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The Magazine of the CALIFORNIA ACADEMY OF SCIENCES |
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Counterpoints in Science Battle of the Xs
Everybody knows about the battle of the sexes. According to the Book of Genesis, it has been raging ever since Adam ribbed Eve and Eve bit his apple. But did you know about The Battle of the Xs? An article with that title in the journal BioEssays (May 2004), by Brian Oliver and Michael Parisi of the National Institutes of Health, tells how the war continues to be fought in the freshly explored territory of the genome. On the genetic playing field, what's good for females is often bad for males, and vice versa. Since males and females need each other, at least if there's to be a next generation, their biological makeup is a compromise in which neither team can be completely victorious over the other. There was a time about a billion years ago when there were no sexes. Single cells, or primitive multicellular organisms, simply divided into two identical individuals. Then things got complicated. In some higher organisms, one member of certain chromosomal pairs became different from the other and the result was two sexes instead of one. Unequal chromosomal divisions frequently occur in the course of evolution. Most are deleterious to the organism and are eliminated by natural selection. But the development of two sexes proved to be beneficial. Sexual reproduction produces more variable offspring than does identical cloning and so promotes survival in changing environmental conditions. In nematode worms, it's not a Y chromosome at all, but a lack of a second X that determines sex. Not all species achieve maleness and femaleness in the same way. For example, fish such as the clownfish start off as one sex but switch to the other in midlife in response to environmental cues. Clearly, these changes are not triggered by sudden chromosomal changes. Still, females and males of the same species share nearly identical genetic information. In humans, both sexes have 22 pairs of autosomal (nonsex) chromosomes. Where they differ is in their pair of sex chromosomes. Females have two X chromosomes, while males have one X and one Y. Yet this one set of chromosomes makes males and females markedly distinct in appearance, biology, behavior, and their roles in reproduction. Though most genes are necessary for the viability of both sexes, some are better for one sex than the other. Genes that favor a particular sex usually put the other at a disadvantage, giving rise to what evolutionary geneticists call "sexually antagonistic selection." For example, in most species of mammals, males compete with each other for access to females so it is advantageous for males to be large and muscular. Females must bear and nourish dependent offspring, so it is generally advantageous for them to have more fat as an energy source. In the Battle of the Xs, X marks the spot where the genetic skirmishes take place between male and female genes. With a two-to-one advantage, you'd think females would be a cinch to win the war. If a male's single X carries a bad gene like the one that causes hemophilia, a severe and sometimes fatal bleeding disorder, he will be a bleeder. Since this disorder is associated with a short life and poor reproductive success, natural selection has kept it at a very low level in the population. In this case, females have a definite advantage. Females with a bad gene on one X chromosome are very unlikely to be bleeders, because their other X will probably be normal and compensate for the defect. It's like carrying a spare tire in case of a flat. But the sword cuts two ways. Favorable X genes take much longer to affect the female population, because most genes are recessive, and the second X-lacking that gene-may mask or cancel its effect. Heredity and natural selection can also turn duplication into a drawback. A male with a favorable gene on board his X, such as one for stronger muscles, will always enjoy its benefits; he has no second X chromosome to mask the good gene's effects. Therefore, geneticists expect to find many male-biased genes on the X chromosome, since they should accumulate over time by natural selection. A beneficial X gene would help make that lucky male more likely to survive and pass the good gene on to future generations. An extreme example of "sexually antagonistic" male adaptation was experimentally induced in fruit flies by William R. Rice, then at the University of California, Santa Cruz, and reported in the journal Nature (16 May 1996). Fruit flies have a similar chromosomal system to humans, with Y determining maleness. Normally, opposite sexes of a species evolve concurrently. Each time one sex gains a competitive advantage, the other evolves a counter-strategy to combat it. Rice circumvented the normal evolutionary process by allowing only the male flies to evolve. In the first generation of the experiment, he allowed a population of males to breed with a population of females. He discarded the female offspring, bred the male offspring with descendants of the original population of females, and continued the process for many generations. In this way, the males were able to adapt, while the females' genes remained static. New females were brought in from the original breeding stock so the females could not adapt to the males or counter whatever genetic advantages they were accumulating. After 30 generations, experimental males were much more successful than control males at producing offspring with control females. Over the extra generations, the experimental males had evolved seminal fluid that inactivated semen from competing males. This advanced formula semen also promoted ovulation in female flies, thereby increasing the male's chance of fathering offspring. But the semen also happened to be toxic to females. The more frequently females copulated with the experimental males, the sooner the females died. In a reverse experiment, Rice allowed "female-only" evolution for 29 generations. The evolved females produced more eggs, which was to their advantage in reproduction, but when their male offspring mixed with female controls, they had a much lower batting average at mating than did control males. The unknown mechanism that made the females more fertile evidently made the males less so. But in both sets of experiments, what helped one sex hurt the other. Evolutionary arms races between parasites and their hosts, and predators and their prey, have long been known to produce continuously changing strategies and counter-strategies. Rice's findings provide evidence that the sometimes conflicting agendas of females and males may also be a potent driver of evolution. The Y chromosome of males presents a simpler situation than the X. In humans, the Y chromosome has only about one-hundredth as many genes as the X, and they are all involved in abetting the male reproductive apparatus. Males pass their Y only to their sons, so its male-biased genes have no effect on the female line. However, males do pass portions of their single X on to their daughters, so male-biased genes on that chromosome could, in theory, have ill effects on female descendants. The X chromosome has not been nearly as thoroughly studied as the Y, so until very recently it was not known whether the X harbored a lot of male-favorable genes, as evolutionary theorists expected. Now, new technology has made it possible to take a detailed look at the gene action inside cells. Every cell in the body contains a complete copy of all the organism's genes, but only a few of those genes are "turned on" in each cell. When a gene is turned on, sets of instructions for making a specific protein are copied. In recent years, scientists have developed an apparatus called the microarray to eavesdrop on this molecular mail. Capable of displaying thousands of these instructions on a small glass chip, several microarrays can expose all the gene activity in a single cell. Microarrays reveal that in as many as 50 percent of an individual's somatic cells-for example, brain, liver, and kidney cells-males and females turn on different sets of genes. Therefore, differences in how males and females function are much greater than one would guess from just studying the X and the Y. This finding demonstrates that males and females compete on a much broader playing field in the game of life. Recent microarray analysis of X chromosomes in fruit flies and nematode worms failed to show a large number of male-biased genes. On the contrary, they contained a predominance of female-biased genes. Researchers are at a loss to explain this unexpected outcome, but you can be sure it will inspire years of further research. The evolution of males and females is a balanced tug-of-war which results in a constant, ongoing compromise, so that neither sex gets all it thinks it wants. On the evidence, a "perfect" male might be deadly to females, and vice versa, so the species would not last long. In the movie Good Will Hunting, a psychiatrist tells one lovelorn character, "Two people don't have to be perfect to be perfect for each other." That advice is a succinct summary of the evolution of sexual reproduction. Jerold Lowenstein is professor of medicine at the University of California, San Francisco. jlowen@itsa.ucsf.edu |
