Introduction to ‘Homology and convergence in nervous system evolution’

Abstract

The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today's brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor.

Conserved gene regulatory module specifies lateral neural borders across bilaterians

“…For example, both the neuroectoderm of annelids and neural plate of vertebrates are subdivided into a sim/hlh-34-expressing midline and longitudinal Nk2.2/ceh-22-, Nkx6/cog-1-, Pax6/vab-3-, Pax3/7/pax-3-, and Msx/ vab-15-expressing domains from medial to lateral, likely representing the molecular architecture of trunk CNS in their last common ancestor, Urbilateria (8). However, there has been debate on the common origin of CNS centralization because some sister or outgroup species of annelids, arthropods, and chordates lack a centralized ventral cord (26,28). For example, hemichordates differ from major chordates by possessing a diffuse nervous system and do not have mediolateral neural patterning (29).…”

“…Between the neural plate and nonneurogenic ectoderm are the NPB and PPE, from which the majority of the vertebrate PNS is derived (24). How nervous system centralization patterns come into being is a long-standing question in neural development and evolution (3,26).…”

Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

“…PNS consists of neurons and ganglia all over the body to allow animals to receive external information from the environment, thus making the PNS essential for animals to adjust their physiology and behavior to external cues. The evolutionary developmental (evo‐devo) biology mechanism underlying the emergence of centralized nervous systems from ancient nerve nets remains one of the most exciting unsolved questions (Arendt, ; Arendt, Tosches, et al., ; Hejnol & Lowe, ; Strausfeld & Hirth, ).…”

Ancestral Regulatory Mechanisms Specify Conserved Midbrain Circuitry in Arthropods and Vertebrates

“…Cross-phyletic studies further revealed corresponding patterns of developmental genetic mechanisms, information processing and pathologies of the vertebrate basal ganglia and the arthropod central complex (9,(21)(22)(23). These similitudes extend to comparisons of the vertebrate hippocampus and arthropod mushroom bodies, centers that support spatial navigation, allocentric memory, and associative learning (10,24).…”