Two people are dancing a waltz, and it is not going well. One is tall and the other short; one is graceful, the other flat-footed; and both are stepping to completely different rhythms. The result is chaos, and the dance falls apart. Their situation mirrors a problem faced by all complex life on Earth. Whether we’re animal or plant, fungus or alga, we all need two very different partners to dance in step with one another. A mismatch can be disastrous.
Virtually all complex cells – better known as eukaryotes – have at least two separate genomes. The main one sits in the central nucleus. There’s also a smaller one in tiny bean-shaped structures called mitochondria, little batteries that provide the cell with energy. Both sets of genes must work together. Neither functions properly without the other.
Mitochondria came from a free-living bacterium that was engulfed by a larger cell a few billion years ago. The two eventually became one. Their fateful partnership revolutionised life on this planet, giving it a surge of power that allowed it to become complex and big (see here for the full story). But the alliance between mitochondria and their host cells is a delicate one.
Both genomes evolve in very different ways. Mitochondrial genes are only passed down from mother to child, whereas the nuclear genome is a fusion of both mum’s and dad’s genes. This means that mitochondria genes evolve much faster than nuclear ones – around 10 to 30 times faster in animals and up to a hundred thousand times faster in some fungi. These dance partners are naturally drawn to different rhythms.
This is a big and underappreciated problem because the nuclear and mitochondrial genomes cannot afford to clash. In a new paper, Nick Lane, a biochemist at University College London, argues that some of the most fundamental aspects of eukaryotic life are driven by the need to keep these two genomes dancing in time. The pressure to maintain this “mitonuclear match” influences why species stay separate, why we typically have two sexes, how many offspring we produce, and how we age.
If you want to see some sex, violence and blackmail, don’t bother with soap operas – try looking at the surface of your local lake or stream. There, you’ll find small insects called water striders (or pond skaters), skimming across the water on outstretched legs. These legs can pick up the vibrations of prey, predators and mates, but they can also produce vibrations by tapping the water surface. And males use this ability to blackmail their way into sex. It’s a drama of sexual tension played out across the surface tension.
Water strider sex begins unceremoniously: the male mounts the female without any courtship rituals or foreplay. She may resist but if she does, he starts to actively strum the water surface with his legs. Each vibration risks attracting the attention of a hungry predator, like a fish or backswimmer (above). And because the female is underneath, she will bear the brunt of any assault. By creating dangerous vibes, the male intimidates the female into submitting to his advances. Faint heart, it is said, never did win fair lady.
Most writers wouldn’t be pleased to see their name in a national newspaper next to the headline “I haven’t had sex for 40 million years. Should I worry?” But what are science writers, if not a little strange…
Releasing a steady stream of urine to attract a mate and then fighting off anyone who still dares to approach you doesn’t seem like a great idea for getting sex. But this bizarre strategy is all part of the mating ritual of the signal crayfish. A female’s urine, strange as it sounds, is a powerful aphrodisiac to a male.
Fiona Berry and Thomas Breithaupt studied these courtship chemicals by organising blind speed-dates between male and female crayfish, whose eyes had been covered with tape. They also injected a fluorescent dye into the animals’ bodies, which accumulated in their bladders. Every time they urinated, a plume of green dispersed through the water.
If the duo blocked the female’s nephropores (her urine-producing glands), the males never showed her any interest. If they met, they did so aggressively. But when the duo injected female urine into the water, things took a more lustful turn, and the males quickly seized the females in an amorous grip. Female urine is clearly a turn-on for males.
But the female doesn’t want just any male – she’s after the best, and she makes her suitors prove their mettle by besting her in a test of strength. As he draws near, she responds aggressively, even though it was her who attracted him in the first place. No quarter is given in these fights. The female only stops resisting if the male can flip her over so that he can deposit his sperm on her underside.
The animal on the right is no ordinary chicken. Its right half looks like a hen but its left half (with a larger wattle, bigger breast, whiter colour and leg spur) is that of a cockerel. The bird is a ‘gynandromorph‘, a rare sexual chimera. Thanks to three of these oddities, Debiao Zhao and Derek McBride from the University of Edinburgh have discovered a truly amazing secret about these most familiar of birds – every single cell in a chicken’s body is either male or female. Each one has its own sexual identity. It seems that becoming male or female is a very different process for birds than it is for mammals.
In mammals, it’s a question of testicles, ovaries and the hormones they produce. Embryos live in sexual limbo until the sex organs (gonads) start to develop. This all depends on a sexual dictator called SRY, a gene found on the Y chromosome. If it’s present, the indifferent gonads go down a male route; if not, they take a female one. The sex organs then secrete a flush of hormones that trigger changes in the rest of the body. The sex chromosomes are only relevant in the cells of the gonads.
But the gynandomorphs show that something very different happens in birds. Birds have Z and W chromosomes; males are ZZ and females are ZW. Zhao and McBride used glow-in-the-dark molecules that stick to the two chromosomes to show that the gynandromorphs do indeed have a mix of ZZ and ZW cells. However, they aren’t split neatly down the middle. Their entire bodies are suffused with a mix of both types, although the male half has more ZZ cells and the female half has more ZW ones.
