Evolution: Assembling the deuterostome body plan.

Starfish, graptolites and humans look as different as can be, yet are more closely related to each other than to any other phylum. Disc-shaped Cambrian fossils join the dots between these disparate body plans to plot out their evolutionary origins.

Protomelission is an early dasyclad alga and not a Cambrian bryozoan.

The animal phyla and their associated body plans originate from a singular burst of evolution occurring during the Cambrian period, over 500 million years ago1. The phylum Bryozoa, the colonial 'moss animals', have been the exception: convincing skeletons of this biomineralizing clade have been absent from Cambrian strata, in part because potential bryozoan fossils are difficult to distinguish from the modular skeletons of other animal and algal groups2,3. At present, the strongest candidate4 is the phosphatic microfossil Protomelission5. Here we describe exceptionally preserved non-mineralized anatomy in Protomelission-like macrofossils from the Xiaoshiba Lagerstätte6. Taken alongside the detailed skeletal construction and the potential taphonomic origin of 'zooid apertures', we consider that Protomelission is better interpreted as the earliest dasycladalean green alga-emphasizing the ecological role of benthic photosynthesizers in early Cambrian communities. Under this interpretation, Protomelission cannot inform the origins of the bryozoan body plan; despite a growing number of promising candidates7-9, there remain no unequivocal bryozoans of Cambrian age.

The Cambrian cirratuliform Iotuba denotes an early annelid radiation.

The principal animal lineages (phyla) diverged in the Cambrian, but most diversity at lower taxonomic ranks arose more gradually over the subsequent 500 Myr. Annelid worms seem to exemplify this pattern, based on molecular analyses and the fossil record: Cambrian Burgess Shale-type deposits host a single, early-diverging crown-group annelid alongside a morphologically and taxonomically conservative stem group; the polychaete sub-classes diverge in the Ordovician; and many orders and families are first documented in Carboniferous Lagerstätten. Fifteen new fossils of the 'phoronid' Iotuba (=Eophoronis) chengjiangensis from the early Cambrian Chengjiang Lagerstätte challenge this picture. A chaetal cephalic cage surrounds a retractile head with branchial plates, affiliating Iotuba with the derived polychaete families 'Flabelligeridae' and Acrocirridae. Unless this similarity represents profound convergent evolution, this relationship would pull back the origin of the nested crown groups of Cirratuliformia, Sedentaria and Pleistoannelida by tens of millions of years-indicating a dramatic unseen origin of modern annelid diversity in the heat of the Cambrian 'explosion'.

Robust Analysis of Phylogenetic Tree Space.

Phylogenetic analyses often produce large numbers of trees. Mapping trees' distribution in "tree space" can illuminate the behavior and performance of search strategies, reveal distinct clusters of optimal trees, and expose differences between different data sources or phylogenetic methods-but the high-dimensional spaces defined by metric distances are necessarily distorted when represented in fewer dimensions. Here, I explore the consequences of this transformation in phylogenetic search results from 128 morphological data sets, using stratigraphic congruence-a complementary aspect of tree similarity-to evaluate the utility of low-dimensional mappings. I find that phylogenetic similarities between cladograms are most accurately depicted in tree spaces derived from information-theoretic tree distances or the quartet distance. Robinson-Foulds tree spaces exhibit prominent distortions and often fail to group trees according to phylogenetic similarity, whereas the strong influence of tree shape on the Kendall-Colijn distance makes its tree space unsuitable for many purposes. Distances mapped into two or even three dimensions often display little correspondence with true distances, which can lead to profound misrepresentation of clustering structure. Without explicit testing, one cannot be confident that a tree space mapping faithfully represents the true distribution of trees, nor that visually evident structure is valid. My recommendations for tree space validation and visualization are implemented in a new graphical user interface in the "TreeDist" R package. [Multidimensional scaling; phylogenetic software; tree distance metrics; treespace projections.].

Phylogenetic Signal and Bias in Paleontology.

