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Molecular Phylogeny of the Euthyneura (Mollusca, Gastropoda) with Special Focus on Opisthobranchia As a Framework for Reconstruction of Evolution of Diet

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Molecular Phylogeny of the Euthyneura (Mollusca, Gastropoda) with Special Focus on Opisthobranchia As a Framework for Reconstruction of Evolution of Diet Thalassas, 27 (2): 121-154 An International Journal of Marine Sciences MOLECULAR PHYLOGENY OF THE EUTHYNEURA (MOLLUSCA, GASTROPODA) WITH SPECIAL FOCUS ON OPISTHOBRANCHIA AS A FRAMEWORK FOR RECONSTRUCTION OF EVOLUTION OF DIET KATRIN GÖBBELER(1,*) & ANNETTE KLUSSMANN-KOLB(1) Key words: character evolution, BayesTraits, molecular systematics, diet, herbivory, Euthyneura ABSTRACT Based on the presented data monophyly of Opisthobranchia is clearly rejected. However, The Opisthobranchia comprise a group of highly monophyly of the Euthyneura (comprising specialized gastropods with uncertain systematic Opisthobranchia and Pulmonata) is supported. affinities. Moreover, monophyly of the whole clade Furthermore, monophyly of most subgroups is has been repeatedly questioned. The present study revealed. The Runcinacea are found as a separate presents the currently most extensive analyses on clade clustering apart from the remaining opisthobranch phylogeny including 58 species from Cephalaspidea, the taxon in which they have been all major subgroups. A combination of four gene formerly classified. Furthermore, Aplysiomorpha markers as well as diverse molecular systematic and Pteropoda are recovered as a monophyletic analytical approaches are applied in order to shed new clade, while the Aplysiomorpha are found to be light on the evolution of this taxon. Special emphasis paraphyletic due to the position of a single taxon. is given to the reconstruction of ancestral diet In addition, Cylindrobullida are revealed as part of preferences since extant Opisthobranchia feed on a the sacoglossan subclade Oxynoacea denying their variety of different food items and the development of current separate status. The enigmatic Acochlidiacea dietary specialization is supposed to be important for are revealed as sister group to Eupulmonata. the evolution of these enigmatic marine gastropods. Ancestral diet preferences are reconstructed for monophyletic Euthyneura and all main subclades since (1) Institute for Ecology, Evolution and Diversity, Goethe- polyphyly of Opisthobranchia impeded reconstruction University Frankfurt, Siesmayerstrasse 70, 60054 Frankfurt am Main, Germany for this clade. Herbivory is found as the most likely e-mail: [email protected] ancestral diet of Euthyneura while carnivory probably *Current address: Department of Integrative Biology, University of Colorado Denver, P.O. Box 173364, Denver, CO evolved several times independently in different 80217, USA clades. 121 Katrin Göbbeler & Annette Klussmann-Kolb Figure 1: Bayesian inference phylogram of the phylogenetic analyses (concatenated alignment of 18S rDNA, 28S rDNA, 16S rDNA and CO1), 50% majority rule consensus tree. Posterior probabilities are provided at the nodes; only support values above 0.5 are given. Taxonomic classifications (following Bouchet and Rocroi, 2005) are indicated and shaded on the right side (“lower Heterobranchia” = white; Opisthobranchia = light grey; Pulmontata = dark grey). The branch leading to the nudipleuran Dexiarchia was shortened by about 50% to allow better visibility. 122 Molecular phylogeny of the Euthyneura (Mollusca, Gastropoda) with special focus on Opisthobranchia as a framework for reconstruction of evolution of diet INTRODUCTION Monophyly of the Opisthobranchia has been challenged by several authors due to the lack The Opisthobranchia are a group of gastro- of proper synapomorphies (Salvini-Plawen pods comprising morphologically diversified spe- and Steiner, 1996; Ponder and Lindberg, 1997) cies which are distributed globally in all marine caused by “rampant parallelism” (Gosliner and habitats. They are composed of about 6000 spe- Ghiselin, 1984) in this taxon. Moreover, previous cies (Wägele et al., 2008) currently divided into phylogenetic analyses often failed to reveal nine main clades: Cephalaspidea, Thecosomata, monophyly of this taxon both in morphology-based Gymnosomata, Aplysiomorpha, Acochlidiacea, studies (Dayrat and Tillier, 2002; Wägele and Sacoglossa, Cylindrobullida, Umbraculida and Klussmann-Kolb, 2005) and molecular systematic Nudipleura (Bouchet and Rocroi, 2005). Monophyly investigations (Thollesson, 1999; Dayrat et of these clades has been well supported in molecular al., 2001; Grande et al., 2004a, b; Klussmann- systematic studies (Wägele et al., 2003; Grande et Kolb et al., 2008; Dinapoli and Klussmann- al., 2004a, b; Vonnemann et al., 2005; Klussmann- Kolb, 2010; Jörger et al., 2010). In a recent Kolb and Dinapoli, 2006; Klussmann-Kolb et al., study focusing on phylogeny and systematics of 2008; Dinapoli and Klussmann-Kolb, 