Yasunori Kano

Vetigastropod phylogeny and a new concept of Seguenzioidea: independent evolution of copulatory organs in the deep-sea habitats

Bayesian and maximum‐likelihood phylogenies of Vetigastropoda (Mollusca: Gastropoda) were reconstructed by separate and combined analyses of one mitochondrial (cytochrome oxidase I, COI) and two nuclear (histone H3 and 18S rRNA) gene sequences, with an emphasis on dense taxonomic sampling. More than 70 vetigastropod species belonging to 13 families and 25 subfamilies constituted a robust clade against the two outgroup clades Neomphalina and Cocculinoidea. The phylogenetically controversial family Seguenziidae appeared as a derived Vetigastropoda and constituted a highly supported clade with eucycline and cataegine trochids, and three skeneimorphs (Adeuomphalus, Ventsia and Xyloskenea). These taxa herein treated as the superfamily Seguenzioidea are morphologically very diverse and grouped only by the combination of symplesiomorphies in the shell, radular and head‐foot characters. Anatomical peculiarities of Seguenziidae, including the presence of the penis and seminal receptacle, are all apomorphic conditions independently derived from those in higher gastropod clades, as a consequence of the small size and in response to deep‐sea habitats, where sperm storage seems to be especially beneficial with low numerical density of individuals and limited periodic cues for gametogenesis. Indeed, internal or semi‐internal fertilization has been evolved at least six times in Vetigastropoda, essentially in deep‐sea lineages, with weak phylogenetic constraints. Other new vetigastropod clades with high support values include: Turbinidae + Tegulinae (Trochidae) + Skeneidae s.s., Clypeosectidae + Lepetodrilidae, Anatominae (Scissurellidae) + Bathyxylophila (Skeneidae) and Lepetodriloidea + Scissurellidae +Bathyxylophila.

Major adaptive radiation in neritopsine gastropods estimated from 28S rRNA sequences and fossil records.

A well–supported phylogeny of the Neritopsina, a gastropod superorder archaic in origin, radiated ecologically and diverse in morphology, is reconstructed based on partial 28S rRNA sequences. The result (Neritopsidae (Hydrocenidae (Helicinidae + Neritiliidae) (Neritidae + Phenacolepadidae))) is highly congruent with the fossil records and the character distribution of reproductive tracts in extant taxa. We suggest that the Neritopsina originated in subtidal shallow waters, invaded the land and became fully terrestrial at least three times in different clades, by the extinct Dawsonellidae in the Late Palaeozoic and by the Helicinidae and Hydrocenidae in the Mesozoic. Invasion of fresh– and brackish waters is prevalent among the Neritopsina as the Jurassic and freshwater ancestory is most probable for helicinids. The Phenacolepadidae, a group exclusively inhabiting dysoxic environments, colonized deep–sea hydrothermal vents and seeps in the Late Cretaceous or Early Cenozoic. Submarine caves have served as refuges for the archaic Neritopsidae since the Early to Middle Cenozoic, and the marine neritopsine slug Titiscania represents a highly specialized but relatively recent offshoot of this family. The Neritiliidae is another clade to be found utilizing submarine caves as shelter by the Oligocene; once adapted to the completely dark environment, but some neritiliids have immigrated to surface freshwater habitats.

The Continuing Debate on Deep Molluscan Phylogeny: Evidence for Serialia (Mollusca, Monoplacophora + Polyplacophora)

Molluscs are a diverse animal phylum with a formidable fossil record. Although there is little doubt about the monophyly of the eight extant classes, relationships between these groups are controversial. We analysed a comprehensive multilocus molecular data set for molluscs, the first to include multiple species from all classes, including five monoplacophorans in both extant families. Our analyses of five markers resolve two major clades: the first includes gastropods and bivalves sister to Serialia (monoplacophorans and chitons), and the second comprises scaphopods sister to aplacophorans and cephalopods. Traditional groupings such as Testaria, Aculifera, and Conchifera are rejected by our data with significant Approximately Unbiased (AU) test values. A new molecular clock indicates that molluscs had a terminal Precambrian origin with rapid divergence of all eight extant classes in the Cambrian. The recovery of Serialia as a derived, Late Cambrian clade is potentially in line with the stratigraphic chronology of morphologically heterogeneous early mollusc fossils. Serialia is in conflict with traditional molluscan classifications and recent phylogenomic data. Yet our hypothesis, as others from molecular data, implies frequent molluscan shell and body transformations by heterochronic shifts in development and multiple convergent adaptations, leading to the variable shells and body plans in extant lineages.

