Abstract
BackgroundThe composition of the arthropod head is one of the most contentious issues in animal evolution. In particular, controversy surrounds the homology and innervation of segmental cephalic appendages by the brain. Onychophora (velvet worms) play a crucial role in understanding the evolution of the arthropod brain, because they are close relatives of arthropods and have apparently changed little since the Early Cambrian. However, the segmental origins of their brain neuropils and the number of cephalic appendages innervated by the brain - key issues in clarifying brain composition in the last common ancestor of Onychophora and Arthropoda - remain unclear.ResultsUsing immunolabelling and neuronal tracing techniques in the developing and adult onychophoran brain, we found that the major brain neuropils arise from only the anterior-most body segment, and that two pairs of segmental appendages are innervated by the brain. The region of the central nervous system corresponding to the arthropod tritocerebrum is not differentiated as part of the onychophoran brain but instead belongs to the ventral nerve cords.ConclusionsOur results contradict the assumptions of a tripartite (three-segmented) brain in Onychophora and instead confirm the hypothesis of bipartite (two-segmented) brain composition. They suggest that the last common ancestor of Onychophora and Arthropoda possessed a brain consisting of protocerebrum and deutocerebrum whereas the tritocerebrum evolved in arthropods.
Highlights
The composition of the arthropod head is one of the most contentious issues in animal evolution
Our results show that the major transverse neuropils of the onychophoran brain arise from only one body segment, and that only the antennae and jaws are innervated by the brain
Strausfeld et al [31] subdivided the adult onychophoran brain into protocerebrum, deutocerebrum and tritocerebrum by analysing series of histological and silver- and osmium-stained sections and assessing the number and spatial separation of brain neuropils. To clarify whether these brain neuropils have independent origins from different segments, we examined brain development in onychophoran embryos using an antibody raised against acetylated a-tubulin
Summary
The composition of the arthropod head is one of the most contentious issues in animal evolution. The onychophoran “head” is not clearly delineated from the trunk, but shows three pairs of modified appendages: sensory antennae, jaws situated within the mouth cavity, and slime papillae, which are used for defence and capturing prey organisms (Figure 1A). These modified appendages have been assigned to each body segment by studying embryogenesis, which revealed that the antennae belong to the first (ocular) body segment, the jaws to the second, and the slime papillae to the third segment [14,15,16,17,18,19,20]. This is supported by the expression data of segment polarity genes in onychophoran embryos [25], which show only three domains anterior to the leg-bearing segments, corresponding to the three cephalic segments (Figure 1B)
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