“Opisthobranchia”! a Review on the Contribution of Mesopsammic Sea Slugs to Euthyneuran Systematics
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Thalassas, 27 (2): 101-112 An International Journal of Marine Sciences BYE BYE “OPISTHOBRANCHIA”! A REVIEW ON THE CONTRIBUTION OF MESOPSAMMIC SEA SLUGS TO EUTHYNEURAN SYSTEMATICS SCHRÖDL M(1), JÖRGER KM(1), KLUSSMANN-KOLB A(2) & WILSON NG(3) Key words: Mollusca, Heterobranchia, morphology, molecular phylogeny, classification, evolution. ABSTRACT of most mesopsammic “opisthobranchs” within a comprehensive euthyneuran taxon set. During the last decades, textbook concepts of “Opisthobranchia” have been challenged by The present study combines our published morphology-based and, more recently, molecular and unpublished topologies, and indicates that studies. It is no longer clear if any precise distinctions monophyletic Rhodopemorpha cluster outside of can be made between major opisthobranch and Euthyneura among shelled basal heterobranchs, acte- pulmonate clades. Worm-shaped, mesopsammic taxa onids are the sister to rissoellids, and Nudipleura such as Acochlidia, Platyhedylidae, Philinoglossidae are the basal offshoot of Euthyneura. Furthermore, and Rhodopemorpha were especially problematic in Pyramidellidae, Sacoglossa and Acochlidia cluster any morphology-based system. Previous molecular within paraphyletic Pulmonata, as sister to remaining phylogenetic studies contained a very limited sampling “opisthobranchs”. Worm-like mesopsammic hetero- of minute and elusive meiofaunal slugs. Our recent branch taxa have clear independent origins and thus multi-locus approaches of mitochondrial COI and 16S their similarities are the result of convergent evolu- rRNA genes and nuclear 18S and 28S rRNA genes tion. Classificatory and evolutionary implications (“standard markers”) thus included representatives from our tree hypothesis are quite dramatic, as shown by some examples, and need to be explored in more detail in future studies. (1) Bavarian State Collection of Zoology. Münchhausenstr. 21, D-81247 Munich, Germany. (2) Institute for Ecology, Evolution and Diversity, Goethe- We do not claim that these concatenated “standard University, Siesmayerstr. 70, 60054 Frankfurt am Main, marker” gene trees reflect the true phylogeny of Germany. (3) The Australian Museum, 6 College Street, Sydney NSW, all groups; exploring additional, suitable markers 2010 Australia. is required. We do claim, however, that improved Email: [email protected], Katharina.Joerger@ zsm.mwn.de, [email protected], Nerida. taxon sampling and improved data quality (such [email protected] as sequences, alignments) were beneficial towards 101 SCHRÖDL M, JÖRGER KM, KLUSSMANN-KOLB A & WILSON NG revealing relationships of higher euthyneuran taxa, into Opisthobranchia (Gosliner, 1981). Commonly and that phylogenetic hypotheses based on this data accepted “core groups” are Cephalaspidea, Anaspidea, set are converging. The traditional taxon concept of Thecosomata, Gymnosomata, Sacoglossa, Acochlidia, Opisthobranchia is clearly artificial and thus obsolete. Tylodinoidea (=Umbraculida) and Nudipleura, the Novel phylogenetic hypotheses, as disturbing they latter consisting of side-gilled Pleurobranchomorpha may be at first glance, give us the opportunity and and Nudibranchia, which are the sea slugs in a strict perhaps the obligation to refine our approaches and sense. Some taxa with more or less well-developed rethink older paradigms. Most importantly, we see helicoidal shells such as Acteonoidea (see Mikkelsen, no more way to explore morphology, systematics and 1996 vs. 2002) and Pyramidelloidea (e.g. Fretter & evolution of “opisthobranchs” separately from “lower Graham, 1949) and the limpet-like Siphonarioidea heterobranchs” and “pulmonates”. have also occasionally been discussed as part of Opisthobranchia (see review by Wägele et al., 2008). INTRODUCTION While the worm-like Rhodopemorpha were either seen as turbellarians or transitional forms between Milne Edwards (1848) split the gastropods into worms and gastropods in early approaches, most Prosobranchia, Pulmonata and Opisthobranchia. The modern authors treated them as euthyneurans or latter two taxa are usually combined as Euthyneura. integral part of opisthobranchs (e.g. Haszprunar & Both researchers and amateurs easily associate Heß, 2005). opisthobranchs as marine slugs or snails, with a more or less reduced or internalized shell, having an almost Establishing the Heterobranchia concept, bilaterally symmetrical body and either a head shield Haszprunar (1985, 1988) reconstructed an apomorphy- or head tentacles, whereas pulmonates appear almost based phylogeny implying a progressive evolution exclusively related to limnic and terrestrial habitats. from simple “allogastropod” (=“lower heterobranch”) Unconventional taxa such as interstitial worm-like taxa such as Valvatoidea, Architectonicoidea forms, limnic opisthobranchs and marine pulmonates and Pyramidelloidea towards Pentaganglionata occur, but are obviously too exceptional to challenge (=Euthyneura). Haszprunar’s phylogeny showed the practical value of the traditional Opisthobranchia- Acteonoidea (Architectibranchia) as the sister to Pulmonata concept. The often beautifully coloured monophyletic Pulmonata (including pentaganglionate and bizarrely shaped approx. 