Sexual reproduction and sharing different DNA gives us a better ability to cope with the unexpected challenges in our environment that would otherwise wipe us out, says John Long.
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LONG AGO, RATHER than simply shedding or budding off a piece of themselves to create a new identical life form - a clone with the exact same DNA - two organisms got together and shared genetic material to create a more variable offspring. This was the true beginning of the sexual revolution. But exactly when did it happen? And why is this kind of reproduction so popular today?
Primitive life forms can largely be divided into those with a nucleus in their cells (eukaryotes) and those without (prokaryotes). Most obvious organisms today - the complex multicellular animals and plants called 'metazoans' - are eukaryotes, which contain nuclear DNA. Although some can reproduce asexually by budding off identical clones, most eukaryotic organisms undergo sexual reproduction: they share genetic material to produce a new generation.
Some animals such as hydras - jellyfish relatives - can reproduce sexually or bud off clones, depending on food availability. 'Sex' in the biological sense is really defined by the process of meiosis, which includes gametogenesis - when cells divide to produce gametes (such as egg or sperm cells) by halving their chromosomes.
When different individuals of the same species unite, the chromosome halves in their gametes recombine to begin making a new, genetically unique, organism. So how can fossils shed light on such microscopic and delicate processes that began not just millions, but probably billions, of years ago?
To answer this question, we need to delve briefly into the life of a truly extraordinary man named Reginald Sprigg, whose work in geology begat a whole new field of study that has since revolutionised our understanding of the early evolution of multicellular organisms.
Sprigg was born in 1919, in Stansbury, on South Australia's Yorke Peninsula. As a boy, he collected fossils and shells from his local beach and later, through a chance meeting with an old miner, became fascinated by minerals. Studying science at the University of Adelaide, he was fortunate to learn under great geologists such as Sir Douglas Mawson and Cecil Madigan, both veterans of Antarctic exploration. Sprigg, reportedly described by Mawson as his "best ever student", was inquisitive and liked to question and challenge the views of his professors at a time when it was not usual to do so.
Sprigg graduated in 1941 and was later brought on board a top-secret Australian government project searching for uranium deposits. It was wartime and a great race was underway to develop and utilise the properties of uranium. Sprigg worked on several key sites in Australia and was sent to study uranium deposits in the U.S., Europe and Britain to extend his knowledge of the geological settings of uranium-bearing ores. On his return to Australia in 1950 he was perhaps the world's most highly regarded source on the subject.
It was, however, a rich deposit of strange fossils that Sprigg stumbled upon in 1946 during his uranium fieldwork in the Ediacara Hills of South Australia's Flinders Ranges that remains his most enduring legacy.
At the time, Sprigg determined the fossils were probably of Early Cambrian age - about 540 million years old, partly because no large metazoan (multicellular) fossils such as these had ever been found in older, Precambrian, rocks. Sprigg identified the fossils as impressions of jellyfish and first exhibited them at an ANZAAS (Australian and New Zealand Association for the Advancement of Science) meeting in 1946. Recognising the significance of the very old age of these finds, he published a short report in Nature in 1948, as well as two important papers in the Transactions of the Royal Society of South Australia, in 1947 and 1949, describing various species of early jellyfish from the new site.
The true significance of the Ediacaran site wasn't appreciated until much later, however, after the work of Martin Glaessner, Bohemian-born paleontologist extraordinaire. Trained in Vienna, Glaessner fled Nazi Germany with his Russian ballerina wife during the war years and found work in New Guinea with petrochemical company Shell before ultimately arriving in Australia. He settled into a job at the University of Adelaide, where Sprigg's Ediacara Hills fossils caught his attention. In 1958, Glaessner published a paper similar to Sprigg's on new forms of Lower Cambrian (that is, lower in rock strata) Ediacaran fossils.
Meanwhile, across the globe and also in 1958, Trevor Ford from the University of Leicester published the first account of confirmed Precambrian-age fossils from a site in the Charnwood Forest of England and described a frond-like organism he named Charnia masoni. Similar forms were known from Ediacara.
Glaessner rushed to print with a landmark paper in Nature on Precambrian jellyfish and other coelenterates (the phylum to which jellyfish and sea anemones belong) from Ediacara, Africa (Namibia) and England, announcing to the world that the oldest known assemblage of fossils came from Australia.
He followed this in 1961 with an article about these ancient fossils that nabbed him the cover of Scientific American. The Ediacaran fossils have been studied and collected intensely ever since, and keep shedding their secrets. Today the Ediacaran biota are accurately dated at around 560 million years old, well before the 'explosion of life' occurred in the Cambrian period 540 million years ago.
Sprigg's legacy lives on in the naming of a new geological time period, the first one to be described in over a century. The Ediacaran period was formally established in 2004, delineating an age range of 542 to 635 million years ago. This is now widely known as the time when multicellular life first emerged in a variety of shapes and sizes. And that is what connects the origin of sex with the Ediacaran fossils. For such a diversity of life to occur at this time in life's history, sex must have already evolved.