2010; Jörger Acochlidiacea, Jörger et. al (2010) propose the new et al., 2010). Furthermore, the pelagic Thecosomata clade Euopisthobranchia uniting Umbraculida, and Gymnosomata have been revealed as sister Aplysiomorpha, Cephalaspidea and Pteropoda. groups forming the Pteropoda (Klussmann-Kolb and This clade presents a “monophyletic remainder Dinapoli, 2006). of the (non-monophyletic) “Opisthobranchia” as traditionally defined” (Jörger et al., 2010, p. 7). The main evolutionary trend in Opisthobranchia is reduction or even loss of the shell (Grande et al., Opisthobranchia are supposed to form a clade 2004a) accompanied by development of diverse with pulmonate gastropods called Euthyneura defensive strategies (Wägele and Klussmann-Kolb, (Spengel, 1881). Monophyly of this clade has been 2005). Radiation of opisthobranchs has lead to detected in morphological (Ponder and Lindberg, parallelism and convergence of morphological 1997; Dayrat and Tillier, 2002) as well as molecular characters (Gosliner and Ghiselin, 1984; Gosliner, systematic studies (Thollesson, 1999; Wade and 1985, 1991) hampering morphology based Mordan, 2000; Knudsen et al., 2006) while other classification. Thus, phylogenetic hypotheses on molecular systematic studies reveal paraphyly of Opisthobranchia vary based on morphological Euthyneura (Dayrat et al., 2001; Grande et al., considerations (Schmekel, 1985; Bieler, 1992; 2004b; Klussmann-Kolb et al., 2008; Dinapoli Salvini-Plawen and Steiner, 1996; Dayrat and Tillier, and Klussmann-Kolb, 2010; Jörger et al., 2010). 2002; Mikkelsen, 2002; Wägele and Klussmann- Nevertheless, Thollesson (1999) as well as Jörger Kolb, 2005). Moreover, molecular phylogenetic et al. (2010) claimed the constant inclusion of both analyses reveal contradictory classifications as well pulmonate and opisthobranch taxa in phylogenetic (Thollesson, 1999; Dayrat et al., 2001; Grande et al., studies due to their possibly common origin. Thus, 2004a, b; Vonnemann et al., 2005; Klussmann-Kolb erroneous monophyly of either clade based on and Dinapoli, 2006; Klussmann-Kolb et al., 2008; incomplete taxon sampling can be avoided. We Dinapoli and Klussmann-Kolb, 2010; Jörger et al., follow this request in the present investigation by 2010) mainly due to differences in taxon sampling, incorporating both opisthobranch and pulmonate employed marker genes and outgroup determination. species in our analyses. Additionally, several “lower Thus, a common solution and a robust phylogeny of heterobranch” taxa are included to test monophyly Opisthobranchia are still lacking. of Euthyneura. 123 Katrin Göbbeler Annette & Klussmann-Kolb 124 Figure 2: Neighbour-net graph of the split decomposition analysis (concatenated alignment of 18S rDNA, 28S rDNA, 16S rDNA and CO1). Taxonomic classification (according to Bouchet and Rocroi, 2005) indicated by braces. Molecular phylogeny of the Euthyneura (Mollusca, Gastropoda) with special focus on Opisthobranchia as a framework for reconstruction of evolution of diet A highly specialized and possibly crucial feature of ancestral character states applying a Bayesian for evolution in Opisthobranchia is represented by their approach. For this purpose, we conducted a thorough diverse diet (Thompson, 1976; Rudman and Willan, literature search on diet of Opisthobranchia to 1998; Mikkelsen, 2002; Wägele, 2004). Many potential enable reconstruction of ancestral preferences. key characters for opisthobranch evolution are related This reconstruction is based on the currently most to diet and supposed to trigger exploration of new food comprehensive molecular systematic study on sources (Wägele, 2004). Some opisthobranch clades opisthobranch phylogeny covering all main subclades feed on algae (Aplysiomorpha, Sacoglossa); others are in order to account for their interrelationships and specialized on Porifera (Umbraculida), while diverse provide the framework for reconstruction of character carnivorous (Nudipleura) or even carnivorous or evolution. herbivorous food items (Cephalaspidea) are preferred in other groups. Some opisthobranch species exhibit MATERIALS AND METHODS remarkable adaptations to a special source of food, e.g. Nudibranchia living in mutualistic symbiosis Taxon sampling with photosynthetic dinoflagellates and sharing metabolites (Burghardt et al., 2005) or Sacoglossa The current study comprises a total of 86 taxa incorporating chloroplasts of their algal food in their with 58 Opisthobranchia covering all subclades. own digestive gland and using metabolites (Rumpho Additionally 18 Pulmonata (including all main et al., 2000; Händeler et al., 2009). The evolution subclades) and nine “lower Heterobranchia” (with of these highly specialized features is largely a special focus on the questionable opisthobranch unknown. Malaquias et al. (2009a) reconstructed the clade Acteonoidea) complement the taxon sampling. ancestral diet of Cephalaspidea comprising diversely The caenogastropod
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