Emily A. Glover

A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S and 28S rRNA genes

A new molecular phylogeny is presented for the highly diverse, bivalve molluscan subclass Heterodonta. The study, the most comprehensive for heterodonts to date, used new sequences of 18S and 28S rRNA genes for 103 species from 49 family groups with species of Palaeoheterodonta (Trigoniidae, Margaritiferidae and Unionidae) as outgroups. Results confirm previous analyses that the Carditidae/Astartidae/Crassatellidae clade is basal to all other heterodonts including Anomalodesmata (often classified as a separate subclass or order). Thyasiroidea occupy a near basal position between the Crassatelloidea and Anomalodesmata. Lucinidae form a well‐supported monophyletic group distinct from Thyasiridae and Ungulinidae. The Solenoidea and Hiatelloidea link as sister groups distant from the Tellinoidea and Myoidea, respectively, where they had been previously associated. The position of the Gastrochaenidae is unstable but does not group with myoidean taxa. Species of four families of Galeommatoidea form a clade that also includes Sportellidae of the Cyamioidea. The Cardioidea and Tellinoidea form highly supported, long branched, individual clades but group as sister taxa. A major clade including Veneroidea, Mactroidea, Myoidea and other families is given the unranked name Neoheterodontei. There is no support for a separate order Myoida (Myoidea and Pholadoidea). Dreissenidae group within the clade including Myidae, Corbulidae, Pholadidae and Teredinidae. The Corbiculoidea is confirmed as polyphyletic with the Sphaeriidae and Corbiculidae forming separate clades within the Neoheterodontei; Corbiculidae grouping with the Glauconomidae. Hemidonacidae are unrelated to the Cardiidae, as previously proposed, but nest within the Neoheterodontei. The Gaimardiidae group near to the Ungulinidae and not with Cyamioidea where most recently classified. The family Ungulinidae, previously classified in the Lucinoidea, forms a well‐supported clade within the Neoheterodontei and is elevated to superfamily rank — Ungulinoidea. The monophyletic status of Glossoidea, Arcticoidea and Veneroidea is unconfirmed. A brief review of the fossil record of the heterodonts indicates that the basal clades of Crassatelloidea, Anomalodesmata and Lucinoidea diverged very early in the Lower Palaeozoic. Other groups such as the Hiatelloidea, Solenoidea, Gastrochaenidae probably were of late Palaeozoic origins. The Cardioidea and Tellinoidea originated in the Triassic while major groups of Neoheterodontei radiated in the Late Mesozoic. The phylogenetic position of the Thyasiroidea and Galeommatoidea suggests a longer fossil history than has so far been recognized.

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.

Functional anatomy, chemosymbiosis and evolution of the Lucinidae

Abstract All Lucinidae species studied so far possess sulphide-oxidizing, chemosymbiotic bacteria housed in bacteriocytes of gill filaments. The ecology, functional anatomy and evolution of the Lucinidae must be considered in relation to this symbiosis. The ctenidia have been extensively studied but other anatomical structures peculiar to lucinids have received much less attention. Reviewed are the morphological diversity of living lucinids, highlighting features of their anatomy including ctenidia, pallial apertures, anterior adductor mucsle, pallial blood vessel and mantle gills. The latter are much more complex than previously understood and are here redescribed. They comprise folded structures located near the anterior adductor muscle in Codakia, Phacoides and Lucina, and on the septum of Anodontia. These are interpreted as secondary respiratory surfaces, their location enabling the separation of the anterior inflow of oxygenated water from sulphide-containing water. The latter is released from the sediment by the probing activities of the highly extensible foot and is pumped over the gill through the pedal gape and perhaps also via the exhalant tube. The shell features of Ilionia from the Silurian Period suggests that the lucinid chemosymbiosis is an ancient association.

Evolutionary relationships of the bivalve family Thyasiridae (Mollusca: Bivalvia), monophyly and superfamily status

Molecular analyses of 13 species of the marine bivalve family Thyasiridae, using sequences from 18S rRNA and 28S rRNA genes, showed that the family is monophyletic despite the anatomical disparity and inclusion of both chemosymbiotic and asymbiotic species. This new analysis also confirmed that the three families (Thyasiridae, Lucinidae and Ungulinidae), previously included in the Lucinoidea, were not closely related. Four species of Ungulinidae grouped within a clade containing Veneridae, Arcticidae and Mactridae. In relation to a range of other heterodont bivalves, Thyasiridae occupied a near basal position, apart from a clade comprising Carditidae/Astartidae/Crassatellidae. The earliest thyasirid recognized in the fossil record is a species from the Lower Cretaceous of England. Within the Thyasiridae, some groups can be identified but relations between these are weakly supported. Amongst the taxa analysed, those with symbiotic bacteria and two ctenidial demibranchs belong to at least three groups, while there is some support for a clade of asymbiotic taxa with single demibranchs. In recognition of the monophyletic status of the Thyasiridae, distinct from all other heterodont bivalves, we elevate the rank to superfamily Thyasiroidea.

