I am an evolutionary biologist fascinated by major transitions in evolution. My main interests are the Animal Kingdom (metazoa), plants, eukaryotes, phylogenetics, and comparative genomics. Address: School of Biological Sciences University of Bristol 24 Tyndall Avenue Bristol BS8 1TQ, UK
The first winged insects underwent profound morphological and functional transformations leading ... more The first winged insects underwent profound morphological and functional transformations leading to the most successful animal radiations in the history of earth. Despite this, we still have a very incomplete picture of the changes in their genomes that underlay this radiation. Mayflies (Ephemeroptera) are one of the extant sister groups of all other winged insects and therefore are at a key phylogenetic position to understand this radiation. Here, we describe the genome of the cosmopolitan mayfly Cloeon dipterum and study its expression along development and in specific organs. We discover an expansion of odorant-binding proteins, some expressed specifically in the breathing gills of aquatic nymphs, suggesting a novel sensory role for gills. In contrast, as flying adults, mayflies make use of an enlarged set of opsins and utilise these visual genes in a sexually dimorphic manner, with some opsins expressed only in males. Finally, to illuminate the origin of wings, we identify a cor...
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest anim... more The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.
Traditional evolutionary scenarios posit that land plants emerged from land plant-like relatives,... more Traditional evolutionary scenarios posit that land plants emerged from land plant-like relatives, the charophytes. New phylogenies suggest a closer affinity to simpler pond scum relatives, and evidence the gradual assembly of the land plant genome, revealing a phenotypic simplification from the complex ancestors envisaged by traditional scenarios
The animal kingdom shows an astonishing diversity, the product of over 550 million years of anima... more The animal kingdom shows an astonishing diversity, the product of over 550 million years of animal evolution. The current wealth of genome sequence data offers an opportunity to better understand the genomic basis of this diversity. Here we analyse a sampling of 102 whole genomes including >2.6 million protein sequences. We infer major genomic patterns associated with the variety of animal forms from the super-phylum to phylum level. We show that a remarkable amount of gene loss occurred during the evolution of two major groups of bilaterian animals, Ecdysozoa and Deuterostomia, and further loss in several deuterostome lineages. Deuterostomes and protostomes also show large genome novelties. At the phylum level, flatworms, nematodes and tardigrades show the largest reduction of gene complement, alongside gene novelty. These findings paint a picture of evolution in the animal kingdom in which reductive evolution at the protein-coding level played a major role in shaping genome composition. The Metazoa encompass an astonishing diversity of body forms. More than 30 animal phyla have been defined, the evolutionary relationships between which are well understood in broad outline, although some are still a matter of debate 1-4. Understanding how their genomes have evolved can help us better comprehend the origin of this diversity and reconstruct their evolutionary history. The Metazoa comprise sponges, ctenophores, cnidarians, placozo-ans and bilaterians, with most of animal diversity found in the last of these groups. The Bilateria can be split into three major groups or superphyla: Deuterostomia, Lophotrochozoa and Ecdysozoa 5 , the latter two forming the Protostomia. Gene losses and gains play major roles in evolution. The gain of new functions via the assembly of modules from older genes or the emergence of de novo coding regions has been proposed to be important during major evolutionary transitions such as the origin of animals 6-8. Gene loss has been associated with the loss of anatomical structures in evolution, consistent with views that evolution can lead to both increases and decreases in complexity 9-11. Previous studies have shown the prevalence of gains and losses of genes and protein domains in the dawning of different groups of animals 10-14. The increasing availability of genome data is creating new oppor tunities to investigate animal genome evolution. For example, recent analyses have shown the importance of using large taxon sampling and a range of out-groups to reconstruct the minimum protein-coding genome present in the ancestor of a clade 6,15,16. To analyse the origins of genes during the early evolution of mammals and Metazoa, a bioinformatics pipeline was introduced that used state-of-the-art methods of homology assignment 15,16. We have previously outlined the limitations of the approach and differences from other methods such as phylostratigraphy 15,16. The approach focuses on protein-coding genes, but other genomic elements (non-coding RNA genes, regulatory regions, transposable elements and so on) most likely also contributed to the diversification of metazoans. Here we apply a new version of this pipeline to a large collection of metazoan genomes (59 genomes from 16 animal phyla) and a greatly expanded representation of outgroups (43 genomes) specifically to investigate patterns of the gain and loss of genes across major lineages of bilaterian animals. The use of complete genome sequences is particularly key to determining gene loss, since its inference from incomplete sources is problematic. The pipeline developed is given in the Methods and Supplementary Fig. 1. Briefly, we assembled a dataset of 102 previously sequenced eukaryotic genomes (Supplementary Table 1 and Supplementary Fig. 2), chosen for their phylogenetic positions and quality as assessed using BUSCO v3 17 (Supplementary Fig. 4). More than 2.6 million proteins were compared using BLAST 18 all-versus-all and were clustered with a Markov cluster algorithm 19 into homology groups (HGs). An HG is a group of protein-coding genes that differ from others consistently, independently of their mechanism of origin (divergence, de novo origin and so on). The extent of gene misassign-ment in HG clustering was assessed using metazoan and eukaryotic BUSCO gene sets for benchmarking, as well as performing receiver operating characteristic analyses (Supplementary Information). The HGs were analysed in a MySQL 5.7 database, which tabulates all species in the study classified according to phylogenetic relationships. For each node of the phylogenetic tree, MySQL finds HGs that are gained or lost by combining taxon presence/absence in each member of that clade. For example, an HG present only in species from the clade Vertebrata is considered a vertebrate novelty 15 (Supplementary Fig. 5 and Supplementary Data 1 and 2). Novel HGs (denoted +) are sets of related genes that emerged in the stem lineage or last common ancestor (LCA) of an ingroup, core novel HGs (++) are novel HGs that are present in 95% of the ingroup taxa (refractory to gene loss), lost HGs (denoted −) specify HGs lost on the stem lineage of the clade (before the LCA) and core lost HGs (−−) are lost HGs that are present in 95% of the outgroup taxa. We propose that both categories of core HG perform essential biological functions in the groups in which they are found, underpinning their preservation. However, the values of core novel HGs are also affected by the number of genomes included in a clade (for example, a clade with two genomes will display higher values of core novel HGs than a clade with ten representatives) and by their evolutionary relatedness (clades composed of closely related genomes will show higher proportions of core novel HGs). Core novel HGs for all nodes were further validated by BLAST against the RefSeq database 20 (Supplementary Data 4 and 6). In the case of phyla with a single genome sampled (for example, rotiferans, orthonectids and brachiopods), HG values may not be representative of the group;
Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move f... more Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move from water to land and the origins of vascular tissues, seeds, and flowers [1]. These have resulted in the evolution of terrestrial flora that has shaped modern ecosystems and the diversification of the Plant Kingdom, Viridiplantae, into over 374,000 described species [2]. Each of these transitions was accompanied by the gain and loss of genes in plant genomes. For example, whole-genome duplications are known to be fundamental to the origins of both seed and flowering plants [3, 4]. With the ever-increasing quality and quantity of whole-genome data, evolutionary insight into origins of distinct plant groups using comparative genomic techniques is now feasible. Here, using an evolutionary genomics pipeline to compare 208 complete genomes, we analyze the gene content of the ancestral genomes of the last common ancestor of land plants and all other major groups of plant. This approach reveals an unprecedented level of fundamental genomic novelties in two nodes related to the origin of land plants: the first in the origin of streptophytes during the Ediacaran and another in the ancestor of land plants in the Ordovician. Our findings highlight the biological processes that evolved with the origin of land plants and emphasize the importance of conserved gene novelties in plant diversification. Comparisons to other eukaryotic studies suggest a separation of the genomic origins of multicellularity and terrestrialization in plants.
Nature is adept at utilising highly similar protein folds to carry out very different functions, ... more Nature is adept at utilising highly similar protein folds to carry out very different functions, yet the mechanisms by which this functional divergence occurs remain poorly characterised. In certain methanotrophic bacteria, two homologous pentacoordinate c-type heme proteins have been identified: a cytochrome P460 (cyt P460) and a cytochrome c 0-b (cyt cp-b). Cytochromes P460 are able to convert hydroxylamine to nitrous oxide (N 2 O), a potent greenhouse gas. This reactivity is similar to that of hydroxylamine oxidoreductase (HAO), which is a key enzyme in nitrifying and methanotrophic bacteria. Cyt P460 and HAO both have unusual protein-heme cross-links, formed by a Tyr residue in HAO and a Lys in cyt P460. In contrast, cyts cp-b (the only known cytochromes c 0 with a b-sheet fold) lack this crosslink and appears to be optimized for binding non-polar molecules (including NO and CO) without enzymatic conversion. Our bioinformatics analysis supports the proposal that cyt cp-b may have evolved from cyt P460 via a gene duplication event. Using high-resolution X-ray crystallography, UV-visible absorption, electron paramagnetic resonance (EPR) and resonance Raman spectroscopy, we have characterized the overall protein folding and active site structures of cyt cp-b and cyt P460 from the obligate methanotroph, Methylococcus capsulatus (Bath). These proteins display a similar b-sheet protein fold, together with a pattern of changes to the heme pocket regions and localised tertiary structure that have converted a hydroxylamine oxidizing enzyme into a gas-binding protein. Structural comparisons provide insights relevant to enzyme redesign for synthetic enzymology and engineering of gas sensor proteins. We also show the widespread occurrence of cyts cp-b and characterise their phylogeny.
Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal ... more Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal axis of animal embryos. They are generally expressed in restricted spatial domains according to their position in the cluster (spatial colinearity)—a feature that is conserved across bilaterians. In jawed vertebrates (gnathostomes), the position in the cluster also determines the onset of expression of Hox genes (a feature known as whole-cluster temporal colinearity (WTC)), while in invertebrates this phenomenon is displayed as a subcluster-level temporal colinearity. However, little is known about the expression profile of Hox genes in jawless vertebrates (cyclostomes); therefore, the evolutionary origin of WTC, as seen in gnathostomes, remains a mystery. Here, we show that Hox genes in cyclostomes are expressed according to WTC during development. We investigated the Hox repertoire and Hox gene expression profiles in three different species—a hagfish, a lamprey and a shark—encompassing the two major groups of vertebrates, and found that these are expressed following a whole-cluster, temporally staggered pattern, indicating that WTC has been conserved during the past 500 million years despite drastically different genome evolution and morphological outputs between jawless and jawed vertebrates.
What makes an animal? To find the answer we need to integrate data from disciplines such as phylo... more What makes an animal? To find the answer we need to integrate data from disciplines such as phylogenetics, paleontology, ecology, development, anatomy, and physiology, as well as molecular biology and genomics. Knowledge of which groups branched before and after the origin of animals is essential. Recent advances in molecular phylogenetics, together with the discovery of new eukaryotic lineages, have drawn a new picture of the ancestry of animals. The nature of the early diverging animal lineages and the timing of the transition are in a state of flux. Various factors have been linked to this striking transition to multicellularity, including changes in environmental conditions and the ecological interactions between unicellular eukaryotes. The current wealth of genomic data has also shed new light on this question. The analysis of the genome of various close relatives of animals has revealed the importance that recycling of ancient genes into metazoan biological functions played into animal origins. A recent study reconstructing the genome of the last common ancestor of extant animals has unveiled an unprecedented emergence of new genes, highlighting the role of genomic novelty in the origin of metazoans.
Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolut... more Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolutionary biology. Many genomic changes took place along the evolutionary lineage that gave rise to the Metazoa. Recent research has revealed the role that co-option of old genes played during this transition, but the contribution of genomic novelty has not been fully assessed. Here, using extensive genome comparisons between metazoans and multiple outgroups, we infer the minimal protein-coding genome of the first animal, in addition to other eukaryotic ancestors, and estimate the proportion of novelties in these ancient genomes. Contrary to the prevailing view, this uncovers an unprecedented increase in the extent of genomic novelty during the origin of metazoans, and identifies 25 groups of metazoan-specific genes that are essential across the Animal Kingdom. We argue that internal genomic changes were as important as external factors in the emergence of animals.
Although animals are among the best studied organisms, we still lack a full description of their ... more Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected.
The metazoan superclade Lophotrochozoa includes mollusks, annelids, and several other animal phyl... more The metazoan superclade Lophotrochozoa includes mollusks, annelids, and several other animal phyla. It is reasonable to assume that this organismal diversity may be traced, in part, to changes in developmentally important genes, such as the homeobox genes. Although most comparative studies have focussed on ancient homeobox gene families conserved across bilaterians, there are also " novel " homeobox genes that have arisen more recently in evolution, presumably by duplication followed by radical divergence and functional change. We classify 136 homeobox genes in the genome sequence of the Pacific oyster, Crassostrea gigas. The genome shows an unusually low degree of homeobox gene clustering, with disruption of the NK, Hox, and ParaHox gene clusters. Among the oyster genes, 31 do not fall into ancient metazoan or bilaterian homeobox gene families; we deduce that they originated in the lophotrochozoan clade. We compared eight lophotrochozoan genomes to trace the pattern of homeobox gene evolution across this clade, allowing us to define 19 new lophotrochozoan-specific clades within the ANTP, PRD, TALE, ZF, SIX, and CUT classes. Using transcriptome data, we compared temporal expression of each homeobox gene in oyster development, and discovered that the lophotrochozoan-specific homeobox genes have peak expression either in early development (egg to gastrula) or in late development (after the trochophore larval stage), but rarely in between. This finding is consistent with the egg-timer, hourglass or phylotypic stage model of developmental evolution, in which there is a conserved central phase of development, but more evolutionarily labile early and late phases.
Streptomyces lividans has a distinct dependence on the bioavailability of copper for its morpholo... more Streptomyces lividans has a distinct dependence on the bioavailability of copper for its morphological development. A cytosolic copper resistance system is operative in S. lividans that serves to preclude deleterious copper levels. This system comprises of several CopZ-like copper chaperones and P 1-type ATPases, predominantly under the transcriptional control of a metalloregulator from the copper sensitive operon repressor (CsoR) family. In the present study, we discover a new layer of cytosolic copper resistance in S. lividans that involves a protein belonging to the newly discovered family of copper storage proteins, which we have named Ccsp (cytosolic copper storage protein). From an evolutionary perspective, we find Ccsp homologues to be widespread in Bacteria and extend through into Archaea and Eukaryota. Under copper stress Ccsp is upregulated and consists of a homotetramer assembly capable of binding up to 80 cuprous ions (20 per protomer). X-ray crystallography reveals 18 cysteines, 3 histidines and 1 aspartate are involved in cuprous ion coordination. Loading of cuprous ions to Ccsp is a cooperative process with a Hill coefficient of 1.9 and a CopZ-like copper chaperone can transfer copper to Ccsp. A Dccsp mutant strain indicates that Ccsp is not required under initial copper stress in S. lividans, but as the CsoR/CopZ/ATPase efflux system becomes saturated, Ccsp facilitates a second level of copper tolerance. Significance to metallomics Streptomyces lividans is an industrially used strain with application in the heterologous production of commercially valuable biomolecules. A distinct dependence on the bioavailability of copper for S. lividans morphological development is known and knowledge of the copper uptake, storage and delivery systems has led to the creation of new strains with improved biotechnological properties. Here, we provide new insights into copper tolerance in S. lividans through the identification and characterisation of a cytosolic copper storage protein (Ccsp). Ccsp is involved in a second layer of copper resistance once the CsoR/CopZ/P 1-ATPase systems become saturated.
Analysis of genome sequences within a phylogenetic context can give insight into the mode and tem... more Analysis of genome sequences within a phylogenetic context can give insight into the mode and tempo of gene and protein evolution, including inference of gene ages. This can reveal whether new genes arose on particular evolutionary lineages and were recruited for new functional roles. Here, we apply MCL clustering with all-versus-all reciprocal BLASTP to identify and phylogenetically date 'Homology Groups' among vertebrate proteins. Homology Groups include new genes and highly divergent duplicate genes. Focusing on the origin of the placental mammals within the Eutheria, we identify 357 novel Homology Groups that arose on the stem lineage of Placentalia, 87 of which are deduced to play core roles in mammalian biology as judged by extensive retention in evolution. We find the human homologues of novel eutherian genes are enriched for expression in pre-implantation embryo, brain, and testes, and enriched for functions in keratinization, reproductive development, and the immune system.
