The evolution of sexes: A specific test of the disruptive selection theory

Abstract

The disruptive selection theory of the evolution of anisogamy posits that the evolution of a larger body or greater organismal complexity selects for a larger zygote, which in turn selects for larger gametes. This may provide the opportunity for one mating type to produce more numerous, small gametes, forcing the other mating type to produce fewer, large gametes. Predictions common to this and related theories have been partially upheld. Here, a prediction specific to the disruptive selection theory is derived from a previously published game‐theoretic model that represents the most complete description of the theory. The prediction, that the ratio of macrogamete to microgamete size should be above three for anisogamous species, is supported for the volvocine algae. A fully population genetic implementation of the model, involving mutation, genetic drift, and selection, is used to verify the game‐theoretic approach and accurately simulates the evolution of gamete sizes in anisogamous species. This model was extended to include a locus for gamete motility and shows that oogamy should evolve whenever there is costly motility. The classic twofold cost of sex may be derived from the fitness functions of these models, showing that this cost is ultimately due to genetic conflict.

Isogamy in large and complex volvocine algae is consistent with the gamete competition theory of the evolution of anisogamy

“…This pattern includes unicellular species, indicating that the degree of anisogamy in anisogamous unicellular species is consistent with an increase in anisogamy with body size. However, many large and complex species are isogamous (figure 1), confirming previous reports of isogamy in large and complex species [7,8].…”

“…We argue that a chloroplast is necessary to provision gametes when gamete encounter rates are low, and that because a chloroplast occupies most of the volume of a gamete, this constrains the minimum gamete size. This minimum size may be large enough to violate the condition for stable anisogamy predicted by the Bulmer & Parker model and shown to be consistent with anisogamy in volvocine algae [8]. As predicted by this hypothesis, isogametes are larger than the microgametes of similar-size species.…”

“…This prediction was tested by plotting gamete volume against protoplasmic volume separately for unicellular and for colonial or multicellular species (figure 2). Unicellular and colonial or multicellular species were analysed separately because zygote volume increases at a higher rate with protoplasmic volume for unicellular species [7,8]. To control for protoplasmic volume, log gamete volume was regressed on log protoplasmic volume and the residuals were compared between isogametes and microgametes (electronic supplementary material, Results).…”

“…One prediction, that zygote size (or egg size) should increase with adult size, is upheld for the volvocine algae [6 -8]. Another prediction, that the degree of gamete dimorphism should increase with adult size or complexity, is also upheld, but with many exceptions [2,[6][7][8][9][10]. The exceptions to this prediction, unicellular species that are anisogamous, even oogamous and colonial and multicellular species that are isogamous, have raised doubts about the completeness of the theory [2,10].…”

“…Some unicellular species may benefit from a large zygote because it increases the survival of the dormant zygospore or because it hastens postzygotic growth [2,10]. However, there are many similarly sized unicellular species that are isogamous and, in apparent contradiction to the original theory, larger and more complex species that are also isogamous [7,8]. The game-theoretic model of Bulmer & Parker [5] may explain isogamy in large and complex species by these species requiring large gametes, with large a, such that the condition for stable anisogamy, b .…”