Assessing segmental versus non-segmental features in the ventral nervous system of onychophorans (velvet worms)

Abstract

BackgroundDue to their phylogenetic position as one of the closest arthropod relatives, studies of the organisation of the nervous system in onychophorans play a key role for understanding the evolution of body segmentation in arthropods. Previous studies revealed that, in contrast to the arthropods, segmentally repeated ganglia are not present within the onychophoran ventral nerve cords, suggesting that segmentation is either reduced or might be incomplete in the onychophoran ventral nervous system.ResultsTo assess segmental versus non-segmental features in the ventral nervous system of onychophorans, we screened the nerve cords for various markers, including synapsin, serotonin, gamma-aminobutyric acid, RFamide, dopamine, tyramine and octopamine. In addition, we performed retrograde fills of serially repeated commissures and leg nerves to localise the position of neuronal somata supplying those. Our data revealed a mixture of segmental and non-segmental elements within the onychophoran nervous system.ConclusionsWe suggest that the segmental ganglia of arthropods evolved by a gradual condensation of subsets of neurons either in the arthropod or the arthropod-tardigrade lineage. These findings are in line with the hypothesis of gradual evolution of segmentation in panarthropods and thus contradict a loss of ancestral segmentation within the onychophoran lineage.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0853-3) contains supplementary material, which is available to authorized users.

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

“…Although first mentioned in the 19 th century (Guilding 1826), onychophorans aroused the interest of evolutionary biologists partly due to their status as one of the closest relatives of arthropods. Their far larger body size compared to tardigrades facilitates their examination, thus leading to many more studies, including detailed investigations of their nervous system (Balfour 1883;Sedgwick 1885;von Kennel 1888;Evans 1901;Holmgren 1916;Hanström 1928;Fedorow 1929;Hanström 1935;Henry 1948;Pflugfelder 1948;Schürmann and Sandeman 1976;Schürmann 1987Schürmann , 1995Eriksson and Budd 2000;Eriksson et al 2003;Strausfeld et al 2006aStrausfeld et al , 2006bHarzsch 2007, 2008;Whitington 2007;Mayer and Whitington 2008;Mayer et al 2010Mayer et al , 2013aMayer et al , 2014Mayer et al , 2015bWhitington and Mayer 2011;Mayer 2014, 2015;Mayer et al 2015b;Mayer 2016;Schumann et al 2016;Martin et al 2017). The onychophoran nervous system consists of an anterior dorsal brain that proceeds into a paired ventral nerve cord ( Fig.…”

“…The two widely separated nerve cords span fairly uniformly throughout the length of the body. Thus a division into ganglia and somata-free connectives is completely lacking, as both neuropil and a perikaryal layer are present throughout the entire nerve cords (Mayer and Harzsch 2007;Mayer 2016;Martin et al 2017).…”

“…Nonetheless, the nerve cords show slight swellings that are segmentally arranged and occur at the same level as the leg pairs (Balfour 1883; Sedgwick 1895; Schürmann 1995; Mayer and Harzsch 2007;Martin et al 2017), in contrast to the anterior shift exhibited by the ganglia of tardigrades and arthropods. These swellings bear the most prominent, segmentally arranged nerves -the paired leg nerves.…”

“…Previous attempts to resolve this were based on a wide range of experimental approaches ranging from molecular phylogenetics to comparative morphology of living and fossil specimens (e.g., Poinar 2000;Hou et al 2004;Strausfeld et al 2006aStrausfeld et al , 2016Harzsch 2007, 2008;Zantke et al 2008;Campbell et al 2011;Legg et al 2012;Ou et al 2012;Persson et al 2012Persson et al , 2014Mayer et al 2013aMayer et al , 2013bMayer et al , 2015bRota-Stabelli et al 2013;Cong et al 2014;Smith and Ortega-Hernández 2014;Boothby et al 2015;Arakawa 2016;Bemm et al 2016;Hashimoto et al 2016;Hering et al 2016;Koutsovoulos et al 2016;Oliveira et al 2016;Martin et al 2017;Ortega-Hernández et al in press). Nevertheless, even despite the recent surge in molecular phylogenetic analyses on many animal groups, thus far these methods have retrieved inconclusive results for clarifying the affinities among panarthropods.…”

Evaluation of contrasting techniques for X‐ray imaging of velvet worms (Onychophora)

“…However, we believe that this situation may be improved in the near future, when specific markers similar to antibody staining used for fluorescent and confocal microscopy (e.g. Mayer & Whitington, ; Martin et al ., ) or gold nanoparticle labelling used for transmission electron microscopy and nanomedicine (Mayhew et al ., ; Cole et al ., ) also become available for SR‐CT imaging. Meanwhile, the results presented herein may be helpful for onychophorologists who apply CT techniques in their research.…”