Gene duplications and gene losses have been frequent events in the evolution of animal genomes, w... more Gene duplications and gene losses have been frequent events in the evolution of animal genomes, with the balance between these two dynamic processes contributing to major differences in gene number between species. After gene duplication, it is common for both daughter genes to accumulate sequence change at approximately equal rates. In some cases, however, the accumulation of sequence change is highly uneven with one copy radically diverging from its paralogue. Such ‘asymmetric evolution’ seems commoner after tandem gene duplication than after whole-genome duplication, and can generate substantially novel genes. We describe examples of asymmetric evolution in duplicated homeobox genes of moths, molluscs and mammals, in each case generating new homeobox genes that were recruited to novel developmental roles. The prevalence of asymmetric divergence of gene duplicates has been underappreciated, in part, because the origin of highly divergent genes
The Acoelomorpha is an animal group comprised
by nearly 400 species of misleadingly inconspicuous... more The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this long-standing issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life.
The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poor... more The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poorly explored phyla, the Mollusca. Here we report the sequencing and assembly of the oyster genome using short reads and a fosmid-pooling strategy, along with transcriptomes of development and stress response and the proteome of the shell. The oyster genome is highly polymorphic and rich in repetitive sequences, with some transposable elements still actively shaping variation. Transcriptome studies reveal an extensive set of genes responding to environmental stress. The expansion of genes coding for heat shock protein 70 and inhibitors of apoptosis is probably central to the oyster's adaptation to sessile life in the highly stressful intertidal zone. Our analyses also show that shell formation in molluscs is more complex than currently understood and involves extensive participation of cells and their exosomes. The oyster genome sequence fills a void in our understanding of the Lophotrochozoa.
Proceedings. Biological sciences / The Royal Society, Jan 22, 2015
MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transc... more MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transcriptional regulation of gene expression. miRNA genes have been posited as highly conserved in the clades in which they exist. Consequently, miRNAs have been used as rare genome change characters to estimate phylogeny by tracking their gain and loss. However, their short length (21-23 bp) has limited their perceived utility in sequenced-based phylogenetic inference. Here, using reference taxa with established phylogenetic relationships, we demonstrate that miRNA sequences are of high utility in quantitative, rather than in qualitative, phylogenetic analysis. The clear orthology among miRNA genes from different species makes it straightforward to identify and align these sequences from even fragmentary datasets. We also identify significant sequence conservation in the regions directly flanking miRNA genes, and show that this too is of utility in phylogenetic analysis, as well as highlight...
Ctenophores have traditionally been treated as eumetazoans, but some recent whole genome studies ... more Ctenophores have traditionally been treated as eumetazoans, but some recent whole genome studies have revived the idea that they are, rather, the sister group to all other metazoans. This deep branching position implies either that nervous systems have evolved twice, in Ctenophora and in Eumetazoa, or that an ancestral metazoan nervous system has been lost in sponges and placozoans. We caution, however, that phylogenetic-tree construction artifacts may have placed ctenophores too deep in the metazoan tree. We discuss nervous system origins under these alternative phylogenies and in light of comparative data of ctenophore and eumetazoan nervous systems. We argue that characters like neuropeptide signaling, ciliary photoreceptors, gap junctions and presynaptic molecules are consistent with a shared ancestry of nervous systems. However, if ctenophores are the sister group to all other metazoans, this ancestral nervous system was likely very simple. Further studies are needed to resolve...
Proceedings of the National Academy of Sciences of the United States of America, Jan 16, 2014
The roles of 2-oxoglutarate (2OG)-dependent prolyl-hydroxylases in eukaryotes include collagen st... more The roles of 2-oxoglutarate (2OG)-dependent prolyl-hydroxylases in eukaryotes include collagen stabilization, hypoxia sensing, and translational regulation. The hypoxia-inducible factor (HIF) sensing system is conserved in animals, but not in other organisms. However, bioinformatics imply that 2OG-dependent prolyl-hydroxylases (PHDs) homologous to those acting as sensing components for the HIF system in animals occur in prokaryotes. We report cellular, biochemical, and crystallographic analyses revealing that Pseudomonas prolyl-hydroxylase domain containing protein (PPHD) contain a 2OG oxygenase related in structure and function to the animal PHDs. A Pseudomonas aeruginosa PPHD knockout mutant displays impaired growth in the presence of iron chelators and increased production of the virulence factor pyocyanin. We identify elongation factor Tu (EF-Tu) as a PPHD substrate, which undergoes prolyl-4-hydroxylation on its switch I loop. A crystal structure of PPHD reveals striking similar...
The first winged insects underwent profound morphological and functional transformations leading ... more The first winged insects underwent profound morphological and functional transformations leading to the most successful animal radiations in the history of earth. Despite this, we still have a very incomplete picture of the changes in their genomes that underlay this radiation. Mayflies (Ephemeroptera) are one of the extant sister groups of all other winged insects and therefore are at a key phylogenetic position to understand this radiation. Here, we describe the genome of the cosmopolitan mayfly Cloeon dipterum and study its expression along development and in specific organs. We discover an expansion of odorant-binding proteins, some expressed specifically in the breathing gills of aquatic nymphs, suggesting a novel sensory role for gills. In contrast, as flying adults, mayflies make use of an enlarged set of opsins and utilise these visual genes in a sexually dimorphic manner, with some opsins expressed only in males. Finally, to illuminate the origin of wings, we identify a cor...
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest anim... more The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.
