Comparative muscular morphology in Archinemertea (Nemertea: Palaeonemertea)

Abstract

Knowledge on the detailed body plan in Palaeonemertea (a group putatively considered to retain ancestral character states within Nemertea) is essential in understanding the morphological evolution among not only nemerteans but also the rest of bilaterians in general; however, such information has been scanty in previous literature. In this study, we examined the body wall musculature, the position of the nervous system, and the musculature of the proboscis apparatus in 14 species of Archinemertea (a palaeonemertean clade comprised of Cephalotrichidae and Cephalotrichellidae) using confocal laser scanning microscopy with phalloidin labeling as well as classical Mallory’s trichrome staining. Unexpectedly, all the archinemerteans possessed a diagonal muscle layer lying directly ‘above’—instead of ‘below’, as usually found in most vermiform animals—the body wall outer circular muscle layer, a character state that has never been reported among Bilateria except for some acoels and proseriates. We speculate that the aberrant position of the outer diagonal muscle layer might have been actualized as a result of a flip-flop in a genetic regulatory circuit that controls the body wall muscular morphogenesis, which must have happened independently among the bilaterian evolution at least once in Acoela (Xenacoelomorpha), Proseriata (Platyhelminthes), and Archinemertea (Nemertea), respectively. Based on available phylogenetic data and the results from the present observation, we reconstructed the evolution of morphological characters within Archinemertea and its subclades. The outer diagonal muscle layer is likely a synapomorphy for Archinemertea (Cephalotrichidae + Cephalotrichellidae). Members of Balionemertes and Cephalotrichella possess some unique states for palaeonemerteans in muscular morphology (muscular strand associated with lateral nerve cord; longitudinal muscles between brain and extraganglionic tissue; proboscis with outer longitudinal muscle strands). We propose that muscle fibers embedded in lateral nerve cords, termed myofibrillae, in hoplo- and heteronemerteans are homologous with the body wall longitudinal muscles near the lateral nerves surrounded by circular muscles.