Capsaspora and the evolution of animals

"The Dynamic Regulatory Genome of Capsaspora and the Origin of Animal Multicellularity"

Cell 165, 1224–1237, May 19, 2016

All animals - which includes, but is not limited to, insects, worms, fish, birds, mice, coral, jellyfish - have a single common ancestor in evolutionary history, a single proto-animal cell that floated in the oceans of our planet hundreds of millions of years ago. This single proto-animal evolved into several different early animals with distinct anatomies. These early animals gave rise to distinct "lineages", and over a period spanning hundreds of millions of years, these lineages grew and grew, giving rise to all the animals that have ever existed: bony fish, land vertebrates, insects, dinosaurs, mammals, birds and many, many more. 

Early animal life

Fossils have helped us understand some of the earliest events in animal evolution, particularly fossil deposits like the Burgess Shale Formation. The Burgess Shale fossils are over 500 million years old and give us some of our clearest glimpses into the form of early animal life.

All animals are multicellular - unlike bacteria and single-celled eukaryotes like yeast or amoeba. They are composed of many cooperating cells that form tissues and organs. All of these tissues and organs arise from a single fertilized egg cell that grows into a multicellular adult through a process called animal development. 

The common ancestor of animals and their closest single-celled cousins must have been single-celled, because all life began with single cells. 

How does a single cell become multicellular? This is one of the big questions in evolutionary biology, and to a large extent it remains a mystery. There are many multicellular organisms that are not animals - plants and fungi for instance. It seems that there are many independent genetic and evolutionary paths that lead to multicellularity. 

How did animals become multicellular? This is a more specific, tractable question. As all animals existing today have a single common unicellular ancestor, we can use comparative biology to understand the manner in which animals became multicellular.

The Evolutionary Tree of Animals

Comparative approaches have long been a powerful tool in evolutionary biology. Key organisms occupy very special positions in the evolutionary history of animals. Consider the extinct dinosaur Archaeopteryx - a transitional intermediate between ancient dinosaurs and modern, feathered birds. 

By comparing the anatomy of Archaeopteryx fossils to both their dinosaur ancestors and their bird descendants, scientists can infer the evolutionary steps that lead to the evolution of structures like feathers and wings. 

The invention of genome sequencing technologies has allowed biologists to extend these comparative approaches to the molecular scale, comparing DNA sequences instead of skeletal anatomy.

Every organism contains a trace of all its ancestors within its DNA, because every genome arises from the evolution of a pre-existing genome. The science of comparative genomics tries to reconstruct the evolutionary and genetic history of organisms by comparing their genome sequences. For example, studies have compared the genome sequences of human beings to chimpanzees, our closest living relatives. Although human and chimpanzee genomes are extremely similar, there are some DNA sequences that are very different in humans. Presumably, these sequences played a key role in the evolution of Homo sapiens from our ape-like ancestors.

So how did animals genetically evolve to become multicellular? Two hypotheses can be put forward:

1. New Genes: animal ancestors evolved completely new genes 
2. New Regulation: animal ancestors evolved new ways to control existing genes

Scanning EM image of Capsaspora owczarzaki
(taken from PNAS)

In order to address this question, a group of scientists studied Capsaspora owczarzaki - an organism that is one of the closest unicellular relatives to the entire animal lineage. 

Iñaki Ruiz-Trillo's group at the Institut de Biologia Evolutiva in Barcelona has published a number of comparative genomic studies on Capsaspora to try and answer some fundamental questions about the evolution of animal multicellularity.

In previous work from the group, the entire Capsaspora genome was sequenced and compared to known animal genomes. Many of the complex genes previously thought to be unique to animals turned out to be present in this simple, unicellular relative. But there are still a large number of genes that appear to be unique to the animal lineage, particularly those involved in communication between cells, a process that is extremely important during animal development.

In their most recent paper, the group applied some new genomic methods to study the Capsaspora genome. While traditional genome sequencing gives a static readout of the DNA sequence, newer methods can provide dynamic snapshots of the genome in action. 

Every gene has associated DNA control elements that limit where and when the gene is turned on - acting as 'switches' and 'regulators'. The processes by which the expression of genes is controlled across space and time are called gene regulation.

All organisms have control elements in their DNA called 'promoters' that are always located close to the genes that they regulate. Some organisms have a second set of control elements called 'enhancers' - these can occupy very distant locations from the genes they control and are thought to expand an organism's capacity for complex gene regulation.

New technologies allow us to visualize the organization of these control elements in different organisms. This paper provides our first view of the organization of gene regulation in Capsaspora, and thus provides a view into what elements of gene regulation are unique to the multicellular animal lineage.

The study finds that although Capsaspora gene regulation has many elements in common with animals, it completely lacks the distant 'enhancer' control elements that are present in all animals. This suggests that the evolution of this mode of gene regulation was absent before the evolution of early animal ancestors, and could have been one of the key genetic innovations that lead to the evolution of animal multicellularity.

So did animal multicellularity require the invention of new genes or new regulation of old genes? As with many things in biology, it was a bit of both.