Traditional evolutionary scenarios posit that land plants emerged from land plant-like relatives,... more Traditional evolutionary scenarios posit that land plants emerged from land plant-like relatives, the charophytes. New phylogenies suggest a closer affinity to simpler pond scum relatives, and evidence the gradual assembly of the land plant genome, revealing a phenotypic simplification from the complex ancestors envisaged by traditional scenarios
The animal kingdom shows an astonishing diversity, the product of over 550 million years of anima... more The animal kingdom shows an astonishing diversity, the product of over 550 million years of animal evolution. The current wealth of genome sequence data offers an opportunity to better understand the genomic basis of this diversity. Here we analyse a sampling of 102 whole genomes including >2.6 million protein sequences. We infer major genomic patterns associated with the variety of animal forms from the super-phylum to phylum level. We show that a remarkable amount of gene loss occurred during the evolution of two major groups of bilaterian animals, Ecdysozoa and Deuterostomia, and further loss in several deuterostome lineages. Deuterostomes and protostomes also show large genome novelties. At the phylum level, flatworms, nematodes and tardigrades show the largest reduction of gene complement, alongside gene novelty. These findings paint a picture of evolution in the animal kingdom in which reductive evolution at the protein-coding level played a major role in shaping genome composition. The Metazoa encompass an astonishing diversity of body forms. More than 30 animal phyla have been defined, the evolutionary relationships between which are well understood in broad outline, although some are still a matter of debate 1-4. Understanding how their genomes have evolved can help us better comprehend the origin of this diversity and reconstruct their evolutionary history. The Metazoa comprise sponges, ctenophores, cnidarians, placozo-ans and bilaterians, with most of animal diversity found in the last of these groups. The Bilateria can be split into three major groups or superphyla: Deuterostomia, Lophotrochozoa and Ecdysozoa 5 , the latter two forming the Protostomia. Gene losses and gains play major roles in evolution. The gain of new functions via the assembly of modules from older genes or the emergence of de novo coding regions has been proposed to be important during major evolutionary transitions such as the origin of animals 6-8. Gene loss has been associated with the loss of anatomical structures in evolution, consistent with views that evolution can lead to both increases and decreases in complexity 9-11. Previous studies have shown the prevalence of gains and losses of genes and protein domains in the dawning of different groups of animals 10-14. The increasing availability of genome data is creating new oppor tunities to investigate animal genome evolution. For example, recent analyses have shown the importance of using large taxon sampling and a range of out-groups to reconstruct the minimum protein-coding genome present in the ancestor of a clade 6,15,16. To analyse the origins of genes during the early evolution of mammals and Metazoa, a bioinformatics pipeline was introduced that used state-of-the-art methods of homology assignment 15,16. We have previously outlined the limitations of the approach and differences from other methods such as phylostratigraphy 15,16. The approach focuses on protein-coding genes, but other genomic elements (non-coding RNA genes, regulatory regions, transposable elements and so on) most likely also contributed to the diversification of metazoans. Here we apply a new version of this pipeline to a large collection of metazoan genomes (59 genomes from 16 animal phyla) and a greatly expanded representation of outgroups (43 genomes) specifically to investigate patterns of the gain and loss of genes across major lineages of bilaterian animals. The use of complete genome sequences is particularly key to determining gene loss, since its inference from incomplete sources is problematic. The pipeline developed is given in the Methods and Supplementary Fig. 1. Briefly, we assembled a dataset of 102 previously sequenced eukaryotic genomes (Supplementary Table 1 and Supplementary Fig. 2), chosen for their phylogenetic positions and quality as assessed using BUSCO v3 17 (Supplementary Fig. 4). More than 2.6 million proteins were compared using BLAST 18 all-versus-all and were clustered with a Markov cluster algorithm 19 into homology groups (HGs). An HG is a group of protein-coding genes that differ from others consistently, independently of their mechanism of origin (divergence, de novo origin and so on). The extent of gene misassign-ment in HG clustering was assessed using metazoan and eukaryotic BUSCO gene sets for benchmarking, as well as performing receiver operating characteristic analyses (Supplementary Information). The HGs were analysed in a MySQL 5.7 database, which tabulates all species in the study classified according to phylogenetic relationships. For each node of the phylogenetic tree, MySQL finds HGs that are gained or lost by combining taxon presence/absence in each member of that clade. For example, an HG present only in species from the clade Vertebrata is considered a vertebrate novelty 15 (Supplementary Fig. 5 and Supplementary Data 1 and 2). Novel HGs (denoted +) are sets of related genes that emerged in the stem lineage or last common ancestor (LCA) of an ingroup, core novel HGs (++) are novel HGs that are present in 95% of the ingroup taxa (refractory to gene loss), lost HGs (denoted −) specify HGs lost on the stem lineage of the clade (before the LCA) and core lost HGs (−−) are lost HGs that are present in 95% of the outgroup taxa. We propose that both categories of core HG perform essential biological functions in the groups in which they are found, underpinning their preservation. However, the values of core novel HGs are also affected by the number of genomes included in a clade (for example, a clade with two genomes will display higher values of core novel HGs than a clade with ten representatives) and by their evolutionary relatedness (clades composed of closely related genomes will show higher proportions of core novel HGs). Core novel HGs for all nodes were further validated by BLAST against the RefSeq database 20 (Supplementary Data 4 and 6). In the case of phyla with a single genome sampled (for example, rotiferans, orthonectids and brachiopods), HG values may not be representative of the group;
Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move f... more Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move from water to land and the origins of vascular tissues, seeds, and flowers [1]. These have resulted in the evolution of terrestrial flora that has shaped modern ecosystems and the diversification of the Plant Kingdom, Viridiplantae, into over 374,000 described species [2]. Each of these transitions was accompanied by the gain and loss of genes in plant genomes. For example, whole-genome duplications are known to be fundamental to the origins of both seed and flowering plants [3, 4]. With the ever-increasing quality and quantity of whole-genome data, evolutionary insight into origins of distinct plant groups using comparative genomic techniques is now feasible. Here, using an evolutionary genomics pipeline to compare 208 complete genomes, we analyze the gene content of the ancestral genomes of the last common ancestor of land plants and all other major groups of plant. This approach reveals an unprecedented level of fundamental genomic novelties in two nodes related to the origin of land plants: the first in the origin of streptophytes during the Ediacaran and another in the ancestor of land plants in the Ordovician. Our findings highlight the biological processes that evolved with the origin of land plants and emphasize the importance of conserved gene novelties in plant diversification. Comparisons to other eukaryotic studies suggest a separation of the genomic origins of multicellularity and terrestrialization in plants.
