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Insights into the segmental identity of post-oral commissures and pharyngeal nerves in Onychophora based on retrograde fills.

Martin C, Mayer G - BMC Neurosci (2015)

Bottom Line: Our fills of post-oral commissures in E. rowelli revealed a graded arrangement of anteriorly shifted somata associated with post-oral commissures #1 to #5.The number of deutocerebral somata associated with each commissure decreases posteriorly, i.e., commissure #1 shows the highest and commissure #5 the lowest numbers of associated somata, whereas none of the subsequent median commissures, beginning with commissure #6, shows somata located in the deutocerebrum.Based on the graded and shifted arrangement of somata associated with the anteriormost post-oral commissures, we suggest that the onychophoran brain, which is a bipartite syncerebrum, might have evolved by a successive anterior/anterodorsal migration of neurons towards the protocerebrum in the last onychophoran ancestor.

View Article: PubMed Central - PubMed

Affiliation: Animal Evolution and Development, Institute of Biology, University of Leipzig, Talstraße 33, 04103, Leipzig, Germany. christine.martin@uni-leipzig.de.

ABSTRACT

Background: While the tripartite brain of arthropods is believed to have evolved by a fusion of initially separate ganglia, the evolutionary origin of the bipartite brain of onychophorans-one of the closest arthropod relatives-remains obscure. Clarifying the segmental identity of post-oral commissures and pharyngeal nerves might provide useful insights into the evolution of the onychophoran brain. We therefore performed retrograde fills of these commissures and nerves in the onychophoran Euperipatoides rowelli.

Results: Our fills of the anterior and posterior pharyngeal nerves revealed groups of somata that are mainly associated with the deutocerebrum. This resembles the innervation pattern of other feeding structures in Onychophora, including the jaws and several lip papillae surrounding the mouth. Our fills of post-oral commissures in E. rowelli revealed a graded arrangement of anteriorly shifted somata associated with post-oral commissures #1 to #5. The number of deutocerebral somata associated with each commissure decreases posteriorly, i.e., commissure #1 shows the highest and commissure #5 the lowest numbers of associated somata, whereas none of the subsequent median commissures, beginning with commissure #6, shows somata located in the deutocerebrum.

Conclusions: Based on the graded and shifted arrangement of somata associated with the anteriormost post-oral commissures, we suggest that the onychophoran brain, which is a bipartite syncerebrum, might have evolved by a successive anterior/anterodorsal migration of neurons towards the protocerebrum in the last onychophoran ancestor. This implies that the composite brain of onychophorans and the compound brain of arthropods might have independent evolutionary origins, as in contrast to arthropods the onychophoran syncerebrum is unlikely to have evolved by a fusion of initially separate ganglia.

No MeSH data available.


Related in: MedlinePlus

Anatomy of the anterior nervous system in the onychophoran Euperipatoides rowelli. Light micrograph (a) and simplified diagram (b) of dissected brain and anterior nerve cords in ventral view. Anterior is up. Anteriormost post-oral commissures numbered (#1 to #5). at antennal tract, cc connecting cord (characterized by the absence of ring commissures), dc deutocerebrum, ey eye, ho hypocerebral organ, jn jaw nerve, L2 and L3 second and third lip papillae nerves; mc, median commissure, nc nerve cord, pc protocerebrum, pn1 and pn2 anterior and posterior pharyngeal nerves, rc ring commissure, sn slime papilla nerves. Scale bar (in a) 200 µm
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Fig2: Anatomy of the anterior nervous system in the onychophoran Euperipatoides rowelli. Light micrograph (a) and simplified diagram (b) of dissected brain and anterior nerve cords in ventral view. Anterior is up. Anteriormost post-oral commissures numbered (#1 to #5). at antennal tract, cc connecting cord (characterized by the absence of ring commissures), dc deutocerebrum, ey eye, ho hypocerebral organ, jn jaw nerve, L2 and L3 second and third lip papillae nerves; mc, median commissure, nc nerve cord, pc protocerebrum, pn1 and pn2 anterior and posterior pharyngeal nerves, rc ring commissure, sn slime papilla nerves. Scale bar (in a) 200 µm

Mentions: Dissected portions of the anterior nervous system of E. rowelli show that the arrangement of the five anteriormost median commissures differs from that of the remaining commissures connecting the two nerve cords of the trunk (Fig. 2a, b). The first commissure links the two ring commissure-free connecting cords at a distance of about one-third between the slime papilla and the jaw nerves. This prominent commissure is longer and thicker than the remaining post-oral commissures, from which it is segregated by a wider gap. The first post-oral commissure forms a ventral loop around the pharynx and is attached to the ventral pharyngeal wall by thin tissue fibers so that this commissure usually has to be dissected from the pharynx during preparation. The commissures #2 to #5 link the nerve cords at the level of the third lip papillae nerve and the slime papillae nerves (Fig. 2a, b). These commissures lie closer to each other than do the remaining median commissures of the trunk.Fig. 2


Insights into the segmental identity of post-oral commissures and pharyngeal nerves in Onychophora based on retrograde fills.

