A new genus-level classification of the Conoidea is presented, based on the molecular phylogeny of Puillandre et al. in the accompanying paper. Fourteen lineages are recognized and ranked as families to facilitate continuity in the treatment of the names Conidae (for 'cones') and Terebridae in their traditional usage. The hitherto polyphyletic 'Turridae' is now resolved as 13 monophyletic families, in which the 358 currently recognized genera and subgenera are placed, or tentatively allocated: Conorbidae (2 (sub)genera), Borsoniidae (34), Clathurellidae (21), Mitromorphidae (8), Mangeliidae (60), Raphitomidae (71), Cochlespiridae (9), Drilliidae (34), Pseudomelatomidae (= Crassispiridae) (59), Clavatulidae ( 14), Horaiclavidae new family (28), Turridae s. s. (16) and Strictispiridae (2). A diagnosis with description of the shell and radulae is provided for each of these families.
The superfamily Conoidea (Mollusca: Gastropoda) constitutes one of the most diverse and taxonomically challenging groups among marine molluscs. Classifications based on shell or radula characters are highly contradictory and disputed. Whereas the monophyly of the Conidae (cone snails) and Terebridae (auger snails) has not been challenged, the other constituents of the superfamily are placed in a "trash" group, the turrids, the non-monophyly of which has been demonstrated by anatomical and molecular evidence. We present here a new molecular phylogeny based on a total of 102 conoidean genera (87 "turrids", 5 cones and 10 terebrids) and three genes (COI, 12S and 16S). The resulting tree recognizes 14 clades. When the Conidae (Conus s.l.) and Terebridae are ranked as families for consistency of usage, then the "turrids" end up being split into 12 families of comparable rank. A new genus-level classification of the Conoidea is published to accompany the new phylogeny.
The superfamily Conoidea is one of the most speciose groups of marine mollusks, with estimates of about 340 recent valid genera and subgenera, and 4000 named living species. Previous classifications were based on shell and anatomical characters, and clades and phylogenetic relationships are far from well assessed. Based on a dataset of ca. 100 terminal taxa belonging to 57 genera, information provided by fragments of one mitochondrial (COI) and three nuclear (28S, 18S and H3) genes is used to infer the first molecular phylogeny of this group. Analyses are performed on each gene independently as well as for a data matrix where all genes are concatenated, using Maximum Likelihood, Maximum Parsimony and Bayesian approaches. Several well-supported clades are defined and are only partly identifiable to currently recognized families and subfamilies. The nested sampling used in our study allows a discussion of the classification at various taxonomical levels, and several genera, subfamilies and families are found polyphyletic.
Transcriptome-based exon capture methods provide an approach to recover several hundred markers from genomic DNA, allowing for robust phylogenetic estimation at deep timescales. We applied this method to a highly diverse group of venomous marine snails, Conoidea, for which published phylogenetic trees remain mostly unresolved for the deeper nodes. We targeted 850 protein coding genes (678,322 bp) in ca. 120 samples, spanning all (except one) known families of Conoidea and a broad selection of non-Conoidea neogastropods. The capture was successful for most samples, although capture efficiency decreased when DNA libraries were of insufficient quality and/or quantity (dried samples or low starting DNA concentration) and when targeting the most divergent lineages. An average of 75.4% of proteins was recovered, and the resulting tree, reconstructed using both supermatrix (IQ-tree) and supertree (Astral-II, combined with the Weighted Statistical Binning method) approaches, are almost fully supported. A reconstructed fossil-calibrated tree dates the origin of Conoidea to the Lower Cretaceous. We provide descriptions for two new families. The phylogeny revealed in this study provides a robust framework to reinterpret changes in Conoidea anatomy through time. Finally, we used the phylogeny to test the impact of the venom gland and radular type on diversification rates. Our analyses revealed that repeated losses of the venom gland had no effect on diversification rates, while families with a breadth of radula types showed increases in diversification rates, thus suggesting that trophic ecology may have an impact on the evolution of Conoidea.
Venom peptides from predatory organisms are a resource for investigating evolutionary processes such as adaptive radiation or diversification, and exemplify promising targets for biomedical drug development. Terebridae are an understudied lineage of conoidean snails, which also includes cone snails and turrids. Characterization of cone snail venom peptides, conotoxins, has revealed a cocktail of bioactive compounds used to investigate physiological cellular function, predator-prey interactions, and to develop novel therapeutics. However, venom diversity of other conoidean snails remains poorly understood. The present research applies a venomics approach to characterize novel terebrid venom peptides, teretoxins, from the venom gland transcriptomes of Triplostephanus anilis and Terebra subulata. Next-generation sequencing and de novo assembly identified 139 putative teretoxins that were analyzed for the presence of canonical peptide features as identified in conotoxins. To meet the challenges of de novo assembly, multiple approaches for cross validation of findings were performed to achieve reliable assemblies of venom duct transcriptomes and to obtain a robust portrait of Terebridae venom. Phylogenetic methodology was used to identify 14 teretoxin gene superfamilies for the first time, 13 of which are unique to the Terebridae. Additionally, basic local algorithm search tool homology-based searches to venom-related genes and posttranslational modification enzymes identified a convergence of certain venom proteins, such as actinoporin, commonly found in venoms. This research provides novel insights into venom evolution and recruitment in Conoidean predatory marine snails and identifies a plethora of terebrid venom peptides that can be used to investigate fundamental questions pertaining to gene evolution.
