Gene family innovation, conservation and loss on the animal stem lineage

Abstract

Choanoflagellates, the closest living relatives of animals, can provide unique insights into the changes in gene content that preceded the origin of animals. However, only two choanoflagellate genomes are currently available, providing poor coverage of their diversity. We sequenced transcriptomes of 19 additional choanoflagellate species to produce a comprehensive reconstruction of the gains and losses that shaped the ancestral animal gene repertoire. We identified ~1944 gene families that originated on the animal stem lineage, of which only 39 are conserved across all animals in our study. In addition, ~372 gene families previously thought to be animal-specific, including Notch, Delta, and homologs of the animal Toll-like receptor genes, instead evolved prior to the animal-choanoflagellate divergence. Our findings contribute to an increasingly detailed portrait of the gene families that defined the biology of the Urmetazoan and that may underpin core features of extant animals.

eLife digest

All animals, from sea sponges and reef-building corals to elephants and humans, share a single common ancestor that lived over half a billion years ago. This single-celled predecessor evolved the ability to develop into a creature made up of many cells with specialized jobs. Reconstructing the steps in this evolutionary process has been difficult because the earliest animals were soft-bodied and microscopic and did not leave behind fossils that scientists can study.

Though their bodies have since disintegrated, many of the instructions for building the first animals live on in genes that were passed on to life forms that still exist. Scientists are trying to retrace those genes back to the first animal by comparing the genomes of living animals with their closest relatives, the choanoflagellates. Choanoflagellates are single-celled, colony-forming organisms that live in waters around the world. Comparisons with choanoflagellates may help scientists identify which genes were necessary to help animals evolve and diversify into so many different species. So far, 1,000 animal and two choanoflagellate genomes have been sequenced. But the gene repertoires of most species of choanoflagellates have yet to be analyzed.

Now, Richter et al. have cataloged the genes of 19 more species of choanoflagellates. This added information allowed them to recreate the likely gene set of the first animal and to identify genetic changes that occurred during animal evolution. The analyses showed that modern animals lost about a quarter of the genes present in their last common ancestor with choanoflagellates and gained an equal number of new genes. Richter et al. identified several dozen core animal genes that were gained and subsequently preserved throughout animal evolution. Many of these are necessary so that an embryo can develop properly, but the precise roles of some core genes remain a mystery. Most other genes that emerged in the first animals have been lost in at least one living animal.

The study of Richter et al. also showed that some very important genes in animals, including genes essential for early development and genes that help the immune system detect pathogens, predate animals. These key genes trace back to animals’ last common ancestor with choanoflagellates and may have evolved new roles in animals.