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Telford, M. J.

Publications and source records attributed to Telford, M. J..

17 recordsLinked to original sources

Are interphylum spiralian relationships resolvable?

The phyla making up the major animal clade of Spiralia have been clear since the advent of molecular phylogenetics; the relationships between these spiralian phyla have not. The lack of consensus over the relationships between these important animal phyla might be a clue implying their emergence in an explosive radiation. Focussing on the five largest spiralian clades (Annelida, Brachiozoa, Mollusca, Nemertea and Platyhelminthes) and using two phylogenomic datasets, we have applied site-bootstrapping and taxon-jackknifing to explore this example of taxonomic instability. Analyses on the 105 possible rooted trees relating them showed that interphylum branches are very short. Preference for rooting Spiralia on Platyhelminthes is enhanced by a long-branch artefact. Most analyses on the 15 unrooted trees showed a preference for the same topology but the support for this tree over other solutions was not significant. We conclude that the spiralian phyla emerged in rapid succession resulting in a difficult to resolve radiation. The deep history we infer for Spiralia has wide ranging implications for our interpretation of Cambrian fossils and for the evolution of traits such as biomineralization, segmentation and larvae. Impact StatementAnalyses of two independent phylogenomic datasets suggest an explosive radiation at the origin of Spiralia, with implications for understanding the groups evolutionary history.

evolutionary biology↗

A phylogeny aware analysis of gene function for the biodiversity genomics era

In the biodiversity genomics era, vast gene catalogs have rapidly accumulated, but how gene functions map onto major evolutionary transitions remains vague. We integrated phylogenomics with functional annotations to trace the emergence of [~]4.5 million genes and their associated functions in 508 representative species across the tree of life. Using this top-down, function-centric approach, we mapped the evolutionary history of well-annotated biological functions, revealing key insights and widespread parallelism. For instance, the largest bursts of gene and function gains aligned with key evolutionary transitions, including the origins of eukaryotes, animals, land plants, and vertebrates. Independent transitions to multicellularity and terrestrial life showed convergent enrichment of semantically similar functions (involving entirely different gene families), and the presence of orthologous genes often belonging to ancient gene families. For example, terrestrialization nodes in slime molds, plants, and animals coincided with gains in stress-tolerance and developmental genes, whereas multicellularity in animals, fungi, plants, and slime molds consistently involved expansions in cell-adhesion and communication functions. Thus, our framework enables scalable interpretation of new genomes in an evolutionary context and offers a roadmap for exploring the genomic basis of biodiversity.

evolutionary biology↗

Support for the deuterostome clade comes from systematic errors

There is a long-standing consensus that the animal phyla closest to our own phylum of Chordata are the Echinodermata and Hemichordata. These three phyla constitute the major clade of Deuterostomia. Recent analyses have questioned the support for the monophyly of Deuterostomia, however, showing that the branch leading to deuterostomes is very short and may be influenced by systematic error. Here we use a site-by-site approach to explore multiple sources of error. Under conditions that promote long-branch attraction (LBA) - especially branch-length heterogeneity and sites constrained in their amino acid composition - we find that deuterostome monophyly is strongly supported. When we make efforts to mitigate these sources of error, we cannot distinguish between monophyletic and paraphyletic Deuterostomia. Our findings have implications for the interpretation of putative deuterostome fossils, for the reconstruction of a bilaterian ancestor and, more generally, for how datasets for deep-time phylogenetic analyses are assembled and analyzed. TeaserThe apparently close relationship between Chordata and Ambulacraria (echinoderms and hemichordates) is boosted by a long-branch attraction artefact.

