Insights into bilaterian evolution from three spiralian genomes

Abstract

Comparative analysis of the genomes of one mollusc (Lottia gigantea) and two annelids (Capitella teleta and Helobdella robusta) enable a more complete reconstruction of genomic features of the last common ancestors of protostomes, bilaterians and metazoans; against this conserved background they provide the first glimpse into lineage-specific evolution and diversity of the lophotrochozoans. This paper presents the draft genome sequences of two annelids — a freshwater leech (Helobdella robusta) and a bristly, segmented marine worm (Capitella teleta) — and a mollusc, the owl limpet (Lottia gigantea). These two phyla account for nearly one-third of known marine species and are of importance both ecologically and as experimental systems, yet they have not been served well by genomics efforts. Comparison of these genomes with those already available reveal some of the genetic changes linked to the origin and diversification of bilateral animals that are thought to have evolved during the 'Cambrian explosion' of multicellular life around 500 million years ago. Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ecologically and as experimental systems in classical embryology1,2,3. Here we describe the draft genomes of the owl limpet (Lottia gigantea), a marine polychaete (Capitella teleta) and a freshwater leech (Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversification of bilaterians from a genomic perspective. We find that the genome organization, gene structure and functional content of these species are more similar to those of some invertebrate deuterostome genomes (for example, amphioxus and sea urchin) than those of other protostomes that have been sequenced to date (flies, nematodes and flatworms). The conservation of these genomic features enables us to expand the inventory of genes present in the last common bilaterian ancestor, establish the tripartite diversification of bilaterians using multiple genomic characteristics and identify ancient conserved long- and short-range genetic linkages across metazoans. Superimposed on this broadly conserved pan-bilaterian background we find examples of lineage-specific genome evolution, including varying rates of rearrangement, intron gain and loss, expansions and contractions of gene families, and the evolution of clade-specific genes that produce the unique content of each genome.