Search

The gastropod infraclass Euthyneura comprises at least 30,000 species of snails and slugs, including nudibranch sea slugs, sea hares and garden snails, that flourish in various environments on earth. A unique morphological feature of Euthyneura is the presence of two pairs of sensory head tentacles with different shapes and functions: the anterior labial tentacles and the posterior rhinophores or eyestalks. Here we combine molecular phylogenetic and microanatomical evidence that suggests the two pairs of head tentacles have originated by splitting of the original single tentacle pair (with two parallel nerve cords in each tentacle) as seen in many other gastropods. Minute deep-sea snails of Tjaernoeia and Parvaplustrum, which in our phylogeny belonged to the euthyneurans’ sister group (new infraclass Mesoneura), have tentacles that are split along much of their lengths but associated nerves and epidermal sense organs are not as specialized as in Euthyneura. We suggest that further elaboration of cephalic sense organs in Euthyneura closely coincided with their ecological radiation and drastic modification of body plans. The monotypic family Parvaplustridae nov., superfamily Tjaernoeioidea nov. (Tjaernoeiidae + Parvaplustridae), and new major clade Tetratentaculata nov. (Mesoneura nov. + Euthyneura) are also proposed based on their phylogenetic relationships and shared morphological traits.

Gastropods (slugs and snails) are prominent and species-rich faunal elements in marine and terrestrial habitats of the tropics. While several clades of snails inhabit freshwater systems, slugs are extremely rare in freshwater: only the centimeter-sized Acochlidiidae, with currently three genera, contain more than one species and live in the lower reaches of island streams in an area comprising Eastern Indonesia, Fiji, and Palau. Where known, the species of this unique group are specialized predators of other amphidromous snails’ egg capsules (Neritidae) and their reproductive biology and adaptations to life in freshwater are complex. Acochlidiidae are thus of special interest for evolutionary biology and ecology. We here describe a new genus of unusually bluish-green acochlidiid to date known only from a single locality on the island of Ambon, Indonesia. Previous molecular data found this charismatic species to link slender Strubellia slugs with broad and flattened Acochlidium and Palliohedyle. We establish Wallacellia siputbiru n. gen. n. sp., the “blue slug” in Bahasa Indonesia, by using scanning electron microscopy of cuticular elements, light microscopy of serial semithin histological sections of the soft body, and 3D reconstruction of all organ systems based on these sections. Special structures of this seemingly rare endemic species include the enlarged kidney and the huge copulatory organ. Our data now clarify that, in the invasion of freshwater habitats in Acochlidiidae, sexual selection (the anterior three-part copulatory organ) preceded ecological selection (posterior flattened habitus with branched or multiplied internal organs).

The genus Micromelo (family Aplustridae) occurs in almost all tropical and subtropical waters across the globe, with the exception of the Eastern Pacific. Most authors consider Micromelo undatus (Bruguière, 1792) as the only valid species in this genus. This study examines populations of specimens identified as M. undatus across its geographic range, using morphological and genetic data from two mitochondrial genes (16S and CO1) and one nuclear gene (Histone H3). The results reveal that M. undatus is a complex of four species with consistent genetic and anatomical differences. A literature review and evaluation of type material indicates that available names exist for three of the four species. Micromelo guamensis, M. undatus and M. scriptus are resurrected for species found in the Western Pacific, the Atlantic Ocean, and widespread in the Indo-Pacific, respectively. A new name is introduced for another species found in the Western Pacific, namely Micromelo barbarae sp. nov. and a neotype is designated for the type species of the genus M. undatus. publishedVersion

