by Nick Lane
The urge for independent sex—welling up as a burst of free radicals from the mitochondria—is also a redox signal. In a colony, damaged cells that attempt to have sex with other cells are likely to jeopardize the survival of the colony as a whole—only chaos can ensue. The very signal for sex is a confession of damage to the cell. It is as much as to say that the cell can no longer perform its normal tasks. In somatic (body) cells, there must have been a strong selection pressure to transmute a redox signal for sex into a signal for death. And in time, the selective removal of damaged cells for the greater good paved the way for the evolution of the individual, in whom common purpose is policed by apoptosis. So the cries for freedom of captive mitochondria, which may once have urged for sex in single cells, were met with death in a multicellular body—their own, along with their damaged host cells.
This answer gives a beautiful insight into the vested interests of different cells, and how these can ebb and flow over time. The final outcome may depend on the environment that the cells find themselves in. In the first eukaryotic cells, the host cells and their mitochondria each had their own selfish interests. For the most part, these interests were aligned, but that was not always the case. In particular, if a host cell became genetically damaged, in a way that prevented it from dividing, the mitochondria were effectively imprisoned, for they no longer had the autonomy to survive outside the host. Their only escape was through the act of sexual fusion, for in this way they can be passed on to another cell directly. One signal for sexual fusion in simple single-celled organisms is a burst of free radicals emanating from the mitochondria, so mitochondria can indeed manipulate their host cells in this way.
When the host cells formed into colonies, however, times changed. There are many advantages to living in primitive colonies, without the constituent cells having to give up the possibility of a return to free living. But for this reason, the path from a colony to a genuine multicellular individual is tricky. The fact that all multicellular individuals make use of apoptosis suggests that cells must accept the death penalty if they step out of line. But why did they do so? Perhaps because the damaged cells were betrayed by their own mitochondria. The free-radical signals, welling up from the mitochondria, amount to a confession of damage to the host cell. In a colony, the future of the other cells is jeopardized: the majority gain if the damaged cell is eliminated. So the battleground shifts from the mitochondria and their host cells, to the cells of the colony, and finally to the more familiar setting of competing multicellular individuals.
One question that emerges from this scenario is, how did the colony as a whole reproduce? If any cells in a colony that ‘want’ to have sex are eliminated, then the colony as a whole is under pressure to find a common, agreed method of reproduction. Today, individuals produce dedicated sex cells from a sequestrated germ-line that is hived off well before birth. How and why such sequestration got started is a conundrum, but if the punishment for sex was generally death, then it must have been much easier to make a single exception rather than many. Surely this must have been a strong selective pressure to sequestrate a germ-line. Such an executive decision might have had a startling outcome. Once a sequestrated germ-line had been established, then multicellular individuals could only replicate by way of sex. The individual no longer persisted from one generation to the next; no more did any of the individual cells, nor even chromosomes. Bodies dissolved and reformed like wisps of cloud, each one fleeting and different. Does this sound at all familiar? I’m repeating myself from the beginning of this Part: these conditions codified the selfish gene. Ironically, the long battles between individual cells that ultimately gave rise to the multicellular individual may in the end have crowned a different victor, who slipped in through the back door: the gene.
Primitive multicellular colonies stand at the gates of sex and death, of selfish cells and selfish genes, and it will be revealing to learn more about their behaviour. It will be revealing, too, to learn more of the mitochondrial signals for sex in single cells. For while sex looks like a good idea from the point of view of mitochondria, the fusion of two cells leads to another conflict—between the two populations of mitochondria derived from the two fusing cells. These populations are not the same, and so can compete among themselves to the detriment of the newly fused host cell. Today, sexual organisms go to extraordinary lengths to block the entry of mitochondria from one of the two parents. Indeed, at a cellular level, the inheritance of mitochondria from only one of the two parents is among the defining attributes of gender. Mitochondria might once have pushed for sex, but they left us everlastingly with two sexes.
PART 6
Battle of the Sexes
Human Pre-History and the Nature of Gender
Males have sperm and females have eggs. Both pass on the genes in their nucleus, but under normal circumstances only the egg passes on mitochondria to the next generation—along with their tiny but critical genomes. The maternal inheritance of mitochondrial DNA has been used to trace the ancestry of all human races back to ‘Mitochondrial Eve’, in Africa 170 000 years ago. Recent data challenge this paradigm, but give a fresh insight into why it is normally the mother who passes on mitochondria. The new findings help explain why it was ever necessary for two sexes to evolve at all.
