Andreas Hejnol

Broad phylogenomic sampling improves resolution of the animal tree of life.

Long-held ideas regarding the evolutionary relationships among animals have recently been upended by sometimes controversial hypotheses based largely on insights from molecular data. These new hypotheses include a clade of moulting animals (Ecdysozoa) and the close relationship of the lophophorates to molluscs and annelids (Lophotrochozoa). Many relationships remain disputed, including those that are required to polarize key features of character evolution, and support for deep nodes is often low. Phylogenomic approaches, which use data from many genes, have shown promise for resolving deep animal relationships, but are hindered by a lack of data from many important groups. Here we report a total of 39.9 Mb of expressed sequence tags from 29 animals belonging to 21 phyla, including 11 phyla previously lacking genomic or expressed-sequence-tag data. Analysed in combination with existing sequences, our data reinforce several previously identified clades that split deeply in the animal tree (including Protostomia, Ecdysozoa and Lophotrochozoa), unambiguously resolve multiple long-standing issues for which there was strong conflicting support in earlier studies with less data (such as velvet worms rather than tardigrades as the sister group of arthropods), and provide molecular support for the monophyly of molluscs, a group long recognized by morphologists. In addition, we find strong support for several new hypotheses. These include a clade that unites annelids (including sipunculans and echiurans) with nemerteans, phoronids and brachiopods, molluscs as sister to that assemblage, and the placement of ctenophores as the earliest diverging extant multicellular animals. A single origin of spiral cleavage (with subsequent losses) is inferred from well-supported nodes. Many relationships between a stable subset of taxa find strong support, and a diminishing number of lineages remain recalcitrant to placement on the tree.

Assessing the root of bilaterian animals with scalable phylogenomic methods

A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.

Higher-level metazoan relationships: recent progress and remaining questions

Metazoa comprises 35–40 phyla that include some 1.3 million described species. Phylogenetic analyses of metazoan interrelationships have progressed in the past two decades from those based on morphology and/or targeted-gene approaches using single and then multiple loci to the more recent phylogenomic approaches that use hundreds or thousands of genes from genome and transcriptome sequencing projects. A stable core of the tree for bilaterian animals is now at hand, and instability and conflict are becoming restricted to a key set of important but contentious relationships. Acoelomorph flatworms (Acoela + Nemertodermatida) and Xenoturbella are sister groups. The position of this clade remains controversial, with different analyses supporting either a sister-group relation to other bilaterians (=Nephrozoa, composed of Protostomia and Deuterostomia) or membership in Deuterostomia. The main clades of deuterostomes (Ambulacraria and Chordata) and protostomes (Ecdysozoa and Spiralia) are recovered in numerous analyses based on varied molecular samples, and also receive anatomical and developmental support. Outstanding issues in protostome phylogenetics are the position of Chaetognatha within the protostome clade, and the monophyly of a group of spiralians collectively named Platyzoa. In contrast to the broad consensus over key questions in bilaterian phylogeny, the relationships of the five main metazoan lineages—Porifera, Ctenophora, Placozoa, Cnidaria and Bilateria—remain subject to conflicting topologies according to different taxonomic samples and analytical approaches. Whether deep bilaterian divergences such as the split between protostome and deuterostome clades date to the Cryogenian or Ediacaran (and, thus, the extent to which the pre-Cambrian fossil record is incomplete) is sensitive to dating methodology.

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.

Xenacoelomorpha is the sister group to Nephrozoa

The position of Xenacoelomorpha in the tree of life remains a major unresolved question in the study of deep animal relationships. Xenacoelomorpha, comprising Acoela, Nemertodermatida, and Xenoturbella, are bilaterally symmetrical marine worms that lack several features common to most other bilaterians, for example an anus, nephridia, and a circulatory system. Two conflicting hypotheses are under debate: Xenacoelomorpha is the sister group to all remaining Bilateria (= Nephrozoa, namely protostomes and deuterostomes) or is a clade inside Deuterostomia. Thus, determining the phylogenetic position of this clade is pivotal for understanding the early evolution of bilaterian features, or as a case of drastic secondary loss of complexity. Here we show robust phylogenomic support for Xenacoelomorpha as the sister taxon of Nephrozoa. Our phylogenetic analyses, based on 11 novel xenacoelomorph transcriptomes and using different models of evolution under maximum likelihood and Bayesian inference analyses, strongly corroborate this result. Rigorous testing of 25 experimental data sets designed to exclude data partitions and taxa potentially prone to reconstruction biases indicates that long-branch attraction, saturation, and missing data do not influence these results. The sister group relationship between Nephrozoa and Xenacoelomorpha supported by our phylogenomic analyses implies that the last common ancestor of bilaterians was probably a benthic, ciliated acoelomate worm with a single opening into an epithelial gut, and that excretory organs, coelomic cavities, and nerve cords evolved after xenacoelomorphs separated from the stem lineage of Nephrozoa.

