The cost of males. John Maynard Smith was the first to recognize that the production of males in sexual populations entails an ecological cost. The cost can be seen as follows. Remember that, on overage, a sexual female in a dioecious population at carrying capacity will replace herself (otherwise the population must be growing or shrinking). Such replacement means that she will, on average, produce one male and one female offspring, assuming a 1:1 sex ratio.

Now consider a rare mutant that is similar to asexual females in all ways, except that she is asexual. This means that she will reproduce clonally and only produce daughters: two daughters on average. Assuming that there is no investment by males in the production of progeny, these two daughters will also produce two daughters. Hence, after only two generations, the clone has produced four times as many daughters as the average sexual female. This advantage in daughter production by clones comes as a direct result of the fact that sexual females produce males, which don't make any progeny on their own. Hence, there is a cost of males. This is not to mean that males contribute nothing to the production of sexual offspring (they contribute genes); it simply means that there is a cost to the sexual population for having 50% on their members not bear their own offspring.

Now it seems reasonable to ask: if this clone has such a tremendous advantage through the more efficient production of daughters, how long will it take for the clone to replace the coexisting sexual population? The answer can be gained by simply following the growth of the clone, beginning with one individual, until there are less than 2 sexual individuals in the population. I did exactly that, using a computer simulation. The results depend on population size, and are rather striking. For example, a clone beginning with a single individual will replace a population of 1 million sexual individuals in less than 50 generations. The graph at the right shows the log number of clonal individuals over time for populations having different carrying capacities (K). The sexual population is driven extinct when the clone reaches K, which is the number of generations at the end of the line (see graph below). The main point is that replacement of the sexual population by a clone should take place on the order of tens of generations. A blink of an eye in evolutionary time! Why then is there sex? And why are there males? Why haven't clones replaced both sexual females and males?

The cost of meiosis. At the risk of complicating things, I should mention the existence of another cost of sex. Fortunately, this cost is easier to see: sexual females are only half as related to their offspring as are asexual females. George Williams called this cost the "cost of meiosis," but what he really means is that there is a dramatic reduction in relatedness in the production of outcrossed sexual offspring. R.A. Fisher hit on exactly this idea when he stated that a mutation increasing the level of self-fertilization in hermaphrodites should increase in frequency, as long as selfed offspring have at least half the expected reproductive success as outcrossed offspring. So, why then do hermaphroditic plants and animals tend to engage in cross-fertilization, rather than exclusive self-fertilization?

The presence of two different kinds of costs poses another problem. Which cost is the relevant cost to producing cross-fertilized progeny, and does it matter? I have worked on this problem with David Lloyd. Our results suggest that the two costs are both real, mutually exclusive, and that they apply to different kinds of offspring. The relevant cost for the snails we work on, however, is clearly the cost of males.

Lively, C.M. and D.G. Lloyd. 1990. The cost of biparental sex under individual selection. American Naturalist 135:489-500

C. M. Lively, Dept. of Biology, Indiana University
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