Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates-a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.

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Acorn worms, also known as enteropneust (literally, ‘gut-breathing’) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal ‘gill’ slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

The crown-of-thorns starfish (COTS, the Acanthaster planci species group) is a highly fecund predator of reef-building corals throughout the Indo-Pacific region 1 . COTS population outbreaks cause substantial loss of coral cover, diminishing the integrity and resilience of reef ecosystems 2-6 . Here we sequenced genomes of COTS from the Great Barrier Reef, Australia and Okinawa, Japan to identify gene products that underlie species-specific communication and could potentially be used in biocontrol strategies. We focused on water-borne chemical plumes released from aggregating COTS, which make the normally sedentary starfish become highly active. Peptide sequences detected in these plumes by mass spectrometry are encoded in the COTS genome and expressed in external tissues. The exoproteome released by aggregating COTS consists largely of signalling factors and hydrolytic enzymes, and includes an expanded and rapidly evolving set of starfish-specific ependymin-related proteins. These secreted proteins may be detected by members of a large family of olfactory-receptor-like G-protein-coupled receptors that are expressed externally, sometimes in a sex-specific manner. This study provides insights into COTS-specific communication that may guide the generation of peptide mimetics for use on reefs with COTS outbreaks.COTS are extremely fecund mass spawners 7 , which predisposes them to population outbreaks that result in a pronounced loss of live coral cover and associated biodiversity. These outbreaks have a higher impact on reef health and resilience than the combined effects of coral bleaching and disease, and increase the susceptibility of reefs to other potentially detrimental events, such as severe storms [2][3][4][5][6] (Supplementary Note 1).Although a range of local in situ control measures have been applied with some success (Supplementary Note 1), mitigation of COTS outbreaks on the necessary regional scale requires mass-deployed, species-specific strategies. In this context, genome-encoded COTSspecific attractants that underpin spawning aggregations have substantial potential as biocontrol agents. To identify attractants, we sequenced the genomes of two wild-caught individuals separated by over 5,000 km, one from the Great Barrier Reef (GBR), Australia and the other from Okinawa (OKI), Japan (Fig. 1c, d and Extended Data Fig. 1). We also sequenced transcriptomes from external organs, and proteins released into the seawater by COTS that were aggregating or were in the presence of their main predator, the giant triton Charonia tritonis (Fig. 1b).We generated separate 384 megabase (Mb) draft assemblies for the GBR and OKI genomes (Extended Data COTS genes are labelled and are marked with red lines; other asteroids, two shades of orange and yellow lines; sea urchins, dark green; hemichordates, light green; molluscs, pink; annelids, purple; cnidarians, black; and vertebrates, blue. The three clades to which COTS sequences belong are indicated by the outer circle. The asterisk denotes the fish-specific tru...

Almost the entire sequences of 18S rDNA were determined for two chaetognaths, five echinoderms, a hemichordate, and two urochordates (a larvacean and a salp). Phylogenetic comparisons ofthe sequences, together with those of other deuterostomes (an ascidian, a cephalochordate, and vertebrates) and protostomes (an arthropod and a mollusc), suggest the monophyly ofthe deuterostomes, with the exception of the chaetognaths. Chaetognaths may not be a group of deuterostomes. The deuterostome group closest to vertebrates was the group of cephalochordates. Ascidians, larvaceans, and salps seem to form a discrete group (urochordates), in which the early divergence of larvaceans is evident. These results support the hypothesis that chordates evolved from free-living ancestors.The evolutionary pathway from advanced invertebrates through primitive chordates to vertebrates has been a subject of extensive investigation and vigorous discussion for more than a century (1-5). Chordates are categorized as deuterostomes, which are characterized by several features that include, for example, radial cleavage, the fate of the blastopore that does not form a mouth, an enterocoelic coelom, and a tripartite body plan (4-7). Traditionally, the deuterostomes include pogonophorans, chaetognaths, echinoderms, hemichordates, and chordates (urochordates, cephalochordates, and vertebrates), but recent studies have forced the categorization of pogonophorans near the annelids (7, 8). The chaetognath (arrowworm) remains a mystery in terms of its ancestry.Recent advances in molecular biology have made it possible to answer some of the questions posed by evolutionary biologists. Comparisons based on molecular data, such as the amino acid sequences of certain proteins and the nucleotide sequences of certain RNAs and DNAs, provide powerful tools with which to examine phylogenetic relationships among animal groups since these molecular characteristics can be interpreted more objectively than others. Unfortunately, pioneer studies with sequences of 5S rRNA (9) and partial sequences of 18S rRNA (10) failed to affirm the monophyly ofdeuterostomes, probably because the radiation of bilaterally symmetrical animals occurred over a very short period of time. However, the monophyly of the deuterostomes was suggested by Lake (11) after application of his original method for the construction ofphylogenetic trees. A recent study by Stock and Whitt (12) provided evidence from sequences of 18S rRNAs that lampreys and hagfishes form a natural group, but conclusive support from molecularphylogenetic analysis for the monophyly of the deuterostomes has not yet been obtained.To further our knowledge of the phylogeny of deuterostomes, we determined almost the entire sequences of 18S rDNAs from two chaetognaths, five echinoderms, a hemichordate, and two urochordates (a larvacean and a salp) and, together with the sequences of other deuterostomes (an ascidian, a cephalochordate, and vertebrates) and protostomes (an arthropod and a mollusc) (13), we reexamined the ...

*Nemerteans (ribbon worms) and phoronids (horseshoe worms) are closely related lophotrochozoans-a group of animals including leeches, snails and other invertebrates. Lophotrochozoans represent a superphylum that is crucial to our understanding of bilaterian evolution. However, given the inconsistency of molecular and morphological data for these groups, their origins have been unclear. Here, we present draft genomes of the nemertean Notospermus geniculatus and the phoronid Phoronis australis, together with transcriptomes along the adult bodies. Our genome-based phylogenetic analyses place Nemertea sister to the group containing Phoronida and Brachiopoda. We show that lophotrochozoans share many gene families with deuterostomes, suggesting that these two groups retain a core bilaterian gene repertoire that ecdysozoans (for example, flies and nematodes) and platyzoans (for example, flatworms and rotifers) do not. Comparative transcriptomics demonstrates that lophophores of phoronids and brachiopods are similar not only morphologically, but also at the molecular level. Despite dissimilar head structures, lophophores express vertebrate head and neuronal marker genes. This finding suggests a common origin of bilaterian head patterning, although different heads evolved independently in each lineage. Furthermore, we observe lineagespecific expansions of innate immunity and toxin-related genes. Together, our study reveals a dual nature of lophotrochozoans, where conserved and lineage-specific features shape their evolution. Articles NaTure eCOLOgy & evOLuTiONphoronids, ectoprocts and brachiopods, although the position of ectoprocts is questionable under a sensitivity analysis. Our results clearly show that lophotrochozoans have a different evolutionary history than other spiralians (or platyzoans), such as flatworms and rotifers. In particular, lophotrochozoans retain a basic bilaterian gene repertoire, which is probably lost in ecdysozoans and other spiralian lineages. Unexpectedly, genes specifically expressed in lophophores of phoronids and brachiopods are strikingly similar to those employed in vertebrate head formation, although novel genes, expanded gene families and redeployment of developmental genes also contribute to the unique molecular identity of lophophores. Furthermore, we provide examples of lineage-specific genomic features in lophotrochozoans, such as the expansion of innate immunity and toxin-related genes. Taken together, our study reveals the dual nature of lophotrochozoan genomes, showing both conservative and innovative characteristics during their evolution.