Acoel development indicates the independent evolution of the bilaterian mouth and anus.

Most bilaterian animals possess a through gut with a separate mouth and anus. It is commonly believed that during the transition from radial to bilateral symmetry, both openings evolved simultaneously by the lateral closure of a slit-like blastopore. Molecular phylogenies however, place the acoel flatworms, which have only one opening to their digestive system, as the sister group to all remaining Bilateria. To address how this single body opening is related to the mouth and anus of the protostomes and deuterostomes, we studied the expression of genes involved in bilaterian foregut and hindgut patterning during the development of the acoel Convolutriloba longifissura. Here we show that the genes brachyury and goosecoid are expressed in association with the acoel mouth, suggesting that this single opening is homologous to the mouth of other bilaterians. In addition, we find that the genes caudal, orthopedia and brachyury—which are expressed in various bilaterian hindguts—are expressed in a small region at the posterior end of the animal, separated from the anterior oral brachyury-expressing region by a dorsal domain of ectodermal bmp2/4 expression. These results contradict the hypothesis that the bilaterian mouth and anus evolved simultaneously from a common blastoporal opening, and suggest that a through gut might have evolved independently in different animal lineages.

Acoel development supports a simple planula-like urbilaterian

Molecular approaches to the study of development and evolution have had profound effects on our understanding of the nature of the evolutionary process. Developmental biologists became intoxicated with fanciful notions of reconstructing genetic pathways of morphogenesis while evolutionary biologists were sobered by the fallacy of reconstructing organismal relationships along increasing grades of morphological complexity. Increased taxon sampling and improvements in analytical techniques are providing a new approach and are forcing biologists to move past historical biases to allow more accurate mapping of morphological and developmental characters through evolutionary time. Here, we discuss the possible developmental and morphological features of the ‘urbilaterian’, the triploblastic animal with anterior-posterior and dorsoventral axes and predecessor of the protostome–deuterostome ancestor. We argue that this animal, with features resembling acoelomorph flatworms, was far simpler morphologically than the protostome–deuterostome ancestor despite possessing a nearly complete eubilaterian genome. We show that the deployment of some genes expected to pattern the protostome–deuterostome ancestor is not deployed in acoels in the predicted manner and thus might have been co-opted after the evolution of the urbilaterian. We also identify the developmental changes related to gastrulation that gave rise to the urbilaterian from a simpler cnidarian-like ancestor.

Broad taxon and gene sampling indicate that chaetognaths are protostomes

Despite advances in phylogenetic methods, there are still a number of enigmatic phyla whose affinities remain poorly resolved. One of the most recalcitrant of these is a group of small predatory marine invertebrates, the chaetognaths (arrow worms). Resolution of the phylogenetic position of the chaetognaths is key for reconstructing the evolutionary history of some of the most fundamental features of animals, including those that have been used to delineate two major clades of animals — the protostomes and deuterostomes.

Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation

Flatworms number among the most diverse invertebrate phyla and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. In this study, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked ‘microturbellarian’ groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates. DOI: http://dx.doi.org/10.7554/eLife.05503.001

A Twist in Time—The Evolution of Spiral Cleavage in the Light of Animal Phylogeny

Recent progress in reconstructing animal relationships enables us to draw a better picture of the evolution of important characters such as organ systems and developmental processes. By mapping these characters onto the phylogenetic framework, we can detect changes that have occurred in them during evolution. The spiral mode of development is a complex of characters that is present in many lineages, such as nemerteans, annelids, mollusks, and polyclad platyhelminthes. However, some of these lineages show variations of this general program in which sub-characters are modified without changing the overlying pattern. Recent molecular phylogenies suggest that spiral cleavage was lost, or at least has deviated from its original pattern, in more lineages than was previously thought (e.g., in rotifers, gastrotrichs, bryozoans, brachiopods, and phoronids). Here, I summarize recent progress in reconstructing the spiralian tree of life and discuss its significance for our understanding of the spiral-cleavage character complex. I conclude that more detailed knowledge of the development of spiralian taxa is necessary to understand the mechanisms behind these changes, and to understand the evolutionary changes and adaptations of spiralian embryos.