Distribution of serotonin in the trunk of Metaperipatus blainvillei (Onychophora, Peripatopsidae): Implications for the evolution of the nervous system in Arhropoda

Abstract

Onychophora ("velvet worms") are a key taxon in the discussion of arthropod phylogeny. Studies that analyze neuroanatomical characters against a phylogenetic background have recently provided new insights into this debate. However, to date only a few studies on nervous system organization, particularly in the trunk, are available in Onychophora. To close this gap and to compare the onychophoran nervous system with that of other bilaterians, we have analyzed the pattern of serotonin-like immunoreactivity in Metaperipatus blainvillei (Peripatopsidae). In addition to confirming previous histological observations, our experiments revealed many new aspects of nervous system organization in Onychophora. The serotonergic nervous system of M. blainvillei consists of five longitudinal nerve strands (the paired dorsolateral nerves, the heart nerve, and the paired ventral cords), which are interconnected at regular intervals by ring commissures as well as median commissures. The ring commissures are absent in the leg-bearing regions. In addition to the main nerve tracts, there are several extensive fiber networks innervating the integument, the nephridial organs, and the body musculature. The leg nerves and nephridial nerves represent the only strictly segmental neuronal structures. We conclude that the general architecture of the onychophoran nervous system in the trunk closely resembles the orthogonal organization that is present in various other groups of Bilateria, which suggests that the arthropod nervous system is derived from such an orthogonal pattern. This finding implies that the "rope ladder-like" nervous system may have arisen independently in Panarthropoda and Annelida and does not represent a synapomorphy of these groups.

Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda

“…S5 C and D). Alternatively, it is possible that the presence of numerous peripheral nerves in the VNC of C. kunmingensis and Onychophora is symplesiomorphic, as comparable structures are also found in the orthogonal CNS of Priapulida (31) and other protostomes (12,13,15). In any event, the postcephalic CNS of C. kunmingensis reveals a unique combination of neurological characters otherwise unknown in any extant group within Panarthropoda (Fig.…”

“…A major difference, however, is that the onychophoran postcephalic CNS is lateralized and lacks morphologically discrete segmental ganglia despite clearly having a segmented organization (SI Text). Although the proximal preservation of the peripheral nerves makes it uncertain whether the C. kunmingensis VNC possessed complete ring commissures like those in onychophorans (12)(13)(14), this feature could potentially add morphological support for the sister-group relationship between Euarthropoda and Onychophora suggested by molecular phylogenies (21,22). Among crown-group euarthropods, there are only a restricted number of intersegmental peripheral nerves emerging from the longitudinal connectives in the VNC of some pancrustaceans (1, 4, 5) (SI Text, Fig.…”

“…2 B-E) is recognized as an ancestral condition that persisted in derived members of upper stem-group Euarthropoda (SI Text). Among extant groups, homologs of the intersegmental peripheral nerves are expressed in both Priapulida (31) and Onychophora (12,13,15,29) but are otherwise greatly reduced in number or completely lost in crown-group Euarthropoda and Tardigrada, respectively (1,5,16,28) (Fig. S5); the secondary reduction/loss is recognized as a result of parallel evolution between these lineages.…”

Palaeontological and Molecular Evidence Linking Arthropods, Onychophorans, and other Ecdysozoa

“…Among these is reference to stem and crown groups, developed from a concept originally devised by the entomologist Willi Hennig. A crown group refers to all descendants of the most recent common ancestor of the (Zantke et al 2008), 6 segmented nephridia (Mayer 2006), 7 commissures in ventral nerve cord in segmental register/rope-ladder nervous system (Mayer and Harzsch 2007), 8 segmented neurons show a reaction to serotonin (Mayer and Harzsch 2008), 9 Pax protein has a pair-rule function (Gabriel and Goldstein 2007) extant members of a clade. Thus, referring to the cladogram in Fig.…”

Onychophora

“…The two widely separated nerve cords, linked together by numerous median commissures, instead have a medullary organization, with neuronal somata distributed along the entire length of each nerve cord Harzsch 2007 , 2008 ). Additional ring commissures interconnect the nerve cords with the two dorsolateral nerves and the dorsal heart nerve in an orthogonal fashion (Mayer and Harzsch 2008 ;Mayer and Whitington 2009a ;Whitington and Mayer 2011 ). Only the leg nerves and the nephridial nerves show a segmental arrangement.…”