6000 opisthobranch Rhodopemorpha), which was itself the sister to species thus are treated as belonging to a clade remaining opisthobranchs (including vermiform in virtually all older field guides and zoological Smeagolidae), rendering “Opisthobranchia” textbooks (e.g. Westheide & Rieger, 2007), current paraphyletic. Haszprunar thus was the first to molluscan classifications (e.g. Bouchet & Rocroi, phylogenetically infer and discuss the artificial 2005), and reviews (e.g. Schmekel & Portmann, 1982, nature of Opisthobranchia rather than comparing Schmekel, 1985, Rudman & Willan, 1998), including similarities and modifying the inclusiveness of the the most recent one by Wägele et al. (2008) that concept. Using cladistic analyses on a morphological was published within a compendium on molluscan dataset, Salvini-Plawén & Steiner (1996) recovered phylogeny and evolution (Ponder & Lindberg, 2008). monophyletic Euthyneura, and Pulmonata plus Recent comprehensive field guides on Caribbean and Thecosomata as sister to remaining Opisthobranchia Indo-Pacific opisthobranchs, however, left monophyly including Rhodopemorpha (as Rhodopida) as sister open (Valdés et al., 2006, Gosliner et al., 2008). to equally shell-less and small-sized Acochlidia and Gymnosomata. Dayrat & Tillier (2002) found There has always been a certain disagreement with Pyramidelloidea within euthyneuran taxa and regards to which major subtaxa should be included summarized an unresolved euthyneuran topology with 102 BYE BYE “OPISTHOBRANCHIA”! A REVIEW ON THE CONTRIBUTION OF MESOPSAMMIC SEA SLUGS TO EUTHYNEURAN SYSTEMATICS „Lower heterobranchs“ inc lu ding Rho dopemorp ha Rissoelloidea Acteonoidea Hetero- Nudipleura branchia Umbraculoidea Runcinacea Cephalaspidea s.s. Euthyneura s.l. Euopistho- Anaspidea branchia Pteropoda Siphonarioidea Tectipleura new name Sacoglossa Glacidorboidea Amphiboloidea Panpulmonata Pyramidellidae Hygrophila Acochlidia Eupulmonata Figure 1: “Opisthobranch” phylogeny as inferred from “standard genes” analyses, combining results by Jörger et al. (2010) and Wilson et al. (2010); robustly supported nodes (bootstrap support >75 and posterior probability >0.95) indicated by black dots. Taxa formerly regarded as opisthobranchs in green, pulmonate taxa in yellow, “lower heterobranch” taxa in blue. Note that the assemblage of “Lower heterobranchs including Rhodopemorpha” is paraphyletic but collapsed for illustrative purposes. monophyletic Pulmonata arising as one of many clades with Acochlidia; Schrödl & Neusser (2010) explained from an opisthobranch grade of organization. An even that by parallel concerted reductions of body-size and more comprehensive morphology-based parsimony organs, but also by convergent evolution of vermiform analysis by Wägele & Klussmann-Kolb (2005) showed bodies having a set of special organs as adaptations to Pteropoda (Gymnosomata plus Thecosomata) as sister a special habitat. Summarizing, 1) the Heterobranchia to Pulmonata plus remaining Opisthobranchia, but concept has always conflicted with a monophyletic this is contradicted by a more focused molecular study Opisthobranchia, 2) no morphology-based analyses (Klussmann-Kolb & Dinapoli, 2006). In the study by have recovered a monophyletic Opisthobranchia, 3) Wägele & Klussmann-Kolb (2005) the remaining morphology-based analyses are mislead by problems Opisthobranchia included a clade of exclusively of interpreting morphological similarities and interstitial (and/or small sized) cephalaspidean a generally high degree of parallelism (Gosliner, subtaxa, Rhodopemorpha and Acochlidia as sister 1981, 1991); in particular, convergences displayed to Sacoclossa, rendering Cephalaspidea polyphyletic. by small-sized slugs that occur in many subgroups In the light of the latest morphology-based cladistic may outnumber characters showing true phylogenetic analysis focussing on Acochlidia (Schrödl & Neusser, signal, and thus lead to unreliable or completely 2010), such results are in doubt. While resolving wrong topologies. inner relationships of Acochlidia quite nicely, other mesopsammic euthyneurans included, regardless Molecular markers, in contrast, offer an extremely their supposed affiliation, had a tendency to cluster large number of characters (via nucleotide sequences) 103 SCHRÖDL M, JÖRGER KM, KLUSSMANN-KOLB A & WILSON NG and