Biodiversity Meets Neuroscience: From the Sequencing Ship (Ship-Seq) to Deciphering Parallel Evolution of Neural Systems in Omic’s Era

Abstract

The origins of neural systems and centralized brains are one of the major transitions in evolution. These events might occur more than once over 570-600 million years. The convergent evolution of neural circuits is evident from a diversity of unique adaptive strategies implemented by ctenophores, cnidarians, acoels, molluscs, and basal deuterostomes. But, further integration of biodiversity research and neuroscience is required to decipher critical events leading to development of complex integrative and cognitive functions. Here, we outline reference species and interdisciplinary approaches in reconstructing the evolution of nervous systems. In the "omic" era, it is now possible to establish fully functional genomics laboratories aboard of oceanic ships and perform sequencing and real-time analyses of data at any oceanic location (named here as Ship-Seq). In doing so, fragile, rare, cryptic, and planktonic organisms, or even entire marine ecosystems, are becoming accessible directly to experimental and physiological analyses by modern analytical tools. Thus, we are now in a position to take full advantages from countless "experiments" Nature performed for us in the course of 3.5 billion years of biological evolution. Together with progress in computational and comparative genomics, evolutionary neuroscience, proteomic and developmental biology, a new surprising picture is emerging that reveals many ways of how nervous systems evolved. As a result, this symposium provides a unique opportunity to revisit old questions about the origins of biological complexity.

Independent origins of neurons and synapses: insights from ctenophores

“…If correct, it would be critically important to identify the genes that were supposedly lost in sponges and placozoans (but preserved in ctenophores) that led to the loss of neurons and synapses. We believe that this massive functional neuronal/synaptic loss is also unlikely, because there is not a single example of a loss of neural systems in any non-parasitic animal lineage [ 68 ]. Indeed, according to the monophyletic hypothesis, it should be assumed that the common ancestor of ctenophores shared the same transmitters and neurogenic genes as the extant members of the Porifera, Placozoa and bilaterian–cnidarian clades.…”

“…Functional analysis of the electrical synapses in ctenophores is in its infancy [ 70 , 117 ]. Interestingly, the PANX/INX genes are one of the most highly expressed transcripts in the adult aboral organ of P. bachei ( figure 5 d ; [ 28 ]), but they are also expressed in the combs and conductive tracts and in the neuron-like subepithelial cells.…”

Development of neuromuscular organization in the ctenophore Pleurobrachia bachei

“…serotonin, dopamine, noradrenalin, adrenalin, octopamine, acetylcholine, histamine) were not detected by ultrasensitive microchemical assays; and 4) initial pharmacological screening of known bilaterian transmitters produced neither detectable changes in muscle conductivity/excitability, nor changed ciliary beating in their combs (Moroz et al, ). These and other molecular findings led to the hypotheses of independent origins of neural systems in ctenophores (see details and historical overviews in Moroz, , ; Moroz, ). Marlow and Arendt (2015) challenged this polygenesis hypothesis by suggesting additional candidates for pan‐synaptic and pan‐neuronal molecular markers that might genealogically unite ctenophore and other nervous systems (Marlow and Arendt, ).…”

Atlas of the neuromuscular system in the Trachymedusa Aglantha digitale: Insights from the advanced hydrozoan

“…Cnidaria and Bilateria are united as the distinct clade of animals with nervous systems that possibly share a common origin. In contrast, ctenophores might have evolved neural and muscular systems independently from the common ancestor of Cnidaria+Bilateria (Moroz, ; Moroz, ; Moroz et al, ; Moroz & Kohn, ). Thus, Eumetazoa could be a polyphyletic taxon, and Cnidaria is a key reference group to understand the origin of integrative systems in bilaterians.…”