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Ancient Genes Reveal Our Precambrian Ancestor

The Amphimedon sponge

The Amphimedon sponge (shown here inside a pink soft coral) is the first sponge to have its genome sequenced. Photo: Maely Gauthier

By Claire Larroux

The genome of a sponge found on the Great Barrier Reef is helping scientists to reconstruct the 600 million-year-old ancestor of the entire animal kingdom.

One of the great questions in evolution is how complexity evolves. How does one go from a single-celled organism to a complex animal?

Fossils appear to tell us that most animal forms we know today arose in a short window of time during the Cambrian explosion approximately 540 million years ago. Creationists use this sudden appearance of complex animals to deny that evolution occurs.

But what happened before the Cambrian? The sparse fossil record of sponges and the enigmatic Ediacaran fauna suggest that animals were already experimenting with multicellular life during this Precambrian period. Was there a gradual increase in complexity in the first animals?

A modest sponge from the Great Barrier Reef is helping us to answer these questions. Amphimedon queenslandica, named after the state of Queensland, has the honour of being the first sponge to have its genome sequenced.

Sponges are the most ancient animals on Earth, dating back to well before the Cambrian period. As a representative of our oldest animal cousins, the Amphimedon sponge genome is helping us to piece together our common ancestor with all other animals, which lived more than
600 million years ago.

To put this ancestor into context, the only visible life-forms in the ocean when it evolved were mats of blue-green bacteria and small filamentous green and red algae. Hence, the appearance of the first animal was a leap ahead in the history of life.

In a recent paper published in Nature, we compared the Amphimedon sponge genome with the genomes of other animals. This enabled us to reconstruct the genome of our Precambrian ancestor and make inferences regarding what this ancestor looked like. We wanted to identify the conditions that were necessary and sufficient for multicellular animals to evolve.

This work is part of the budding research field of palaeogenomics, which is taking advantage of the increasing number of genomes being sequenced thanks to improved sequencing techniques and the accompanying drop in costs. Our research has shown that although our Precambrian ancestor essentially had most of the characteristics that make up modern animals, it was fundamentally less complex than all the younger animals that appeared during the Cambrian explosion.

Whether we’re looking at the internal combustion engine, human societies or the biology of living creatures, specialisation of their “parts” leads to a more complex “whole”. In the same way, a multicellular organism needs specialised cells to perform specific functions. These specialised cells, or organs, must be organised spatially into a body plan. This occurs during embryonic development, and is governed by underlying genes and the proteins they produce.

At the molecular level, signalling pathways during development enable long-range communication between cells, while transcription factors switch genes on and off . Most animals studied to date share these genetic tools, but were they present in the first animals?

The Amphimedon genome tells us that this genetic toolkit arose in the first animals, albeit in a simplified form. Furthermore, the number of genes increased in the period preceding the Cambrian explosion. Could this gene increase be responsible for the Cambrian explosion and the huge biodiversity displayed among living animals?

After all, a sponge has remained a sponge for millions of years. Perhaps their limited genetic toolkit prevented them from becoming more complex while the genetic expansion in Cambrian animals allowed them to explore body plans as different as those of a sea star, a worm and a human.

Increasing evidence from sponge genes suggest that this is the case. Evidence of evolution occurring step-by-step in the first animals links Hox master control genes to the origin of complex body plans.

Hox genes are fundamental genes that control where cells and organs end up along the anterior–posterior body axis of very different animals. This is why the brain is always at the anterior end of animals as diverse as worms, flies and humans.

Sponges do have a basic body axis in their larva but they lack complex structures along this axis as well as Hox genes in their genome. However, some signalling molecules seem to arrange sponges in a basic manner, with a head at one end, a tail at the other and nothing specific in between. Thus our Precambrian ancestor may have been spatially organised from two opposite poles, with complex organisation along an axis evolving later when Hox genes arose.

What else does a multicellular animal need?

• Its cells must stick together.

• It needs to have control of the proliferation and growth of cells in order to fight cancer. This also includes mechanisms of programmed cell death.

• It must recognise self from non-self to defend itself against foreign organisms.

The genes responsible for these fundamental animal characteristics are present in the Amphimedon genome, confirming that they were necessary for the evolution of multicellularity. Interestingly, we found that these essential genes are often associated with cancer in humans. Hence multicellularity and cancer evolved side-by-side in animals. With hindsight this is not surprising because cancer essentially results from a malfunction of the mechanisms of multicellularity.

An important invention in animals was the epithelium, a sealed sheet of cells that allows an organism to isolate its internal environment and control exchanges with the external environment. Organs are also separated from the rest of the body by an epithelial layer. Hence, the evolution of an epithelium was also crucial for the compartmentalisation and specialisation that organs allow.

While the sponge genome has many of the genes underlying epithelial structure, it is missing some crucial ones. Hence sponges lack a true epithelium and organs. The epithelium may therefore be a later innovation that was not necessary for multicellular animals to evolve but was nevertheless crucial to the increased complexity in the body plans of Cambrian animals.

If you had to pick one trait that separates humans and other animals from plants or fungi, it would have to be the brain. Not only does the brain enable us to think but it also allows us to sense our environment and move in it with a purpose. From jellyfish to humans, neurons interact with muscles and sensory organs such as eyes, enabling us to react to our surroundings in a fast and co­ordinated manner. Unlike our distant multicellular cousins, the fungi and plants, we animals can behave in complex manners due to this invention.

Yet sponges and a small group of little-known animals called placozoans are the only animals that don’t have neurons. Based on the sponge genome, the key players that enabled neurons to evolve during the Cambrian period were axon guidance molecules and fast-response neurotransmitter receptors. The former enable neurons to send out axons and connect with other neurons. The latter allow the electrical signal to be transmitted quickly from one neuron to another through the synapse gap.

But what did neurons evolve from? Although they are not neurons, certain sponge cells can sense their environment. This allows sponge larvae to respond to light or taste. The presence of these cells in sponges does not automatically entail that they are related to neurons. After all, sensory cells have evolved independently in various plants and single-celled organisms.

Take the sunflower, for example. The mechanism by which the sunflower turns towards the sun is similar to what occurs in the sponge larva: it is the individual response of each cell to light that turns the flower. In the sponge larva, swimming away from the light is the sum-total of the individual reaction of each cell. There is no coordination between the cells.

So, at first glance, sponge sensory cells are just as likely to be an independent sponge invention than to be related to the neurons of other animals. However, if we find that the same genes are used in sponge cells as in neurons, we can then conclude relatively confidently that the two cell types are related and descended from a common ancestor.

One of the striking features of the sponge genome is that for an animal without neurons it contains an intriguingly high number of genes that are generally associated with brain development. It turns out that these genes are involved in the formation of the simple taste- and light-sensing cells of the sponge larva. Hence, neurons do seem to have evolved from simple sensory cells. The implied gradual increase in complexity – from sensory cells to neurons – is an example of a small evolutionary step resulting in a huge leap: the origin of complex behaviour.

So what did happen before the Cambrian explosion? How did complexity and biodiversity evolve?

The transition from a single-cell organism to a complex animal seems to have occurred gradually. However, once a certain level of complexity in gene networks was reached and key new genes evolved, there was a boom in the diversity of body forms during the Cambrian explosion, ultimately leading to the complexity we see in humans today.

Claire Larroux completed her PhD at the University of Queensland, and is now a Humboldt postdoctoral fellow in the Department of Earth & Environmental Sciences, Palaeontology & Geobiology at the Ludwig-Maximilians-University in Munich.