An unprecedented amount of evidence now illuminates the phylogeny of living mammals and birds on the Tree of Life. We use this tree to measure the phylogenetic value of data typically used in paleontology (bones and teeth) from six data sets derived from five published studies. We ask three interrelated questions: 1) Can these data adequately reconstruct known parts of the Tree of Life? 2) Is accuracy generally similar for studies using morphology, or do some morphological data sets perform better than others? 3) Does the loss of non-fossilizable data cause taxa to occur in misleadingly basal positions? Adding morphology to DNA data sets usually increases congruence of resulting topologies to the well-corroborated tree, but this varies among morphological data sets. Extant taxa with a high proportion of missing morphological characters can greatly reduce phylogenetic resolution when analyzed together with fossils. Attempts to ameliorate this by deleting extant taxa missing morphology are prone to decreased accuracy due to long-branch artifacts. We find no evidence that fossilization causes extinct taxa to incorrectly appear at or near topologically basal branches. Morphology comprises the evidence held in common by living taxa and fossils, and phylogenetic analysis of fossils greatly benefits from inclusion of molecular and morphological data sampled for living taxa, whatever methods are used for phylogeny estimation. [Concatenation; fossilization; morphology; parsimony; systematics; taphonomy; total-evidence.].

Using Information Theory to Detect Rogue Taxa and Improve Consensus Trees.

"Rogue" taxa of uncertain affinity can confound attempts to summarize the results of phylogenetic analyses. Rogues reduce resolution and support values in consensus trees, potentially obscuring strong evidence for relationships between other taxa. Information theory provides a principled means of assessing the congruence between a set of trees and their consensus, allowing rogue taxa to be identified more effectively than when using ad hoc measures of tree quality. A basic implementation of this approach in R recovers reduced consensus trees that are better resolved, more accurate, and more informative than those generated by existing methods. [Consensus trees; information theory; phylogenetic software; Rogue taxa.].

A 'hermit' shell-dwelling lifestyle in a Cambrian priapulan worm.

The Cambrian 'explosion', about 530 million years ago, marks a rapid diversification of the major animal lineages1. A concomitant increase in the complexity of ecosystems is believed to have accelerated this evolutionary radiation2, but direct evidence of the ecological modes of Cambrian taxa is nevertheless scarce - even in exceptional Burgess Shale-type deposits3. Here, we present new fossil material from the Cambrian (Stage 4) Guanshan biota in southern China that reveals the consistent occurrence of the priapulan worm ?Eximipriapulus4 within the conical shells of hyoliths. This represents the first direct evidence of a 'hermiting' life strategy - the adoption of a different organism's exoskeleton - in the priapulans and within the Palaeozoic era. It highlights the intense degree of convergent evolution during the Cambrian radiation. Hermiting behaviour has previously been linked with the escalation of predation pressure during the Mesozoic marine revolution5; such intensity of predation may also have characterised early Cambrian oceans.

Information theoretic generalized Robinson-Foulds metrics for comparing phylogenetic trees.

MOTIVATION: The Robinson-Foulds (RF) metric is widely used by biologists, linguists and chemists to quantify similarity between pairs of phylogenetic trees. The measure tallies the number of bipartition splits that occur in both trees-but this conservative approach ignores potential similarities between almost-identical splits, with undesirable consequences. 'Generalized' RF metrics address this shortcoming by pairing splits in one tree with similar splits in the other. Each pair is assigned a similarity score, the sum of which enumerates the similarity between two trees. The challenge lies in quantifying split similarity: existing definitions lack a principled statistical underpinning, resulting in misleading tree distances that are difficult to interpret. Here, I propose probabilistic measures of split similarity, which allow tree similarity to be measured in natural units (bits). RESULTS: My new information-theoretic metrics outperform alternative measures of tree similarity when evaluated against a broad suite of criteria, even though they do not account for the non-independence of splits within a single tree. Mutual clustering information exhibits none of the undesirable properties that characterize other tree comparison metrics, and should be preferred to the RF metric. AVAILABILITY AND IMPLEMENTATION: The methods discussed in this article are implemented in the R package 'TreeDist', archived at https://dx.doi.org/10.5281/zenodo.3528123. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Congruence, fossils and the evolutionary tree of rodents and lagomorphs.

Given an evolutionary process, we expect distinct categories of heritable data, sampled in ever larger amounts, to converge on a single tree of historical relationships. We tested this assertion by undertaking phylogenetic analyses of a new morphology-DNA dataset for mammals, focusing on Glires and including the oldest known skeletons of geomyoid and Ischyromys rodents. Our results support geomyoids in the mouse-related clade (Myomorpha) and a ricochetal locomotor pattern for the common ancestor of geomyoid rodents. They also support Ischyromys in the squirrel-related clade (Sciuromorpha) and the evolution of sciurids and Aplodontia from extinct, 'protrogomorph'-grade rodents. Moreover, ever larger samples of characters from our dataset increased congruence with an independent, well-corroborated tree. Addition of morphology from fossils increased congruence to a greater extent than addition of morphology from extant taxa, consistent with fossils' temporal proximity to the common ancestors of living species, reflecting the historical, phylogenetic signal present in our data, particularly in morphological characters from fossils. Our results support the widely held but poorly tested intuition that fossils resemble the common ancestors shared by living species, and that fossilizable hard tissues (i.e. bones and teeth) help to reconstruct the evolutionary tree of life.

