The Atavism

Sunday, July 3, 2011

Sunday Spinelessness - The first animals (modern analogs)

The last time I tried to work out what the first animals might have looked like I decided fossils probably weren't much help. So, today I'm going stop looking back into the depths of time, and see if any modern creatures might provide clues as how animals got their start in life.

Remember from the last post, the major challenge for ideas about the origin of animals is explaining how a group of single celled organisms, each with their own evolutionary interests, can join together to create a mutli-cellular creature in which almost all of the cells can never reproduce in their own right. Our glance at earliest animal fossils record showed us that the resolution of this record just isn't fine enough for us to isolate the first cells to go in for this sort of arrangement, but there are a wealth of modern organisms that seem to have gone some way down this road, and they provide useful models for us to study.

Let's start by looking at the closest living relatives of animals the choanoflagellates:

(photo is CC 3.0 from Choano-wiki (really!) user Mark J. Dayel)

Choanoflagellates are a widespread a diverse group of single-celled creatures that live in the ocean as well as freshwater. At first glance it might seem a stretch to propose a relationship between these ten micrometre long cells and animals, but there is good reason to believe the relationship is real. Choanoflagellates, with their characteristic 'collar' around the tip of the cell body and the the flagellum extending from it are almost identical to a class of cells called choanocytes found in sponges. In fact, the two cells work in exactly the same way - the flagellum pushes water and nutrients into the cell body through collar were than are digested or, in the case of sponges, moved from one cell to another. By comparing molecular sequences, biologists have confirmed the choanoflagelletes are close relatives to animals, and also established they aren't simply a lineage discended of a sponge1 that gave up the multi-cellular lifestyle

The shared anatomy and feeding methods of sponge cells and choanoflagelletes gives us a clue as to how animals might have evolved. If a sponge is a bunch of cells that are held together by proteins that feeds using choanocytles, could the first animals have evolved from choanoflagellates that formed colonies? You don't have to imagine too hard here, because there are modern choanoflagellates that do just that:

In fact, colonial behaviour appears to have evolved multiple times within the choanoflagellates. This behaviour might crop up so often because even the solitary species have a wealth or sticky proteins that they use to trap bacteria and other food items in their collars. However it arises, colonial behaviour is obviously worthwhile for some choanoflagellates because they been doing it for millions of years, either forming spheres like the Sphaeroeca shown above, clusters like Protero below or as small groups sitting on a stalk like Proteospongia 2

Colonial choanoflagellates might well have been the first step on the road to true mulit-cellularity, but an agglomeration of cells each doing well out of their association with each other is still a long way from the specialisation we see in modern animals. Thankfully, there are organisms out there that give us a glimpse as to what the next step might have looked like. And some of them are stunningly beautiful:

B0007761 Colony of <span class= (photo is CC 2.0 from Wellcome Images)

The sphere you see above us an alga called Volvox that makes blurs the line between a colony of single celled organisms and a multi-cellular life form. Of course, algae are only very distantly related to animals, but we are looking for models of how simple multi-cellular life might work, and Volvox is interesting because it's a very simple organism that has a clear distinction between reproductive cells and the rest of the organism. The closest realtives of these beautiful creatures are single celled algae called Chlamydomonas. Most of the time Chlamydomonas are free swimming cells, propelled about in search of sunlight for photosynthesis by two flagella:

When it comes time for them to divide they draw their flagella in and begin a series of cell-divisions, keeping between two and eight daughter cells within the 'old' cell wall before they burst out and get back to the swimming lifestyle

Volvox has ditched this two-stage life cycle, instead, the individual (or colony if you'd rather) simultaneously contains reproductive and 'swimming' cells. That dotted sphere is made up of thousands of cells very similar to swimming Chlamydomonas each connected in an extra-cellular matrix of proteins and carbohydrates. Importantly, those outer cells don't divide. Reproduction is down to a set of immobile cells within the sphere, called gonidia. Each gonidia can go through a set of programmed cell divisions that create all the cells that make up a new Volvox individual. Volvox is probably the simplest example of an organism that displays a division of labour between 'body cells' (in this case the swimming cells that move the individual around) and reproductive ones. As I said, algae are not closely related to animals, but the larvae of some sponges seem in some ways analogous to an individual Volvox. Like all sedentary animals, sponges have larvae that can move, and in sponge larvae that movement comes courtesy of a set of ciliated cells that form the lower portion of the larva:

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A glass model of a sponge larvae, photo provided by Welsh Museum

So, between Volvox and sponge larvae we have an idea of what a very simple free swimming animal with specialised cell types might look like. But how might that division of labour between different cell types have evolved? Now we really are heading into some murky waters. Animal multi-cellularity happened once, at least 600 millions ago. Obviously any answer we offer as to why this happened is going to be at best a tentative explanation, but I've always like an idea developed by New Zealand evolutionary biologist Paul Rainey (and not just because he has been the head of a Centre for Research Excellence of which I'm a member!)