Nature is adept at utilising highly similar protein folds to carry out very different functions, ... more Nature is adept at utilising highly similar protein folds to carry out very different functions, yet the mechanisms by which this functional divergence occurs remain poorly characterised. In certain methanotrophic bacteria, two homologous pentacoordinate c-type heme proteins have been identified: a cytochrome P460 (cyt P460) and a cytochrome c 0-b (cyt cp-b). Cytochromes P460 are able to convert hydroxylamine to nitrous oxide (N 2 O), a potent greenhouse gas. This reactivity is similar to that of hydroxylamine oxidoreductase (HAO), which is a key enzyme in nitrifying and methanotrophic bacteria. Cyt P460 and HAO both have unusual protein-heme cross-links, formed by a Tyr residue in HAO and a Lys in cyt P460. In contrast, cyts cp-b (the only known cytochromes c 0 with a b-sheet fold) lack this crosslink and appears to be optimized for binding non-polar molecules (including NO and CO) without enzymatic conversion. Our bioinformatics analysis supports the proposal that cyt cp-b may have evolved from cyt P460 via a gene duplication event. Using high-resolution X-ray crystallography, UV-visible absorption, electron paramagnetic resonance (EPR) and resonance Raman spectroscopy, we have characterized the overall protein folding and active site structures of cyt cp-b and cyt P460 from the obligate methanotroph, Methylococcus capsulatus (Bath). These proteins display a similar b-sheet protein fold, together with a pattern of changes to the heme pocket regions and localised tertiary structure that have converted a hydroxylamine oxidizing enzyme into a gas-binding protein. Structural comparisons provide insights relevant to enzyme redesign for synthetic enzymology and engineering of gas sensor proteins. We also show the widespread occurrence of cyts cp-b and characterise their phylogeny.
Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal ... more Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal axis of animal embryos. They are generally expressed in restricted spatial domains according to their position in the cluster (spatial colinearity)—a feature that is conserved across bilaterians. In jawed vertebrates (gnathostomes), the position in the cluster also determines the onset of expression of Hox genes (a feature known as whole-cluster temporal colinearity (WTC)), while in invertebrates this phenomenon is displayed as a subcluster-level temporal colinearity. However, little is known about the expression profile of Hox genes in jawless vertebrates (cyclostomes); therefore, the evolutionary origin of WTC, as seen in gnathostomes, remains a mystery. Here, we show that Hox genes in cyclostomes are expressed according to WTC during development. We investigated the Hox repertoire and Hox gene expression profiles in three different species—a hagfish, a lamprey and a shark—encompassing the two major groups of vertebrates, and found that these are expressed following a whole-cluster, temporally staggered pattern, indicating that WTC has been conserved during the past 500 million years despite drastically different genome evolution and morphological outputs between jawless and jawed vertebrates.
What makes an animal? To find the answer we need to integrate data from disciplines such as phylo... more What makes an animal? To find the answer we need to integrate data from disciplines such as phylogenetics, paleontology, ecology, development, anatomy, and physiology, as well as molecular biology and genomics. Knowledge of which groups branched before and after the origin of animals is essential. Recent advances in molecular phylogenetics, together with the discovery of new eukaryotic lineages, have drawn a new picture of the ancestry of animals. The nature of the early diverging animal lineages and the timing of the transition are in a state of flux. Various factors have been linked to this striking transition to multicellularity, including changes in environmental conditions and the ecological interactions between unicellular eukaryotes. The current wealth of genomic data has also shed new light on this question. The analysis of the genome of various close relatives of animals has revealed the importance that recycling of ancient genes into metazoan biological functions played into animal origins. A recent study reconstructing the genome of the last common ancestor of extant animals has unveiled an unprecedented emergence of new genes, highlighting the role of genomic novelty in the origin of metazoans.
Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolut... more Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolutionary biology. Many genomic changes took place along the evolutionary lineage that gave rise to the Metazoa. Recent research has revealed the role that co-option of old genes played during this transition, but the contribution of genomic novelty has not been fully assessed. Here, using extensive genome comparisons between metazoans and multiple outgroups, we infer the minimal protein-coding genome of the first animal, in addition to other eukaryotic ancestors, and estimate the proportion of novelties in these ancient genomes. Contrary to the prevailing view, this uncovers an unprecedented increase in the extent of genomic novelty during the origin of metazoans, and identifies 25 groups of metazoan-specific genes that are essential across the Animal Kingdom. We argue that internal genomic changes were as important as external factors in the emergence of animals.
Although animals are among the best studied organisms, we still lack a full description of their ... more Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected.