Mitochondrial DNA—a tiny circular genome in the mitochondria, inherited from the mother
What is the deepest biological difference between the sexes? Most of us, I imagine, would venture the Y chromosome, but this isn’t actually the case. The Y chromosome is allegedly pivotal to our sexual development, yet its presence is far from categorical, even for us. About 1 in 60 000 women are known to carry a Y chromosome, giving them the typical masculine chromosome combination of XY, yet they are nonetheless female. One unfortunate example was the Spanish 60-metre hurdles champion Maria Patino, who was publicly humiliated and stripped of her medals in 1985 after failing a mandatory sex test, despite the fact she was plainly not a man, nor a drugs cheat. She was in fact ‘androgen resistant’—her body could not respond to the natural presence of testosterone, and so she developed by default as a woman. She had no ‘unfair’ hormonal or muscular advantage. After a legal battle she was reinstated by the International Amateur Athletics Federation nearly three years later. The IAAF abolished the tests altogether in 1992, and in May 2004, in time for the Athens Olympics, the International Olympic Committee ruled that even transsexuals would be permitted to compete in the Games, as they, too, do not gain a hormonal advantage.
Interestingly, 1 in 500 female Olympic athletes carry a Y chromosome, substantially more than the general population, implying there might be some kind of physical advantage, albeit not hormonal. A relatively high proportion of models and actresses also carry a single Y chromosome. It seems to promote a long, leggy physique, ironically attractive to heterosexual men. Conversely, some men carry two X chromosomes but no Y chromosome; in their case, one X chromosome usually incorporates a tiny fragment of the Y chromosome, bearing a critical sex-determining gene, which stimulates development as a man, but this is not always the case: it’s possible to develop as a man without any Y chromosome genes at all. Rather more common (about 1 in 500 male births) is the XXY combination, known as Klinefelter’s syndrome. Strangely enough, men with this combination would once have qualified for the women’s Olympic Games by the same test that disqualified Maria Patino—the second X chromosome marks them histologically as women, even though they are not. Various other unusual combinations are also possible, some giving rise to hermaphroditism, in which the organs of both sexes are present, for example both ovaries and testes.
The superficiality of the Y chromosome is exposed if we consider sex determination more widely across species. Essentially all mammals share the familiar X/Y chromosome system, but there are some exceptions. As regularly publicized in the media, the Y chromosome is in perpetual decline. With no possibility of recombination between Y chromosomes (men usually only have one copy), it is difficult to corre
ct mutations, as there is no ‘clean’ copy that can act as a template, so mutations accumulate over many generations, potentially leading to a mutational melt-down. The Y chromosome has duly degenerated completely in some species, such as the Asiatic ‘mole voles’ Ellobius tancrei and E. lutescens. In E. tancrei, both sexes have unpaired X chromosomes; in E. lutescens, the females and males both carry two X chromosomes. Exactly how their sexes are determined remains an enigma, but it is reassuring to know that the decay of the Y chromosome does not inevitably herald the demise of men.
If we venture further afield the X and Y chromosomes soon begin to look parochial. The sex chromosomes of birds, for example, contain a different set of genes to the mammalian chromosomes, implying that they evolved independently; accordingly, they are denoted W and Z. Their inheritance reverses the mammalian pattern: males carry two Z chromosomes making them chromosomally equivalent to female mammals, whereas females carry a single copy of the W and Z chromosomes. Interestingly, in reptiles, the evolutionary ancestors of birds and mammals, both chromosomal systems exist, along with other variations. Most startlingly, sex determination in the cold-blooded reptiles often depends not on sex chromosomes at all, but on the temperature at which the eggs are incubated. In alligators, for example, males are produced from eggs incubated above about 34°C, and females from eggs cooler than about 30°C; if the temperature is intermediate, a mixture is produced. This relationship is reversed in other reptiles; in sea turtles, the females develop from eggs incubated at higher temperatures.
Even reptiles fail to exhaust the cornucopia of sex determinators. In Hymenoptera, such as ants, wasps, and bees, the males often develop from an unfertilized egg, whereas the females develop from fertilized eggs. So if a queen bee mates with a drone, the daughters share three quarters of their genes, rather than half, as in the X/Y or W/Z systems. Such genetic similarities might have favoured selection at the level of the colony over that of individuals, facilitating the evolution of eusocial structures (in which reproduction is carried out by a specialized caste in a colony of non-reproductive individuals).
In some crustaceans, sex is not fixed but plastic: individuals can undergo a sex-change. Perhaps the most peculiar example is furnished by the diverse range of arthropods that become infected with the reproductive bacteria Wolbachia, which converts males into females, thus ensuring its own transmission in the egg (they are not passed on in sperm). In other words, sex is determined by infection. Other examples of sexual plasticity are unrelated to infection. For example, many tropical fish change sex, notably the colourful teleosts (the most common type of bony fish) that dwell in coral reefs—a source of confusion that could have added a whole new dimension to Finding Nemo. In fact, most reef fish switch sex at some point in their lives, and the few shrinking violets that don’t are contemptuously labelled gonochoristic. The rest are ardently transsexual: males change to females and vice versa; some change sex in both directions, and others manage to be both sexes at the same time (hermaphrodites).
If any order emerges from this sexual cacophony, it’s certainly not the Y chromosome. From an evolutionary point of view, sex seems as accidental and shifting as a kaleidoscope. One of the few enduring pillars is the occurrence of two sexes. With the exception of some fungi (which we’ll come to later) there are few unequivocal examples of more than two sexes. What is rather more curious, though, is the need for any sexes at all. The trouble is that having two sexes halves the number of possible mates. This begs the question what’s wrong with having only one sex, which amounts to having no sexes at all? That would give everyone twice the choice of partners, and indeed would spirit away the distinction between homosexuals and heterosexuals; couldn’t everyone be happy? Unfortunately not. In Part 6, we shall see that, for better or worse, we are generally doomed to two sexes. The culprits, need I say it, are mitochondria.
