“Why all this silly rigmarole of sex? Why this gavotte of chromosomes? Why all these useless males, this striving and wasteful bloodshed, these grotesque horns, colors…and why, in the end, novels, like Cancer Ward, about love?”
~WD Hamilton, 1975, Quart Rev Biol 50: page 175
Consider a sexual population in which a single sexual female produces a daughter with an unusual mutation. The mutation renders the daughter asexual. Instead of mating with a male to produce sons and daughters, she clones herself, making more asexual females. The daughter is equal to her mother in every other way: she occupies the same ecological niche, she can produce the same number of offspring, and her offspring have the same probability of surviving to reproduce.
In this scenario, the mutation to asexuality will rapidly spread to fixation. The ancestral sexual lineage will disappear in tens of generations. Why? Males! John Maynard Smith first explained that investing in sons reduces the per-capita birth rate of sexual females. If 50% of a sexual female’s offspring are sons, she has spent ~50% of her resources on offspring that are unable to bear children. Hence, by shunting all of those resources into making reproductive daughters, a rare asexual mutant can double in frequency each generation. This model is known as the two-fold cost of males (Maynard Smith 1971, 1978).
Can such a simple model apply to natural populations? In particular, is the simplifying assumption, that asexual and sexual females are otherwise equal, realistic? We tried to answer this question in Gibson et al. (2017, Evolution Letters). Sexual and asexual morphs of the freshwater snail Potamopyrgus antipodarum coexist in lakes and streams throughout New Zealand. Prior studies of this snail showed that sexual and asexual females occupy the same ecological niche and produce equal numbers of eggs (Jokela et al. 1997a; Jokela et al. 1997b; Paczesniak et al. 2014). What we did not know for P. antipodarum, or for any system in fact, is if sexual and asexual females produce an equal number of surviving offspring (Meirmans et al. 2012). This assumption is the crux of the two-fold cost of males.
We built upon Maynard Smith’s original model to make testable predictions. Specifically, our expanded theory enabled us to predict how frequent asexual offspring should be given 1) how frequent their parents were in the prior generation and 2) how costly sex is. To experimentally test this prediction, we reared field-collected populations of P. antipodarum in semi-natural mesocosms. From these populations, we obtained the frequency of asexual parents and offspring. The cost of sex was then easily estimated. We found that our experimental data were consistent with a two-fold, or slightly greater, cost of sex. Assuming a sex ratio of 50% males in P. antipodarum, this result requires that asexual females make as many, or slightly more, surviving offspring than do sexual females. This work presents a direct estimate of the cost of sex. Clearly, Maynard Smith’s simple model has natural relevance.
- Jokela, J., C. Lively, J. Fox, and M. Dybdahl. 1997a. Flat reaction norms and “frozen” phenotypic variation in clonal snails (Potamopyrgus antipodarum). Evolution 51:1120-1129.
- Jokela, J., C. M. Lively, M. F. Dybdahl, and J. Fox. 1997b. Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum. Ecology 78:452-460.
- Maynard Smith, J. 1971a. The origin and maintenance of sex. Pp. 163-175 in G. C. Williams, ed. Group Selection. Aldine Atherton, Chicago.
- Maynard Smith, J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge, UK.
- Meirmans, S., P. G. Meirmans, and L. R. Kirkendall. 2012. The costs of sex: facing real-world complexities. Quart Rev Biol 87:19-40.
- Paczesniak, D., S. Adolfsson, K. Liljeroos, K. Klappert, C. M. Lively, and J. Jokela. 2014. Faster clonal turnover in high-infection habitats provides evidence for parasite-mediated selection. J Evol Biol 27:417-428.