Bayesian and parsimony approaches reconstruct informative trees from simulated morphological datasets.

Phylogenetic analysis aims to establish the true relationships between taxa. Different analytical methods, however, can reach different conclusions. In order to establish which approach best reconstructs true relationships, previous studies have simulated datasets from known tree topologies, and identified the method that reconstructs the generative tree most accurately. On this basis, researchers have argued that morphological datasets should be analysed by Bayesian approaches, which employ an explicit probabilistic model of evolution, rather than parsimony methods-with implied weights parsimony sometimes identified as particularly inaccurate. Accuracy alone, however, is an inadequate measure of a tree's utility: a fully unresolved tree is perfectly accurate, yet contains no phylogenetic information. The highly resolved trees recovered by implied weights parsimony in fact contain as much useful information as the more accurate, but less resolved, trees recovered by Bayesian methods. By collapsing poorly supported groups, this superior resolution can be traded for accuracy, resulting in trees as accurate as those obtained by a Bayesian approach. By contrast, equally weighted parsimony analysis produces trees that are less resolved and less accurate, leading to less reliable evolutionary conclusions.

An algorithm for Morphological Phylogenetic Analysis with Inapplicable Data.

Morphological data play a key role in the inference of biological relationships and evolutionary history and are essential for the interpretation of the fossil record. The hierarchical interdependence of many morphological characters, however, complicates phylogenetic analysis. In particular, many characters only apply to a subset of terminal taxa. The widely used "reductive coding" approach treats taxa in which a character is inapplicable as though the character's state is simply missing (unknown). This approach has long been known to create spurious tree length estimates on certain topologies, potentially leading to erroneous results in phylogenetic searches-but pratical solutions have yet to be proposed and implemented. Here, we present a single-character algorithm for reconstructing ancestral states in reductively coded data sets, following the theoretical guideline of minimizing homoplasy over all characters. Our algorithm uses up to three traversals to score a tree, and a fourth to fully resolve final states at each node within the tree. We use explicit criteria to resolve ambiguity in applicable/inapplicable dichotomies, and to optimize missing data. So that it can be applied to single characters, the algorithm employs local optimization; as such, the method provides a fast but approximate inference of ancestral states and tree score. The application of our method to published morphological data sets indicates that, compared to traditional methods, it identifies different trees as "optimal." As such, the use of our algorithm to handle inapplicable data may significantly alter the outcome of tree searches, modifying the inferred placement of living and fossil taxa and potentially leading to major differences in reconstructions of evolutionary history.

Hyoliths with pedicles illuminate the origin of the brachiopod body plan.

Hyoliths are a taxonomically problematic group of Palaeozoic lophotrochozoans that are among the first shelly fossils to appear in the Cambrian period. On the basis of their distinctive exoskeleton, hyoliths have historically been classified as a separate phylum with possible affinities to the molluscs, sipunculans or lophophorates-but their precise phylogenetic position remains uncertain. Here, we describe a new orthothecide hyolith from the Chengjiang Lagerstätte (Cambrian Series 2 Stage 3), Pedunculotheca diania Sun, Zhao et Zhu gen. et sp. nov., which exhibits a non-mineralized attachment structure that strikingly resembles the brachiopod pedicle-the first report of a peduncular organ in hyoliths. This organ establishes a sessile, suspension feeding ecology for these orthothecides and-together with other characteristics (e.g. bilaterally symmetrical bivalve shell enclosing a filtration chamber and the differentiation of cardinal areas)-identifies hyoliths as stem-group brachiopods. Our phylogenetic analysis indicates that both hyoliths and crown brachiopods derived from a tommotiid grade, and that the pedicle has a single origin within the brachiopod total group.

Orthrozanclus elongata n. sp. and the significance of sclerite-covered taxa for early trochozoan evolution.