Martin C, Mayer G - BMC Neurosci (2015)

Anatomy of the anterior nervous system in the onychophoran Euperipatoides rowelli. Light micrograph (a) and simplified diagram (b) of dissected brain and anterior nerve cords in ventral view. Anterior is up. Anteriormost post-oral commissures numbered (#1 to #5). at antennal tract, cc connecting cord (characterized by the absence of ring commissures), dc deutocerebrum, ey eye, ho hypocerebral organ, jn jaw nerve, L2 and L3 second and third lip papillae nerves; mc, median commissure, nc nerve cord, pc protocerebrum, pn1 and pn2 anterior and posterior pharyngeal nerves, rc ring commissure, sn slime papilla nerves. Scale bar (in a) 200 µm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4549126&req=5

Fig2: Anatomy of the anterior nervous system in the onychophoran Euperipatoides rowelli. Light micrograph (a) and simplified diagram (b) of dissected brain and anterior nerve cords in ventral view. Anterior is up. Anteriormost post-oral commissures numbered (#1 to #5). at antennal tract, cc connecting cord (characterized by the absence of ring commissures), dc deutocerebrum, ey eye, ho hypocerebral organ, jn jaw nerve, L2 and L3 second and third lip papillae nerves; mc, median commissure, nc nerve cord, pc protocerebrum, pn1 and pn2 anterior and posterior pharyngeal nerves, rc ring commissure, sn slime papilla nerves. Scale bar (in a) 200 µm
Mentions: Dissected portions of the anterior nervous system of E. rowelli show that the arrangement of the five anteriormost median commissures differs from that of the remaining commissures connecting the two nerve cords of the trunk (Fig. 2a, b). The first commissure links the two ring commissure-free connecting cords at a distance of about one-third between the slime papilla and the jaw nerves. This prominent commissure is longer and thicker than the remaining post-oral commissures, from which it is segregated by a wider gap. The first post-oral commissure forms a ventral loop around the pharynx and is attached to the ventral pharyngeal wall by thin tissue fibers so that this commissure usually has to be dissected from the pharynx during preparation. The commissures #2 to #5 link the nerve cords at the level of the third lip papillae nerve and the slime papillae nerves (Fig. 2a, b). These commissures lie closer to each other than do the remaining median commissures of the trunk.Fig. 2

Bottom Line: Our fills of post-oral commissures in E. rowelli revealed a graded arrangement of anteriorly shifted somata associated with post-oral commissures #1 to #5.The number of deutocerebral somata associated with each commissure decreases posteriorly, i.e., commissure #1 shows the highest and commissure #5 the lowest numbers of associated somata, whereas none of the subsequent median commissures, beginning with commissure #6, shows somata located in the deutocerebrum.Based on the graded and shifted arrangement of somata associated with the anteriormost post-oral commissures, we suggest that the onychophoran brain, which is a bipartite syncerebrum, might have evolved by a successive anterior/anterodorsal migration of neurons towards the protocerebrum in the last onychophoran ancestor.

View Article: PubMed Central - PubMed

Affiliation: Animal Evolution and Development, Institute of Biology, University of Leipzig, Talstraße 33, 04103, Leipzig, Germany. christine.martin@uni-leipzig.de.

ABSTRACT

Background: While the tripartite brain of arthropods is believed to have evolved by a fusion of initially separate ganglia, the evolutionary origin of the bipartite brain of onychophorans-one of the closest arthropod relatives-remains obscure. Clarifying the segmental identity of post-oral commissures and pharyngeal nerves might provide useful insights into the evolution of the onychophoran brain. We therefore performed retrograde fills of these commissures and nerves in the onychophoran Euperipatoides rowelli.

Results: Our fills of the anterior and posterior pharyngeal nerves revealed groups of somata that are mainly associated with the deutocerebrum. This resembles the innervation pattern of other feeding structures in Onychophora, including the jaws and several lip papillae surrounding the mouth. Our fills of post-oral commissures in E. rowelli revealed a graded arrangement of anteriorly shifted somata associated with post-oral commissures #1 to #5. The number of deutocerebral somata associated with each commissure decreases posteriorly, i.e., commissure #1 shows the highest and commissure #5 the lowest numbers of associated somata, whereas none of the subsequent median commissures, beginning with commissure #6, shows somata located in the deutocerebrum.

Conclusions: Based on the graded and shifted arrangement of somata associated with the anteriormost post-oral commissures, we suggest that the onychophoran brain, which is a bipartite syncerebrum, might have evolved by a successive anterior/anterodorsal migration of neurons towards the protocerebrum in the last onychophoran ancestor. This implies that the composite brain of onychophorans and the compound brain of arthropods might have independent evolutionary origins, as in contrast to arthropods the onychophoran syncerebrum is unlikely to have evolved by a fusion of initially separate ganglia.

No MeSH data available.


Related in: MedlinePlus