From sea to land and beyond – New insights into the evolution of euthyneuran Gastropoda (Mollusca)

Abstract

BackgroundThe Euthyneura are considered to be the most successful and diverse group of Gastropoda. Phylogenetically, they are riven with controversy. Previous morphology-based phylogenetic studies have been greatly hampered by rampant parallelism in morphological characters or by incomplete taxon sampling. Based on sequences of nuclear 18S rRNA and 28S rRNA as well as mitochondrial 16S rRNA and COI DNA from 56 taxa, we reconstructed the phylogeny of Euthyneura utilising Maximum Likelihood and Bayesian inference methods. The evolution of colonization of freshwater and terrestrial habitats by pulmonate Euthyneura, considered crucial in the evolution of this group of Gastropoda, is reconstructed with Bayesian approaches.ResultsWe found several well supported clades within Euthyneura, however, we could not confirm the traditional classification, since Pulmonata are paraphyletic and Opistobranchia are either polyphyletic or paraphyletic with several clades clearly distinguishable. Sacoglossa appear separately from the rest of the Opisthobranchia as sister taxon to basal Pulmonata. Within Pulmonata, Basommatophora are paraphyletic and Hygrophila and Eupulmonata form monophyletic clades. Pyramidelloidea are placed within Euthyneura rendering the Euthyneura paraphyletic.ConclusionBased on the current phylogeny, it can be proposed for the first time that invasion of freshwater by Pulmonata is a unique evolutionary event and has taken place directly from the marine environment via an aquatic pathway. The origin of colonisation of terrestrial habitats is seeded in marginal zones and has probably occurred via estuaries or semi-terrestrial habitats such as mangroves.

Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): New insights from increased taxon sampling

“…1B): Pulmonata is monophyletic, although Siphonariidae may not be included within Pulmonata; Eupulmonata (Stylommatophora, Ellobiidae, Onchidiidae) is monophyletic (although veronicellids were not sampled); Otina and Trimusculus are nested within Eupulmonata (Stylommatophora, Ellobiidae, Onchidiidae), and seem to be closely related to ellobiids; the monophyly of Ellobiidae is not supported; Amphiboloidea and Pyramidellidae are sister-taxa; Hygrophila is monophyletic, including Chilinoidea (Chilinidae and Latiidae) and Lymnaeoidea. The analyses focusing on basal heterobranchs (Dinapoli and Klussmann-Kolb, 2010) based on a subsample of pulmonate species from Klussmann-Kolb et al (2008) yielded similar results (Fig. 1C).…”

“…Overall, the results based on complete mitochondrial genomes (Grande et al, 2008) and individual markers (Klussmann-Kolb et al, 2008) are incongruent and depict two different phylogenetic scenarios. Possible explanations for this incongruence are discussed below.…”

“…The two most comprehensive data sets thus far for euthyneuran (opisthobranch and pulmonate) phylogenetics have been published by Grande et al (2008), based on mitochondrial genomes, and by Klussmann-Kolb et al (2008), based on 18S, 28S, 16S, and COI data. Dinapoli and Klussmann-Kolb (2010) also published a study focusing on early heterobranchs, i.e., the lineages that branched off just before euthyneurans.…”

“…1A): Siphonariidae is nested within Opisthobranchia, closely related to a shelled sacoglossan (Ascobulla); Stylommatophora (land snails and slugs) emerge at the base of Euthyneura; Eupulmonata (=Stylommatophora, Veronicellidae, Onchidiidae, and Ellobiidae) are polyphyletic; Pulmonata is not monophyletic; and, Pyramidellidae is nested within Euthyneura, closely related to Onchidiidae. Klussmann-Kolb et al (2008), who focused on both opisthobranchs and pulmonates, targeted shorter sequence data but broader taxon sampling: they presented a data set including 29 species of pulmonates (one marker is missing for nine of those 29 species, generating gaps in the data set) and 24 species of opisthobranchs, with most higher-level taxa of pulmonates and opisthobranchs represented by at least one species. Some interesting, well-supported results from Klussmann-Kolb et al (2008) are (Fig.…”

“…Klussmann-Kolb et al (2008), who focused on both opisthobranchs and pulmonates, targeted shorter sequence data but broader taxon sampling: they presented a data set including 29 species of pulmonates (one marker is missing for nine of those 29 species, generating gaps in the data set) and 24 species of opisthobranchs, with most higher-level taxa of pulmonates and opisthobranchs represented by at least one species. Some interesting, well-supported results from Klussmann-Kolb et al (2008) are (Fig. 1B): Pulmonata is monophyletic, although Siphonariidae may not be included within Pulmonata; Eupulmonata (Stylommatophora, Ellobiidae, Onchidiidae) is monophyletic (although veronicellids were not sampled); Otina and Trimusculus are nested within Eupulmonata (Stylommatophora, Ellobiidae, Onchidiidae), and seem to be closely related to ellobiids; the monophyly of Ellobiidae is not supported; Amphiboloidea and Pyramidellidae are sister-taxa; Hygrophila is monophyletic, including Chilinoidea (Chilinidae and Latiidae) and Lymnaeoidea.…”