Friday, 3 May 2013

Maynard Smith (1958) on the advantage of sexual reproduction

[Update 15.07.2017: See also this article on the history of the making of the paradox of sex by George C. Williams and John Maynard Smith including evidence from their correspondence: Joachim L. Dagg (2016) On recognising the paradox of sex. Philosophy and Theory in Biology 8: e703.]

Sometime in the late 1950s it dawned on evolutionary biologists that their explanation for the evolutionary advantage of sex implied group selection, but that was not yet seen as an anomaly. One record of this awakening to the implication stems from R. A. Fisher (1958[1999]). Another particularly lucid passage comes from The Theory of Evolution by John Maynard Smith. He first describes the cost of sex as halving the rate of increase of a population and then describes the advantage of sex as more than doubling a population's range of potential variation (Maynard Smith 1958, p. 138f).
"If the rate of increase of an animal population were limited by the number of eggs which each female could lay, which in turn depended on how much food a female could eat and transform into eggs, then a population consisting entirely of parthenogenetic females would increase twice as fast as would a population of equal numbers of males and females. From the point of view of reproduction, males are a waste of living material. (This argument does not hold for hermaphroditic organisms, or for those animals in which both parents help to feed the young.)     The compensating advantage of the sexual process is that it increases the range of potential variation in a population, and therefore its evolutionary plasticity." Maynard Smith (1958, p. 138)
He adds a numerical example showing that 10 mutations would yield only ten variant genotypes in an asexual population but 3^10 in a sexual one, because each mutation will yield three genotypes AA, Aa and aa. Maynard Smith is aware that seeing the advantage of sex in increasing population plasticity implies group selection,
but that is no cause for crisis at that time in history:
"Now if the advantage of sexual reproduction is that it increases the range of potential variation in a population, then the advantage refers to the population as a whole, and not to any particular individual in it. It follows that sexual reproduction has been established as the rule, both in animals and plants, because selection has favoured some populations at the expense of others. This forms a contrast to the examples discussed in the last chapter, in which the 'unit' selected was the individual and not the population." Maynard Smith (1958, p. 139)
The following paragraphs descends into an individual advantage scenario for the origin of sex starting from a supposedly cannibalistic ancestor, and the rest of the chapter is about mating types, sexual differentiation, sexual selection and other related issues.

P.S.: Strikingly, Maynard Smith never referred to this passage in his penguin book later, when describing the cost of sex, the paradox of sex, or the evolutionary problem of the maintenance of sex.