Background Heterobranchia is a diverse clade of marine, freshwater, and terrestrial gastropod molluscs. It includes such disparate taxa as nudibranchs, sea hares, bubble snails, pulmonate land snails and slugs, and a number of (mostly small-bodied) poorly known snails and slugs collectively referred to as the “lower heterobranchs”. Evolutionary relationships within Heterobranchia have been challenging to resolve and the group has been subject to frequent and significant taxonomic revision. Mitochondrial (mt) genomes can be a useful molecular marker for phylogenetics but, to date, sequences have been available for only a relatively small subset of Heterobranchia. Results To assess the utility of mitochondrial genomes for resolving evolutionary relationships within this clade, eleven new mt genomes were sequenced including representatives of several groups of “lower heterobranchs”. Maximum likelihood analyses of concatenated matrices of the thirteen protein coding genes found weak support for most higher-level relationships even after several taxa with extremely high rates of evolution were excluded. Bayesian inference with the CAT + GTR model resulted in a reconstruction that is much more consistent with the current understanding of heterobranch phylogeny. Notably, this analysis recovered Valvatoidea and Orbitestelloidea in a polytomy with a clade including all other heterobranchs, highlighting these taxa as important to understanding early heterobranch evolution. Also, dramatic gene rearrangements were detected within and between multiple clades. However, a single gene order is conserved across the majority of heterobranch clades. Conclusions Analysis of mitochondrial genomes in a Bayesian framework with the site heterogeneous CAT + GTR model resulted in a topology largely consistent with the current understanding of heterobranch phylogeny. However, mitochondrial genomes appear to be too variable to serve as good phylogenetic markers for robustly resolving a number of deeper splits within this clade.

Rhodopemorphs are small, interstitial or psammobiotic heterobranch slugs, which have been troubling to place phylogenetically. Their small size and habit of living in or among sediment have led to a correlated reduction and simplification of morphology, and consequently to contradictory phylogenetic signal from anatomical features. When morphological data have previously been used to generate phylogenetic hypotheses, these were vulnerable to the effects of homoplasy. We collected multiple species of Rhodope, along with another rhodopemorph genus Helminthope, to produce DNA sequence data for the first time to test their monophyly. We sequenced mitochondrial and nuclear genes, and analysed the data under maximum likelihood and Bayesian inference. By analysing these data in a broader heterobranch dataset, we also examined the placement of Rhodopemorpha within Heterobranchia. Despite rhodopemorphs showing aspects of a euthyneurous (and pentaganglionate) condition, their placement in a molecular phylogeny occurs outside the taxon defined by this term (i.e. Euthyneura = Pentaganglionata). Instead, model-based inferences placed rhodopemorphs among basal heterobranch taxa, usually as a clade sister to a shelled group (Murchisonellidae) that was recently removed from the Pyramidelloidea. The Rhodopemorpha + Murchisonellidae clade is herein termed Allomorpha. Three-dimensional reconstruction methods have elucidated potential morphological homologies for Rhodopemorpha and comparisons with Murchisonellidae have also uncovered morphological support for this placement. Thus, we consider the phylogenetic placement of Rhodopemorpha solved, although relationships among lower Heterobranchia lineages remain challenging.

The Thecosomata are pelagic euopisthobranch pteropods that are important for marine food chains, but threatened by ocean acidification. Members of the suborder Euthecosomata are either torted snails with a coiled, sinistral shell (Limacinidae) or are straight-shelled with a symmetrical body and an unusual ventral mantle cavity (Orthoconcha). The classification and taxonomy of euthecosomes still depends on shells, but is being challenged by initial molecular data. There is a large body of morphoanatomical information dating from the beginning of the last century, and only biological (rather than soft-part anatomical) detail has been added since. For our initial study on pteropod morphoanatomy we have selected the potentially basal orthoconch genus Creseis Rang, 1828. Supplementing Meisenheimer’s (1905) monographic work, we redescribe the microanatomy of the Mediterranean C. clava (Rang, 1828) from serial semithin sections and present 3D-models of all major organ systems. In the absence of histological differences we interpret the head to be fused with the foot, forming the wings with reduced labial tentacles and rhinophores. The postpharyngeal nerve ring is strongly condensed, showing fused buccal ganglia and a short visceral loop with two discernable ganglia. The genital system is monaulic and hermaphroditic, with female glands and a potential allosperm receptacle of unclear homology. An open seminal groove connects with the frontal copulatory organ, which shows complex penial infoldings. We confirm the 1808 longitudinal rotation of the visceral organs relative to the condition in limacinids. As an alternative to ontogenetic detorsion, progenesis may have skipped torsion. Other obvious paedomorphoses such as single, basally forked tentacular nerves, suggest that heterochrony has been a driving force in thecosome evolution. Retaining the mantle cavity in a ventral position, Creseis has its large mantle gland—necessary for creating a mucus web for feeding—close to the mouth. Further comparative microanatomical data on orthoconchs and limacinids are needed to corroborate our assumptions of homology, and for reconstructing pteropod evolution once reliable molecular phylogenetic hypotheses are available.

