Rüdiger Bieler

Nomenclator of Bivalve Families with a Classification of Bivalve Families

ABSTRACT Some 1,048 names at the rank of subtribe, tribe, subfamily, family and superfamily have been proposed for Recent and fossil bivalves. All names are listed in a nomenclator giving full bibliographical reference, date of publication, type genus, and their nomenclatural availability and validity under the International Code of Zoological Nomenclature. Another 274 names, established for categories above the family-group are listed separately. A working classification attempts to group all bivalve family-group names into a single system based on current hypotheses of relations and synonymies. At several rank levels, the groups are given in alphabetical rather than some assumed phylogenetic arrangement, reflecting current uncertainties and conflicting results from anatomical, molecular, and fossil data. Altogether, the classification recognizes as valid a total of 324 families, of which 214 are known exclusively as fossils and 110 occur in the Recent with or without a fossil record.

Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters

Abstract. To re-evaluate the relationships of the major bivalve lineages, we amassed detailed morpho-anatomical, ultrastructural and molecular sequence data for a targeted selection of exemplar bivalves spanning the phylogenetic diversity of the class. We included molecular data for 103 bivalve species (up to five markers) and also analysed a subset of taxa with four additional nuclear protein-encoding genes. Novel as well as historically employed morphological characters were explored, and we systematically disassembled widely used descriptors such as gill and stomach ‘types’. Phylogenetic analyses, conducted using parsimony direct optimisation and probabilistic methods on static alignments (maximum likelihood and Bayesian inference) of the molecular data, both alone and in combination with morphological characters, offer a robust test of bivalve relationships. A calibrated phylogeny also provided insights into the tempo of bivalve evolution. Finally, an analysis of the informativeness of morphological characters showed that sperm ultrastructure characters are among the best morphological features to diagnose bivalve clades, followed by characters of the shell, including its microstructure. Our study found support for monophyly of most broadly recognised higher bivalve taxa, although support was not uniform for Protobranchia. However, monophyly of the bivalves with protobranchiate gills was the best-supported hypothesis with incremental morphological and/or molecular sequence data. Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata and Imparidentia new clade ( = Euheterodonta excluding Anomalodesmata) were recovered across analyses, irrespective of data treatment or analytical framework. Another clade supported by our analyses but not formally recognised in the literature includes Palaeoheterodonta and Archiheterodonta, which emerged under multiple analytical conditions. The origin and diversification of each of these major clades is Cambrian or Ordovician, except for Archiheterodonta, which diverged from Palaeoheterodonta during the Cambrian, but diversified during the Mesozoic. Although the radiation of some lineages was shifted towards the Palaeozoic (Pteriomorphia, Anomalodesmata), or presented a gap between origin and diversification (Archiheterodonta, Unionida), Imparidentia showed steady diversification through the Palaeozoic and Mesozoic. Finally, a classification system with six major monophyletic lineages is proposed to comprise modern Bivalvia: Protobranchia, Pteriomorphia, Palaeoheterodonta, Archiheterodonta, Anomalodesmata and Imparidentia.

Changing identities: tRNA duplication and remolding within animal mitochondrial genomes

Although the majority of metazoan mitochondrial genomes (mtDNAs) contain the same 37 genes, including 22 encoding transfer RNAs (tRNAs), the recognition of orthologs is not always straightforward. Here we demonstrate that inferring tRNA orthologs among taxa by using anticodon triplets and deduced secondary structure can be misleading: through a process of tRNA duplication and mutation in the anticodon triplet, remolded leucine (LUUR) tRNA genes have repeatedly taken over the role of isoaccepting LCUN leucine tRNAs within metazoan mtDNA. In the present work, data from within the gastropods and a broad survey of metazoan mtDNA suggest that tRNA leucine duplication and remolding events have occurred independently at least seven times within three major animal lineages. In all cases where the mechanism of gene remolding can be inferred with confidence, the direction is the same: from LUUR to LCUN. Gene remolding and its apparent asymmetry have significant implications for the use of mitochondrial tRNA gene orders as phylogenetic markers. Remolding complicates the identification of orthologs and can result in convergence in gene order. Careful sequence-based analysis of tRNAs can help to recognize this homoplasy, improving gene-order-based phylogenetic hypotheses and underscoring the importance of careful homology assessment. tRNA remolding also provides an additional mechanism by which gene order changes can occur within mtDNA: through the changing identity of tRNA genes themselves. Recognition of these remolding events can lead to new interpretations of gene order changes, as well as the discovery of phylogenetically relevant gene dynamics that are hidden at the level of gene order alone.