Even though the three chickens were both male and female, one of them only had a testicle on one side, the second only had an ovary on one side, and the third had a strange hybrid organ that was part testis and part ovary. These malformed organs pumped the same soup of hormones throughout the birds’ bodies but, clearly, each side responded differently.
Zhao and McBride started to suspect that each cell has its very own sexual identity, and that this individuality exists from the chicken’s first days of embryonic life. They proved that by transplanting cells from embryonic sex organs from one animal to another. All the transplants produced a glowing green protein so Zhao and McBride could track their whereabouts, and those of their daughters.
When our lives are in danger, some humans go on the run, seeking refuge in other countries far away from the threats of home. Animals too migrate to escape danger but one group – the pond-living bdelloid rotifers – have taken this game of hide-and-seek to an extreme.
If they are threatened by parasitic fungi, they completely remove any trace of water in their bodies, drying themselves out to a degree that their parasites can’t stand. In this desiccated state, they ride the wind to safety, seeking fresh pastures where they can establish new populations free of any parasites.
This incredible strategy may be partially responsible for another equally remarkable one – the complete abandonment of sex. For over 80 million years, the bdelloids (pronounced with a silent ‘b’) have lived an asexual existence. Daughters are identical clones of their mothers
, budded off from her body. No males have ever been discovered. For this reason, Olivia Judson once described bdelloid rotifers as an “evolutionary scandal”. Their sexless lifestyles simply shouldn’t work in the long run.
Ditching sex allows an animal to efficiently pass all of its genes to the next generation without having to seek out a mate. This should give asexual animals a big advantage but not so. Sex provides fuel for evolution. Every time two individuals meet in flagrante, their chromosomes are joined, shuffled and re-dealt to the next generation. In this way, sex begets diversity, remixing genes into exciting new combinations.
This diversity is a vital weapon in the never-ending war against parasites. Parasites, with their large populations and short generations, are quick to evolve new ways of exploiting their hosts. They could have their run of a genetically uniform population and soon bring it to its knees. A sexually active species is a harder target. With genes that shuffle every generation, new anti-parasite adaptations are always just one bout of mating away. And so it goes, again and again, with hosts constantly having to outrun their parasites and sex acting as the getaway vehicle.
So asexual reproduction, for all its immediate gains, should be a poor long-term strategy compared to the dynamic nature of sex. Bdelloids have clearly addressed this problem and thanks to the last few years of research, we know how. They have evolved ways of achieving every single one of the many benefits of sex, without actually doing the deed. Escape parasites? They’ve got that covered. Shuffle their genes? They do that too. Generate genetic diversity? Check.
Normally, the duck keeps its penis inside-out within a sac in its body. When the time for mating arrives, the penis explodes outwards to a fully-erect 20cm, around a quarter of the animal’s total body length. The whole process takes just a third of a second and Brennan captures it all on high-speed camera. This isn’t just bizarre voyeurism. Duck penises are a wonderful example of the strange things that happen when sexual conflict shapes the evolution of animal bodies.
Childhood… violated… Innocence… lost… SCIENCE!Many ducks form bonds between males and females that last for a whole mating season. But rival males often violently force themselves onto females. To gain the edge in these conflicts, drakes have evolved large corkscrew phalluses, lined with ridges and backward-pointing spines, which allow them to deposit their sperm further into a female than their rivals. These extreme penises are even more unusual when you consider that 97% of bird species lack any penises whatsoever.
But female ducks have developed countermeasures. Their vaginas are equally long and twisting, lined with dead-end pockets and spirals that curve in the opposite direction. They are organic chastity belts, evolved to limit the effectiveness of the males’ lengthy genitals. Two years ago, Brennan showed that duck species whose males have the longest penises tend to have females with the most elaborate vaginas. Now, she has found further evidence that these complex genitals are the result of a long-lasting war of the sexes.
By directing the evolution of a worm, scientists have confirmed answers to the age-old question: “What is the point of having sex with someone else?” For most people, that would hardly be a tricky query but it’s no reflection on the lives of evolutionary scientists that sex has been one of biology’s oldest puzzles.
The problem is this: many creatures can reproduce by fertilising themselves instead of getting someone else to do it, and at first glance they should do much better individuals that cross-fertilise. For a start, they’d ensure that all of their genes reach the next generation, while mating with another individual reproduction halves their genetic legacy. And without having to find males, self-fertilising females should be able to produce twice as many offspring. This is the “two-fold cost of males”.
And yet, cross-fertilisation is the more common strategy in the animal world, so it must have advantages that compensate for its cons. Scientists typically name two. The first is that by shuffling the genes of two parents, cross-fertilisation deals the next generation with a fresh genetic hand, better equipping it to rapidly adapt to changing environments, predators and parasites. The second is that having sex with someone else prevents harmful mutations from building up (the genetic defects that plague inbred families would be even worse in lineages that only ever have sex with themselves). They’re the same reasons why sex itself is usually a better long-term solution than asexual cloning.
