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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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Phylogenetic position of the last common ancestor of the three investigated pycnogonid species. Simplified phylograms of the two most comprehensive phylogenetic analyses of internal pycnogonid relationships (For simplicity, Nymphon floridanum, which renders Nymphonidae polyphyletic in Arango and Wheeler (2007), has been omitted). Depending on which hypothesis is favored, the last common ancestor (green arrows) of the three investigated species is the stem species of crown-group pycnogonids (Arango and Wheeler 2007, left side) or of all extant pycnogonids to the exclusion of Austrodecidae (Arabi et al. 2010, right side). The groups highlighted in green include the three species investigated in this study
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Fig10: Phylogenetic position of the last common ancestor of the three investigated pycnogonid species. Simplified phylograms of the two most comprehensive phylogenetic analyses of internal pycnogonid relationships (For simplicity, Nymphon floridanum, which renders Nymphonidae polyphyletic in Arango and Wheeler (2007), has been omitted). Depending on which hypothesis is favored, the last common ancestor (green arrows) of the three investigated species is the stem species of crown-group pycnogonids (Arango and Wheeler 2007, left side) or of all extant pycnogonids to the exclusion of Austrodecidae (Arabi et al. 2010, right side). The groups highlighted in green include the three species investigated in this study

Mentions: The discovery of considerable similarities in the SLI pattern of all three species leads to the question of the ancestral pattern of Pycnogonida. A handful of phylogenetic analyses performed mainly during the last decade have sought to resolve the internal phylogeny of extant pycnogonid taxa [63–67]. Yet, whereas some hypotheses based on earlier ideas (e.g. [68, 69]) could be clearly rejected, an uncontested stable pycnogonid phylogeny has still not emerged. For this reason, we here refrain from proposing any of the three species-specific SLI patterns to represent a more ancestral or derived state within crown-group pycnogonids. However, despite the lack of a reliable internal phylogeny, a comparison between the investigated species can nonetheless yield a provisional minimal SLI pattern for their last common ancestor, which may have been the stem species of crown-group pycnogonids (depending on which of the phylogenetic hypotheses is favored; see Fig. 10).Fig. 10


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)

Phylogenetic position of the last common ancestor of the three investigated pycnogonid species. Simplified phylograms of the two most comprehensive phylogenetic analyses of internal pycnogonid relationships (For simplicity, Nymphon floridanum, which renders Nymphonidae polyphyletic in Arango and Wheeler (2007), has been omitted). Depending on which hypothesis is favored, the last common ancestor (green arrows) of the three investigated species is the stem species of crown-group pycnogonids (Arango and Wheeler 2007, left side) or of all extant pycnogonids to the exclusion of Austrodecidae (Arabi et al. 2010, right side). The groups highlighted in green include the three species investigated in this study
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig10: Phylogenetic position of the last common ancestor of the three investigated pycnogonid species. Simplified phylograms of the two most comprehensive phylogenetic analyses of internal pycnogonid relationships (For simplicity, Nymphon floridanum, which renders Nymphonidae polyphyletic in Arango and Wheeler (2007), has been omitted). Depending on which hypothesis is favored, the last common ancestor (green arrows) of the three investigated species is the stem species of crown-group pycnogonids (Arango and Wheeler 2007, left side) or of all extant pycnogonids to the exclusion of Austrodecidae (Arabi et al. 2010, right side). The groups highlighted in green include the three species investigated in this study
Mentions: The discovery of considerable similarities in the SLI pattern of all three species leads to the question of the ancestral pattern of Pycnogonida. A handful of phylogenetic analyses performed mainly during the last decade have sought to resolve the internal phylogeny of extant pycnogonid taxa [63–67]. Yet, whereas some hypotheses based on earlier ideas (e.g. [68, 69]) could be clearly rejected, an uncontested stable pycnogonid phylogeny has still not emerged. For this reason, we here refrain from proposing any of the three species-specific SLI patterns to represent a more ancestral or derived state within crown-group pycnogonids. However, despite the lack of a reliable internal phylogeny, a comparison between the investigated species can nonetheless yield a provisional minimal SLI pattern for their last common ancestor, which may have been the stem species of crown-group pycnogonids (depending on which of the phylogenetic hypotheses is favored; see Fig. 10).Fig. 10

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