A phylogenetic backbone for Bivalvia: an RNA-seq approach.

Bivalves are an ancient and ubiquitous group of aquatic invertebrates with an estimated 10 000–20 000 living species. They are economically significant as a human food source, and ecologically important given their biomass and effects on communities. Their phylogenetic relationships have been studied for decades, and their unparalleled fossil record extends from the Cambrian to the Recent. Nevertheless, a robustly supported phylogeny of the deepest nodes, needed to fully exploit the bivalves as a model for testing macroevolutionary theories, is lacking. Here, we present the first phylogenomic approach for this important group of molluscs, including novel transcriptomic data for 31 bivalves obtained through an RNA-seq approach, and analyse these data with published genomes and transcriptomes of other bivalves plus outgroups. Our results provide a well-resolved, robust phylogenetic backbone for Bivalvia with all major lineages delineated, addressing long-standing questions about the monophyly of Protobranchia and Heterodonta, and resolving the position of particular groups such as Palaeoheterodonta, Archiheterodonta and Anomalodesmata. This now fully resolved backbone demonstrates that genomic approaches using hundreds of genes are feasible for resolving phylogenetic questions in bivalves and other animals.

Sessile snails, dynamic genomes: gene rearrangements within the mitochondrial genome of a family of caenogastropod molluscs

BackgroundWidespread sampling of vertebrates, which comprise the majority of published animal mitochondrial genomes, has led to the view that mitochondrial gene rearrangements are relatively rare, and that gene orders are typically stable across major taxonomic groups. In contrast, more limited sampling within the Phylum Mollusca has revealed an unusually high number of gene order arrangements. Here we provide evidence that the lability of the molluscan mitochondrial genome extends to the family level by describing extensive gene order changes that have occurred within the Vermetidae, a family of sessile marine gastropods that radiated from a basal caenogastropod stock during the Cenozoic Era.ResultsMajor mitochondrial gene rearrangements have occurred within this family at a scale unexpected for such an evolutionarily young group and unprecedented for any caenogastropod examined to date. We determined the complete mitochondrial genomes of four species (Dendropoma maximum, D. gregarium, Eualetes tulipa, and Thylacodes squamigerus) and the partial mitochondrial genomes of two others (Vermetus erectus and Thylaeodus sp.). Each of the six vermetid gastropods assayed possessed a unique gene order. In addition to the typical mitochondrial genome complement of 37 genes, additional tRNA genes were evident in D. gregarium (trnK) and Thylacodes squamigerus (trnV, trnLUUR ). Three pseudogenes and additional tRNAs found within the genome of Thylacodes squamigerus provide evidence of a past duplication event in this taxon. Likewise, high sequence similarities between isoaccepting leucine tRNAs in Thylacodes, Eualetes, and Thylaeodus suggest that tRNA remolding has been rife within this family. While vermetids exhibit gene arrangements diagnostic of this family, they also share arrangements with littorinimorph caenogastropods, with which they have been linked based on sperm morphology and primary sequence-based phylogenies.ConclusionsWe have uncovered major changes in gene order within a family of caenogastropod molluscs that are indicative of a highly dynamic mitochondrial genome. Studies of mitochondrial genomes at such low taxonomic levels should help to illuminate the dynamics of gene order change, since the telltale vestiges of gene duplication, translocation, and remolding have not yet been erased entirely. Likewise, gene order characters may improve phylogenetic hypotheses at finer taxonomic levels than once anticipated and aid in investigating the conditions under which sequence-based phylogenies lack resolution or prove misleading.

Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca)

Revived interest in molluscan phylogeny has resulted in a torrent of molecular sequence data from phylogenetic, mitogenomic, and phylogenomic studies. Despite recent progress, basal relationships of the class Bivalvia remain contentious, owing to conflicting morphological and molecular hypotheses. Marked incongruity of phylogenetic signal in datasets heavily represented by nuclear ribosomal genes versus mitochondrial genes has also impeded consensus on the type of molecular data best suited for investigating bivalve relationships. To arbitrate conflicting phylogenetic hypotheses, we evaluated the utility of four nuclear protein-encoding genes-ATP synthase β, elongation factor-1α, myosin heavy chain type II, and RNA polymerase II-for resolving the basal relationships of Bivalvia. We sampled all five major lineages of bivalves (Archiheterodonta, Euheterodonta [including Anomalodesmata], Palaeoheterodonta, Protobranchia, and Pteriomorphia) and inferred relationships using maximum likelihood and Bayesian approaches. To investigate the robustness of the phylogenetic signal embedded in the data, we implemented additional datasets wherein length variability and/or third codon positions were eliminated. Results obtained include (a) the clade (Nuculanida+Opponobranchia), i.e., the traditionally defined Protobranchia; (b) the monophyly of Pteriomorphia; (c) the clade (Archiheterodonta+Palaeoheterodonta); (d) the monophyly of the traditionally defined Euheterodonta (including Anomalodesmata); and (e) the monophyly of Heteroconchia, i.e., (Palaeoheterodonta+Archiheterodonta+Euheterodonta). The stability of the basal tree topology to dataset manipulation is indicative of signal robustness in these four genes. The inferred tree topology corresponds closely to those obtained by datasets dominated by nuclear ribosomal genes (18S rRNA and 28S rRNA), controverting recent taxonomic actions based solely upon mitochondrial gene phylogenies.

A family-level Tree of Life for bivalves based on a Sanger-sequencing approach

The systematics of the molluscan class Bivalvia are explored using a 5-gene Sanger-based approach including the largest taxon sampling to date, encompassing 219 ingroup species spanning 93 (or 82%) of the 113 currently accepted bivalve families. This study was designed to populate the bivalve Tree of Life at the family level and to place many genera into a clear phylogenetic context, but also pointing to several major clades where taxonomic work is sorely needed. Despite not recovering monophyly of Bivalvia or Protobranchia-as in most previous Sanger-based approaches to bivalve phylogeny-our study provides increased resolution in many higher-level clades, and supports the monophyly of Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Heterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata, Imparidentia, and Neoheterodontei, in addition to many other lower clades. However, deep nodes within some of these clades, especially Pteriomorphia and Imparidentia, could not be resolved with confidence. In addition, many families are not supported, and several are supported as non-monophyletic, including Malletiidae, Nuculanidae, Yoldiidae, Malleidae, Pteriidae, Arcidae, Propeamussiidae, Iridinidae, Carditidae, Myochamidae, Lyonsiidae, Pandoridae, Montacutidae, Galeommatidae, Tellinidae, Semelidae, Psammobiidae, Donacidae, Mactridae, and Cyrenidae; Veneridae is paraphyletic with respect to Chamidae, although this result appears to be an artifact. The denser sampling however allowed testing specific placement of species, showing, for example, that the unusual Australian Plebidonax deltoides is not a member of Donacidae and instead nests within Psammobiidae, suggesting that major revision of Tellinoidea may be required. We also showed that Cleidothaerus is sister group to the cementing member of Myochamidae, suggesting that Cleidothaeridae may not be a valid family and that cementation in Cleidothaerus and Myochama may have had a single origin. These results highlight the need for an integrative approach including as many genera as possible, and that the monophyly and relationships of many families require detailed reassessment. NGS approaches may be able to resolve the most recalcitrant nodes in the near future.