The man who discovered sex in the Ediacaran fossil record would not realise his breakthrough until 2008, almost three decades after he first began collecting in the Ediacara Hills. Jim Gehling, a colleague and friend who is now curator at the South Australian Museum in Adelaide, began working on the Ediacaran fossils in 1971, tracing out layers containing the fossils in other regions of the Flinders Ranges. In 1972, he and fellow worker Colin Ford found a remarkable new site where fossils showed what appeared to be frond-like organisms with the broad base of the animal that held it to the sea floor in the same bedding planes.
These fossils challenged previous interpretations by Glaessner that the Ediacaran fossils were washed-up remains on intertidal flats. Gehling's work hinted that they could be much deeper water dwellers. The debate about Ediacaran organisms: what they actually are and how deep they lived, goes on to this day.
A recent discovery made international headlines when published in Science in March 2008, announcing the discovery of the origin of sex. The paper, by Mary Droser and Jim Gehling, described a new kind of organism from the Ediacara site, which they named Funisia. Funisia was a worm-like tubular organism, the fossils of which are found abundantly at the Ediacara sites, so much so that different stages of its growth can be studied and measured in detail.
Droser and Gehling identified that these organisms were budding off 'sprats', or juveniles from the adults, which were all at a similar growth stage. Hence instead of shedding or budding asexually (shedding identical clones of itself), as expected for primitive organisms of this period, it is likely that the 'sprats' developed all at the same time due to an act that begat them all: sex.
Put simply, if they were budding asexually then a wider range of sizes would be expected in the juveniles. The fact that they were always at the same size suggested an act that was timed, a mutual shedding of sperm and eggs into the water, such as occurs for corals.
A London Times story about the discovery explained that "the knobbly animal, named Funisia dorothea, is thought most likely to have reproduced in a similar way to modern corals and sponges, but little else is understood of its biology". And, of course, the journalist went on to ask the scientists if Funisia would have enjoyed sex: "Sex for the creature would have been a functional rather than a social affair," Droser, of the University of California, Riverside, said at the time. "I think they would have been way too basic to have enjoyed the sex. I don't think they would wind around each other. But I could be wrong - I would like to think they enjoyed it."
THESE EDIACARAN fossils provide circumstantial evidence, given the rigorous analysis of data carried out by the scientists, of a very early sexual reproductive event occurring in a similar way to how corals and sponges shed their gametes into the water before a period of new population growth. This begs the question: could this form of sexual reproduction have been going on even further back in time?
The oldest known eukaryotic fossils are possibly the weird spirals resembling swirling party streamers known as Grypania, which have been found in rocks as old as 1.8 billion years in sites in both Michigan and Montana in the U.S. One theory is that they are giant algae.
But others hold they could be large cyanobacteria - colonial blue-green algae that build mounds of layered structures called stromatolites by trapping floating particles of sediment.(Excellent examples of these can be found alive today at Western Australia's Hamlin Bay). Bacteria do not use sex to reproduce; they just clone themselves. But it is more likely, given the rarity of large coil-shaped bacteria today, that the fossils are actually algae, which all reproduce by sexual means. So Grypania could represent the oldest fossil evidence we have of sexually reproducing organisms.
Yet fossils can be more than just the remains of once-living creatures. Sometimes, chemical biomarkers leave us traces of where life was before, like ghosts in rocks. In 1999, for instance, Jochen Brocks of the then Australian Geological Survey Organisation, in Canberra, and his colleagues pushed back the tentative origin of eukaryotes to about 2.7 billion years ago. This was based on their identification of complex biomarkers in the form of certain lipids (fats) in ancient rocks from the Western Australian Pilbara region, which are unique in their chemical signature to those of living eukaryotic tissues.
In August 2008, Birger Rasmussen of Curtin University in Western Australia and colleagues published a paper in Nature that critically reassessed the ages of biomarkers for eukaryotic cells. Their work shot down this earlier age of 2.7 billion years by chemical arguments that the biomarkers entered the rocks after metamorphic events - rocks being heated and crushed at great temperature and pressure. Their new estimates for the origins of reliable eukaryotic fossils now rest at 1.78 to 1.68 billion years ago, and this is where we must currently park the idea of when sex first became popular.
The age-old question that follows is why did sexual reproduction begin? Why didn't life just keep evolving through cloning and asexual budding systems? Wouldn't it be easier if we were all like freshwater hydras, where instead of having complex mating rituals we humans simply grew a rather large lump on our bodies which eventually budded off like a festering sore, and from it emerged a perfect clone of ourselves?
Easier, perhaps, but no fun at all, especially as we would all look the same and have the same personality traits. Imagine a world of just one person, multiplied billions of times. True, it would make life easier for shoe and clothing manufacturers, but the first new disease through mutation to come along could potentially wipe out the whole population. Aside from the social benefits, sexual populations have two main evolutionary advantages over asexual ones. Firstly, they can adapt more readily to changes in environment, and secondly, they are less prone to accumulation of deleterious mutations in their genes.
