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Serotonin-immunoreactivity in the ventral nerve cord of Pycnogonida--support for individually identifiable neurons as ancestral feature of the arthropod nervous system.

Brenneis G, Scholtz G - BMC Evol. Biol. (2015)

Bottom Line: They can be clearly homologized across different ganglia and different specimens as well as across the three species.By contrast, overall similarities between the pycnogonid and myriapod patterns may be indicative of single cell homologies in these two taxa.This notion awaits further substantiation from future studies.

View Article: PubMed Central - PubMed

Affiliation: Humboldt-Universität zu Berlin, Institut für Biologie/Vergleichende Zoologie, Philippstraße 13, 10115, Berlin, Germany. georg.brenneis@gmx.de.

ABSTRACT

Background: The arthropod ventral nerve cord features a comparably low number of serotonin-immunoreactive neurons, occurring in segmentally repeated arrays. In different crustaceans and hexapods, these neurons have been individually identified and even inter-specifically homologized, based on their soma positions and neurite morphologies. Stereotypic sets of serotonin-immunoreactive neurons are also present in myriapods, whereas in the investigated chelicerates segmental neuron clusters with higher and variable cell numbers have been reported. This led to the suggestion that individually identifiable serotonin-immunoreactive neurons are an apomorphic feature of the Mandibulata. To test the validity of this neurophylogenetic hypothesis, we studied serotonin-immunoreactivity in three species of Pycnogonida (sea spiders). This group of marine arthropods is nowadays most plausibly resolved as sister group to all other extant chelicerates, rendering its investigation crucial for a reliable reconstruction of arthropod nervous system evolution.

Results: In all three investigated pycnogonids, the ventral walking leg ganglia contain different types of serotonin-immunoreactive neurons, the somata of which occurring mostly singly or in pairs within the ganglionic cortex. Several of these neurons are readily and consistently identifiable due to their stereotypic soma position and characteristic neurite morphology. They can be clearly homologized across different ganglia and different specimens as well as across the three species. Based on these homologous neurons, we reconstruct for their last common ancestor (presumably the pycnogonid stem species) a minimal repertoire of at least seven identified serotonin-immunoreactive neurons per hemiganglion. Beyond that, each studied species features specific pattern variations, which include also some neurons that were not reliably labeled in all specimens.

Conclusions: Our results unequivocally demonstrate the presence of individually identifiable serotonin-immunoreactive neurons in the pycnogonid ventral nerve cord. Accordingly, the validity of this neuroanatomical feature as apomorphy of Mandibulata is questioned and we suggest it to be ancestral for arthropods instead. The pronounced disparities between the segmental pattern in pycnogonids and the one of studied euchelicerates call for denser sampling within the latter taxon. By contrast, overall similarities between the pycnogonid and myriapod patterns may be indicative of single cell homologies in these two taxa. This notion awaits further substantiation from future studies.

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Comparison of ALNs and PLNs in WLG2 of the investigated pycnogonids. SLI signal shown in inverted b/w images for better contrast. One hemiganglion shown, the midline region is located towards the right. In order to reveal as many details of the neurites as possible, clipping planes have been applied to Imaris volumes. Images to the left (a-c) depict ganglion regions further ventral than corresponding images to the right (a’-c’). Red asterisks highlight ALN somata, red arrowheads illustrate the course of the primary neurite of one of the ALNs. Corresponding blue markings have been applied to the PLNs. Stars and black asterisks mark signal-free regions of elongate and ovoid glomerulus-like neuropils, respectively. a,a’: P. litorale. Note the high number of ALNs, the somata of which being spread out in a loose cluster-like array from ventral to dorsal. b,b’: Meridionale sp. The second PLN with comparable neurite course is not visible in the section shown in b. c,c’: C. japonicus
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Fig8: Comparison of ALNs and PLNs in WLG2 of the investigated pycnogonids. SLI signal shown in inverted b/w images for better contrast. One hemiganglion shown, the midline region is located towards the right. In order to reveal as many details of the neurites as possible, clipping planes have been applied to Imaris volumes. Images to the left (a-c) depict ganglion regions further ventral than corresponding images to the right (a’-c’). Red asterisks highlight ALN somata, red arrowheads illustrate the course of the primary neurite of one of the ALNs. Corresponding blue markings have been applied to the PLNs. Stars and black asterisks mark signal-free regions of elongate and ovoid glomerulus-like neuropils, respectively. a,a’: P. litorale. Note the high number of ALNs, the somata of which being spread out in a loose cluster-like array from ventral to dorsal. b,b’: Meridionale sp. The second PLN with comparable neurite course is not visible in the section shown in b. c,c’: C. japonicus

Mentions: Each walking leg hemiganglion contains a dense meshwork of SL-ir dendritic arborizations and axon collaterals that extends almost through its entire neuropilar core (Figs. 1d-f; 3b; 4; 5; see also Additional files 1, 2 and 3). This SL-ir meshwork engulfs also the elongate and ovoid GLNs of the ventral lobe. However, while it penetrates into their outer layers, the inner cores of the GLNs are almost devoid of signal. (Fig. 3b; see also Fig. 8a,a’,c). In the midline region, an unpaired antero-posteriorly elongated SL-ir domain is recognizable, being laterally defined by some of the longitudinal tracts that pass through the ganglionic neuropil (e.g. Figs. 4; 6b-c’; Additional file 4). Especially in P. litorale, this median domain has distinct transverse extensions, which connect it with the SL-ir domains in the hemiganglia (Figs. 4a; 5a,a’; 7a; Additional file 1). To all appearances, these transverse extensions are predominantly of neuropilar nature; they do not include any of the tubulin-positive commissural tracts, nor do they show any continuous SL-ir axonal projections within.Fig. 5


Serotonin-immunoreactivity in the ventral nerve cord of Pycnogonida--support for individually identifiable neurons as ancestral feature of the arthropod nervous system.