The metazoan superclade Lophotrochozoa includes mollusks, annelids, and several other animal phyl... more The metazoan superclade Lophotrochozoa includes mollusks, annelids, and several other animal phyla. It is reasonable to assume that this organismal diversity may be traced, in part, to changes in developmentally important genes, such as the homeobox genes. Although most comparative studies have focussed on ancient homeobox gene families conserved across bilaterians, there are also " novel " homeobox genes that have arisen more recently in evolution, presumably by duplication followed by radical divergence and functional change. We classify 136 homeobox genes in the genome sequence of the Pacific oyster, Crassostrea gigas. The genome shows an unusually low degree of homeobox gene clustering, with disruption of the NK, Hox, and ParaHox gene clusters. Among the oyster genes, 31 do not fall into ancient metazoan or bilaterian homeobox gene families; we deduce that they originated in the lophotrochozoan clade. We compared eight lophotrochozoan genomes to trace the pattern of homeobox gene evolution across this clade, allowing us to define 19 new lophotrochozoan-specific clades within the ANTP, PRD, TALE, ZF, SIX, and CUT classes. Using transcriptome data, we compared temporal expression of each homeobox gene in oyster development, and discovered that the lophotrochozoan-specific homeobox genes have peak expression either in early development (egg to gastrula) or in late development (after the trochophore larval stage), but rarely in between. This finding is consistent with the egg-timer, hourglass or phylotypic stage model of developmental evolution, in which there is a conserved central phase of development, but more evolutionarily labile early and late phases.
Streptomyces lividans has a distinct dependence on the bioavailability of copper for its morpholo... more Streptomyces lividans has a distinct dependence on the bioavailability of copper for its morphological development. A cytosolic copper resistance system is operative in S. lividans that serves to preclude deleterious copper levels. This system comprises of several CopZ-like copper chaperones and P 1-type ATPases, predominantly under the transcriptional control of a metalloregulator from the copper sensitive operon repressor (CsoR) family. In the present study, we discover a new layer of cytosolic copper resistance in S. lividans that involves a protein belonging to the newly discovered family of copper storage proteins, which we have named Ccsp (cytosolic copper storage protein). From an evolutionary perspective, we find Ccsp homologues to be widespread in Bacteria and extend through into Archaea and Eukaryota. Under copper stress Ccsp is upregulated and consists of a homotetramer assembly capable of binding up to 80 cuprous ions (20 per protomer). X-ray crystallography reveals 18 cysteines, 3 histidines and 1 aspartate are involved in cuprous ion coordination. Loading of cuprous ions to Ccsp is a cooperative process with a Hill coefficient of 1.9 and a CopZ-like copper chaperone can transfer copper to Ccsp. A Dccsp mutant strain indicates that Ccsp is not required under initial copper stress in S. lividans, but as the CsoR/CopZ/ATPase efflux system becomes saturated, Ccsp facilitates a second level of copper tolerance. Significance to metallomics Streptomyces lividans is an industrially used strain with application in the heterologous production of commercially valuable biomolecules. A distinct dependence on the bioavailability of copper for S. lividans morphological development is known and knowledge of the copper uptake, storage and delivery systems has led to the creation of new strains with improved biotechnological properties. Here, we provide new insights into copper tolerance in S. lividans through the identification and characterisation of a cytosolic copper storage protein (Ccsp). Ccsp is involved in a second layer of copper resistance once the CsoR/CopZ/P 1-ATPase systems become saturated.
Analysis of genome sequences within a phylogenetic context can give insight into the mode and tem... more Analysis of genome sequences within a phylogenetic context can give insight into the mode and tempo of gene and protein evolution, including inference of gene ages. This can reveal whether new genes arose on particular evolutionary lineages and were recruited for new functional roles. Here, we apply MCL clustering with all-versus-all reciprocal BLASTP to identify and phylogenetically date 'Homology Groups' among vertebrate proteins. Homology Groups include new genes and highly divergent duplicate genes. Focusing on the origin of the placental mammals within the Eutheria, we identify 357 novel Homology Groups that arose on the stem lineage of Placentalia, 87 of which are deduced to play core roles in mammalian biology as judged by extensive retention in evolution. We find the human homologues of novel eutherian genes are enriched for expression in pre-implantation embryo, brain, and testes, and enriched for functions in keratinization, reproductive development, and the immune system.
Gene duplications and gene losses have been frequent events in the evolution of animal genomes, w... more Gene duplications and gene losses have been frequent events in the evolution of animal genomes, with the balance between these two dynamic processes contributing to major differences in gene number between species. After gene duplication, it is common for both daughter genes to accumulate sequence change at approximately equal rates. In some cases, however, the accumulation of sequence change is highly uneven with one copy radically diverging from its paralogue. Such ‘asymmetric evolution’ seems commoner after tandem gene duplication than after whole-genome duplication, and can generate substantially novel genes. We describe examples of asymmetric evolution in duplicated homeobox genes of moths, molluscs and mammals, in each case generating new homeobox genes that were recruited to novel developmental roles. The prevalence of asymmetric divergence of gene duplicates has been underappreciated, in part, because the origin of highly divergent genes
The Acoelomorpha is an animal group comprised
by nearly 400 species of misleadingly inconspicuous... more The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this long-standing issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life.
The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poor... more The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poorly explored phyla, the Mollusca. Here we report the sequencing and assembly of the oyster genome using short reads and a fosmid-pooling strategy, along with transcriptomes of development and stress response and the proteome of the shell. The oyster genome is highly polymorphic and rich in repetitive sequences, with some transposable elements still actively shaping variation. Transcriptome studies reveal an extensive set of genes responding to environmental stress. The expansion of genes coding for heat shock protein 70 and inhibitors of apoptosis is probably central to the oyster's adaptation to sessile life in the highly stressful intertidal zone. Our analyses also show that shell formation in molluscs is more complex than currently understood and involves extensive participation of cells and their exosomes. The oyster genome sequence fills a void in our understanding of the Lophotrochozoa.