British scientists Peter Keightley and Adam Eyre-Walker undertook some experiments (published in Science, 2000) that estimated genetic mutation rates in a range of animal species, but in particular focussed on fruit flies (Drosophila). They concluded that sex is maintained not just to purge the genome (the complete genetic material) of seriously harmful mutations; it is also principally driven by adaptive evolution, perhaps in combination with other mechanisms. In simple terms, sexual reproduction, and sharing different DNA, gives us a better ability to cope with the unexpected challenges in our environment that would otherwise wipe us out.
Sarah Otto from the University of British Columbia has written extensively about the evolutionary implications of sexual reproduction and rightly points out that, while enabling diversity, it is a costly exercise to reproduce sexually. The animal or plant has to find or stumble upon a suitable partner, risk sharing diseases, and become an easy target for predators during mating, sometimes even a target for the mate itself, as with praying mantises and some other invertebrate species.
Sex is not an efficient way of sharing genes. When we mate sexually we combine only 50% of our genetic material with our partner's, whereas asexually budding organisms have 100% of their genetic material carried into the next generation. And Otto highlights what biologists call the 'cost' of sex, in that sexually reproducing organisms need to produce twice as many offspring as asexual organisms or they lose out in the population race.
Despite these drawbacks, evolution has shaped the living world in such a way that few large creatures today actually reproduce asexually (only about 0.1% of all living organisms, excluding bacteria). Sex generates variation, and that is certainly a good thing when dealing with constant and unpredictable changes in our environment: continents are slowly moving to new latitudes, ocean currents change, the climate shifts, or sudden traumatic events occur with volcanic eruptions or rapid (in geological terms) sea-level changes.
Populations with genetic variability can adapt more readily to such pressures than those without much variation. The great German biologist August Weissman first said this back in 1889 and, despite much new work analysing the pros and cons of sexuality, it still holds true today.
Once single-celled organisms began building more complex bodies, sexual reproduction became the dominant method of reproduction. The explosion of life at the start of the Cambrian period, 540 million years ago, heralded the coming of many different kinds of animal body plans, most of which are still with us today.
The key to understanding how sex works is to understand fertilisation. Today we know well that a sperm must fertilise an egg to start the biological process of baby-making. Since antiquity, people have known copulating will sometimes bring forth a child, but how this happened was, for a long time, a mystery. The ancient Greeks believed 'female seminal fluids' formed the foetus while the males' seminal fluids provided nourishment, and this idea prevailed for more than a thousand years.
Sir Thomas Aquinas, a prolific writer and philosopher of the 13th century, thought the active power was the froth in the semen, which had a special heat of its own, derived not from the soul of man but from the action of the heavenly bodies. Indeed, throughout the Middle Ages, intellectual battles were waged between the two sides of biological thought on the matter, the spermists and the ovists: some thought that entire human beings were pre-formed and bundled up inside each male sperm, whereas others thought the egg was the sacrosanct body containing the undeveloped embryo and that the male only played a role in supplying fluid to nourish it.
Strange experiments were performed in the late 1700s to try to determine the exact roles that male and female seminal fluids played. The famous Italian abbot Lazzaro Spallanzani made little pairs of taffeta pants and fixed them onto frogs before watching them mate. Unsurprisingly to us, he found that frogs wearing his special pants could not fertilise the female's eggs.
He then took the semen from the frogs' pants, applied them to the eggs and discovered they would develop into tadpoles. Spallanzani was also the first scientist to artificially inseminate a dog, so his work proved that male semen was a necessary part of fertilisation. But, strangely, after a lifetime of precise experimental work in which he made many groundbreaking discoveries, he concluded that the little animalcules (as he called them - what we call sperm) had nothing at all to do with fertilisation.
If asked to name biology's greatest mystery, many people assume the answer is evolution. Yet Charles Darwin published a book espousing his theory of evolution in 1859, some 17 years before the millennia-old enigma of what causes animal and human fertilisation was finally solved.
Not long ago I gave my standard lecture about the origins of sex based on fossil discoveries to learned audiences at U.S. museums, colleges and universities. I posed one question at the end of each lecture: who was the great scientist who discovered the secret of fertilisation?
Not one person in any of these well-educated crowds gave me the correct answer. It seemed to me there is even more of this fascinating story of sex to be told, from the ancient Greeks to modern researchers developing such things as in-vitro fertilisation. It seems my unexpected journey into the world of sex is not over. And, by the way, the great genius credited with the discovery of how fertilisation really works is Oscar Hertwig (1849-1922), a professor of biology at Berlin University.
John Long is vice-president of research and collections at the Natural History Museum of Los Angeles. This is an edited extract from his book Hung Like an Argentine Duck, 4th Estate; RRP: $29.99.
