Sex Wars: Genes, Bacteria, and Biased Sex Ratios. Michael E. N. Majerus. Princeton University Press, Princeton, NJ, 2003. 280 pp., illus. $45.00 (ISBN 0691009813 cloth).
To paraphrase Robert Ricklefs, it is remarkable how many populations have a 1:1 sex ratio—and how many exceptions there are to this rule. To me, even more remarkable is that we now understand the evolutionary forces that produce the rule, as well as the forces that produce most of the exceptions. This triumph of 20th-century science has provided perhaps the best case for a selfish-gene view of life. In Sex Wars, Michael Majerus, a Cambridge entomologist, argues that some of the exceptions are explained not just by an organism's own genes but also by the genes of its inherited microorganisms.
In many species, mothers pass a veritable zoo of microorganisms on to their offspring, including bacteria, microsporidia, and mycoplasmas. These live in cell cytoplasm, and because almost all cytoplasm in offspring is derived from the mother, a microorganism that ends up in the cytoplasm of a male is going nowhere. The heart of this book is concerned with how these organisms usurp their hosts to avoid that dead-end outcome.
It is great stuff—it can hardly fail to be, given the fantastic natural history involved, so much of which has been learned in the last decade or so. In retrospect, much of it could have been predicted. As a maternally inherited microorganism, what options do you have for avoiding the black hole of life in a male? If you are unlucky enough to get into a male, you could turn him into a female. If you cannot do that, you could kill him, if that releases resources for his sisters that are infected with your sisters. Or you could kill him and try to transmit yourself from his corpse to another host. Better yet, perhaps you could force your host to abandon producing male offspring altogether and become parthenogenetic. Then you would get into all of her offspring.
All these options have been exploited by some microorganisms. Wolbachia species, a group of gram-negative bacteria, have the widest repertoire. They are adept feminizers. In the case of one wood louse species, they have proved so good at their work that some populations are all genetically male, with the feminizing Wolbachia keeping the host species going. Other species of Wolbachia also induce parthenogenesis and kill males. In one African butterfly species, male-killing by Wolbachia has meant that just 5 percent of the population is male. Curiously, the advantage of male-killing remains unclear in that case.
The advantage of male-killing in ladybirds is well understood, thanks to work that Majerus himself has conducted. An array of microorganisms are involved, including Rickettsia, Spiroplasma, and Wolbachia, as well as unknown flavobacteria and γ-protobacteria. All these can be male-killers. The explanation for this suicide is simple. Ladybird larvae eat eggs that fail to hatch. This gives them a nutritional advantage early in life. Male-killers prevent male eggs from hatching, thus increasing the fitness of their clone mates in the sisters of their dead host.
All of this must have some fairly profound evolutionary consequences for the host. Majerus speculates on many of these, but makes it very clear that there is little supporting evidence. For instance, in a species with 95 percent females, there must be huge selection pressure on uninfected hosts to produce highly male-biased sex ratios. Similarly, parthenogenesis could be a way of keeping a host lineage free of these symbionts.
One of the book's strengths is that speculations are liberally sprinkled about. For instance, where sex is determined by the sperm chromosomes, symbionts should not want the egg they are in to be fertilized by male-chromosome-bearing sperm. Do symbiont-infected eggs thus reject male sperm? There is no evidence either way, but as Majerus points out, the ingenuity with which these organisms achieve their goals cannot be overestimated.
Ultraselfish elements are intrinsically interesting, with a fascinating natural history and great theory. Yet the excitement struggles to emerge from Sex Wars. A third of the book describes sex, sexual selection, sex-determining mechanisms, and the like, in a level of detail that is not needed to understand the symbionts. Indeed, the only aspect of this that I found interesting was a refutation of the divine explanation of 1:1 sex ratios—and what made that interesting was that there apparently is a divine explanation (Adam, Eve, the ark, etc.), and that Majerus's refutation of it was so uncompelling.
Indeed, it is not really clear for whom the book was written. It is not a research monograph or a racy popular science book (despite the title, it is far too dry and jargon laden to be racy), and I cannot quite envisage the undergraduate course that could be built around it. Half the book would be great for a graduate course, but any PhD student in evolutionary genetics should already know the remaining content.
Nevertheless, I hope graduate students do read this book. It makes painfully clear how few people are working in this field and how important new molecular technology is going to be in sorting things out. Majerus clearly feels that inherited symbionts are going to figure large in accounts of host evolution. The jury is still out: They may turn out to be just weird oddities. But given how much so few have found out with so little, he may prove to be correct. What is very clear, though, is that modern evolutionary analysis has the power not only to explain the natural history revealed to Victorian vicars but also to understand the radical natural history being uncovered today.
