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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

Localization of neuronal somata associated with the anterior and posterior pharyngeal nerves in Euperipatoides rowelli. Retrograde fills. Maximum projection confocal micrographs in dorsal view. Anterior is up. Syringes indicate the corresponding fill sites. a Fill of the first pharyngeal nerve showing two groups of somata (I and II) associated with the deutocerebrum. b Fill of the second pharyngeal nerve illustrating neuronal somata within the deutocerebrum as well as in the connecting cord. Arrowhead points to fibers terminating contralaterally. cc connecting cord, dc deutocerebrum. Scale bars 100 µm
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Fig6: Localization of neuronal somata associated with the anterior and posterior pharyngeal nerves in Euperipatoides rowelli. Retrograde fills. Maximum projection confocal micrographs in dorsal view. Anterior is up. Syringes indicate the corresponding fill sites. a Fill of the first pharyngeal nerve showing two groups of somata (I and II) associated with the deutocerebrum. b Fill of the second pharyngeal nerve illustrating neuronal somata within the deutocerebrum as well as in the connecting cord. Arrowhead points to fibers terminating contralaterally. cc connecting cord, dc deutocerebrum. Scale bars 100 µm

Mentions: Of the two pairs of nerves supplying the pharynx in E. rowelli, the anterior pair enters the brain ventrally, where it is associated with the anterior portion of the deutocerebrum (Figs. 2a, b, 6a). In contrast, the posterior pair of pharyngeal nerves is associated with the portions of the connecting cords anterior to the first post-oral commissure (Figs. 2a, b, 6b). Retrograde fills of the anterior pharyngeal nerve revealed ~60 somata located exclusively within the deutocerebrum in the same brain hemisphere, posterior to the basis of this nerve (Fig. 6a). There are two major groups of somata: those of group I (Fig. 6a) project their axons exclusively anteriorly, whereas the axons of group II (Fig. 6a) leave the somata posteriorly and are then reoriented anteriorly. In addition, there are a few somata that are located further anteriorly within the deutocerebrum (Fig. 6a). Some of the fibers associated with the anterior pharyngeal nerve extend further anteriorly in the protocerebrum as well as in the contralateral brain hemisphere, where they terminate.Fig. 6


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)

Localization of neuronal somata associated with the anterior and posterior pharyngeal nerves in Euperipatoides rowelli. Retrograde fills. Maximum projection confocal micrographs in dorsal view. Anterior is up. Syringes indicate the corresponding fill sites. a Fill of the first pharyngeal nerve showing two groups of somata (I and II) associated with the deutocerebrum. b Fill of the second pharyngeal nerve illustrating neuronal somata within the deutocerebrum as well as in the connecting cord. Arrowhead points to fibers terminating contralaterally. cc connecting cord, dc deutocerebrum. Scale bars 100 µm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig6: Localization of neuronal somata associated with the anterior and posterior pharyngeal nerves in Euperipatoides rowelli. Retrograde fills. Maximum projection confocal micrographs in dorsal view. Anterior is up. Syringes indicate the corresponding fill sites. a Fill of the first pharyngeal nerve showing two groups of somata (I and II) associated with the deutocerebrum. b Fill of the second pharyngeal nerve illustrating neuronal somata within the deutocerebrum as well as in the connecting cord. Arrowhead points to fibers terminating contralaterally. cc connecting cord, dc deutocerebrum. Scale bars 100 µm
Mentions: Of the two pairs of nerves supplying the pharynx in E. rowelli, the anterior pair enters the brain ventrally, where it is associated with the anterior portion of the deutocerebrum (Figs. 2a, b, 6a). In contrast, the posterior pair of pharyngeal nerves is associated with the portions of the connecting cords anterior to the first post-oral commissure (Figs. 2a, b, 6b). Retrograde fills of the anterior pharyngeal nerve revealed ~60 somata located exclusively within the deutocerebrum in the same brain hemisphere, posterior to the basis of this nerve (Fig. 6a). There are two major groups of somata: those of group I (Fig. 6a) project their axons exclusively anteriorly, whereas the axons of group II (Fig. 6a) leave the somata posteriorly and are then reoriented anteriorly. In addition, there are a few somata that are located further anteriorly within the deutocerebrum (Fig. 6a). Some of the fibers associated with the anterior pharyngeal nerve extend further anteriorly in the protocerebrum as well as in the contralateral brain hemisphere, where they terminate.Fig. 6

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