evolutionary biology↗

Dollo parsimony overestimates ancestral gene content reconstructions

Ancestral reconstruction is a widely-used technique that has been applied to understand the history of gain and loss of gene families over evolutionary time scales, and to produce hypotheses on how these gains and losses may have influenced the evolutionary trajectories of extant organisms. Ancestral gene content can be reconstructed via different phylogenetic methods, such as maximum likelihood or Bayesian inference, but many current and previous studies employ Dollo parsimony. We hypothesize that Dollo parsimony is not appropriate for ancestral gene content reconstruction inferences based on sequence homology, as Dollo parsimony is derived from the assumption that a complex character can only be gained once in evolutionary history. This premise does not accurately model molecular sequence evolution, in which false orthology can result from sequence convergence (including random sequence similarity and parallel gene gains), non-orthologous homology or lateral gene transfer. The aim of this study is to test Dollo parsimonys suitability for ancestral gene content reconstruction and to compare its inferences with a maximum likelihood-based approach which allows a gene family to be gained more than once within a tree. In order to test our hypothesis, we first compared the performance of the two approaches on a series of artificial datasets each of 5,000 genes that were simulated according to a spectrum of evolutionary rates. Next, we reconstructed protein domain evolution on a phylogeny representing known eukaryotic diversity. We observed that Dollo parsimony produced numerous ancestral gene content overestimations, which were more pronounced at nodes closer to the root of the tree. These observations led us to the conclusion that, confirming our hypothesis, Dollo parsimony is not an appropriate method for ancestral reconstruction studies based on sequence homology.

evolutionary biology↗

Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Pelagic larval stages are widespread across animals, yet it is unclear if larvae were present in the last common ancestor of animals or whether they evolved multiple times due to common selective pressures. Many marine larvae are at least superficially similar, they are small, swim through beating of ciliated bands and sense the environment with an apical organ structure. To understand these similarities, we have generated single cell atlases for marine larvae from two animal phyla and have compared their cell types. We found clear similarities among ciliary band cells and neurons of the apical organ in the two larvae pointing to possible homology of these structures suggesting a single origin of larvae within the clade analysed here (Lophotrochozoa). We also find several clade specific innovations in each larva, including distinct myocytes and shell gland cells in the oyster larva. Oyster shell gland cells express many novel genes which have made previous gene age estimates for trochophore larvae too young.

evolutionary biology↗

Single cell atlas of Xenoturbella bocki highlights the limited cell-type complexity of a non-vertebrate deuterostome lineage

Evidence for a sister relationship between Xenacoelomorpha and Ambulacraria (Xenambulacraria) has revived the longstanding debate surrounding the complexity of the Urdeuterostomian and Urbilaterian ancestors and has led to a reassessment of early bilaterian features. Employing whole organism single-cell RNA-seq in the marine xenacoelomorph worm Xenoturbella bocki, we show that Xenambulacrarian nerve nets share regulatory features and a peptidergic identity with those found in cnidarians and protostomes. We also suggest that Xenacoelomorpha muscles are likely to have evolved their "smooth" phenotype convergently. Furthermore, we identify pigmented cells as a potential synapomorphy of the Xenambulacraria. Taken together, these data are consistent with a simplification from an ancestral urbilaterian/urdeuterostomian body plan and a non-centralized nerve net, minimally differentiated contractile cells and evidence of deuterostome cell-type synapomorphies.

evolutionary biology↗

Genome assembly of the polyclad flatworm Prostheceraeus crozieri

Polyclad flatworms are widely thought to be one of the least derived of the flatworm classes and, as such, are well placed to investigate evolutionary and developmental features such as spiral cleavage and larval diversification lost in other platyhelminths. Prostheceraeus crozieri, formerly Maritigrella crozieri, is an emerging model polyclad flatworm that already has some useful transcriptome data but, to date, no sequenced genome. We have used high molecular weight DNA extraction and long read PacBio sequencing to assemble the highly repetitive (67.9%) P. crozieri genome (2.07 Gb). We have annotated 43,325 genes, with 89.7% BUSCO completeness. Perhaps reflecting its large genome, introns were considerably larger than other free-living flatworms, but evidence of abundant transposable elements suggests genome expansion has been principally via transposable elements activity. This genome resource will be of great use for future developmental and phylogenomic research.

genomics↗

The slow evolving genome of the xenacoelomorph worm Xenoturbella bocki

The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can help to elucidate phylogenetic relationships and provide important comparative data. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian and deuterostome evolution. Our highly contiguous genome assembly of X. bocki has a size of [~]111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. We conclude that X. bocki has a complex genome typical of bilaterians, in contrast to the apparent simplicity of its body plan. Overall, our data do not provide evidence supporting the idea that Xenacoelomorpha are a primitively simple outgroup to other bilaterians and gene presence/absence data support a relationship with Ambulacraria.