The problem is that both of these explanations have proven very difficult to test. But that didn’t stop Levi Morran and colleagues from the University of Oregon, who demonstrated that both justifications are correct, by manipulating the evolution of the nematode worm Caenorhabditis elegans.
Like humans, C.elegans has two sexes but unlike us, they are males and hermaphrodites (with males making up just one in every two thousand individuals). Equipped with both sets of genitals, hermaphrodites worms can fertilise themselves without male help – far from being rude, telling C.elegans to go &$&! itself is a feasible lifestyle suggestion. Hermaphrodites could also mate with males, but they do that on less than one in 20 occasions.
However, the genetics of this animal are so well-known that Morran managed to use two mutations to create strains of C.elegans that either always had sex with themselves, or always had sex with other worms. Morran subjected these two engineered strains, as well as a normal one, to two challenges.
Some were exposed to a chemical called ethyl methanesulphonate (EMS) that quadruples the normal mutation rate of DNA, riddling their genomes with potentially harmful genetic changes. To make matters worse, they were placed in a new environment that should weed out all but the fittest individuals.
Despite these challenges, the strain that always mated with others were still successful after 50 generations and fared much better than the strain that only had sex with itself. Even the normal worms moved towards a cross-fertilising strategy under these harsh conditions. These are all signs that having sex with others else provides a way of purging harmful mutations from a population. By contrast, Morran estimated that the genetic burden carried by the worms that only ever mated with themselves would drive them to extinction after a few hundred generations.
Morran also exposed some of his worms to a bacterium called Serratia marcescens, a bacterium so virulent that it kills 80% of the worms it infects. It was a test of their ability to rapidly adapt to new challenges, and one that the cross-fertilisers passed with flying colours. They quickly evolved to resist the bacterium, while the populations that only mated with themselves did not. As before, the normal worms shifted towards a cross-fertilisation strategy when faced with the new threat.
So both theories are correct – compared to having sex with yourself, doing it with someone else provides a way of resisting harmful mutations and adapting quickly to new challenges. Morran says that species that evolve to always self-fertilise become trapped in an “evolutionary dead-end” and are “ultimately doomed to extinction”.
Reference: Nature doi:10.1038/nature08496
More on sex and reproduction:
Image: C.elegans by Bob Goldstein
If the idea of a cold, motionless sexual partner isn’t one of your turn-ons, then you’re clearly not an echidna. The males of these spiny Australian animals will happily mate with females even if they’re hibernating.
Gemma Morrow and Stewart Nicol from the University of Tasmania have spent the last decade studying the short-beaked echidnas of Tasmania. Over that time, they discovered many instances of males mating with torpid females in deep hibernation, or with females who roused themselves briefly only to re-enter their deep slumber. Over the last two years, the voyeuristic duo use a combination of cameras, radio-trackers and infrared motion detectors to get a more intimate glimpse at the bizarre sex life of these animals.
They found echidnas having sex on 26 occasions over the last two years. In 11 of these sessions, the female was accompanied by more than one male and one three occasions, she was with no less than four! Over a third of the females were torpid – slow to react to things going on around them, and with body temperatures of 10 to 29 degrees Celsius. The males, on the other hand, were always active and had the normal echidna body temperature of 32C. When the duo swabbed the genitals of some of the hibernating females, they found that the majority were full of sperm, some of it fresh and often from the same male
Morrow and Nicol think that these sexual habits are the result of extreme competition among males, who have large ranges in a relatively small island. This competition is apparent elsewhere in Australia. On Kangaroo Island, echidnas often form “mating trains”, where up to 11 males and females gather together and follow each other around for 2-6 weeks in intense bouts of courtship and sex. On Tasmania, when a male finds a female, he’ll mate with her – hibernating or not – and guard her from rivals for some time.
Timing is also an issue. Males and females hibernate with slightly offset schedules so that males rouse from their wintery slumbers about a month before females do. This means that there’s a chunk of time every year, round about July and August, where the Tasmanian countryside is rife with randy males and sleepy females.
Bumbling echidna, filmed by me at Tower Hill Game Reserve
For humans, sex is a simple matter of chromosomes: two Xs and we become female; one X and a Y and we develop into males. But things aren’t so straightforward for many lizards – many studies have found that the temperature of the nest also has a say, even overriding the influence of the chromosomes. But the full story of how the lizard got its sex is even more complicated. For at least one species, the size of its egg also plays a role, with larger eggs producing females, and smaller ones yielding males.
The discovery comes from Richard Shine’s group at the University of Sydney. In earlier work, they showed that if the Eastern three-lined skink (Bassiana duperreyi) incubates its eggs at low nest temperatures, XX carriers develop into males regardless of their chromosomes.
Now, Rajkumar Radder, a former member of Shine’s team, has shown that the amount of yolk also determines the sex of a skink, but only at low temperatures. By deliberately adding and removing yolk from eggs using a syringe, he managed to alter the sex of the hatchlings. This degree of complexity is totally unprecedented – it means that for the skink, sex is a question of its chromosomes, the temperature it was reared under and the amount of yolk it had.