Marine bivalves of the Florida Keys: discovered biodiversity

Abstract A survey of marine bivalve biodiversity in the Florida Keys, an island archipelago off southern Florida, was compiled from original collecting, museum specimens and the literature. Assembly of over 6000 records resulted in 325 species, 47% of which can be considered common to abundant in the Keys. This represents a 100% increase over the previously known fauna, largely attributable to critical review of museum specimens. Capture of species occurrences from the literature, especially when non-traditional sources (newsletters, agency reports) are excluded, is shown to be least effective, producing only 44% of the total. Bivalve distributions within the Keys show that the fauna is tropical. One-third of the species are wide ranging along the island chain; however, a latitudinal cline in faunal similarity exists from the Upper Keys southwestwards to Dry Tortugas. The fauna of Florida Bay is the most divergent within the study region and also compared to other, ecologically complex, western Atlantic tropical-subtropical regions. Limited historical records indicate little species turnover in the Keys, although population reductions along the main highway and habitat shifts (from natural to artificial substrata) are evident. These results have implications for biodiversity survey methods and, more locally, for management of the Florida Keys National Marine Sanctuary.

Deconstructing Dendropoma: A Systematic Revision of a World-Wide Worm-Snail Group, with Descriptions of New Genera (Caenogastropoda: Vermetidae)

ABSTRACT Identifying natural groups within the caenogastropod family Vermetidae has proven challenging. The sessile lifestyle of vermetids, with associated xenomorphically distorted, overgrown and corroded shells, has resulted in a long and confused taxonomic history based primarily on adult shell characters. In this study, we use morphological, anatomical and molecular data to clarify systematics and phylogenetic relationships within the genus Dendropoma s.l. We assess generic names previously used in the Dendropoma group for availability and recognize Veristoa Iredale, 1937, as a junior synonym of Dendropoma Mörch, 1861. We describe 21 species, eight of which are new, place them into four robustly supported genera (Dendropoma s.s.; Novastoa Finlay, 1926; Ceraesignum n. gen.; Cupolaconcha n. gen.), and outline the current state of knowledge of the distribution of these taxa. The genus Dendropoma s.s. is well supported in our phylogenetic analysis and is additionally supported by features of the operculum, reproductive traits and a novel mitochondrial gene order. Among the four genera, members of Dendropoma s.s. alone maintain unstalked egg capsules in the mantle cavity rather than attaching them to the shell via a slit in the female mantle. The opercula of examined species within the genus Novastoa are characterized by a well-developed mammilla on the internal surface and upright tightly packed spiral lamina on the external surface. In Ceraesignum n. gen., the operculum lacks a mammilla and displays a fingerprint-like texture on its inner surface. The genera Ceraesignum n. gen. and Novastoa form a well-supported monophyletic group with the genus Dendropoma s.s., although sister group relationships among these genera are not resolved. The fourth genus, Cupolaconcha n. gen. is more closely related to the vermetid genera Eualetes Keen, 1971a, Thylaeodus Mörch, 1860, and Petaloconchus Lea, 1843, demonstrating that Dendropoma s.l. is not a monophyletic group. The calcified operculum of Cupolaconcha n. gen. is unique in the Vermetidae and examined species in this genus are also characterized by a translocation of the valine mitochondrial tRNA. Further study will encompass the full range of morphological diversity in the Vermetidae to clarify the major lineages within this remarkable family of snails.

Bivalvia—A Discussion of Known Unknowns*

Abstract. Bivalves share many of the “deeper” questions with the other molluscan groups - issues such as their origin and sister-group relationships within the Mollusca, and their suitability to explore molecular data in a “known” fossil framework. Other questions are more specific to bivalves, a group that radiated so successfully and nowadays predominantly specializes as infaunal and sessile epifaunal suspension feeders. This paper highlights and explores unanswered questions, from the seemingly trivial and mundane (e.g., how many species are actually out there?), to exploring enigmatic clades about which we know extremely little besides their shells, to macroevolutionary questions that could best be addressed by bivalve-based data. Fast-developing molecular approaches, including the first genome-level and transcriptomic data, a resurgence of detailed morphological and soft-anatomical research, and a renewed focus on Bivalvia by biological and paleontological workers provide us with an opportunity to address such issues. Coordination of efforts - and reciprocal illumination - across traditional disciplinary boundaries will be key factors in such endeavors.