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...

Vertebrates have highly methylated genomes at CpG positions whereas invertebrates have sparsely methylated genomes. This increase in methylation content is considered a major regulatory innovation of vertebrate genomes. However, here we report that a marine sponge, proposed as the sister group to the rest of animals, has a highly methylated genome. Despite major differences in genome size and architecture, we find similarities between the independent acquisitions of the Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

The most widely held, but rarely tested, hypothesis for the origin of animals is that they evolved from a unicellular ancestor with an apical cilium surrounded by a microvillar collar that structurally resembled modern sponge choanocytes and choanoflagellates 1-4. Here we test this traditional view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types-choanocytes, pluripotent mesenchymal archeocytes and epithelial pinacocytes-with choanoflagellates and other unicellular holozoans. Unexpectedly, we find the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. In contrast, pluripotent archeocytes up-regulate genes controlling cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archeocytes, which can differentiate into a range of other cell types. These sponge cell type conversions are similar to the temporal cell state changes that occur in unicellular holozoans 5. Together, these analyses offer no support for the homology of sponge choanocytes and choanoflagellates, nor for the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells. References 1 Cavalier-Smith, T. Origin of animal multicellularity: precursors, causes, consequences-the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion.

Main 46The last common ancestor of all living animals appears to have possessed epithelial and 47 mesenchymal cell types that could transdifferentiate over an ontogenetic life cycle 48 ( Fig.1a) 1,4 . This capacity to develop and differentiate required a regulatory capacity to 49 control spatial and temporal gene expression, and included a diversified set of signalling 50 pathways, transcription factors, enhancers, promoters and non-coding RNAs (Fig. 1a) [5][6][7][8][9] . 51Recent analyses of the genomes and life cycles of unicellular holozoan relatives of 52 animals have revealed that the regulatory repertoire present in multicellular animals 53 largely evolved first in a unicellular ancestor ( Fig. 1a) 2,5,6 . These insights contrast with a 54 widely-held view that all animals evolved from a stem organism that was a simple ball 55 of ciliated cells 1,3,4 . Implicit in this traditional perspective is that (i) regulatory systems 56 necessary for cell differentiation evolved after the divergence of metazoan and 57 choanoflagellates lineages, and (ii) morphological features shared between 58 choanoflagellate and choanocytes are homologous and were present in the original 59 animal cell. While the former is not supported by recent data -unicellular holozoans 60 can change cell states by environmentally-induced temporal shifts in gene expression 61 ( Fig. 1a) 5,6,10-12 -the latter is contingent upon the still controversial aspect of whether 62 extant choanocytes and choanoflagellates accurately reflect the ancestral animal cell 63 type. 64To test this, we first compared cell type-specific transcriptomes 13 from the sponge 65Amphimedon queenslandica with each other, and with transcriptomes expressed during 66 the life cycles of closely-related unicellular holozoans, the choanoflagellate Salpingoeca 67 rosetta, the filasterean Capsaspora owczarzaki and the ichthyosporean Creolimax 68 fragrantissima (Fig. 1a) 10-12 . We chose three sponge somatic cell types hypothesised to 69 be homologous to cells present in the last common ancestor of contemporary Extended Data Figure 2: Percentage of KEGG cellular processes and 663 environmental information processing (i.e. cell signalling) genes present in each 664 cell type, corresponding to the number of components making up each KEGG 665 category identified. 666 a, Cellular processes genes. b, Environmental information processing (i.e. cell 667 signalling) genes. 668 669 Extended Data Figure 3: Evolutionary age of genes expressed in Amphimedon 670 queenslandica choanocytes, archeocytes and pinacocytes using different 671 expression thresholds. 672 *