Caught in the Act: the Origin of Sex in the Fossil Record

Sex.  Doing the dirty. A bit of the old in and out.  Making teenage boys giggle and girls blush since the beginning of time.  Or was it?  Has sex always been around? If not, who ever thought that an awkward fumble followed by a nine month wait was a good way of continuing the species? Perhaps sex hasn’t always been the taboo subject that it is now, and we know that there are other ways than doing it like they do on the Discovery Channel, but the origin of sexual reproduction is still far from being resolved.

Why, for example, is it so prevalent?  Why would you go to the effort of finding a mate and performing some intricate act with them, if you can more efficiently clone yourself instead?  Cloning takes just one to make one more, rather than sex, which needs a matching pair to reproduce.  There must be a good reason to keep such an inefficient process going.

And indeed there is.  When it comes down to it, sex is not about the bump and grind, or the fancy feathers and elaborate mating rituals.  It’s all about what goes on in the cells.  Meiosis is the first stage, with a ‘normal’ cell dividing twice to make gametes with half the right amount of DNA – in our case sperm and eggs.  Two gametes, usually from different individuals, come together at fertilisation, making up the full complement of DNA, and then the fertilised egg, or zygote, starts dividing and keeps on dividing until it has the right number of cells to make an organism.  The whole thing is a lengthy and complicated process that is seemingly designed to confuse biology students.

But there is meaning behind the madness.  Sex is what allows organisms to mix up their genes – first during the random allocation of gene variants to gametes, and secondly during the random choice of fertilising pairs – and is the reason that no two sexually reproducing organisms look identical.  One of the greatest misconceptions in evolution is that random mutation in DNA drives the variation exploited by natural selection, when in actual fact it is sex.   Sex effectively shuffles the genetic material of a whole species every time an organism reproduces – a much more effective way of experimenting with variation than waiting a few generations for just one, potentially damaging mutation to one gene.

So, that’s why sex is a more attractive prospect than cloning yourself. But it doesn’t explain how, when, or where it got started.  When was the first time the earth moved? Do we owe the discovery of sex to animals, or were they latecomers to the sexual arena, following in the footsteps of earlier, smaller, and simpler organisms in the deep past?  Scientists have no firm answers yet, but there are a few clues.

When trying to work out when something evolved, scientists have two choices.  They can look at living organisms and use the information contained in their DNA to work out when it first appeared.  Or they can use the fossil record to trace a creature back in time to when it first appeared.  Both methods are useful, but both are beset with problems.  The creature in question may survived until today, or its fossil record may be incomplete and misleading. This is just the case with sex.

Sex is easy to spot and study in living organisms today.  In addition to bizarre sexual practices, like the mid-act cannibalism practiced by many praying mantids, or the colour coded treasuries of Australian bowerbirds, there are some more clear morphological adaptations that can be spotted in living or dead creatures.  First and most obvious, is sexual organs.  Chances are, if you are a sexually reproducing animal, you are going to have some specialised organs to do so whether you’re a barnacle with the largest penis in the world or boast a four-headed member like the modest echidna.

Sexual dimorphism is an indirect consequence of a sexual lifestyle. Most notable amongst elaborately plumed birds, like peacocks or birds of paradise, sexual dimorphism is also extremely realised in terms of body size in certain species of fish.  The male angler fish, arguably the smallest vertebrate in the world, is forty times smaller than the female.

File:Peacock (PSF).png

But all these products of sex appeared at a late stage in the history of cellular sexual reproduction.  If we want to find the origin, we need to look at modern examples of much more primitive creatures.  Many eukaryotic organisms (those with a nucleus, as opposed to bacteria) consist of just a single cell, and still manage to reproduce sexually without all the adaptive trappings.  And these single-celled creatures, called protists, evolved much earlier than animals.  So does sex predate the animals? Possibly.  Assuming that those sexually reproducing protists that are living today have been doing it ever since they evolved, then yes.  But what evidence do we have to prove this is the case?  Like the ancestors of humans haven’t always walked on two feet, perhaps today’s protists haven’t always been reproducing sexually.  We need to turn to the fossil record.

