The emergence of multicellular animals from single-celled ancestors over 600 million years ago required the evolution of mechanisms for coordinating cell division, growth, specialization, adhesion and death. Dysfunction of these mechanisms drives diseases such as cancers, in which social controls on multicellularity fail, and autoimmune disorders, in which distinctions between self and non-self are disrupted. The hallmarks of metazoan multicellularity are therefore intimately related to those of cancer1
, relying on oncogenes, tumour suppressors and cell-surface and signalling components.
Sponges have a critical role in the search for the origins of metazoan multicellular processes3
, as they are generally recognized as the oldest surviving metazoan phyletic lineage. Although the kinship of sponges to other animals was recognized by the nineteenth century4
, the absence of a gut and nervous system had relegated sponges to the ‘Parazoa’5
, a grade below the ‘Eumetazoa’ or ‘true animals’ (for example, cnidarians, ctenophores and bilaterians)6
. Nevertheless, sponges share key adhesion and signalling genes7–11
with eumetazoans, as well as other genes important in body plan patterning such as developmental transcription factors12–15
; sponge embryos and larvae () are readily comparable to those of other animals12,16
. Sponges are diverse and their phylogeny is poorly resolved17–19
, allowing for the possibility that sponges are paraphyletic20
, which implies that other animals evolved from sponge-like ancestors.
Figure 1 a, Amphimedon queenslandica adult. Scale bar, 5 cm. b, Embryos in a brood chamber. Scale bar, 1 mm. c, Larva. Scale bar, 100 µm. d, Animal phylogeny based on whole-genome data. This unrooted tree is inferred from 229 concatenated nuclear protein-coding (more ...)
Here we report on the genome of Amphimedon queenslandica, a haplosclerid demosponge, the adult organization and lifestyle of which is typical for sponges, feeding on microbes and particulate organic matter filtered by flagellated collar cells that resemble choanoflagellates. Although the diversity of sponges, and their uncertain phylogeny, makes it doubtful that any single species can reveal the intricacies of early animal evolution, comparison of the A. queenslandica draft genome with sequences from other species can provide a conservative estimate of the genome of the common ancestor of all animals and the timing and nature of the genomic events that led to the origin and early evolution of animal lineages.
The A. queenslandica genome harbours an extensive repertoire of developmental signalling and transcription factor genes, indicating that the metazoan ancestor had a developmental ‘toolkit’ similar to that in modern complex bilaterians. The origins of many of these and other genes specific to animal processes such as cell adhesion, and social control of cell proliferation, death and differentiation can be traced to genomic events (gene birth, subfamily expansions, intron gain/loss, and so on) that occurred in the lineage that led to the metazoan ancestor, after animals diverged from their unicellular ‘cousins’. In addition to possessing a wide range of metazoan-specific genes, the Amphimedon draft genome is missing some genes that are conserved in other animals, indicative of gene origin and expansion in eumetazoans after their divergence from the demosponge lineage and/or gene loss in Amphimedon.