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BOOK REVIEW

Reproductive Success Story

Norman Johnson

Promiscuity: An Evolutionary History of Sperm Competition. Tim Birkhead. xiv + 272 pp. Harvard University Press, 2000. $24.95.

Sexual reproduction can often seem bizarre. For example, slugs, which are hermaphrodites, usually copulate with one another by simultaneously inserting their extra-long penises. But in some species, the slugs intertwine their penises (which can be as much as seven times as long as the body) and exchange sperm at the tips. Sometimes they can't untangle themselves, and one slug will have to bite off its penis at the base to escape; afterward it functions only as a female. Reproductive traits also can be extremely diverse. The duration of copulation in animals ranges widely, from a fraction of a second (for dunnocks) to months (for stick insects). Within a single genus, Drosophila, sperm lengths can vary between species by as much as two orders of magnitude. In Promiscuity, Tim Birkhead presents these and other case studies of reproductive systems, going beyond natural history to provide evolutionary explanations for diverse, weird and nonintuitive findings.

Two paradigm shifts have shaped the history of evolutionary reproductive biology. The first happened in the 1960s and 1970s when Robert Trivers, Geoff Parker and other evolutionists revolutionized how we view reproduction and social behavior. Rejecting the prevailing view that reproduction was a collaboration between the sexes, these evolutionary biologists started with the assumption that "reproduction occurs neither for the good of the species nor as a mutually beneficial interaction between males and females," a view that has been borne out by recent research. Trivers's insight was in connecting intensity of sexual selection with amount of parental investment. He noted that the sex that invests more in offspring (usually female) is more likely to become a resource for the other sex (male). The less-investing sex then experiences the most intense sexual selection as it competes to reproduce. Thus males and females have different agendas. Trivers's hypothesis came in part from a previously overlooked paper by Angus Bateman, published in 1948, that examined the relationship in Drosophila between number of mating partners and reproductive success (measured by the number of offspring produced). Reproductive success of a male fly increased almost linearly as it mated with more females. In contrast, the reproductive success of a female who had mated once did not increase with additional copulations.

At left, a male . . .Click to Enlarge Image

Parker, based on his observations of dungflies, extended Trivers's idea to include what he termed sperm competition: Not only must males compete for a mate, but if that mate has recently copulated, or soon copulates, with other males, their sperm must compete within her reproductive tract for the fertilization of the egg. In this evolutionary arms race, males face selective pressure to devise ways of disabling rival sperm while protecting their own. This form of sexual selection is very common.

Most of Promiscuity considers the second paradigm shift in evolutionary reproductive biology, which started around 1990 and focused more on female reproductive behavior. In contrast to the old model, in which males compete for females to increase their reproductive success, newer studies show that females are often active participants in reproductive events. Indeed, Birkhead's title refers to the importance of female promiscuity (or polyandry, as he prefers to call it) in evolution. Birkhead does not deny that in most species sexual selection is usually more intense in males and that males are generally more promiscuous than females. He does argue, however, that variation in female promiscuity has a predominant role in shaping the diversity of reproductive systems.

The use of molecular markers has aided researchers in uncovering the extent of female promiscuity among many species. By the early 1990s, marker-assisted paternity analyses in many species of seemingly monogamous birds established that a large proportion of offspring were the result of extra-pair copulations. Later research showed that in some species, females often sought out such copulations. Why—especially given Bateman's study showing that female reproductive success does not increase with more partners—would females seek copulations with more than one male? Some plausible reasons include trading sex for material benefits (for example, food) or parental care; increasing the likelihood that they have mated with a fertile, genetically compatible male; ensuring that they have sufficient good-quality sperm stored; and improving the genetic quality of their offspring. Birkhead discusses experiments that address these hypotheses. He also notes that even in Bateman's original paper, female reproductive success actually did increase with more mates under some conditions.

In this new era of evolutionary reproductive biology, the role of female choice has also been extended. For example, William Eberhard has championed the importance of cryptic female choice, in which a multiply inseminated female "chooses" after copulation which male's sperm will fertilize her eggs. Choice in this context does not imply conscious choice, only preferential utilization. Although cryptic female choice is probably quite prevalent, Birkhead cautions that distinguishing it from sperm competition can be very difficult.

Although he highlights the current excitement in evolutionary reproductive biology, Birkhead also accurately explains the science without unnecessary fanfare. I would have liked to see more discussion of the more general evolutionary implications of sexual selection, such as the hypothesis that sexual selection may drive speciation in some taxa. This, however, is a minor quibble. What is more important is the diversity of material that Birkhead does cover in this relatively slim volume. I highly recommend it to anyone interested in the mysteries of reproduction.—Norman A. Johnson, Entomology and Organismic and Evolutionary Biology, University of Massachusetts, Amherst


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