Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny

Abstract

BackgroundThe organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.ResultsThe serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.DiscussionThe organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some “deuterostome-like” features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system

“…However, phoronid morphology and embryology have more in common with deuterostomes than protostomes [7,8]. For this reason, the affiliation of phoronids with the protostomian clade cannot be regarded as strictly established.…”

Larval nervous systems: true larval and precocious adult

“…There is much variation in the number and structure of the cells in the organ. A characteristic pattern of eight flask-shaped serotonergic cells, each with one cilium, is found in many species, but the number may increase during development, for example in the phoronid Phoronopsis (Temereva and Wanninger, 2012;Temereva and Tsitrin, 2014). Other types of serotonergic cells may also be present (Page, 2002).…”

Phoronida

“…Although a possible vestigial ventral nerve cord has been reported for Phoronopsis harmeri (Temereva 2012 ), the cytoarchitecture of these neural fi bers has very little in common with the ventral nerve cords of molluscan or annelid larvae in that phoronid larvae do not have centralized ventral nerve cords with repeated neuronal cell bodies along them Denes et al 2007 ;Meyer and Seaver 2009 ). Overall, there are several structural and neurochemical aspects of the larval nervous system that vary among species (Santagata and Zimmer 2002 ;Sonnleitner et al 2013 ;Temereva and Tsitrin 2014 ). However, it should be noted that some of this variation in the larval nervous system may be due to unrecognized cryptic speciation when comparing what are believed to be the same larval types from geographically distant populations.…”

“…Beyond the apical organ, signifi cant larval nerves include the main hood nerve and two dorsolateral nerves that run down into the collar (mesosome) region of the larval body and merge with the minor and major tentacle nerve rings. From these nerve rings, the larval tentacles (and sometimes the juvenile tentacle rudiments; Santagata and Zimmer 2002 ) are innervated on frontal and abfrontal sides (Hay-Schmidt 1989Lacalli 1990 ;Santagata 2002 ;Temereva and Wanninger 2012 ;Sonnleitner et al 2013 ;Temereva and Tsitrin 2014 ). Basiepithelial fi bers also project from these nerve rings through the larval trunk epithelium and merge with a telotrochal nerve ring at the posterior end of the larva (Hay-Schmidt 1990 ; Santagata and Zimmer 2002 ;Temereva and Wanninger 2012 ;Sonnleitner et al 2013 ).…”

“…Both conserved and derived features also comprise the larval nervous system among various phoronid species. The greatest concentration of neuronal cells in the larval nervous system is found in the apical organ, a U-shaped structure containing at least four different neuronal cell types, all of which send axonal fi bers into a central neuropil (Hay-Schmidt 1989Lacalli 1990 ;Santagata 2002 ;Temereva and Wanninger 2012 ;Sonnleitner et al 2013 ;Temereva and Tsitrin 2014 ). Cellular domains within the apical organ include groups of cells that express serotonin (Hay-Schmidt 1990 ;Santagata 2002 ;Temereva and Wanninger 2012 ;Sonnleitner et al 2013), catecholamines (Hay-Schmidt 1990Santagata 2002), FMRFamide (Hay-Schmidt 1990Sonnleitner et al 2013 ), and a cardioactive B-like peptide (Sonnleitner et al 2013 ).…”