Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera) or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites or can be shell-less but with a typical molluscan radula and serially repeated gills. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.
BackgroundMany marine meiofaunal species are reported to have wide distributions, which creates a paradox considering their hypothesized low dispersal abilities. Correlated with this paradox is an especially high taxonomic deficit for meiofauna, partly related to a lower taxonomic effort and partly to a high number of putative cryptic species. Molecular-based species delineation and barcoding approaches have been advocated for meiofaunal biodiversity assessments to speed up description processes and uncover cryptic lineages. However, these approaches show sensitivity to sampling coverage (taxonomic and geographic) and the success rate has never been explored on mesopsammic Mollusca.ResultsWe collected the meiofaunal sea-slug Pontohedyle (Acochlidia, Heterobranchia) from 28 localities worldwide. With a traditional morphological approach, all specimens fall into two morphospecies. However, with a multi-marker genetic approach, we reveal multiple lineages that are reciprocally monophyletic on single and concatenated gene trees in phylogenetic analyses. These lineages are largely concordant with geographical and oceanographic parameters, leading to our primary species hypothesis (PSH). In parallel, we apply four independent methods of molecular based species delineation: General Mixed Yule Coalescent model (GMYC), statistical parsimony, Bayesian Species Delineation (BPP) and Automatic Barcode Gap Discovery (ABGD). The secondary species hypothesis (SSH) is gained by relying only on uncontradicted results of the different approaches (‘minimum consensus approach’), resulting in the discovery of a radiation of (at least) 12 mainly cryptic species, 9 of them new to science, some sympatric and some allopatric with respect to ocean boundaries. However, the meiofaunal paradox still persists in some Pontohedyle species identified here with wide coastal and trans-archipelago distributions.ConclusionsOur study confirms extensive, morphologically cryptic diversity among meiofauna and accentuates the taxonomic deficit that characterizes meiofauna research. We observe for Pontohedyle slugs a high degree of morphological simplicity and uniformity, which we expect might be a general rule for meiofauna. To tackle cryptic diversity in little explored and hard-to-sample invertebrate taxa, at present, a combined approach seems most promising, such as multi-marker-barcoding (i.e., molecular systematics using mitochondrial and nuclear markers and the criterion of reciprocal monophyly) combined with a minimum consensus approach across independent methods of molecular species delineation to define candidate species.
The discovery of four new Xenoturbella species from deep waters of the eastern Pacific Ocean is reported here. The genus and two nominal species were described from the west coast of Sweden, but their taxonomic placement remains unstable. Limited evidence placed Xenoturbella with molluscs, but the tissues can be contaminated with prey. They were then considered deuterostomes. Further taxon sampling and analysis have grouped Xenoturbella with acoelomorphs (=Xenacoelomorpha) as sister to all other Bilateria (=Nephrozoa), or placed Xenacoelomorpha inside Deuterostomia with Ambulacraria (Hemichordata + Echinodermata). Here we describe four new species of Xenoturbella and reassess those hypotheses. A large species (>20 cm long) was found at cold-water hydrocarbon seeps at 2,890 m depth in Monterey Canyon and at 1,722 m in the Gulf of California (Mexico). A second large species (~10 cm long) also occurred at 1,722 m in the Gulf of California. The third large species (~15 cm long) was found at ~3,700 m depth near a newly discovered carbonate-hosted hydrothermal vent in the Gulf of California. Finally, a small species (~2.5 cm long), found near a whale carcass at 631 m depth in Monterey Submarine Canyon (California), resembles the two nominal species from Sweden. Analysis of whole mitochondrial genomes places the three larger species as a sister clade to the smaller Atlantic and Pacific species. Phylogenomic analyses of transcriptomic sequences support placement of Xenacoelomorpha as sister to Nephrozoa or Protostomia.