Rubyspira, New Genus and Two New Species of Bone-Eating Deep-Sea Snails With Ancient Habits

Rubyspira, a new genus of deep-sea snails (Gastropoda: Abyssochrysoidea) with two living species, derives its nutrition from decomposing whalebones. Molecular phylogenetic and morphological evidence places the new genus in an exclusively deep-sea assemblage that includes several close relatives previously known as fossils associated with Cretaceous cold seeps, plesiosaur bones, and Eocene whalebones. The ability to exploit a variety of marine reducing environments may have contributed to the evolutionary longevity of this gastropod lineage.

Gastropods from Recent Hot Vents and Cold Seeps: Systematics, Diversity and Life Strategies

Since the first discovery of hydrothermal vents at the Galapagos Spreading Center in 1977, gastropods have gained considerable attention as a major constituent of the chemosynthesis-based biological communities, especially the colonies of large species like Alviniconcha, Ifremeria and Lepetodrilus, or morphologically strange ones like the scaly-foot snail. Various types of symbiotic relations to bacteria have broadened the interest in them. During more than 30 years numerous vent and seep biotopes have been found mainly in temperate seas, but recently hydrothermal vents off Jan Mayen in the North Atlantic at 80°N and cold seeps off Norway between 67°N and 70°N (Haakon Mosby Mud Volcano) with chemosynthesis-based fauna (see Waren and Bouchet 2001; Desbruyeres et al. 2006: 516–517 for map). Biology of these vent/seep organisms is still in an early state of exploration; much of what is known is summarized in the monographs by Van Dover (2000) and Desbruyeres et al. (2006). Vent/seep taxa have also been a major target in research on higher phylogeny and systematics of gastropods. Several new families were established in the 1980s, based on seemingly “great differences” in morphology.

Molecular phylogenetic investigations of the relationships of the echinoderm-parasite family Eulimidae within Hypsogastropoda (Mollusca)

The gastropod family Eulimidae has attracted considerable attention as one of the most diverse groups of parasitic molluscs in terms of number of species and ranges of body plans and parasitic strategies. However, the phylogenetic position of the family has not been established within the Hypsogastropoda and this has hampered the inference of ancestral states in the evolution of the morphology and parasitic strategies. Here we present Bayesian and maximum likelihood phylograms of Hypsogastropoda based on nuclear and mitochondrial loci (18S and 28S rRNA, Histone H3, COI and 16S rRNA) and a better taxonomic sampling than in previous molecular analyses, to determine the position of Eulimidae. The resulting trees suggest Vanikoridae as the sister group of Eulimidae; the two families are collectively placed in the newly redefined superfamily Vanikoroidea, with Truncatelloidea and (potentially paraphyletic) Rissooidea as closest relatives. Vanikorids are protandrous hermaphrodites as are many eulimids and are essentially carnivorous, differing from the mostly gonochoristic and herbivorous/detritivorous Truncatelloidea and Rissooidea. The mode of feeding may have a phylogenetic signal also within Eulimidae, where radula-less species constitute a robust clade. Other new findings include a close affinity of the submarine-cave Pickworthiidae to Cerithioidea and a terminal position of Nystiellidae within the paraphyletic Epitoniidae.

Living Monoplacophora: morphological conservatism or recent diversification?

Kano, Y., Kimura, S., Kimura, T. & Warén, A. (2012) Living Monoplacophora: morphological conservatism or recent diversification? —Zoologica Scripta, 41, 471–488.

