Comparative myoanatomy of Echinoderes (Kinorhyncha): a comprehensive investigation by CLSM and 3D reconstruction

Abstract

IntroductionKinorhyncha is a clade of marine invertebrate meiofauna. Their body plan includes a retractable introvert bearing rings of cuticular spines, and a limbless trunk with distinct segmentation of nervous, muscular and epidermal organ systems. As derived members within the basal branch of Ecdysozoa, kinorhynchs may provide an important example of convergence on the evolution of segmentation within one of three bilaterian superclades. We describe the myoanatomy of Echinoderes, the most specious kinorhynch genus, and build upon historical studies of kinorhynch ultrastructure and gross morphology. This is the first multi-species comparison of a complete organ system by confocal microscopy and three-dimensional reconstruction within Kinorhyncha.ResultsMyoanatomy of adult Echinoderes is composed of the following: Head with two mouth cone circular muscles, nine pairs of oral style muscles, ten introvert retractors, one introvert circular muscle, and fourteen introvert circular muscle retractors; Neck with one circular muscle; Trunk showing distinct pairs of ventral and dorsal muscles within segments 1–10, dorsoventral muscles within segments 3–10, diagonal muscles within segments 1–8, longitudinal fibers spanning segments 1–9, three pairs of terminal spine muscles, and one pair of male penile spine muscles; Gut showing a pharynx with ten alternating rings of radial and circular muscle fibers enclosed in a complex sheath of protractors and retractors, an orthogonal grid of longitudinal and circular fibers surrounding the intestine, and paired hindgut dilators.ConclusionsMyoanatomy is highly conserved between species of Echinoderes. Interspecific variation is observed in the arrangement and number of introvert fibers and the composition of pharyngeal muscles. Segmented trunk musculature facilitates the movements of articulated cuticular plates along the anterior-posterior axis. Intersegmental muscle fibers assist with dorsoventral and lateral trunk movements. Protractors, retractors and circular muscles coordinate eversion and retraction of the introvert and mouth cone, and relocation of the pharynx during locomotion and feeding behaviors. Pairs of posterior fibers suggest independent movements of terminal spines, and male penile spines. Within Scalidophora, myoanatomy is more similar between Kinorhyncha and Loricifera, than either group is to Priapulida. Kinorhynch myoanatomy may reflect a convergent transition from vermiform to segmented body plans during the early radiation of Ecdysozoa.

The neuromuscular system of Pycnophyes kielensis (Kinorhyncha: Allomalorhagida) investigated by confocal laser scanning microscopy

“…The system is moved by muscles attached to the pharyngeal bulb and probably also by a synchronous contraction of the dorsoventral trunk musculature which builds up pressure [9, 14]. The use of internal pressure, caused by contraction of the dorsoventral musculature to push the introvert out is very likely, as neither the pharyngeal bulb protractors nor the pharyngeal bulb retractors of P. kielensis appear very strong.…”

“…The musculature in kinorhynchs has previously been studied using confocal laser scanning microscopy for five cyclorhagid species of the genus Echinoderes , Antygomonas sp., and Pycnophyes kielensis [14, 35–37]. Many of the described muscles are similar among species.…”

“…Kinorhynchs use their introvert to move in between sand grains on the sea floor and to feed on bacteria [12, 13]. The musculature and nervous system of members of the cyclorhagid kinorhynch genus Echinoderes have been investigated previously [14, 15]. These studies found a combination of segmented and unsegmented features in the myoanatomy and nervous system of kinorhynchs.…”

“…Using immunostainings and confocal laser scanning microscopy, musculature has already been studied in the cyclorhagids Antygomonas sp. and members of Echinoderes [14, 37]. …”

First account on kinorhynchs from Portugal, with the description of two new species: Echinoderes lusitanicus sp. nov. and E. reicherti sp. nov.

“…Bianchelli et al 2010). More recently, Echinoderes dujardinii Claparède, 1863, Echinoderes hispanicus Pardos et al 1998 and a third undescribed species of Echinoderes from the Algarve, the southernmost region of Portugal, were used in a comparative study on the myoanatomy of this genus (Herranz et al 2014a). However, any attempt to identify or describe new species of kinorhynchs from Portugal has never been carried out.…”