The Murchisonellidae are a small taxon of minute snails with a high-spired shell that occur in shallow marine habitats. Molecular phylogenetics recently revealed that they are not members of the externally similar yet phylogenetically derived Pyramidellidae, but instead potentially one of the oldest clades among the heterobranch Gastropoda. Furthermore, current data surprisingly indicate a sister-group relationship with Rhodopemorpha, highly aberrant marine slugs with previously unclear affinities. Murchisonellidae are characterized by a specialized pincer-like radula, but very little further data exist on soft-body anatomy for most species, and there are only a few observations of living animals. Investigation of the anatomy of Murchisonellidae may thus yield new data providing insights into early heterobranch evolution and that of enigmatic Rhodopemorpha. We collected live specimens of the murchisonellid Koloonella cf. minutissima (Laseron, 1951), a member of a genus known mainly from eastern Australia. We provide detailed live photographs and interactive 3D data on all major organ systems, based on serial histological sections. The mantle cavity is shown to contain several distinct glands, a pair of which is conspicuously similar to glands found in Rhodopemorpha. The anterior digestive system contains a unique four-toothed radula, a feeble pharynx and a special, vacuolated oesophageal bulb. The reproductive system is complex and diaulic, and contains unusual structures. These results highlight structural diversity among minute lower Heterobranchia. Soft-body characters do not contradict, and may even support, the counterintuitive sister-group relationship with shell-less, wormshaped Rhodopemorpha. The classification of Murchisonellidae is discussed and a revised scheme is proposed.

Yasunori Kano1, Hiroaki Fukumori1,2, Bastian Brenzinger3 and Anders Waren4 Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan; Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan; Bavarian State Collection of Zoology, Munchhausenstr. 21, D-81247 Munich, Germany; and Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden

The monophyly of the panpulmonate, usually marine benthic Sacoglossa—and its basal division into shelled Oxynoacea and shell-less Plakobranchacea—is undisputed, but family relationships are in doubt. Of particular interest is the potentially basal plakobranchacean family Platyhedylidae, comprising morphologically aberrant members lacking head tentacles or body appendages. Herein we re-describe the type species of the genus Gascoignella, G. aprica Jensen, 1985, from Hong Kong. Morphological data was generated by three-dimensional reconstruction from serial semi-thin sections using Amira software. Our microanatomical results largely confirm the original description. The anterior digestive system is sacoglossan-like but modified, e.g. the ascus is not demarcated externally and pharyngeal pouches are lacking. The digestive gland is bipartite, with two rami separated by a longitudinal, muscular, median septum, but fused in the rear end. The postpharyngeally situated nerve ring contains fused cerebropleural ganglia; the short visceral loop has three ganglia. Two major cerebral nerves were identified as rhinophoral and labiotentacular nerves, innervating sensory areas on the head velum. Gascoignella aprica is a hermaphrodite with a truly androdiaulic genital system of which some originally ambiguous characters are clarified. Bursa and prostate insert into a fertilization chamber proximal to a sac-like albumen gland and a tubular mucus gland. The cephalic copulatory apparatus contains a penis armed with a short and straight stylet and an accessory gland of unclear function; the presumed mode of sperm transfer is discussed. A well-developed heart and a large H-shaped kidney are present; the nephroduct opens into the intestine. Epidermal glands and body tissues are described for the first time. The presence of a unique longitudinal, median septum is considered diagnostic for Platyhedylidae, multiple further apomorphies are given. Morphological evidence supports the molecular phylogenetic hypothesis that the Platyhedylidae could be a basal non-shelled sacoglossan lineage.

Euthyneuran gastropods represent one of the most diverse lineages in Mollusca (with over 30,000 species), play significant ecological roles in aquatic and terrestrial environments and affect many aspects of human life. However, our understanding of their evolutionary relationships remains incomplete due to missing data for key phylogenetic lineages. The present study integrates such a neglected, ancient snail family Ringiculidae into a molecular systematics of Euthyneura for the first time and is supplemented by the first microanatomical data. Surprisingly, both molecular and morphological features present compelling evidence for the common ancestry of ringiculid snails with the highly dissimilar Nudipleura—the most species-rich and well-known taxon of sea slugs (nudibranchs and pleurobranchoids). A new taxon name Ringipleura is proposed here for these long-lost sisters, as one of three major euthyneuran clades with late Palaeozoic origins, along with Acteonacea (Acteonoidea + Rissoelloidea) and Tectipleura (Euopisthobranchia + Panpulmonata). The early Euthyneura are suggested to be at least temporary burrowers with a characteristic ‘bubble’ shell, hypertrophied foot and headshield as exemplified by many extant subtaxa with an infaunal mode of life, while the expansion of the mantle might have triggered the explosive Mesozoic radiation of the clade into diverse ecological niches.

