Evolution of basal deuterostome nervous systems

Abstract

Understanding the evolution of deuterostome nervous systems has been complicated by the ambiguous phylogenetic position of the Xenocoelomorpha (Xenoturbellids, acoel flat worms, nemertodermatids), which has been placed either as basal bilaterians, basal deuterostomes or as a sister group to the hemichordate/ echinoderm clade (Ambulacraria), which is a sister group of the Chordata. None of these groups has a single longitudinal nerve cord and a brain. A further complication is that echinoderm nerve cords are not likely to be evolutionarily related to the chordate central nervous system. For hemichordates, opinion is divided as to whether either one or none of the two nerve cords is homologous to the chordate nerve cord. In chordates, opposition by two secreted signaling proteins, bone morphogenetic protein (BMP) and Nodal, regulates partitioning of the ectoderm into central and peripheral nervous systems. Similarly, in echinoderm larvae, opposition between BMP and Nodal positions the ciliary band and regulates its extent. The apparent loss of this opposition in hemichordates is, therefore, compatible with the scenario, suggested by Dawydoff over 65 years ago, that a true centralized nervous system was lost in hemichordates. KEY WORDS: Cephalochordate, Deuterostomes, Echinoderm, Hemichordate, Nervous system evolution IntroductionDeuterostomes include at least the Chordata (vertebrates, tunicates and cephalochordates) and the Ambulacraria (echinoderms and hemichordates). The enigmatic Xenoturbellida has been placed either basally in the deuterostomes or together with acoel flatworms as the Xenocoelomorpha -the sister group of the Ambulacraria. Alternatively, the Xenocoelomorpha have been placed basal to the bilateria (reviewed in Achatz et al., 2013). Xenoturbella has a very simple body plan with a nerve net and is thought to have lost a number of ancestral features (Philippe et al., 2011). Therefore, it is unclear whether it is at all relevant to the evolution of deuterostome nervous systems. However, there is no question that echinoderms and hemichordates are deuterostomes. In most phylogenetic analyses, Ambulacraria are the sister group of the chordates (Blair and Hedges, 2005; Delsuc et al., 2008; Edgecombe et al., 2011). However, a recent analysis based on 586 nuclear genes places cephalochordates as the sister group of the Ambulacraria with high bootstrap support and cephalochordates plus Ambulacraria as the sister group of tunicates plus vertebrates (Moroz et al., 2014). Because the nervous systems of echinoderms, hemichordates and chordates are so very different, it has been controversial whether the ancestral deuterostome had a longitudinal nerve cord or a nerve net or a combination of both.Several schemes for the evolution of deuterostome nervous systems have focused on the possible contribution of the larval REVIEW Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, USA.*Author for correspondence (lzholland@ucsd.edu)...

Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain

“…Previous studies using gene markers have shown that the developing amphioxus CNS displays marked spatial molecular heterogeneity at different developmental stages ([61,97,102,108–112] and see S1 Table). However, most of these studies focused on individual genes across diverse developmental time points, making it difficult to precisely compare the relative positions of their expression patterns and to elaborate a unified map.…”

Resynthesizing behavior through phylogenetic refinement

“…The rest of the BNS remained on the ventral side of the body in protostomes (annelids, mollusks, arthropods, etc. ), but in our branch, the deuterostomes, the body inverted such that the entire nervous system now became dorsally oriented and separate from the mouth and digestive tract (Holland, 2015; Lowe et al, 2006). Finally, in chordates, the nervous system folded inward into the body, forming what defines the basic neural plan to the present day (Nieuwenhuys & Puelles, 2016), as is shown in the inset of Fig.…”

Neural anatomy of echinoid early juveniles and comparison of nervous system organization in echinoderms

“…Echinoderms, together with hemichordates, form the ambulacrarians, which along with the chordates constitute the deuterostomes (Cannon et al, 2014; Satoh, Rokhsar, & Nishikawa, 2014). Although there is little doubt that the last common ancestor of chordates featured a centralized nervous system (Holland, 2015a), the reconstruction of the ancestral deuterostome nervous system is much less straightforward (Holland, 2015b; Lowe, Clarke, Medeiros, Rokhsar, & Gerhart, 2015). In particular, interpretations of hemichordate data have proven to be polarized (Kaul‐Strehlow, Urata, Minokawa, Stach, & Wanninger, 2015; Lowe et al, 2003; Nomaksteinsky et al, 2009), and the current lack of information on the evolutionary diversification of echinoderm nervous systems further complicates this issue (Formery, Schubert, & Croce, 2019; Holland, 2015b; Nakano et al, 2006).…”

“…Although there is little doubt that the last common ancestor of chordates featured a centralized nervous system (Holland, 2015a), the reconstruction of the ancestral deuterostome nervous system is much less straightforward (Holland, 2015b; Lowe, Clarke, Medeiros, Rokhsar, & Gerhart, 2015). In particular, interpretations of hemichordate data have proven to be polarized (Kaul‐Strehlow, Urata, Minokawa, Stach, & Wanninger, 2015; Lowe et al, 2003; Nomaksteinsky et al, 2009), and the current lack of information on the evolutionary diversification of echinoderm nervous systems further complicates this issue (Formery, Schubert, & Croce, 2019; Holland, 2015b; Nakano et al, 2006). Additional information on the basic architecture of the adult nervous system of key representatives of different echinoderm classes, involving contemporary imaging approaches and a broad selection of markers, is thus needed to establish a comparative framework and enable novel evolutionary inferences.…”