The >10,000 living venomous marine snail species [superfamily Conoidea (Fleming, 1822)] include cone snails (Conus), the overwhelming focus of research. Hastula hectica (Linnaeus, 1758), a venomous snail in the family Terebridae (Mörch, 1852) was comprehensively investigated. The Terebridae comprise a major monophyletic group within Conoidea. H. hectica has a striking radular tooth to inject venom that looks like a perforated spear; in Conus, the tooth looks like a hypodermic needle. H. hectica venom contains a large complement of small disulfide-rich peptides, but with no apparent overlap with Conus in gene superfamilies expressed. Although Conus peptide toxins are densely post-translationally modified, no post-translationally modified amino acids were found in any Hastula venom peptide. The results suggest that different major lineages of venomous molluscs have strikingly divergent toxinological and venom-delivery strategies.
The superfamily Buccinoidea is distributed across the oceans of the world from the Arctic Ocean to the Antarctic and from intertidal to abyssal depths. It encompasses 3351 recent species in 337 genera. The latest taxonomic account recognized eight full families. For the first time, the monophyly of the superfamily and the relationships among the families are tested with molecular data supplemented by anatomical and radula data. Five genetic markers were used: fragments of mitochondrial COI, 16S rRNA, 12S rRNA and nuclear Histone 3 (H3) and 28S rRNA genes (for 225 species of 117 genera). Our analysis recovered Buccinoidea monophyletic in Bayesian analyses. The relationships between the formerly recognized families and subfamilies are drastically revised and a new classification of the superfamily is here proposed, now including 20 taxa of family rank and 23 subfamilies. Five new families (Chauvetiidae, Dolicholatiridae, Eosiphonidae, Prodotiidae and Retimohniidae) and one subfamily of Nassariidae (Tomliniinae) are described. Austrosiphonidae and Tudiclidae are resurrected from synonymy and employed in a new taxonomical extension. All but 40 recent genera are reclassified. Our results demonstrate that anatomy is rather uniform within the superfamily. With exceptions, the rather uniform radular morphology alone does not allow the allocation of genera to a particular family without additional molecular data.
The superfamily Olivoidea is broadly distributed in the world's oceans mostly in coastal waters at tropical and subtropical latitudes. It encompasses around 30 Recent genera and 460 species. Two families -Olividae and Olivellidae -are classically recognized within the superfamily. Their shell is very characteristic due to the presence of a modified callused anterior end and a fasciole. Prior to the present work, neither the monophyly of the superfamily nor the relationships among its genera had been tested with molecular phylogenetics. Four genetic markers [cytochrome c oxidase subunit I (COI), 16S and 12S rRNA mitochondrial genes, and Histone 3 (H3) nuclear gene] were sequenced for 42 species in 14 genera. Additionally, 18 species were sequenced for COI only. The molecular dataset was supplemented by anatomical and radula data. Our analysis recovered, albeit with weak support, a monophyletic Olivoidea, which in turn includes with 100% support, in addition to traditional olivoideans, representatives of a paraphyletic Pseudolividae. The relationships between the former families and subfamilies are drastically revised and a new classification of the superfamily is here proposed, now including five families: Bellolividae fam. nov., Benthobiidae fam. nov., Olividae, Pseudolividae and Ancillariidae. Within Olividae four subfamilies are recognized, reflecting the high morphological disparity within the family: Olivinae, Olivellinae, Agaroniinae and Calyptolivinae subfam. nov. All the recent genera are discussed and reclassified based on molecular phylogeny and/or morphology and anatomy. The homology of different features of the shells is established for the first time throughout the superfamily, and a refined terminology is proposed. Based on a correlation between anatomical characteristics and shell features and observations of live animals, we make hypotheses on which part of the mantle is responsible for depositing which callused feature of the shell. Our results demonstrate that morphological data alone should be used with caution for phylogenetic reconstructions. For instance, the radula -that is otherwise considered to be of fundamental importance in the taxonomy of Neogastropoda -is extremely variable within the single family Olividae, with a range of variation larger than within the rest of the entire superfamily. In the refined classification, Pseudolividae are nested within Olivoidea, which is partially returning to 'the roots', that is to the classification of Thiele (1929).
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