Strong currents and deep passages of water can be barriers for larval dispersal of continental marine animals, but potential effects on direct developers are under-investigated. We examined the genetic structure of Doris kerguelenensis, a directly developing sea slug that occurs across the Drake Passage, the body of water separating Antarctica from South America. We found deep mitochondrial divergences within populations on both sides of the Drake Passage, and South American animals formed multiple sister-group relationships with Antarctic animals. A generalised molecular clock suggested these trans-Drake pairs diverged during the Pliocene–Pleistocene, after the formation of the Drake Passage. Statistical parsimony methods recovered 29 separate haplotype networks (many sympatric) that likely correlate with allopatric events caused by repeated glacial cycles. Data from 16S were congruent but more conserved than COI, and the estimated ancestral 16S haplotype was widespread. The marked difference in the substitution rates between these two mitochondrial genes results in different estimates of connectivity. Demographic analyses on networks revealed some evidence for selection and expanding populations. Contrasting with the Northern Hemisphere, glaciation in Antarctica appears to have increased rather than reduced genetic diversity. This suggests orbitally forced range dynamics based on Northern Hemisphere phylogeography do not hold for Antarctica. The diverse lineages found in D. kerguelenensis point towards a recent, explosive radiation, likely reflecting multiple refuges during glaciation events, combined with limited subsequent dispersal. Whether recognised as cryptic species or not, genetic diversity in Antarctic marine invertebrates appears higher than expected from morphological analyses, and supports the Antarctic biodiversity pump phenomenon.
Sea cucumbers (Holothuroidea) are a morphologically diverse, ecologically important, and economically valued clade of echinoderms; however, the understanding of the overall systematics of the group remains controversial. Here, we present a phylogeny of extant Holothuroidea assessed with maximum parsimony, maximum likelihood, and Bayesian approaches using approximately 4.3kb of mt- (COI, 16S, 12S) and nDNA (H3, 18S, 28S) sequences from 82 holothuroid terminals representing 23 of the 27 widely-accepted family-ranked taxa. Currently five holothuroid taxa of ordinal rank are accepted. We find that three of the five orders are non-monophyletic, and we revise the taxonomy of the groups accordingly. Apodida is sister to the rest of Holothuroidea, here considered Actinopoda. Within Actinopoda, Elasipodida in part is sister to the remaining Actinopoda. This latter clade, comprising holothuroids with respiratory trees, is now called Pneumonophora. The traditional Aspidochirotida is paraphyletic, with representatives from three orders (Molpadida, Dendrochirotida, and Elasipodida in part) nested within. Therefore, we discontinue the use of Aspidochirotida and instead erect Holothuriida as the sister group to the remaining Pneumonophora, here termed Neoholothuriida. We found four well-supported major clades in Neoholothuriida: Dendrochirotida, Molpadida and two new clades, Synallactida and Persiculida. The mapping of traditionally-used morphological characters in holothuroid systematics onto the phylogeny revealed marked homoplasy in most characters demonstrating that further taxonomic revision of Holothuroidea is required. Two time-tree analyses, one based on calibrations for uncontroversial crown group dates for Eleutherozoa, Echinozoa and Holothuroidea and another using these calibrations plus four more from within Holothuroidea, showed major discrepancies, suggesting that fossils of Holothuroidea may need reassessment in terms of placing these forms with existing crown clades.
Sampling at appropriate spatial scales in the Southern Ocean is logistically challenging and may influence estimates of diversity by missing intermediate representatives. With the assistance of sampling efforts especially influenced by the International Polar Year 2007-2008, we gathered nearly 1500 specimens of the crinoid species Promachocrinus kerguelensis from around Antarctica. We used phylogeographic and phylogenetic tools to assess its genetic diversity, demographic history and evolutionary relationships. Six phylogroups (A-F) identified in an earlier study are corroborated here, with the addition of one new phylogroup (E2). All phylogroups are circumpolar, sympatric and eurybathic. The phylogeny of Promachocrinus phylogroups reveals two principal clades that may represent two different cryptic species with contrasting demographic histories. Genetic diversity indices vary dramatically within phylogroups, and within populations, suggesting multiple glacial refugia in the Southern Ocean: on the Kerguelen Plateau, in the East Weddell Sea and the South Shetland Islands (Atlantic sector), and on the East Antarctic continental shelf in the Dumont d'Urville Sea and Ross Sea. The inferences of gene flow vary among the phylogroups, showing discordant spatial patterns. Phylogroup A is the only one found in the Sub-Antarctic region, although without evident connectivity between Bouvet and Kerguelen populations. The Scotia Arc region shows high levels of connectivity between populations in most of the phylogroups, and barriers to gene flow are evident in East Antarctica.
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