evolutionary biology↗

CeLaVi: An Interactive Cell Lineage Visualisation Tool

Recent innovations in genetics and imaging are providing the means to reconstruct cell lineages, either by tracking cell divisions using live microscopy, or by deducing the history of cells using molecular recorders. A cell lineage on its own, however, is simply a description of cell divisions as branching events. A major goal of current research is to integrate this description of cell relationships with information about the spatial distribution and identities of the cells those divisions produce. Visualising, interpreting and exploring these complex data in an intuitive manner requires the development of new tools. Here we present CeLaVi, a web-based visualisation tool that allows users to navigate and interact with a representation of cell lineages, whilst simultaneously visualising the spatial distribution, identities and properties of cells. CeLaVis principal functions include the ability to explore and manipulate the cell lineage tree; to visualise the spatial distribution of cell clones at different depths of the tree; to colour cells in the 3D viewer based on lineage relationships; to visualise various cell qualities on the 3D viewer (e.g. gene expression, cell type, tissue layer) and to annotate selected cells/clones. All these capabilities are demonstrated with four different example data sets. CeLaVi is available at http://www.celavi.pro.

developmental biology↗

Systematic errors in orthology inference: a bug or a feature for evolutionary analyses?

Introductory paragraphThe availability of complete sets of genes from many organisms makes it possible to identify genes unique to (or lost from) certain clades. This information is used to reconstruct phylogenetic trees; to identify genes involved in the evolution of clade specific novelties; and for phylostratigraphy - identifying ages of genes in a given species. These investigations rely on accurately predicted orthologs. Here we use simulation to produce sets of orthologs which experience no gains or losses. We show that errors in identifying orthologs increase with higher rates of evolution. We use the predicted sets of orthologs, with errors, to reconstruct phylogenetic trees; to count gains and losses; and for phylostratigraphy. Our simulated data, containing information only from errors in orthology prediction, closely recapitulate findings from empirical data. We suggest published downstream analyses must be informed to a large extent by errors in orthology prediction which mimic expected patterns of gene evolution.

evolutionary biology↗

Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria.

The bilaterally symmetric animals (Bilateria) are considered to comprise two monophyletic groups, Protostomia and Deuterostomia. Protostomia contains the Ecdysozoa and the Lophotrochozoa; Deuterostomia contains the Chordata and the Xenambulacraria (Hemichordata, Echinodermata and Xenacoelomorpha). Their names refer to a supposed distinct origin of the mouth (stoma) in the two clades, but these groups have been differentiated by other embryological characters including embryonic cleavage patterns and different ways of forming their mesoderm and coeloms. Deuterostome monophyly is not consistently supported by recent studies. Here we compare support for Protostomia and Deuterostomia using five recently published, phylogenomic datasets. Protostomia is always strongly supported, especially by longer and higher quality genes. Support for Deuterostomia is always equivocal and barely higher than support for paraphyletic alternatives. Conditions that can cause tree reconstruction errors - inadequate models, short internal branch, faster evolving genes, and unequal branch lengths - correlate with statistical support for monophyletic deuterostomes. Simulation experiments show that support for Deuterostomia could be explained by systematic error. A survey of molecular characters supposedly diagnostic of deuterostomes shows many are not valid synapomorphies. The branch between bilaterian and deuterostome common ancestors, if real, is very short. This finding fits with growing evidence suggesting the common ancestor of all Bilateria had many deuterostome characteristics. This finding has important implications for our understanding of early animal evolution and for the interpretation of some enigmatic Cambrian fossils such as vetulicolians and banffiids.

evolutionary biology↗

Spermiogenesis in the acoel Symsagittifera roscoffensis: nucleus-plasma membrane contact sites and microtubules.