13
The Asymmetry of Sex
There are two fundamental aspects to sex: the first is the need for a mate at all, and the second is the need for specialized mating types, which is to say, for having two sexes rather than just any old partner. We touched on the need to mate in Part 5. Sex is often said to be the ultimate existential absurdity, as there is a twofold cost to overcome—two partners are required to produce one offspring—while in clonal, or parthenogenic, reproduction (in which an organism produces an exact replica of itself), only one parent is required to produce two identical copies. Radical feminists and evolutionists agree that males are a serious cost to society.
Most evolutionists believe that the advantage of sex lies in the recombination of DNA from distinct sources, which may help to eliminate broken genes and to foster variety, keeping one step ahead of inventive parasites, or rapid changes in environmental conditions (although any of this has yet to be proved by experiment). Of course it takes two to recombine, hence the need for at least two parents; but even if we accept the need to recombine genes, and so to mate, why can’t we be free to mate with anyone? Why do we need specialized sexes, rather than all being the same sex, or, given the mechanical constraints of fertilization, hermaphrodites, uniting both sexual functions in the same body?
A quick look at the hermaphrodite lifestyle answers this question: they don’t have it easy, by any means. The misogynist German philosopher Arthur Schopenhauer once asked why men seemed to get along with each other quite amicably, whereas women were rather bitchy. His answer was that all women were occupied in the same profession—the business, presumably, of winning men—while men had their own professions and so didn’t need to compete so ruthlessly with each other. I hasten to say I couldn’t disagree more, but his words do help to explain why so few species are hermaphrodites (plants excepted)—they must all compete with each other, using the same tools of the trade.
Just how awkward this can be is illustrated by the marine flatworm Pseudobiceros bedfordi, which engages in a sperm battle when mating. Each is equipped with two penises, with which they fence, attempting to smear sperm onto the other without being fertilized themselves. The ejaculate burns a hole in the skin of the recipient, which is sometimes cavernous enough to cause the loser to tear in half. The problem is that the flatworms all want to be male. The female, almost by definition, invests more of her resources in the offspring, which means that individuals pass on more of their genes if they succeed in fertilizing others, while avoiding being fertilized themselves. This equates to spraying sperm around liberally without becoming pregnant. Penis envy is more than mere psychology. According to the Belgian evolutionary biologist Nico Michiels, the male mating strategy—of spraying sperm—is often adopted by the entire species, leading to such bizarre mating conflicts as penis fencing flatworms. Having two specialized sexes offers a way out of this trap. Females and males have their own ideas about when to mate, and with whom; males tend to be keener, females choosier. The outcome is an evolutionary arms race in which each sex exerts an influence over the adaptations of the other, countering some of the more preposterous mating strategies. As a rule of thumb, the hermaphrodite lifestyle works well if the prospects of finding a mate are slim, for example in low-density or immobile populations (explaining why many plants are hermaphrodites), while separate sexes develop in species with higher population densities or greater mobility.
This is all very well, but it conceals a deeper mystery: the origin of the asymmetry between the male and female roles. I mentioned that females ‘almost by definition’ invest more of their resources in the offspring. To some this may sound a rather chauvinist remark, implying the father is somehow free to walk away. I do not mean it in that sense. In many sexually reproducing creatures, there is little difference in the input of parental care. Amphibians and fish, for example, produce eggs that are fertilized outside the body, which often develop without any further parental input; and in some crustaceans, only the fathers guard the young. In sea horses, the father nurses the fertilized eggs in his brood pouch, effectively undergoing pregnancy, and giving birth to as many as
150 offspring. Nonetheless there is still a basic inequality of input that is evident at the level of the sex cells, or gametes, themselves—the difference between the sperm and the eggs. Sperm are tiny and disposable. Men, and males in general, produce them by the bucket-load. In contrast women, and females in general, produce far fewer, much larger eggs. Unlike the slippery distinction between the sexes on the basis of their sex chromosomes, this distinction is definitive. Females produce large, immobile eggs, whereas males produce small, motile sperm.
What is the basis of this asymmetry? Various explanations have been put forward. One of most convincing is the destabilizing tug between quality and quantity—between a small number of large gametes, and a large number of small gametes. This is because the fertilized egg provides not just the genes, but also all the nutrients and cytoplasm (including all the mitochondria) required for the new organism to grow. Inevitably there is a tension between the needs of the offspring and the parents. For a good start in life, the offspring ‘wants’ to be lavishly supplied with nutrients and cytoplasm, whereas the parents ‘want’ to sacrifice as little as possible, and to fertilize as much as possible. Parental sacrifice is all the more costly if the parents are microscopically small, as was the case early in the evolution of sex, more than a billion years ago.
