Comparison of neuromuscular development in two dinophilid species (Annelida) suggests progenetic origin of Dinophilus gyrociliatus

Abstract

BackgroundSeveral independent meiofaunal lineages are suggested to have originated through progenesis, however, morphological support for this heterochronous process is still lacking. Progenesis is defined as an arrest of somatic development (synchronously in various organ systems) due to early maturation, resulting in adults resembling larvae or juveniles of the ancestors. Accordingly, we established a detailed neuromuscular developmental atlas of two closely related Dinophilidae using immunohistochemistry and CLSM. This allows us to test for progenesis, questioning whether i) the adult smaller, dimorphic Dinophilus gyrociliatus resembles a younger developmental stage of the larger, monomorphic D. taeniatus and whether ii) dwarf males of D. gyrociliatus resemble an early developmental stage of D. gyrociliatus females.ResultsBoth species form longitudinal muscle bundles first, followed by circular muscles, creating a grid of body wall musculature, which is the densest in adult D. taeniatus, while the architecture in adult female D. gyrociliatus resembles that of prehatching D. taeniatus. Both species display a subepidermal ganglionated nervous system with an anterior dorsal brain and five longitudinal ventral nerve bundles with six sets of segmental commissures (associated with paired ganglia). Neural differentiation of D. taeniatus and female D. gyrociliatus commissures occurs before hatching: both species start out forming one transverse neurite bundle per segment, which are thereafter joined by additional thin bundles. Whereas D. gyrociliatus arrests its development at this stage, adult D. taeniatus condenses the thin commissures again into one thick commissural bundle per segment. Generally, D. taeniatus adults demonstrate a seemingly more organized (= segmental) pattern of serotonin-like and FMRFamide-like immunoreactive elements. The dwarf male of D. gyrociliatus displays a highly aberrant neuromuscular system, showing no close resemblance to any early developmental stage of female Dinophilus, although the onset of muscular development mirrors the early myogenesis in females.ConclusionThe apparent synchronous arrest of nervous and muscular development in adult female D. gyrociliatus, resembling the prehatching stage of D. taeniatus, suggests that D. gyrociliatus have originated through progenesis. The synchrony in arrest of three organ systems, which show opposing reduction and addition of elements, presents one of the morphologically best-argued cases of progenesis within Spiralia.

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.…”

“…These subregions of the brain include cells with common function to either directly process sensory input or serve as higher organization/integration centers (Uyeno & Kier, ; Williamson & Chrachri, ). Many small annelids, however, have seemingly uniform brains without any obvious ganglionic substructure (Müller & Westheide, ; Worsaae & Rouse, ; Meyer & Seaver, ; Kerbl et al, ). This raises the question of whether (and how) these brains are regionalized and whether neurons are multifunctional and thereby less specific for individual neurotransmitters.…”

“…The nervous systems of all species, but especially of D. gyrociliatus , have been studied previously (Kotikova, ; Windoffer & Westheide, ; Beniash, Yerlikova, & Yevdonin, ; Müller & Westheide, ; Fofanova & Voronezhskaya, ; Fofanova, Nezlin, & Voronezhskaya, ). Furthermore, the recently created detailed atlas of neuromuscular development in two Dinophilus ‐species (Kerbl et al, ) provides the foundation for a detailed comparative analysis of neurotransmitter patterns in this taxon. Dinophilidae therefore offer a comprehensive system to investigate (a) conservation versus variation of immunoreactivity patterns of specific neurotransmitters and (b) possible compartmentalization and/or functional regionalization of a superficially uniform brain.…”

Two new meiofaunal species of Trilobodrilus (Dinophilidae, Annelida) from California, USA

“…No species of Trilobodrilus exhibits sexual dimorphism as known from D. gyrociliatus O. Schmidt, 1848 and some other Dinophilus species (Schmidt 1858;Repiachoff 1886;Jones & Ferguson 1957;Fofanova et al 2014;Kerbl et al 2016). Trilobodrilus axi Westheide, 1967 andT.…”

“…All dinophilids are found in interstitial habitats of shallow marine waters in medium to coarse sand or shell gravel. Some species may also be found on biofilm of macroalgae in littoral marine regions (Harmer 1889;Jägersten 1944Jägersten , 1951Kerbl et al 2016).…”