Hitchhiking behaviour in the obligatory upstream migration of amphidromous snails

Migratory animals endure high stress during long-distance travel in order to benefit from spatio-temporally fluctuating resources, including food and shelter or from colonization of unoccupied habitats. Along with some fishes and shrimps, nerite snails in tropical to temperate freshwater systems are examples of amphidromous animals that migrate upstream for growth and reproduction after a marine larval phase. Here I report, to my knowledge, the first example of ‘hitchhiking’ behaviour in the obligatory migration of animals: the nerite snail Neritina asperulata appears to travel several kilometres as minute juveniles by firmly attaching to the shells of congeneric, subadult snails in streams of Melanesian Islands, presumably to increase the success rate of migration.

Mitogenomics of Vetigastropoda: insights into the evolution of pallial symmetry

The nucleotide sequences of the complete or nearly complete mitochondrial (mt) genomes of seven vetigastropods were determined: Angaria neglecta (Angarioidea), Phasianella solida (Phasianelloidea), Granata lyrata (Seguenzioidea), Tegula lividomaculata and Bolma rugosa (Trochoidea), Diodora graeca (Fissurelloidea) and Lepetodrilus schrolli (Lepetodriloidea). While the mt genomes of the superfamilies Angarioidea, Phasianelloidea, Seguenzioidea and Trochoidea conform generally to the ancestral gene order of Vetigastropoda and Gastropoda, those of the superfamilies Fissurelloidea and Lepetodriloidea have suffered important rearrangements. The gene order of the mtDNA of Chrysomallon squamiferum, a representative of Neomphalina, was also analysed since it has been proposed to be closely related to Vetigastropoda, and showed a distinct arrangement. The reconstructed phylogenies recovered Neomphalina as a distinct gastropod lineage that is the sister group (only with moderate bootstrap support) of a clade including Vetigastropoda and Neritimorpha + Caeno‐gastropoda while the relative position of Heterobranchia and Patellogastropoda in the gastropod tree could not be determined definitively due to their long branches. Within the monophyletic Vetigastropoda, the superfamily Fissurelloidea was recovered as the sister group of two lineages, one including Lepetodriloidea as the sister group of Seguenzioidea + Halitoidea, the other including Phasianelloidea, Angarioidea and Trochoidea without resolved relationships. The long branches of Fissurelloidea were found to introduce significant tree instability in phylogenetic reconstruction. The new phylogeny supports that the loss of the right pallial gill occurred multiple times in vetigastropod evolution as previously suggested and that Phasianelloidea, Angarioidea and Trochoidea radiated from a common asymmetric (single‐gilled) ancestor that lived in the middle Palaeozoic.

Cenozoic climate change and diversification on the continental shelf and slope: evolution of gastropod diversity in the family Solariellidae (Trochoidea).

Recent expeditions have revealed high levels of biodiversity in the tropical deep-sea, yet little is known about the age or origin of this biodiversity, and large-scale molecular studies are still few in number. In this study, we had access to the largest number of solariellid gastropods ever collected for molecular studies, including many rare and unusual taxa. We used a Bayesian chronogram of these deep-sea gastropods (1) to test the hypothesis that deep-water communities arose onshore, (2) to determine whether Antarctica acted as a source of diversity for deep-water communities elsewhere and (3) to determine how factors like global climate change have affected evolution on the continental slope. We show that although fossil data suggest that solariellid gastropods likely arose in a shallow, tropical environment, interpretation of the molecular data is equivocal with respect to the origin of the group. On the other hand, the molecular data clearly show that Antarctic species sampled represent a recent invasion, rather than a relictual ancestral lineage. We also show that an abrupt period of global warming during the Palaeocene Eocene Thermal Maximum (PETM) leaves no molecular record of change in diversification rate in solariellids and that the group radiated before the PETM. Conversely, there is a substantial, although not significant increase in the rate of diversification of a major clade approximately 33.7 Mya, coinciding with a period of global cooling at the Eocene–Oligocene transition. Increased nutrients made available by contemporaneous changes to erosion, ocean circulation, tectonic events and upwelling may explain increased diversification, suggesting that food availability may have been a factor limiting exploitation of deep-sea habitats. Tectonic events that shaped diversification in reef-associated taxa and deep-water squat lobsters in central Indo-West Pacific were also probably important in the evolution of solariellids during the Oligo-Miocene.