Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda

A fundamental question in biology is how animal segmentation arose during evolution. One particular challenge is to clarify whether segmental ganglia of the nervous system evolved once, twice, or several times within the Bilateria. As close relatives of arthropods, Onychophora play an important role...

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Bibliographic Details
Published in:Developmental biology 2009-11, Vol.335 (1), p.263-275
Main Authors: Mayer, Georg, Whitington, Paul M.
Format: Article
Language:English
Subjects:
Animals
Arthropoda
Axon growth
Axonogenesis
Bilateria
Biological Evolution
Body Patterning - physiology
Body plan
Ecdysozoa
Female
Ganglia
Invertebrates - anatomy & histology
Invertebrates - classification
Invertebrates - embryology
Nervous System - anatomy & histology
Nervous System - embryology
Neuromere
Onychophora
Panarthropoda
Phylogeny
Tardigrada
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Summary:A fundamental question in biology is how animal segmentation arose during evolution. One particular challenge is to clarify whether segmental ganglia of the nervous system evolved once, twice, or several times within the Bilateria. As close relatives of arthropods, Onychophora play an important role in this debate since their nervous system displays a mixture of both segmental and non-segmental features. We present evidence that the onychophoran “ventral organs,” previously interpreted as segmental anlagen of the nervous system, do not contribute to nerve cord formation and therefore cannot be regarded as vestiges of segmental ganglia. The early axonal pathways in the central nervous system arise by an anterior-to-posterior cascade of axonogenesis from neuronal cell bodies, which are distributed irregularly along each presumptive ventral cord. This pattern contrasts with the strictly segmental neuromeres present in arthropod embryos and makes the assumption of a secondary loss of segmentation in the nervous system during the evolution of the Onychophora less plausible. We discuss the implications of these findings for the evolution of neural segmentation in the Panarthropoda (Arthropoda + Onychophora + Tardigrada). Our data best support the hypothesis that the ancestral panarthropod had only a partially segmented nervous system, which evolved progressively into the segmental chain of ganglia seen in extant tardigrades and arthropods.
ISSN:0012-1606
1095-564X
DOI:10.1016/j.ydbio.2009.08.011