Tracking sex though the fossil record is a tricky business, mostly because of the extreme bias in what can be preserved.  The bulk of the fossil record is a record of hard parts and sex is generally concerned with the softer parts of anatomy (no jokes).  Whether occurring in animals or in tiny protists, the adaptations and cellular products of the sexual process are not made of hard mineralised substances and so are easily decayed away after death.  Sexual dimorphism too is difficult to recognise unequivocally, with different sized skeletons often interpreted as different species, or as younger forms, rather than different genders.  So the fossil record of sex must be built on the rare examples where soft parts are preserved, or the indirect effects that sexual reproduction may have on a species.

Two big clues both come from around a time of major revolution in the biological world, the so-called Cambrian explosion of animal life, around 540 million years ago, when all the animal groups appeared in the fossil record for the very first time.  This was not only a time of extraordinary fossil diversity, but also of exceptional fossil preservation.  Microscopic algae and intricate macroscopic animals are preserved in the finest possible detail. Amongst these, just before the appearance of animals, scientists found tiny remains which looked like balls of cells, with different number of cells in each – one, two, four, eight, sixteen, and so on.  In fact, these fossils looked just like embryos.  The now infamous Doushantuo embryos, named after the formation in China from which they were first described, have been the subject of intense scientific debate for the last 15 years, with many scientists arguing that they are just giant bacteria.  If they are embryos though, then they provide evidence that the sexual processes that must have formed them were well established before the majority of animals emerged.

A second piece of evidence, and one which supports the similar idea that sex got started before animals, is more indirect.  Given that today, sex is responsible for much of the variation we see amongst eukaryotic organisms, it is reasonable to assume that when sex first got started, it would have been marked by a sharp increase in the variation of the creatures alive at the time, which would be recognised as a peak in species diversity.  Looking for peaks in diversity is quite easy in the fossil record, and once compared with information from other time periods, there remains one gigantic spike – the Cambrian explosion itself.  Could the invention of sex by eukaryotic protists have sparked the beginning of the animal kingdom as we know it?  Quite possibly.

The evidence from the fossil record seems to point to an origin of sex just before the evolution of the animals, and as far as we can interpret it, the patterns of diversity of living creatures seems to point in that direction too.   It may be that we will never be able to place an exact date on the origin.  But it is clear that without sex, without that mucky, clumsy, long-winded process that is the bane and the joy of so many, we wouldn’t be here – not just those who are able to read this text, but every animal alive today.

This article was written for, and originally published in, Aberdeen University Science Magazine Issue 3 

Lynn Margulis: An Unforgettable Woman

I received the sad news today that Lynn Margulis, celebrated eccentric and evolutionary revolutionary, passed away last night, the evening of the 22nd November, 2011.  She had suffered from a severe stroke and was discharged from UMass Medical Centre on the 19th November to receive hospice care at home.  Her family were with her.

I had the great fortune of working with Lynn for two years on various projects and investigations, including the evolutionary origin of sex, symbiosis in foraminifera, definitions of life, and NASA exobiology projects.  She visited Oxford for a year where she taught me vast amounts about microbial evolution and diversity, hosted countless seminars and symposia, even a debate with Richard Dawkins.  She worked closely with myself and my supervisor Martin Brasier, and became a cherished friend.

In the short time that I knew her, she was unfailingly kind and generous, warm, and welcoming.  Lynn first made a name for herself with the maverick suggestion that Eukaryotes evolved from the long term symbiotic association between different kinds of bacteria.  Her theory seemed crazy at the time, but gradually it has slipped into common acceptance and for evolutionary microbiologists, Lynn Margulis became a household name.

Since then, Lynn continued to walk a knife edge of eccentricity.  Her theories were always a little outside the norm, and some dismissed her as a quack or even, cruelly, an ’embarassment’.  No scientist deserves to be described in that way, especially a person as hard-working and dedicated as Lynn.  Especially when she herself set the precedent for ‘crazy’ hypothesis to accepted theory.  To people like Lynn we owe some great leaps in scientific theory, and the world would be a much lesser place without them.

Lynn was a strong woman.  I last saw her just over a year ago, at a NASA symposium in Washington DC.  She was vibrant and outrageous and outspoken.  She held tightly to my hand while she laughingly gossiped about delegates behind their back. When we parted, she hugged me and told me never to be dull.  And after knowing her, I never could be.

I know she touched a lot of people during her life.  She was a person that inspires great feeling, good or bad.  But Lynn Margulis shaped the course of my research career, and inspired the kind of scientist, and the kind of person, I try to be.  Her legacy will live on in those who were fortunate enough to know her.  She is, and always will be, truly unforgettable.

Lynn Margulis

Lynn Margulis

1938 – 2011