At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

Abstract

BackgroundGastropods are among the most diverse animal clades, and have successfully colonized special habitats such as the marine sand interstitial. Specialized meiofaunal snails and slugs are tiny and worm-shaped. They combine regressive features – argued to be due to progenetic tendencies – with convergent adaptations. Microscopic size and concerted convergences make morphological examination non-trivial and hamper phylogenetic reconstructions. The enigmatic turbellarian-like Rhodopemorpha are a small group that has puzzled systematists for over a century. A preliminary molecular framework places the group far closer to the root of Heterobranchia – one of the major gastropod groups – than previously suggested. The poorly known meiofaunal Helminthope psammobionta Salvini-Plawen, 1991 from Bermuda is the most worm-shaped free-living gastropod and shows apparently aberrant aspects of anatomy. Its study may give important clues to understand the evolution of rhodopemorphs among basal heterobranchs versus their previously thought origin among ‘higher’ euthyneuran taxa.ResultsWe describe the 3D-microanatomy of H. psammobionta using three-dimensional digital reconstruction based on serial semithin histological sections. The new dataset expands upon the original description and corrects several aspects. Helminthope shows a set of typical adaptations and regressive characters present in other mesopsammic slugs (called ‘meiofaunal syndrome’ herein). The taxonomically important presence of five separate visceral loop ganglia is confirmed, but considerable further detail of the complex nervous system are corrected and revealed. The digestive and reproductive systems are simple and modified to the thread-like morphology of the animal; the anus is far posterior. There is no heart; the kidney resembles a protonephridium. Data on all organ systems are compiled and compared to Rhodope.ConclusionsHelminthope is related to Rhodope sharing unique apomorphies. We argue that the peculiar kidney, configuration of the visceral loop and simplicity or lack of other organs in Rhodopemorpha are results of progenesis. The posterior shift of the anus in Helminthope is interpreted as a peramorphy, i.e. hypertrophy of body length early in ontogeny. Our review of morphological and molecular evidence is consistent with an origin of Rhodopemorpha slugs among shelled ‘lower Heterobranchia’. Previously thought shared ‘diagnostic’ features such as five visceral ganglia are either plesiomorphic or convergent, while euthyneury and a double-rooted cerebral nerve likely evolved independently in Rhodopemorpha and Euthyneura.

Flashback and foreshadowing—a review of the taxon Opisthobranchia

“…In Fig. 5 we modify the tree proposed by Brenzinger et al (2013a) by collapsing the Ectobranchia (Valvatoidea) into a basal polytomy, considering that morphological evidence (see Hawe et al 2013) conflicts with molecular evidence and sperm ultrastructure, as far as is known (see Brenzinger et al 2013a for discussion). Reviewing current morphological knowledge (Fig.…”

“…Neusser et al 2006), paved the way for comparative studies across euthyneurans (e.g., Rückert et al 2008;Neusser et al 2009bNeusser et al , 2011aGolding 2010;Wägele et al 2010;Brenzinger et al 2011a, b;Eder et al 2011;Haszprunar et al 2011;Kohnert et al 2013). For example, Brenzinger et al (2013a) could show that the close affinities of Rhodopemorpha with "lower heterobranchs" related to Murchisonellidae, and morphological features similar to Doridoidea, are due to convergences. The phylogenetic signal of previously neglected or misunderstood complex organ systems still needs to be unraveled.…”

“…2a) (Haszprunar 1985a), but was later included in the latter (Haszprunar 1988). Ectobranchia (name preferable over Valvatoidea Gray, 1840, see Haszprunar et al 2011) were also added to Heterobranchia as their earliest offshoot; this is still regarded as valid (Haszprunar et al 2011;Brenzinger et al 2013a). …”

“…Acteonoidea are now considered to belong to the "lower Heterobranchia", based on results by Göbbeler and Klussmann-Kolb (2010a) and . "Lower heterobranchs" also include now Rhodopemorpha (Wilson et al 2010;Brenzinger et al 2013a). …”

“…They also stressed that the results of these analyses differ radically from those of traditional hypotheses. Most recently, Brenzinger et al (2013a) highlighted the robust nodes in a simplified cladogram (combined from Jörger et al 2010;Schrödl et al 2011a, b;Dayrat et al 2011) and summarised putative morphological apomorphies discussed, e.g., by Haszprunar (1985a), Dayrat and Tillier (2002), and Haszprunar et al (2011). In Fig.…”