Evolution of neuronal types and families

Abstract

Major questions in the evolution of neurons and nervous systems remain unsolved, such as the origin of the first neuron, the possible convergent evolution of neuronal phenotypes, and the transition from a relatively simple decentralized nerve net to the complex, centralized nervous systems found in modern bilaterian animals. In recent years, comparative single-cell transcriptomics has opened up new research avenues addressing these issues. Here, we review recent conceptual progress toward an evolutionary definition of cell types, and how it facilitates the identification and large-scale comparison of neuronal types and neuron type families from single-cell data - with the family of GABAergic neurons in distinct parts of the vertebrate forebrain as prime example. We also highlight strategies to infer cell type-specific innovation, so-called apomeres, from single-cell data.

Figure 1

From neural precursors to nerve net to nerve cords: evolution of the nervous system. The first neural cell types may have resembled choanocyte-like cells, reminiscent of unicellular choanoflagellates — polarized cells with an apical cilium surrounded by an apical microvillar collar, as frequently observed in today’s sensory neuronal morphologies [4]. Another candidate precursor are mesenchymal cells with cellular protrusions, resembling today’s interneuron and motoneuron morphologies. The nerve net is depicted as described for cnidarians, and the centralized nervous system is drawn to represent a prototype vertebrate system.

Figure 2

Hypothetical scheme illustrating cell type diversification in animal evolution. For each tree, the cell type branching events that had already occurred in a given ancestor are drawn in the color of that ancestor. Older cell type families are shared between remote phyla, whereas younger families are phylum-specific, or specific to smaller taxonomic units. The birth of the first neuron is indicated by a black box and the family of neurons demarcated by brackets, the (hypothetical) emergence of a second, neuron-like cell type family in stem bilaterians by grey box and brackets. For simplicity, other possible modes of cell type evolution such as fusion are not represented here.

Figure 3

GABA-ergic cell types express Dlx, Arx and Lhx6 transcription factors: (a) in the mouse cortex [15] and (b) in hypothalamus [14]. Red branches in the cell type trees indicate GABAergic neurons; blue branches indicate glutamatergic neurons. Transcription factor expression in the hypothalamus has been plotted by us according to Supplementary Table 6 in Ref. [14].