Orthrozanclus is a shell-bearing, sclerite covered Cambrian organism of uncertain taxonomic affinity, seemingly representing an intermediate between its fellow problematica Wiwaxia and Halkieria. Attempts to group these slug-like taxa into a single 'halwaxiid' clade nevertheless present structural and evolutionary difficulties. Here we report a new species of Orthrozanclus from the early Cambrian Chengjiang Lagerstätte. The scleritome arrangement and constitution in this material corroborates the link between Orthrozanclus and Halkieria, but not with Wiwaxia - and calls into question its purported relationship with molluscs. Instead, the tripartite construction of the halkieriid scleritome finds a more compelling parallel in the camenellan tommotiids, relatives of the brachiopods and phoronids. Such a phylogenetic position would indicate the presence of a scleritome in the common ancestor of the three major trochozoan lineages, Mollusca, Annelida and Brachiozoa. On this view, the absence of fossil Ediacaran sclerites is evidence against any 'Precambrian prelude' to the explosive diversification of these phyla in the Cambrian, c. 540-530 million years ago.

Hyoliths are Palaeozoic lophophorates.

Hyoliths are abundant and globally distributed 'shelly' fossils that appear early in the Cambrian period and can be found throughout the 280 million year span of Palaeozoic strata. The ecological and evolutionary importance of this group has remained unresolved, largely because of their poorly constrained soft anatomy and idiosyncratic scleritome, which comprises an operculum, a conical shell and, in some taxa, a pair of lateral spines (helens). Since their first description over 175 years ago, hyoliths have most often been regarded as incertae sedis, related to molluscs or assigned to their own phylum. Here we examine over 1,500 specimens of the mid-Cambrian hyolith Haplophrentis from the Burgess Shale and Spence Shale Lagerstätten. We reconstruct Haplophrentis as a semi-sessile, epibenthic suspension feeder that could use its helens to elevate its tubular body above the sea floor. Exceptionally preserved soft tissues include an extendable, gullwing-shaped, tentacle-bearing organ surrounding a central mouth, which we interpret as a lophophore, and a U-shaped digestive tract ending in a dorsolateral anus. Together with opposing bilateral sclerites and a deep ventral visceral cavity, these features indicate an affinity with the lophophorates (brachiopods, phoronids and tommotiids), substantially increasing the morphological disparity of this prominent group.

Evolution: Velvet Worm Biogeography.

The present-day distribution of velvet worms corresponds neatly to the ancient supercontinent Gondwana - except for a puzzling outpost in southeast Asia. Jaw-dropping new fossil material now establishes when and how peripatid onychophorans reached this isolated spot.

Onychophoran-like musculature in a phosphatized Cambrian lobopodian.

The restricted, exclusively terrestrial distribution of modern Onychophora contrasts strikingly with the rich diversity of onychophoran-like fossils preserved in marine Cambrian Lagerstätten The transition from these early forebears to the modern onychophoran body plan is poorly constrained, in part owing to the absence of fossils preserving details of the soft anatomy. Here, we report muscle tissue in a new early Cambrian (Stage 3) lobopodian, Tritonychus phanerosarkus gen. et sp. nov., preserved in the Orsten fashion by three-dimensional replication in phosphate. This first report of Palaeozoic onychophoran musculature establishes peripheral musculature as a characteristic of the ancestral panarthropod, but documents an unexpected muscular configuration. Phylogenetic analysis reconstructs T. phanerosarkus as one of a few members of the main onychophoran lineage-which was as rare and as cryptic in the Cambrian period as it is today.

New reconstruction of the Wiwaxia scleritome, with data from Chengjiang juveniles.

Wiwaxiids are a problematic group of scale-covered lophotrochozoans known from Cambrian Stages 3-5. Their imbricating dorsal scleritome of leaf-like scales has prompted comparison with various annelids and molluscs, and has been used as a template to reconstruct the articulation pattern of isolated Small Shelly Fossils. The first articulated specimens of Wiwaxia from the Cambrian Stage 3 Chengjiang Konservat-Lagerstätte show that the Wiwaxia scleritome comprised nine equivalent transverse rows associated with outgrowths of soft tissue, but did not possess a separate zone of anterior sclerites. This serial construction is fundamentally incompatible with the circumferential disposition of sclerites in early molluscs, but does closely resemble the armature of certain annelids. A deep homology with the annelid scleritome must be reconciled with Wiwaxia's mollusc-like mouthparts and foot; together these point to a deep phylogenetic position, close to the common ancestor of annelids and molluscs.