Symsagittifera roscoffensis is a small marine worm found in the intertidal zone of sandy beaches around the European shores of the Atlantic. S. roscoffensis is a member of the Acoelomorpha, a group of flatworms formerly classified with the Platyhelminthes, but now recognised as Xenacoelomorpha, a separate phylum of disputed affinity. We have used electron microscopy to examine the process of spermiogenesis (the final stage of spermatogenesis) in S. roscoffensis, by which spermatids form highly elongated spermatozoa. Their nuclei are long and thread-like, running most of the cells length and during the process a pair of flagella are fully incorporated into the cell body. Two previously undescribed inter-organelle contact sites form at different stages of spermiogenesis. Strikingly, there is an extensive nucleus-plasma membrane contact site. Golgi-derived granules containing electron-dense filaments line up along the spermatid plasma membrane, undergo a conformational change, and donate material that forms a peri-nuclear layer that cements this contact site. We also show in earlier stage spermatids that the same granules are associated with microtubules, presumably for traffic along the elongating cell. We identify a second spermiogenesis-specific contact site where sheaths engulfing each internalising flagellum contact the nuclear envelope. Finally, detailed studies of the spermatozoon axonemes show that the central keel has varying numbers of microtubules along the length of the cell, and is likely to be a centriole derivative.\n\nSummary sentenceDuring spermiogenesis in the acoel flatworm Symsagittifera roscoffensis, two previously unidentified contact sites contribute to the structure of the mature spermatozoon and the axonemal structures show direct continuity between doublet and dense core microtubules.

cell biology↗

Computational discovery of hidden breaks in 28S rRNA across eukaryotes and consequences for RNA Integrity Numbers

In some eukaryotes, a hidden break has been described in which the 28S ribosomal RNA molecule is cleaved into two subparts. The break is common in protostome animals (arthropods, molluscs, annelids etc.) but a break has also been reported in some vertebrates and non-metazoan eukaryotes. We present a new computational approach to determine the presence of the hidden break in 28S rRNAs using mapping of RNA-Seq data. We find a homologous break is present across protostomes although has been lost in a small number of taxa. We show that rare breaks in vertebrate 28S rRNAs are not homologous to the protostome break. A break is found in just 4 out of 331 species of non-animal eukaryotes studied and three of these are located in the same position as the protostome break suggesting a striking instance of convergent evolution. RNA Integrity Numbers (RIN) rely on intact 28s rRNA and will be consistently underestimated in the great majority of animal species with a break.

bioinformatics↗

Studying early embryogenesis in the flatworm Maritigrella crozieri indicates a unique modification of the spiral cleavage program in polyclad flatworms

BackgroundSpiral cleavage is a conserved early developmental mode found in several phyla of Lophotrochozoans with highly diverse adult body plans. While the cleavage pattern has clearly been broadly conserved, it has also undergone many modifications in various taxa. The precise mechanisms of how different adaptations have altered the ancestral spiral cleavage pattern is an important ongoing evolutionary question and adequately answering this question requires obtaining a broad developmental knowledge of different spirally cleaving taxa.\n\nIn flatworms (Platyhelminthes), the spiral cleavage program has been lost or severely modified in most taxa. Polyclad flatworms, however, have retained the pattern up to the 32-cell stage. Here we study early embryogenesis of the cotylean polyclad flatworm Maritigrella crozieri to investigate how closely this species follows the canonical spiral cleavage pattern and to discover any potential deviations from it.\n\nResultsUsing live imaging recordings and 3D reconstructions of embryos, we give a detailed picture of the events that occur during spiral cleavage in M. crozieri. We suggest, contrary to previous observations, that the 4-cell stage is a product of unequal cleavages. We show that that the formation of third and fourth micromere quartets are accompanied by strong blebbing events; blebbing also accompanies the formation of micromere 4d. We find an important deviation from the canonical pattern of cleavages with clear evidence that micromere 4d follows an atypical cleavage pattern, so far exclusively found in polyclad flatworms.\n\nConclusionsOur findings highlight that early development in M. crozieri deviates in several important aspects from the canonical spiral cleavage pattern. We suggest that some of our observations extend to polyclad flatworms in general as they have been described in both suborders of the Polycladida, the Cotylea and Acotylea.

evolutionary biology↗

Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment

Animals detect light using opsin photopigments. One recently classified opsin clade, the xenopsins, found in lophotrochozoans, challenges our views on opsin and photoreceptor evolution. Originally thought to belong to the Gi-coupled ciliary opsins, xenopsins are now understood to have diverged from ciliary opsins in pre-bilaterian times, but little is known about the cells that deploy these proteins, or if they form a photopigment and drive phototransduction. We characterized xenopsin in a flatworm, Maritigrella crozieri, and found that it is expressed in a larval eyespot, and in an abundant extraocular cell type around the adult brain. These distinct cells house hundreds of cilia in an intra-cellular vacuole (a phaosome). Cellular assays show Mc xenopsin forms a photopigment and couples to Gi/o in response to light. These findings reveal a novel photoreceptor cell type and opsin/G-protein couple, and highlight the convergent enclosure of photosensitive cilia in flatworm phaosomes and jawed vertebrate rods.

zoology↗

Is it possible to reconstruct an accurate cell lineage using CRISPR recorders?

