Insights into early animal evolution from the genome of the xenacoelomorph worm Xenoturbella bocki

Elife. 2024 Aug 7:13:e94948. doi: 10.7554/eLife.94948.

Abstract

The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help understand the evolution and biology of enigmatic species better. Here, we assemble and analyze the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome-like scaffolds, with repeat content and intron, exon, and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signaling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.

Keywords: Deuterostomia; Xenacoelomorpha; Xenoturbella; animal evolution; evolutionary biology; genetics; genome analysis; genomics; xenoturbella bocki.

Plain language summary

Xenoturbella bocki is a small marine worm predominantly found on the seafloor of fjords along the west coast of Sweden. This simple organism’s unusual evolutionary history has long intrigued zoologists as it is not clear how it is related to other animal groups. The worm may belong to one of the earliest branches of the animal kingdom, which would explain its simple body. On the other hand, it could be related to a more complex group, the deuterostomes, which includes a wide range of animals, from mammals and birds to sea urchins and starfish. Understanding X. bocki’s evolution could provide valuable insights into how bilaterians evolved as a whole. Unlike its close relatives, the acoelomorphs, X. bocki evolves more slowly, which makes it simpler to study its genome. As a result, it serves as a starting point for investigating the evolutionary processes and genetics underpinning the broader group of bilaterians. To better understand the evolution of X. bocki’s simple body, Schiffer et al. asked whether its genome is simpler or differs in other ways from that of more complex bilaterian organisms. Sequencing the entire X. bocki genome revealed that it has a similar number of genes to that of other animals and includes the genes required for complex biochemical pathways. Reconstructing the worm’s chromosomes – the structures that house genetic information – showed that the X. bocki genes are also distributed in a manner similar to those in other animals. The findings suggest that, despite its simple body plan, X. bocki has a complex genome that is typical of bilaterians. This challenges the idea that X. bocki belongs to a more primitive, simplified sister group to Bilateria and provides a starting point for further studies of how this simple worm evolved.

MeSH terms

  • Animals
  • Biological Evolution
  • Evolution, Molecular
  • Genome*
  • Invertebrates / genetics
  • Phylogeny
  • Synteny