Brenneis G, Scholtz G - BMC Evol. Biol. (2015)

Comparison of ALNs and PLNs in WLG2 of the investigated pycnogonids. SLI signal shown in inverted b/w images for better contrast. One hemiganglion shown, the midline region is located towards the right. In order to reveal as many details of the neurites as possible, clipping planes have been applied to Imaris volumes. Images to the left (a-c) depict ganglion regions further ventral than corresponding images to the right (a’-c’). Red asterisks highlight ALN somata, red arrowheads illustrate the course of the primary neurite of one of the ALNs. Corresponding blue markings have been applied to the PLNs. Stars and black asterisks mark signal-free regions of elongate and ovoid glomerulus-like neuropils, respectively. a,a’: P. litorale. Note the high number of ALNs, the somata of which being spread out in a loose cluster-like array from ventral to dorsal. b,b’: Meridionale sp. The second PLN with comparable neurite course is not visible in the section shown in b. c,c’: C. japonicus
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4496856&req=5

Fig8: Comparison of ALNs and PLNs in WLG2 of the investigated pycnogonids. SLI signal shown in inverted b/w images for better contrast. One hemiganglion shown, the midline region is located towards the right. In order to reveal as many details of the neurites as possible, clipping planes have been applied to Imaris volumes. Images to the left (a-c) depict ganglion regions further ventral than corresponding images to the right (a’-c’). Red asterisks highlight ALN somata, red arrowheads illustrate the course of the primary neurite of one of the ALNs. Corresponding blue markings have been applied to the PLNs. Stars and black asterisks mark signal-free regions of elongate and ovoid glomerulus-like neuropils, respectively. a,a’: P. litorale. Note the high number of ALNs, the somata of which being spread out in a loose cluster-like array from ventral to dorsal. b,b’: Meridionale sp. The second PLN with comparable neurite course is not visible in the section shown in b. c,c’: C. japonicus
Mentions: Each walking leg hemiganglion contains a dense meshwork of SL-ir dendritic arborizations and axon collaterals that extends almost through its entire neuropilar core (Figs. 1d-f; 3b; 4; 5; see also Additional files 1, 2 and 3). This SL-ir meshwork engulfs also the elongate and ovoid GLNs of the ventral lobe. However, while it penetrates into their outer layers, the inner cores of the GLNs are almost devoid of signal. (Fig. 3b; see also Fig. 8a,a’,c). In the midline region, an unpaired antero-posteriorly elongated SL-ir domain is recognizable, being laterally defined by some of the longitudinal tracts that pass through the ganglionic neuropil (e.g. Figs. 4; 6b-c’; Additional file 4). Especially in P. litorale, this median domain has distinct transverse extensions, which connect it with the SL-ir domains in the hemiganglia (Figs. 4a; 5a,a’; 7a; Additional file 1). To all appearances, these transverse extensions are predominantly of neuropilar nature; they do not include any of the tubulin-positive commissural tracts, nor do they show any continuous SL-ir axonal projections within.Fig. 5

Bottom Line: They can be clearly homologized across different ganglia and different specimens as well as across the three species.By contrast, overall similarities between the pycnogonid and myriapod patterns may be indicative of single cell homologies in these two taxa.This notion awaits further substantiation from future studies.

View Article: PubMed Central - PubMed

Affiliation: Humboldt-Universität zu Berlin, Institut für Biologie/Vergleichende Zoologie, Philippstraße 13, 10115, Berlin, Germany. georg.brenneis@gmx.de.

ABSTRACT

Background: The arthropod ventral nerve cord features a comparably low number of serotonin-immunoreactive neurons, occurring in segmentally repeated arrays. In different crustaceans and hexapods, these neurons have been individually identified and even inter-specifically homologized, based on their soma positions and neurite morphologies. Stereotypic sets of serotonin-immunoreactive neurons are also present in myriapods, whereas in the investigated chelicerates segmental neuron clusters with higher and variable cell numbers have been reported. This led to the suggestion that individually identifiable serotonin-immunoreactive neurons are an apomorphic feature of the Mandibulata. To test the validity of this neurophylogenetic hypothesis, we studied serotonin-immunoreactivity in three species of Pycnogonida (sea spiders). This group of marine arthropods is nowadays most plausibly resolved as sister group to all other extant chelicerates, rendering its investigation crucial for a reliable reconstruction of arthropod nervous system evolution.

Results: In all three investigated pycnogonids, the ventral walking leg ganglia contain different types of serotonin-immunoreactive neurons, the somata of which occurring mostly singly or in pairs within the ganglionic cortex. Several of these neurons are readily and consistently identifiable due to their stereotypic soma position and characteristic neurite morphology. They can be clearly homologized across different ganglia and different specimens as well as across the three species. Based on these homologous neurons, we reconstruct for their last common ancestor (presumably the pycnogonid stem species) a minimal repertoire of at least seven identified serotonin-immunoreactive neurons per hemiganglion. Beyond that, each studied species features specific pattern variations, which include also some neurons that were not reliably labeled in all specimens.

Conclusions: Our results unequivocally demonstrate the presence of individually identifiable serotonin-immunoreactive neurons in the pycnogonid ventral nerve cord. Accordingly, the validity of this neuroanatomical feature as apomorphy of Mandibulata is questioned and we suggest it to be ancestral for arthropods instead. The pronounced disparities between the segmental pattern in pycnogonids and the one of studied euchelicerates call for denser sampling within the latter taxon. By contrast, overall similarities between the pycnogonid and myriapod patterns may be indicative of single cell homologies in these two taxa. This notion awaits further substantiation from future studies.

Show MeSH
Related in: MedlinePlus