Cell lineages provide the framework for understanding how multicellular organisms are built and how cell fates are decided during development. Describing cell lineages in most organisms is challenging, given the number of cells involved; even a fruit fly larva has ~50,000 cells and a small mammal has more than 1 billion cells. Recently, the idea of using CRISPR to induce mutations during development as heritable markers for lineage reconstruction has been proposed and trialled by several groups. While an attractive idea, its practical value depends on the accuracy of the cell lineages that can be generated by this method. Here, we use computer simulations to estimate the performance of this approach under different conditions. Our simulations incorporate empirical data on CRISPR-induced mutation frequencies in Drosophila. We show significant impacts from multiple biological and technical parameters - variable cell division rates, skewed mutational outcomes, target dropouts and different mutation sequencing strategies. Our approach reveals the limitations of recently published CRISPR recorders, and indicates how future implementations can be optimised to produce accurate cell lineages.

developmental biology↗

Molecular data from Orthonectid worms show they are highly degenerate members of phylum Annelida not phylum Mesozoa.

SummaryThe Mesozoa are a group of tiny, extremely simple, vermiform endoparasites of various marine animals (Fig. 1). There are two recognised groups within the Mesozoa: the Orthonectida (Fig. 1a,b; with a few hundred cells including a nervous system made up of just 10 cells [1]) and the Dicyemids (Fig. 1c; with at most 42 cells [2]). They are classic Problematica [3] - the name Mesozoa suggests an evolutionary position intermediate between Protozoa and Metazoa (animals) [4] and implies their simplicity is a primitive state, but molecular data have shown they are members of Lophotrochozoa within Bilateria [5-8] which would mean they derive from a more complex ancestor. Their precise phylogenetic affinities remain uncertain, however, and ascertaining this is complicated by the very fast evolution observed in genes from both groups, leading to the common systematic error of Long Branch Attraction (LBA) [9]. Here we use mitochondrial and nuclear gene sequence data, and show beyond doubt that both dicyemids and orthonectids are members of the Lophotrochozoa. Carefully addressing the effects of systematic errors due to unequal rates of evolution, we show that the phylum Mesozoa is polyphyletic. While the precise position of dicyemids remains unresolved within Lophotrochozoa, we unequivocally identify orthonectids as members of the phylum Annelida. This result reveals one of the most extreme cases of body plan simplification in the animal kingdom; our finding makes sense of an annelid-like cuticle in orthonectids [1] and suggests the circular muscle cells repeated along their body [10] may be segmental in origin.\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=71 SRC=\"FIGDIR/small/235549_fig1.gif\" ALT=\"Figure 1\">\nView larger version (22K):\norg.highwire.dtl.DTLVardef@76ca5org.highwire.dtl.DTLVardef@16df6eaorg.highwire.dtl.DTLVardef@6da877org.highwire.dtl.DTLVardef@14f3056_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFig. 1:C_FLOATNO The mesozoans Intoshia variabili and Dicyema typus A. Differential Interference contrast micrograph of an Intoshia variabili female showing repeated bands of ciliated cells. Picture G. Slyusarev (St Petersburg State University, Russia).\n\nB. Confocal image of a phalloidin stained female specimen of Intoshia linei reveals repeated set of circular muscles. Picture G. Slyusarev (St Petersburg State Univ.).\n\nC. Rhombogen stage of a dicyemid (Dicyema typus from the Octopus) adapted from Hyman L.H. The Invertebrates: Protozoa through Ctenophora McGraw-Hill, New York 1940(19). Anterior to right in all images.\n\nC_FIG

evolutionary biology↗