Testing paternity can be difficult, but DNA-fingerprinting and molecular studies have produced some unexpected results, revealing much greater extra-pair paternity in some species than behavioural studies had suggested. Birkhead also touches on the "once cherished" notion of female sexual monogamy (it is in fact the exception rather than the rule) and the various forms of mate guarding or consortship.
A chapter on genitalia describes the female oviductual "obstacle course", needed to keep out parasites and prevent infection, and then the testes, sperm production and storage systems (and their temperature sensitivity), and some of the diversity in penis form, function, and evolution. One remarkable case is a hermaphroditic slug where penises frequently become knotted during copulation, forcing individuals to bite their own penises off at the base to free themselves.
This is followed by a chapter on sperm, ejaculates and ova — mostly on sperm size and number and the role of seminal fluid. An extreme case here is a fruitfly where the seminal fluid not only kills sperm from other males but poisons the female, making repeated insemination fatal. There are less drastic reasons than this, however, why females attempt to control the number and source of sperm. Also covered briefly is the early history of reproductive biology: the debate between the ovists and spermists and Spallanzani's experimental work, including the first artificial insemination.
Turning to copulation and insemination, Birkhead surveys the various approaches: from external broadcast to internal fertilisation, as well as "deviant" forms such as traumatic insemination through the body wall or skin (most spectacularly with the giant squid's 20cm long spermatophores). Copulation varies greatly in form — the greater vasa parrot mates side-by-side — and frequency — a queen fire ant will mate once in her life, while a single female Soay sheep has been observed copulating 163 times with 7 males in a 5 hour period.
Next comes a look at mechanisms of sperm competition. One common phenomenon is "last-male sperm precedence" where the sperm from the last insemination are used. Some clever experiments and field studies tease out possible mechanisms for this. And in some species there is tantalising evidence for cryptic female choice, where females exert post-copulatory control over which sperm are used. (One possibility is selection for genetic compatibility in species where inbreeding depression is a serious problem.)
A final chapter looks at female promiscuity and its evolutionary origins. Birkhead confusingly appropriates the term "polyandry" from anthropology (where it is used for social systems in which women can have multiple husbands) in order to avoid the negative connotations of "promiscuity". Of course this didn't stop him, or perhaps his publisher, using "promiscuity" in the title and back cover blurb! Promiscuity can have obvious direct benefits — a sufficient supply of sperm, "gifts" of various kinds that can accompany insemination, avoidance of rejection costs, and paternal care — and there are also possible indirect genetic benefits (though testing for these is difficult).
Birkhead has (like many scientists) a tendency to make more of his own specialty than is really warranted. At one point he writes: "because [sperm competition] dealt directly with variation in reproductive success its evolutionary significance was much more immediate than that of other behaviours, such as foraging". But organisms that starve to death before reaching sexual maturity can leave no offspring — just as "immediate" an effect on their fitness. His approach is also focused on reproductive biology and not on intra-genomic and inter-sexual "conflict" and their effects on such mundane things as offspring size.
While Birkhead is not afraid to venture into the more complex world of human sexuality, he clearly recognises the dangers of careless sociobiology. He even begins Promiscuity with a story about Italian men in the United States returning home to Italy to shoot a honey buzzard (a ritual supposed to ensure their wives will be faithful) — while leaving their wives behind, unattended. But there are some slip ups. After a look at human paternity studies, for example, he comes to the carefully worded conclusion that "extra-pair paternity undoubtedly exists and ... its level in contemporary Western human society appears to be fairly modest compared with that of chimps and many socially monogamous bird species". But he then lurches immediately to "if further evidence was required that humans have evolved to deal with rather modest levels of sperm competition..." (my emphasis), simply assuming the extrapolation from modern Western populations to the very different environments of most of human evolutionary history. And on page 33 he writes that "the most obvious way in which men's preoccupation with paternity manifests itself is in jealousy", when it seems far more plausible that it is jealousy which drives more cognitive preoccupation with abstract notions of paternity. These are minor points, but this kind of thing tends to upset social scientists, so it's an area where biologists should be careful.
November 2000
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