Early central nervous system evolution: an era of skin brains?

2003 ◽  
Vol 4 (8) ◽  
pp. 617-627 ◽  
Author(s):  
Nicholas D. Holland
2021 ◽  
Author(s):  
Dylan Z. Faltine-Gonzalez ◽  
Jamie A Havrilak ◽  
Michael J Layden

Understanding if bilaterian centralized nervous systems (CNS) evolved once or multiple times has been debated for over a century. Recent efforts determined that the nerve chords found in bilaterian CNSs likely evolved independently, but the origin(s) of brains remains debatable. Developing brains are regionalized by stripes of gene expression along the anteroposterior axis. Gene homologs are expressed in the same relative order in disparate species, which has been interpreted as evidence for homology. However, regionalization programs resemble anteroposterior axial patterning programs, which supports an alternative model by which conserved expression in brains arose convergently through the independent co-option of deeply conserved axial patterning programs. To begin resolving these hypotheses, we sought to determine when the neurogenic role for axial programs evolved. Here we show that the nerve net in the cnidarian Nematostella vectensis and bilaterian brain are regionalized by the same molecular programs, which indicates nervous system regionalization predates the emergence of bilaterians and CNSs altogether. This argues that shared regionalization mechanisms are insufficient to support the homology of brains and supports the notion that axial programs were able to be co-opted multiple times during evolution of brains.


2004 ◽  
Vol 44 (6) ◽  
pp. 509-538 ◽  
Author(s):  
Jean-Marc Alessandri ◽  
Philippe Guesnet ◽  
Sylvie Vancassel ◽  
Pierre Astorg ◽  
Isabelle Denis ◽  
...  

2016 ◽  
Vol 26 (20) ◽  
pp. R1101-R1108 ◽  
Author(s):  
Irving E. Wang ◽  
Thomas R. Clandinin

2010 ◽  
Vol 12 (4) ◽  
pp. 416-424 ◽  
Author(s):  
Norio Miyamoto ◽  
Yoko Nakajima ◽  
Hiroshi Wada ◽  
Yasunori Saito

2011 ◽  
Vol 53 (5) ◽  
pp. 740-759 ◽  
Author(s):  
Verena Rieger ◽  
Yvan Perez ◽  
Carsten H. G. Müller ◽  
Thurston Lacalli ◽  
Bill S. Hansson ◽  
...  

2015 ◽  
Vol 370 (1684) ◽  
pp. 20150045 ◽  
Author(s):  
Andreas Hejnol ◽  
Christopher J. Lowe

Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized medullary cord and a partitioned brain is homologous across bilaterians. However, the ability to precisely reconstruct ancestral neural architectures from molecular genetic information requires that these gene networks specifically map with particular neural anatomies. A growing body of literature representing the development of a wider range of metazoan neural architectures demonstrates that patterning gene network complexity is maintained in animals with more modest levels of neural complexity. Furthermore, a robust phylogenetic framework that provides the basis for testing the congruence of these homology hypotheses has been lacking since the advent of the field of ‘evo-devo’. Recent progress in molecular phylogenetics is refining the necessary framework to test previous homology statements that span large evolutionary distances. In this review, we describe recent advances in animal phylogeny and exemplify for two neural characters—the partitioned brain of arthropods and the ventral centralized nerve cords of annelids—a test for congruence using this framework. The sequential sister taxa at the base of Ecdysozoa and Spiralia comprise small, interstitial groups. This topology is not consistent with the hypothesis of homology of tripartitioned brain of arthropods and vertebrates as well as the ventral arthropod and rope-like ladder nervous system of annelids. There can be exquisite conservation of gene regulatory networks between distantly related groups with contrasting levels of nervous system centralization and complexity. Consequently, the utility of molecular characters to reconstruct ancestral neural organization in deep time is limited.


2016 ◽  
Vol 371 (1685) ◽  
pp. 20150034 ◽  
Author(s):  
Nicholas J. Strausfeld ◽  
Frank Hirth

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.


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