Increasing molecular evidence suggests that the phylogeny of euthyneuran gastropods differs greatly from centenary textbook concepts. The presence, homology and evolution of characters in major subgroups thus need to be reinvestigated. Traditionally basal opisthobranch Cephalaspidea (“head-shield snails and slugs”) were pruned to a new taxon concept, with benthic euopisthobranch and tentacle-bearing cephalaspidean lineages basal to burrowing, head-shield bearing philinoidean species. Among the latter, mesopsammic “microslug” lineages evolved at least twice. Herein we explore in 3D microanatomical detail the putatively basal philinoglossan Pluscula cuica (Marcus, Boletim da Faculdade de Filosofia, Ciencias e Letras. Universidade de Sao Paulo 164:165–203, 1953a) from its type locality in Brazil. The species possesses several “accessory” ganglia and a reduced posterior mantle cavity that retains some putative shell-building tissue and an osphradium. The hermaphroditic, monaulic genital system opens in a posterior position; it retains a bursa copulatrix but lacks a distinct receptaculum seminis. Autosperm is transferred to the cephalic copulatory organ via an external sperm groove, not through the hemocoel, as suggested in the original description. The penis opens through the oral tube, sperm is transferred by a “kiss”. A conspicuous yellow gland is discussed as a modified Blochmann’s gland. Retaining several putative symplesiomorphies with philinoids, Pluscula is discussed as the most basal offshoot in meiofaunal Philinoglossidae. However, the supposed “primitiveness” of the fused rather than separate cerebropleural ganglia and the triganglionate rather than pentaganglionate visceral nerve cord was based on misobservations. Higher categories such as Philinoglossacea for Philinoglossidae, and a separate family Plusculidae for P. cuica are no longer warranted. Inner cephalaspidean relationships and a scenario of more or less successive philinoglossid adaptation to meiofaunal environments should be investigated by molecular studies with more comprehensive taxon sampling.

The turbellarian-like, radula-lacking Rhodope has been a mystery to taxonomists for over 160 years and was considered a specialized off-shoot of either opisthobranch or pulmonate Euthyneura. Occasionally reported from intertidal waters and sand habitats from all continents, most species of these minute slugs are poorly known and characterized mainly by differences in pigmentation. To understand the evolution of heterobranch microslugs, we established a morphological dataset for Rhodope by describing a new species found in the temperate waters of southern Australia. To set a standard for rhodopids, all major organ systems of R. rousei n. sp. are reconstructed three-dimensionally from series of semithin sections using the software Amira. Microanatomy confirms the loss of many general gastropod features such as foot, cephalic tentacles, shell, radula, mantle cavity, gill and heart. Excretory and digestive systems are heavily modified, with free rhogocytes in the presumed position of the heart, and a secondary buccal bulb replacing the function of the vestigial pharynx. Structural details of the monaulic but hermaphroditic genital system suggest cutaneous fertilization via spermatophores formed in specialized glands. The highly concentrated central nervous system is compared to those of other species of the genus and targets of all detectable nerves are summarized. These characters are compared with adaptations shown by other interstitial gastropods.

