“All organisms with complex cells have sex, so why is it that simple, single-celled organisms never evolved to do so? The answer might lie in mitochondria” (Image: Everett Anderson/SPL)
SEX seems to be everywhere we look – on billboards, TV and in every corner of the internet. It is pervasive in nature too. Almost all animals, plants and fungi partake in it. Despite this, sex has mystified biologists from the time of Darwin to the present day.
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Sex is a puzzle because it makes far more sense to produce clones. Why go to all the trouble of finding a mate if you can make offspring asexually? An asexual organism can produce many more offspring than a sexual one, which must find a partner and only passes on half of its DNA. This twofold cost of sex means that, in theory, asexuals should quickly replace sexuals in a population. So why doesn’t this happen? I decided to wade into this contentious area.
“Why make the effort to find a mate to reproduce, when you can generate clones?”
Adaptation isn’t enough
There are many theories about why sex evolved. Did it originate as a mechanism for organisms to evade being eaten from within by parasites, or to better adapt to environmental changes? One thing most of these theories hinge on is that sex offers a great benefit: the reshuffling of genetic information into novel combinations, helping organisms adapt. It can also help spread beneficial mutations throughout a population and eliminate harmful ones.
But as explanations for sex, these fall short in two key ways. If genetic recombination is so beneficial that all eukaryotes – organisms, including animals and plants, with complex cells that contain a nucleus – have sex, why is it that prokaryotes (simple, single-celled bacteria and archaea) never evolved to do so? Conversely, because of the costs associated with sex, natural selection ought to favour asexual reproduction – so why are eukaryotes so reliant on sex?
The answer might lie in a fundamental difference between the eukaryotes and prokaryotes: mitochondria. They provide the vast amount of energy needed to power cellular functions, and are found exclusively in eukaryotic cells. I, together with evolutionary biologists Damian Dowling and Matthew Hall of Monash University in Melbourne, Australia, , and that the acquisition of mitochondria made the evolution of sex an absolute inevitability in eukaryotes (BioEssays, vol 37, p 951).
Life on Earth originated about 4 billion years ago, but remained simple for the first 2 billion years, when the only living things were prokaryotes. Then eukaryotes came on the scene. The details of how this happened are still the subject of research, but most biologists now agree that eukaryotes arose when one prokaryote engulfed another in a symbiotic relationship. Over millions of years, this lineage would give rise to all Earth’s eukaryotes.
Even today, the signature of this interaction is manifest in us all, and each partner in this symbiosis has retained its own genetic material. Essentially, one symbiont gave rise to the genome within the cell nucleus, while the other became our mitochondria, which house their own genome.
Despite its small size, the mitochondrial genome is critical for eukaryotic life, but it can’t do anything by itself. It can’t make energy, produce proteins or even replicate its DNA without lots of help from proteins that are encoded by the nuclear genome. For example, the machinery of the cell’s electron transport system, which creates cellular fuel, is made of proteins encoded by both the mitochondrial and nuclear genomes. Maintaining the interactions between the two sets of proteins is essential for energy generation and life as we know it.
This is where our theory about sex comes in. We think that sex was an ingenious way to maintain protein interactions in the face of a certain breakdown in mitochondrial function. This breakdown is inevitable because the mitochondrial genome accumulates mutations at a higher rate than the nuclear genome – about 10 times as fast in mammals, for example. This means that nuclear proteins will always be playing catch-up with the ever-changing mitochondrial proteins, trying to offset mitochondrial mutations that would otherwise be harmful without a nuclear counterattack. We contend that sex, and its associated trick of genetic recombination, levels the playing field by providing novel combinations of nuclear genes.
According to our model, these new genetic variants are “screened” by natural selection for their ability to offset changes in the mitochondrial genome. In other words, if new nuclear genetic combinations provide a better match to the mitochondrial proteins, they will spread throughout the population due to natural selection, while those that present a significant mismatch will be purged.
What is the evidence for our idea that mitochondrial mutational meltdown drove the evolution of sex? No direct studies have examined this, but the concept of ““, which describes how the nuclear genomes of a population or species have adapted to the mitochondrial genome, provides indirect support.
Studies of mammals, arthropods and yeast provide plenty of support for the related concept of mitonuclear “mismatch”. For example, when we genetically modify organisms to express a foreign mitochondrial genome alongside their native nuclear genome, we see . Since mismatch leads to disaster, a mechanism to avoid it is crucial, and our hypothesis provides this.
Plant-based test bed
Other evidence comes from the observation that plants, which generally have low rates of mitochondrial mutations, are also less reliant on sex. In May I went to Greece to collect seeds and tissue from several species of the plant genus Silene. These plants are useful experimentally as closely related species vary widely in their mitochondrial mutation rates, so they can be used to test the effects of these mutations on the nucleus. Another way to test our hypothesis would be to see whether mitonuclear mismatch and sexual reproduction are correlated.
It is too early to tell whether our hypothesis is correct, but there is likely to be more than one driver for the origin of sex. We argue it’s a safe bet that it was tied to the emergence of the eukaryotes (and hence to the origin of mitochondria), although this will no doubt be debated for many years. Our theory doesn’t conflict with previous ones: genetic recombination also provides ways to adapt to parasites and the environment.
Our work highlights the importance of mitochondria and mitonuclear interactions in shaping complex life on Earth. Mitonuclear interactions have been used to account for processes as diverse as speciation and ageing. Sex is only one of many mysteries that mitochondria will probably shed light on.
- Find out more about how evolution has shaped sex at New Scientist‘s lecture in Melbourne, Australia, on 1 October. See for more details and tickets
This article appeared in print under the headline “It takes two… but why? Blame an ancient hook-up”