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.

Cryptic diversity of chemosymbiotic bivalves: A systematic revision of worldwide Anodontia (Mollusca: Bivalvia: Lucinidae)

Abstract Marine bivalves of the family Lucinidae possess a likely obligate chemosymbiosis with sulphide‐oxidising bacteria from which they derive much of their nutrition. Molecular analysis has shown that species of the ’Anodontia’ group form a distinct clade within the monophyletic Lucinidae. Species identification of the largely tropical ’Anodontia’ group, has been confused because of the white, sub‐spherical, smooth, toothless shells, with the name Anodontia edentula used uncritically for most Indo‐West Pacific species. Preliminary morphological analysis also showed that the group was much more diverse than previously realised. The present systematic revision of the world Anodontia species, based on museum collections, field sampling, anatomical and molecular data, now recognises 25 species (eight of these new). These species are divided into eight subgenera (four of these, Euanodontia, Afrophysema, Crytophysema and Bythosphaera are new) on the basis of shell morphology, corroborated by some molecular data. Two species are known from the tropical eastern Pacific, two from the Western Atlantic, five from the eastern Atlantic and 16 from the Indo‐West Pacific. Two new genera, Neophysema (type species N. aphanes sp. nov.) and Leucosphaera (type species Loripinus salamensis Thiele & Jaeckel, 1931), are proposed for species previously confused with Anodontia.

Marine Carbonate Cements, Biofilms, Biomineralization, and Skeletogeneis: Some Bivalves Do It All

Recent years have seen a growing interest in the direct and indirect roles of organisms, and more explicitly of organic matter, in the crystallization of minerals in sediments. Two bivalve genera form extensive biofilms that are apparently responsible for the growth of a variety of isolated crystals together with a marine cement. Granicorium indutum and Samarangia quadrangularis are infaunal species that cover their shells with a cemented coating of sand, sculpted to mimic the surface ornament typical of many bivalves. Granicorium has an exceptionally mobile mantle margin that produces large volumes of mucus, harboring a diverse microbial community. The sand grains surrounding both species are initially bound by a biofilm that provides structural integrity but also acts, like others, as a template for the crystallization of a variety of carbonate polymorphs. These include varied prismatic crystals, rice-grain and wheatsheaf forms and, more importantly, large volumes of acicular crystals indistinguishable from typical marine cements. The distribution of these crystals is related to positions accessible to the mantle of the animal and in Samarangia appears to result from the active emplacement of grains and mucus several times a year. Summing the evidence, it seems that these species are responsible not only for the biomineralization involved in the formation of their shells but also for crystallization mediated through biofilms and for the generation of cements that are morphologically indistinguishable from typical marine cements. The boundaries between these three strategies may be closer than we think.

Diet of olives: Oliva tigridella Duclos, 1835 in Queensland

Abstract Field observations of Oliva tigridella in Queensland revealed a diet of small gastropods, bivalves, echinoids and holothurians. Foraging animals were observed carrying prey attached to the rear of the foot. Up to seven prey items were recorded on the foot. Analysis of gut co ntents showed a high frequency of holothurian spicules although these were rare amongst items found on the foot. This study reveals a previously unrecorded catholic diet of olives although small gastropods and bivalves are important components.

New lucinid bivalves from shallow and deeper water of the Indian and West Pacific Oceans (Mollusca, Bivalvia, Lucinidae).

Abstract Four new species and a new genus of lucinid bivalves are described from shallow and deeper waters in the Indian and West Pacific Oceans. The new genus Scabrilucina (subfamily Lucininae) includes the little-known Scabrilucina victorialis (Melvill, 1899) from the Arabian Sea and Scabrilucina vitrea (Deshayes, 1844) from the Andaman Sea as well as a new species Scabrilucina melvilli from the Torres Strait off northeastern Australia. Ferrocina brunei new species (Lucininae) was recovered from 60 m near oil drilling activities off Borneo; its anatomy confirmed the presence of symbiotic bacteria. Two unusual deeper water species of Leucosphaerinae are described, both species included in on-going molecular analyses; Gonimyrtea ferruginea from 400–650 m in the southwest Pacific and Myrtina reflexa from 200–825 m off Zanzibar and Madagascar.