Nudibranch molluscs of the genus Corambe differ from most other Doridoidea by having ventral rather than dorsal anus and gills. Because of these and other features, such as separate cerebral and pleural ganglia, corambids have been considered as an archaic or enigmatic group. The first tropical eastern Pacific Corambe species is described in morphological and some histological detail. Selected organs such as circulatory and central nervous features are reconstructed from serial semithin histological slides and visualized in three dimensions using Amira software. Anatomical findings include two separate ganglia on the visceral loop and an additional ganglion on the right side of the body that is connected to the pedal ganglion. Corambe mancorensis n. sp. is dorsoventrally depressed, has an oval, fleshy notum covered with a cuticle, and has a wide posterior medial notch that can be closed completely by unique lobules. Gills are arranged in an unusual horseshoe-like manner including both phanerobranch anal (=medial) gills and corambid lateroventral gill rows, and are connected to the atrium by a complex vessel system. The three medial gills arise from a posterodorsal gill cavity within the notal notch, similar to the case in Corambe evelinae Marcus, 1958. By scanning electron microscopy a vestigial gill cavity is also detectable in C. pacifica MacFarland & O'Donoghue, 1929, but here it is situated ventrally. Our new information on adult corambids is compared with new and published ontogenetic data on phanerobranch and cryptobranch dorids, to contribute to a novel interpretation of the ontogeny of dorid mantle and gill complexes. The progenetic evolution of corambids 'recapitulates' early juvenile dorid stages - turning Haeckel's Law upside down.

The evolution and diversification of euthyneuran slugs and snails was likely strongly influenced by habitat transitions from marine to terrestrial and limnic systems. Well-supported euthyneuran phylogenies with detailed morphological data can provide information on the historical, biological and ecological background in which these habitat shifts took place allowing for comparison across taxa. Acochlidian slugs are "basal pulmonates" with uncertain relationships to other major panpulmonate clades. They present a unique evolutionary history with representatives in the marine mesopsammon, but also benthic lineages in brackish water, limnic habitats and (semi-)terrestrial environments. We present the first comprehensive molecular phylogeny on Acochlidia, based on a global sampling that covers nearly 85% of the described species diversity, and additionally, nearly doubles known diversity by undescribed taxa. Our phylogenetic hypotheses are highly congruent with previous morphological analyses and confirm all included recognized families and genera. We further establish an ancestral area chronogram for Acochlidia, document changes in diversification rates in their evolution via the birth-death-shift-model and reconstruct the ancestral states for major ecological traits. Based on our data, Acochlidia originated from a marine, mesopsammic ancestor adapted to tropical waters, in the mid Mesozoic Jurassic. We found that the two major subclades present a remarkably different evolutionary history. The Microhedylacea are morphologically highly-adapted to the marine mesopsammon. They show a circum-tropical distribution with several independent shifts to temperate and temperate cold-habitats, but remained in stunning morphological and ecological stasis since the late Mesozoic. Their evolutionary specialization, which includes a remarkable and potentially irreversible "meiofaunal syndrome", guaranteed long-term survival and locally high species densities but also resembles a dead-end road to morphological and ecological diversity. In contrast, the Hedylopsacea are characterized by morphological flexibility and ecologically by independent habitat shifts out of the marine mesopsammon, conquering (semi-)terrestrial and limnic habitats. Originating from interstitial ancestors with moderate adaptations to the mesopsammic world, they reestablished a benthic lifestyle and secondary "gigantism" in body size. The major radiations and habitat shifts in hedylopsacean families occured in the central Indo-West Pacific in the Paleogene. In the Western Atlantic only one enigmatic representative is known probably presenting a relict of a former pan-Tethys distribution of the clade. This study on acochlidian phylogeny and biogeography adds another facet of the yet complex panpulmonate evolution and shows the various parallel pathways in which these snails and slugs invaded non-marine habitats. Given the complex evolutionary history of Acochlidia, which represent only a small group of Panpulmonata, this study highlights the need to generate comprehensively-sampled species-level phylogenies to understand euthyneuran evolution.

Sediment-covered ocean floors constitute one of the largest and at the same time least explored habitats on Earth, still hiding an unknown level of species diversity. Coastal areas of this marine mesopsammic habitat harbor a variety of heterobranch snails and slugs. These gastropods long were puzzling due to their unclear phylogenetic positions, their aberrant morphologies and the lack of knowledge regarding their biology and diversity. Herein, we briefly review the advances of interstitial gastropod exploration, emphasizing that molecular approaches on formerly enigmatic mesopsammic groups like rhodopemorphs or acochlidians contributed to a drastic reconsideration of heterobranch systematics and evolution. We give an overview of the known diversity of mesopsammic heterobranchs and a list of type localities. In order to enhance surveys on the biodiversity of yet unexplored coasts, we then provide a suitable method to take samples of mesopsammic heterobranchs, and to extract and document slugs an...