Neuromuscular study of early branching Diuronotus aspetos (Paucitubulatina) yields insights into the evolution of organs systems in Gastrotricha

Abstract

BackgroundDiuronotus is one of the most recently described genera of Paucitubulatina, one of the three major clades in Gastrotricha. Its morphology suggests that Diuronotus is an early branch of Paucitubulatina, making it a key taxon for understanding the evolution of this morphologically understudied group. Here we test its phylogenetic position employing molecular data, and provide detailed descriptions of the muscular, nervous, and ciliary systems of Diuronotus aspetos, using immunohistochemistry and confocal laser scanning microscopy.ResultsWe confirm the proposed position of D. aspetos within Muselliferidae, and find this family to be the sister group to Xenotrichulidae. The muscular system, revealed by F-actin staining, shows a simple, but unique organization of the trunk musculature with a reduction to three pairs of longitudinal muscles and addition of up to five pairs of dorso-ventral muscles, versus the six longitudinal and two dorso-ventral pairs found in most Paucitubulatina. Using acetylated α-tubulin immunoreactivity, we describe the pharynx in detail, including new nervous structures, two pairs of sensory cilia, and a unique canal system. The central nervous system, as revealed by immunohistochemistry, shows the general pattern of Gastrotricha having a bilobed brain and a pair of ventro-longitudinal nerve cords. However, in addition are found an anterior nerve ring, several anterior longitudinal nerves, and four ventral commissures (pharyngeal, trunk, pre-anal, and terminal). Two pairs of protonephridia are documented, while other Paucitubulatina have one. Moreover, the precise arrangement of multiciliated cells is unraveled, yielding a pattern of possibly systematic importance.ConclusionSeveral neural structures of Diuronotus resemble those found in Xenotrichula (Xenotrichulidae) and may constitute new apomorphies of Paucitubulatina, or even Gastrotricha. In order to test these new evolutionary hypotheses, comparable morphological data from other understudied gastrotrich branches and a better resolution of the basal nodes of the gastrotrich phylogeny are warranted. Nonetheless, the present study offers new insights into the evolution of organ systems and systematic importance of so-far neglected characters in Gastrotricha.

High diversity in neuropeptide immunoreactivity patterns among three closely related species of Dinophilidae (Annelida)

“…Studies on the annelid brain and major nerves conducted by serial sectioning and TEM‐studies go back several decades (Windoffer & Westheide, ; Purschke, ; Orrhage & Müller, ). The advancements in immunocytochemistry in combination with CLSM facilitated new neural descriptions in a broad range of invertebrates and has proven especially well‐suited for studies on microscopic representatives (e.g., meiofaunal taxa or temporary meiofauna such as embryos, larvae and juveniles of macroscopic species), where not only the nervous system but also its intricate relation to musculature and ciliated structures can be exposed (e.g., Hay‐Schmidt, ; Müller & Sterrer, ; Wanninger, Koop, Bromham, Noonan, & Degnan, ; McDougall, Chen, Shimeld, & Ferrier, ; Worsaae & Rouse, ; Nielsen & Worsaae, ; Worsaae & Rouse, ; Schwaha & Wanninger, ; Worsaae, Sterrer, Kaul‐Strehlow, Hay‐Schmidt, & Giribet, ; Kerbl, Bekkouche, Sterrer, & Worsaae, ; Schmidt‐Rhaesa, Harzsch, & Purschke, ; Bekkouche & Worsaae, ; ; Rimskaya‐Korsakova, Kristof, Malakhov, & Wanninger, ; Worsaae, Rimskaya‐Korsakova, & Rouse, ; Kerbl, Fofanova, Mayorova, Voronezhskaya, & Worsaae, ; Gasiorowski, Bekkouche, & Worsaae, ; Henne, Friedrich, Hammel, Sombke, & Schmidt‐Rhaesa, ; Henne, Sombke, & Schmidt‐Rhaesa, 2007b). Yet, few studies have taken advantage of the small‐sized meiofauna for studying the distribution of the numerous and proposedly highly conserved neuropeptides in adult nervous systems, using immunocytochemistry to identify putative morphological or functional regionalizations in their small and compact brain and nervous system.…”

Evolutionary Implications of the microRNA- and piRNA Complement of Lepidodermella squamata (Gastrotricha)

“…They show a direct development, and are bilaterally symmetric, with an acoelomate body, and worm-like body plan [5]. Most gastrotrich species have a commissural brain [6,7,8,9] and within the clade there is a large variety of reproductive strategies [5,10]. Interestingly, most gastrotrichs lack an ectodermal hindgut, and a specialized respiratory system has not been described [5].…”

Evolutionary implications of the microRNA- and piRNA complement of Lepidodermella squamata (Gastrotricha)

“…Most gastrotrich species have a commissural brain [6][7][8][9] and within the clade there is a large variety of reproductive strategies [5,10] . Interestingly, most gastrotrichs lack an ectodermal hindgut, and a specialized respiratory system has not been described [5] .…”

“…However, this Gastrotricha-Platyhelminthes clade is still controversial because there is no morphological apomorphy supporting the monophyly of the clade. Even though gastrotrichs and most flatworms ingest food with a simple pharynx [6,22,23] , this common alimentary strategy is not necessarily an autapomorphy of Gastrotricha and Platyhelminthes.…”