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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

Segmental identity of cephalic appendages and head development in onychophorans. a Simplified diagram of the innervation of segmental cephalic appendages. Body segments, each carrying a pair of appendages, are numbered. b–e Head development in embryos of subsequent developmental stages in the onychophoran Euperipatoides rowelli. The jaws are highlighted artificially in yellow. Modified from Ou et al. [15]. an antenna, cc connecting cord, dc deutocerebrum, ey eye, jw jaw, le1 and le2 first and second legs, lp lip papillae, mc median commissure, nc nerve cord, pc protocerebrum, st stomodeum, sp slime papilla. Scale bars (in b–e) 200 µm
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Fig1: Segmental identity of cephalic appendages and head development in onychophorans. a Simplified diagram of the innervation of segmental cephalic appendages. Body segments, each carrying a pair of appendages, are numbered. b–e Head development in embryos of subsequent developmental stages in the onychophoran Euperipatoides rowelli. The jaws are highlighted artificially in yellow. Modified from Ou et al. [15]. an antenna, cc connecting cord, dc deutocerebrum, ey eye, jw jaw, le1 and le2 first and second legs, lp lip papillae, mc median commissure, nc nerve cord, pc protocerebrum, st stomodeum, sp slime papilla. Scale bars (in b–e) 200 µm

Mentions: The typical arthropod brain is composed of three segmental regions: the protocerebrum, deutocerebrum, and tritocerebrum [1–6]. In contrast, the brain of one of the closest arthropod relatives, the Onychophora (velvet worms), contains only two segmental regions corresponding to the arthropod proto- and deutocerebrum [7, 8]. Alternative hypotheses suppose a tripartite onychophoran brain [9] but are based on a misinterpretation of the onychophoran neuroanatomy, as the authors mistook the jaw nerve for the slime papilla nerve. Furthermore, a recent study [10] proposes that the onychophoran brain is a monopartite structure based on engrailed mRNA expression [11, 12], a method that is not suitable for addressing brain segmentation, as the anterior engrailed stripe is on the non-neuroectodermal side [13]. Despite the lack of a distinct border delineating these two brain regions, the protocerebrum of onychophorans contains the central body and the mushroom bodies and innervates the antennae and eyes, whereas the deutocerebrum is defined by the position of neuronal somata supplying the appendages of the second body segment, i.e., the jaws [7, 8, 14] (Fig. 1a). The onychophoran jaws are the only appendages that become incorporated into the definitive mouth cavity during embryonic development [14, 15] (Fig. 1b–e). In contrast to the antennae and jaws, the third pair of cephalic appendages of onychophorans, the slime papillae, is not innervated by the brain but rather by the anterior portions of the ventral nerve cords [7, 8, 16] (Fig. 1a).Fig. 1


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)

Segmental identity of cephalic appendages and head development in onychophorans. a Simplified diagram of the innervation of segmental cephalic appendages. Body segments, each carrying a pair of appendages, are numbered. b–e Head development in embryos of subsequent developmental stages in the onychophoran Euperipatoides rowelli. The jaws are highlighted artificially in yellow. Modified from Ou et al. [15]. an antenna, cc connecting cord, dc deutocerebrum, ey eye, jw jaw, le1 and le2 first and second legs, lp lip papillae, mc median commissure, nc nerve cord, pc protocerebrum, st stomodeum, sp slime papilla. Scale bars (in b–e) 200 µm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Segmental identity of cephalic appendages and head development in onychophorans. a Simplified diagram of the innervation of segmental cephalic appendages. Body segments, each carrying a pair of appendages, are numbered. b–e Head development in embryos of subsequent developmental stages in the onychophoran Euperipatoides rowelli. The jaws are highlighted artificially in yellow. Modified from Ou et al. [15]. an antenna, cc connecting cord, dc deutocerebrum, ey eye, jw jaw, le1 and le2 first and second legs, lp lip papillae, mc median commissure, nc nerve cord, pc protocerebrum, st stomodeum, sp slime papilla. Scale bars (in b–e) 200 µm
Mentions: The typical arthropod brain is composed of three segmental regions: the protocerebrum, deutocerebrum, and tritocerebrum [1–6]. In contrast, the brain of one of the closest arthropod relatives, the Onychophora (velvet worms), contains only two segmental regions corresponding to the arthropod proto- and deutocerebrum [7, 8]. Alternative hypotheses suppose a tripartite onychophoran brain [9] but are based on a misinterpretation of the onychophoran neuroanatomy, as the authors mistook the jaw nerve for the slime papilla nerve. Furthermore, a recent study [10] proposes that the onychophoran brain is a monopartite structure based on engrailed mRNA expression [11, 12], a method that is not suitable for addressing brain segmentation, as the anterior engrailed stripe is on the non-neuroectodermal side [13]. Despite the lack of a distinct border delineating these two brain regions, the protocerebrum of onychophorans contains the central body and the mushroom bodies and innervates the antennae and eyes, whereas the deutocerebrum is defined by the position of neuronal somata supplying the appendages of the second body segment, i.e., the jaws [7, 8, 14] (Fig. 1a). The onychophoran jaws are the only appendages that become incorporated into the definitive mouth cavity during embryonic development [14, 15] (Fig. 1b–e). In contrast to the antennae and jaws, the third pair of cephalic appendages of onychophorans, the slime papillae, is not innervated by the brain but rather by the anterior portions of the ventral nerve cords [7, 8, 16] (Fig. 1a).Fig. 1

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