Proceedings. Biological sciences / The Royal Society, Jan 22, 2015
MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transc... more MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transcriptional regulation of gene expression. miRNA genes have been posited as highly conserved in the clades in which they exist. Consequently, miRNAs have been used as rare genome change characters to estimate phylogeny by tracking their gain and loss. However, their short length (21-23 bp) has limited their perceived utility in sequenced-based phylogenetic inference. Here, using reference taxa with established phylogenetic relationships, we demonstrate that miRNA sequences are of high utility in quantitative, rather than in qualitative, phylogenetic analysis. The clear orthology among miRNA genes from different species makes it straightforward to identify and align these sequences from even fragmentary datasets. We also identify significant sequence conservation in the regions directly flanking miRNA genes, and show that this too is of utility in phylogenetic analysis, as well as highlight...
Ctenophores have traditionally been treated as eumetazoans, but some recent whole genome studies ... more Ctenophores have traditionally been treated as eumetazoans, but some recent whole genome studies have revived the idea that they are, rather, the sister group to all other metazoans. This deep branching position implies either that nervous systems have evolved twice, in Ctenophora and in Eumetazoa, or that an ancestral metazoan nervous system has been lost in sponges and placozoans. We caution, however, that phylogenetic-tree construction artifacts may have placed ctenophores too deep in the metazoan tree. We discuss nervous system origins under these alternative phylogenies and in light of comparative data of ctenophore and eumetazoan nervous systems. We argue that characters like neuropeptide signaling, ciliary photoreceptors, gap junctions and presynaptic molecules are consistent with a shared ancestry of nervous systems. However, if ctenophores are the sister group to all other metazoans, this ancestral nervous system was likely very simple. Further studies are needed to resolve...
Proceedings of the National Academy of Sciences of the United States of America, Jan 16, 2014
The roles of 2-oxoglutarate (2OG)-dependent prolyl-hydroxylases in eukaryotes include collagen st... more The roles of 2-oxoglutarate (2OG)-dependent prolyl-hydroxylases in eukaryotes include collagen stabilization, hypoxia sensing, and translational regulation. The hypoxia-inducible factor (HIF) sensing system is conserved in animals, but not in other organisms. However, bioinformatics imply that 2OG-dependent prolyl-hydroxylases (PHDs) homologous to those acting as sensing components for the HIF system in animals occur in prokaryotes. We report cellular, biochemical, and crystallographic analyses revealing that Pseudomonas prolyl-hydroxylase domain containing protein (PPHD) contain a 2OG oxygenase related in structure and function to the animal PHDs. A Pseudomonas aeruginosa PPHD knockout mutant displays impaired growth in the presence of iron chelators and increased production of the virulence factor pyocyanin. We identify elongation factor Tu (EF-Tu) as a PPHD substrate, which undergoes prolyl-4-hydroxylation on its switch I loop. A crystal structure of PPHD reveals striking similar...
Uploads
by nearly 400 species of misleadingly inconspicuous flatworms.
Despite this, acoelomorphs have been at the centre
of a heated debate about the origin of bilaterian animals for
150 years. The animal tree of life has undergone major changes
during the last decades, thanks largely to the advent of
molecular data together with the development of more rigorous
phylogenetic methods. There is now a relatively robust
backbone of the animal tree of life. However, some crucial
nodes remain contentious, especially the node defining the
root of Bilateria. Some studies situate Acoelomorpha (and
Xenoturbellida) as the sister group of all other bilaterians,
while other analyses group them within the deuterostomes
which instead suggests that the last common bilaterian ancestor
directly gave rise to deuterostomes and protostomes. The
resolution of this node will have a profound impact on our
understanding of animal/bilaterian evolution. In particular, if
acoelomorphs are the sister group to Bilateria, it will point to a
simple nature for the first bilaterian. Alternatively, if
acoelomorphs are deuterostomes, this will imply that they
are the result of secondary simplification. Here, we review
the state of this question and provide potential ways to solve
this long-standing issue. Specifically, we argue for the benefits
of (1) obtaining additional genomic data from acoelomorphs,
in particular from taxa with slower evolutionary rates; (2) the
development of new tools to analyse the data; and (3) the use
of metagenomics or metatranscriptomics data. We believe the
combination of these three approaches will provide a definitive
answer as to the position of the acoelomorphs in the animal
tree of life.
by nearly 400 species of misleadingly inconspicuous flatworms.
Despite this, acoelomorphs have been at the centre
of a heated debate about the origin of bilaterian animals for
150 years. The animal tree of life has undergone major changes
during the last decades, thanks largely to the advent of
molecular data together with the development of more rigorous
phylogenetic methods. There is now a relatively robust
backbone of the animal tree of life. However, some crucial
nodes remain contentious, especially the node defining the
root of Bilateria. Some studies situate Acoelomorpha (and
Xenoturbellida) as the sister group of all other bilaterians,
while other analyses group them within the deuterostomes
which instead suggests that the last common bilaterian ancestor
directly gave rise to deuterostomes and protostomes. The
resolution of this node will have a profound impact on our
understanding of animal/bilaterian evolution. In particular, if
acoelomorphs are the sister group to Bilateria, it will point to a
simple nature for the first bilaterian. Alternatively, if
acoelomorphs are deuterostomes, this will imply that they
are the result of secondary simplification. Here, we review
the state of this question and provide potential ways to solve
this long-standing issue. Specifically, we argue for the benefits
of (1) obtaining additional genomic data from acoelomorphs,
in particular from taxa with slower evolutionary rates; (2) the
development of new tools to analyse the data; and (3) the use
of metagenomics or metatranscriptomics data. We believe the
combination of these three approaches will provide a definitive
answer as to the position of the acoelomorphs in the animal
tree of life.