Mis-attributing the cost of meiosis to Maynard Smith

The cost of sex has been defined as the cost of inheriting only half the genome to the offspring (Williams 1975) and the cost of wasting half the resources of a female on sons that do not contribute anything but genes to reproduction in turn (Maynard Smith 1971, 1978). These are now known as the cost of genome dilution (Williams called it the cost of meiosis) and the cost of males respectively. I already detailed how Williams continued to develop his conception of the cost of meiosis from mere genome dilution towards the sociobiological cost of cooperation between unrelated (out-crossing) gametes (see here and here). That is, gamete cooperation cannot be explained by kin selection in out-crossing species, because the gametes are not related.

While this change of Williams's conception has not been received by his peers, the ambiguity between the cost of genome dilution and the cost of males may still cause confusion.

For example, Ullica Segerstrale mis-attributes the genome dilution conception of the cost of sex to John Maynard Smith.

In 1971 John Maynard Smith had usefully characterized the problem when it came to sexual versus asexual reproduction as 'the twofold cost of sex'. (this refers to the fact that in meiosis half of the genetic material is lost, whereas in asexual reproduction it is kept intact.)⁹

9 Narrow Roads, vol 1, p 362. This was also Williams' view. For Hamilton, see n 15. Segerstrale 2013, p. 225 and p. 396 n 9

Additionally, she explains the twofold cost of sexual reproduction in the glossary as follows:

"twofold cost" of sexual reproduction

For Hamilton this was the fact that a sexually reproducing species loses half of its biomass through the production of males, compared with an asexual species that produces entirely female offspring. (This is a consequence of the sex ratio in species in which only the female rear offspring). However, George Williams regarded the twofold cost as the cost of meiosis, that is, loss of the genetic material, following Maynard Smith (1971). Segerstrale (2013, p. 422)

Descending down the cascade of footnotes yields statements of Hamilton corroborating that he regarded the cost of sex as that of investing into lazy males in 1975, 1988 and 1996, but that does not give him priority over Maynard Smith (1958, 1971). The following statement of Hamilton (1975), however, may explain how Segerstrale has been mislead to believing Maynard Smith held a genome dilution conception of the cost of sex:

The crucial snag for more facile theories of sex is that which John Maynard Smith first brought fully to our attention: what Williams refers to as the twofold cost of meiosis. Hamilton 1975 reprinted in Hamilton 1996, p. 362)

Okay, this is nit-picking, but the above quotes of Segerstrale are simply wrong  in claiming that John Maynard Smith held a genome dilution conception of the cost of sex -- and Hamilton's quote apparently mislead her in this respect.

While Williams (1975, p. 8)  did cite Maynard Smith (1971) as a "more exact" source for those readers who doubt his explanation of the cost of sex, he clearly did not follow Maynard Smith in his conception of the cost of sex as wasting resources on lazy males and instead conceived it in terms of genome dilution. Maynard Smith, however, never wavered in his conception of the cost of sex as that of wasting resources on males. This is not only true for 1971 but even for 1958, when the paradox of sex had not yet been noticed.

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 of living material. (This argument does not hold for hermaphroditic organisms, or for those animals in which both parents help to feed the young). Maynard Smith (1958, p. 138)

Later, Maynard Smith (1971, p. 170) reformulated the cost of males as accruing to individuals, propped the argument up with some math and reconsidered his claim concerning hermaphrodites. Still later, Maynard Smith (1978, p. 3) repeated his argument from 1971 verbatim, but added a criticism of the idea that the cost of sex is due to genome dilution by showing that genome dilution costs nothing in isogamy (gametes of equal size). This in turn prompted Williams to re-consider and change his concept of the cost of meiosis from genome dilution to gamete cooperation, which cannot be explained by kin selection in out-crossing species.

References

• Hamilton W.D. 1996. Narrow Roads of Gene Land, vol. 1. W.H. Freeman.
• Maynard Smith J. 1958. The Theory of Evolution. A Pelican Book, Penguin Books.
• Maynard Smith J. 1971. "The origin and maintenance of sex." In: Williams G.C. (ed) Group Selection. Aldine-Atherton.
• Maynard Smith J. 1978. The Evolution of Sex. Cambridge Univ. Press.
• Segerstrale U. 2013. Nature's Oracle. Oxford Univ. Press.
• Williams G.C. 1975. Sex and Evolution. Princeton Univ. Press.