite its well-known morphology data on the nervous system are scarce. Therefore we examined this organ using various microscopic techniques, including histology, conventional histochemistry, electron microscopy, and immunocytochemistry in combination with CLSM and discuss our results in light of recently established phylogenies.ResultsThe nervous system of Isodiametra pulchra consists of a bilobed brain with a dorsal posterior commissure, a frontal ring and tracts, four pairs of longitudinal neurite bundles, as well as a supramuscular and submuscular plexus. Serotonin-like immunoreactivity (SLI) is displayed in parts of the brain, the longitudinal neurite bundles and a large part of the supramuscular plexus, while FMRFamide-like immunoreactivity (RFLI) is displayed in parts of the brain and a distinct set of neurons, the longitudinal neurite bundles and the submuscular plexus. Despite this overlap SLI and RFLI are never colocalized. Most remarkable though is the presence of a distinct functional neuro-muscular system consisting of the statocyst, tracts, motor neurons and inner muscles, as well as the presence of various muscles that differ with regard to their ultrastructure and innervation.ConclusionsThe nervous system of Isodiametra pulchra consists of an insunk, bilobed brain, a peripheral part for perception and innervation of the smooth body-wall musculature as well as tracts and motor neurons that together with pseudostriated inner muscles are responsible for steering and quick movements. The insunk, bilobed brains with two to three commissures found in numerous acoels are homologous and evolved from a ring-commissural brain that was present in the stem species of acoelomorphs. The acoelomorph brain is bipartite, consisting of a Six3/6-dependend animal pole nervous system that persists throughout adulthood and an axial nervous system that does not develop by exhibiting a staggered pattern of conserved regulatory genes as in other bilaterians but by a nested pattern of these genes. This indicates that acoelomorphs stem from an ancestor with a simple brain or with a biphasic life cycle.

Xenacoelomorpha: a case of independent nervous system centralization?

“…Neurite bundles are simple clusters of neurites arranged in parallel, giving rise to a bunch of tracks that extend longitudinally. They are not arranged in the form of a neuropile surrounded by a cellular cortex as occurs in a typical cord [6,23].…”

“…One set of characters that has been used regularly in this and other groups of animals is the neuroanatomical characters [25][26][27][28]. We have already shown elsewhere that the architecture of the NS within the Xenacoelomorpha shows different grades of NS morphological complexity [6] (see also fig. 1 in [29]).…”

“…More clear evidence of evolutionary transformation is seen in the clade Prosopharyngida (including: Hallangiidae, Hofsteniidae and Solenofilomorphidae; fig. 12 in [6]). For instance, within Hofsteniidae, there are species with the NS located in different positions with respect to the epidermis: from a NS built as a basiepidermal plexus to a NS completely positioned below the epidermis, with some species showing some intermediate states (as in the case of Marcusiola tinga, where the dorsal neurite bundles are at the base of the epidermis while the rest is positioned clearly below it [54]).…”

“…They are triploblastic and acoelomate, with an outer epidermis of multiciliated cells and a single gut opening. Together with nemertodermatids, they constitute a taxon called Acoelomorpha, which is characterized by shared morphological features such as the epidermal ciliation, intestinal organization, certain glandular and sensory structures, and the limited presence of an extracellular matrix [1][2][3][4][5][6][7]. Recent phylogenetic analysis maintains that together with xenoturbellids [8], which form another taxon of considerably larger marine worms, they constitute the phylogenetic group Xenacoelomorpha [9][10][11].…”

“…In fact, the acoel NS is characterized by its high plasticity, which is evident in the very different neuronal arrangements that the acoel species show. A quick comparison of, for instance, acoels belonging to the most basal family (Diopisthoporidae) and those of the most divergent families within the class Crucimusculata reveals very striking differences in neural system arrangement [4,6,[48][49][50][51]. Using the knowledge obtained from several studies, old and new, we are in a position to understand, for the first time, the evolution of the NS within this group (see also [6]), always in accordance with the latest available phylogeny of the Acoela [48].…”