Rainey is an experimental evolutionary biologist, taking advantage of the speed at which miroogranisms reproduce to answer questions those of us that wander about in the field couldn't even begin to ask. One of his experiments involved growing bacteria in a stable environment, which reliably procudes mutants that are rather charmingly called "wrinkly spreaders". The wrinkly spreaders form mat-like colonies on the top of the tubes that they live in:

To be part of that mat each cell has to pay a small cost in the form proteins that stick the cells together, but that cost is more than repaid by the fact only cells in that mat can access oxygen from the barrier between the fluid in the cell and air above it. For this reason wrinkly spreaders soon take over the population in the tubes. Natural selection acts on individuals, not colonies, and very often selection acting on cells within the mat will lead to its destruction. Cells within the mat can take advantage of their neighbours by not producing the adhesive proteins that hold the mat together while still enjoying the benefit of being within it. In time, the small advantage these mutant cells gain by not paying the price in adhesive proteins will be enough to see them out compete their neighbours. But, of course, once such 'cheating' cells predominate the mat won't be able to sustain itself and it will fall apart.

Here's were is gets really interesting. Each mat seems like an evolutionary dead end, because the mats themselves can't reproduce (a prerequisite for evolution by natural selection) - when the mat falls apart the cells fall into the oxygen-free zone and die. But 'cheating' cells can reproduce and they can leave the mat and, most remarkably, because there are so many cells in a population that, in time, it's likely one of them will mutate back to the co-operative wrinkly spreader type. Now stand back and think about the big picture here. You have a larger stationary structure, the mat, that can give rise to small, mobile cells (the cheaters) that can each go on to establish a new large structure. That sounds very similar to a larval-adult life cycle, or even the distinction between body cells and reproductive cells that we are trying to explain. Since the 'cheater' cells probably arise by mutations that break existing genes, the switch between cheater and wrinkly spreader could, in time, be controlled by gene expression rather than by waiting for mutations.

Of course, I'm not trying to argue that animals evolved from wrinkly spreaders specifically, or even this sort of pattern generally. The really neat idea in Rainey's description of the dynamics of wrinkly spreaders is the way the cohesive nature of multi-cellular organisms might have evolved from competition rather than co-operation. Hundreds of co-operative systems have been identified within colonies and populations of single celled organisms and all of them are prone to sabotage by cheaters, so it's definitely something to think about, but, like all the ideas in this field, it is speculative and may turn out to be wrong.

So, modern organisms can give us a few clues as to animals might have got their start. Colonial choanoflagellates are an example of how simple colonies that feed in the same way as modern sponges could form. Volvox is an example of a very simple organism that has a distinction between reproductive and body cells and Rainey's wrinkly spreading bacteria show us one possible route to how that distinction would arise in the first place. In this peice of really presumed that the first animals fed in much they way modern sponges do, but not everyone thinks is the case. Next week I'll turn to genes, genomes and the family trees we can estimate from them to explain some of the slightly more outre ideas about the origin of animals.

1 I really wanted to call this post "To be descended of a sponge", but I called the first "The first animals" so I guess I'm stuck with it for the series

2 The world's number one protist fan, Psi Wavefunction, would like it to be known that the Proteospongia species you might read about that is meant to have specialised cell types similar to a sponge's ameboid cells probably doesn't exist (being recorded in error a in the 1880s and not seen since)

Lots of references today: Choanoflagellate biologists have their own wiki, and it's pretty cool The free online version of Molecular Biology of the Cell has a section on the evolution of multi-cellularity including Volvox as does Scitable, Nature's education website.
Paul Rainey's ideas are more thoroughly explained in:
Rainey, Paul B. 2007. “Unity from conflict.” Nature 446 (7136): 616. doi:10.1038/446616a.

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Posted by David Winter 9:47 PM


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