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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

Simplified diagrams summarizing the results of retrograde fills of commissures #1 to #6 in Euperipatoides rowelli. Anterior is up. Syringes point to the corresponding fill sites. a–f  Note the diminishing number of somata within the deutocerebrum and a decreasing shift in position of somata within the connecting cords from anterior to posterior (commissure #6 is the first post-oral commissure that shows no anterior shift in position of the associated somata). at antennal tract, cc connecting cord, dc deutocerebrum, ey eye, jn jaw nerve, nc ventral nerve cord, pc protocerebrum, sn slime papilla nerves
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Fig8: Simplified diagrams summarizing the results of retrograde fills of commissures #1 to #6 in Euperipatoides rowelli. Anterior is up. Syringes point to the corresponding fill sites. a–f  Note the diminishing number of somata within the deutocerebrum and a decreasing shift in position of somata within the connecting cords from anterior to posterior (commissure #6 is the first post-oral commissure that shows no anterior shift in position of the associated somata). at antennal tract, cc connecting cord, dc deutocerebrum, ey eye, jn jaw nerve, nc ventral nerve cord, pc protocerebrum, sn slime papilla nerves

Mentions: Our fills of trunk commissures revealed that their supplying neurons are grouped around each commissural basis. This holds true for all median commissures of the trunk, including commissure #6 (Fig. 8f). In contrast, post-oral commissures #1 to #5 display numerous anteriorly shifted somata, some of which clearly lie within the deutocerebrum (Fig. 8a–e). The anteriorly shifted position of somata makes it difficult to assign each post-oral commissure to a particular head segment. However, the position of somata within the deutocerebrum as well as in portions of nerve cords supplying the slime papillae suggests that commissures #2 to #5 receive fibers from both the second (jaw) and the third (slime papilla) segments (Fig. 8b–e). This pattern resembles the innervation of the first post-oral commissure in various arthropods, which contains both deutocerebral and tritocerebral fibers [1, 22–26] (Fig. 9a, b).Fig. 8


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)

Simplified diagrams summarizing the results of retrograde fills of commissures #1 to #6 in Euperipatoides rowelli. Anterior is up. Syringes point to the corresponding fill sites. a–f  Note the diminishing number of somata within the deutocerebrum and a decreasing shift in position of somata within the connecting cords from anterior to posterior (commissure #6 is the first post-oral commissure that shows no anterior shift in position of the associated somata). at antennal tract, cc connecting cord, dc deutocerebrum, ey eye, jn jaw nerve, nc ventral nerve cord, pc protocerebrum, sn slime papilla nerves
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig8: Simplified diagrams summarizing the results of retrograde fills of commissures #1 to #6 in Euperipatoides rowelli. Anterior is up. Syringes point to the corresponding fill sites. a–f  Note the diminishing number of somata within the deutocerebrum and a decreasing shift in position of somata within the connecting cords from anterior to posterior (commissure #6 is the first post-oral commissure that shows no anterior shift in position of the associated somata). at antennal tract, cc connecting cord, dc deutocerebrum, ey eye, jn jaw nerve, nc ventral nerve cord, pc protocerebrum, sn slime papilla nerves
Mentions: Our fills of trunk commissures revealed that their supplying neurons are grouped around each commissural basis. This holds true for all median commissures of the trunk, including commissure #6 (Fig. 8f). In contrast, post-oral commissures #1 to #5 display numerous anteriorly shifted somata, some of which clearly lie within the deutocerebrum (Fig. 8a–e). The anteriorly shifted position of somata makes it difficult to assign each post-oral commissure to a particular head segment. However, the position of somata within the deutocerebrum as well as in portions of nerve cords supplying the slime papillae suggests that commissures #2 to #5 receive fibers from both the second (jaw) and the third (slime papilla) segments (Fig. 8b–e). This pattern resembles the innervation of the first post-oral commissure in various arthropods, which contains both deutocerebral and tritocerebral fibers [1, 22–26] (Fig. 9a, b).Fig. 8

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