The rate of facultative sex governs the number of expected mating types in isogamous species

Abstract

It is unclear why sexually reproducing isogamous species frequently contain just two self-incompatible mating types. Deterministic theory suggests that since rare novel mating types experience a selective advantage (by virtue of their many potential partners), the number of mating types should consistently grow. However, in nature, species with thousands of mating types are exceedingly rare. Several competing theories for the predominance of species with two mating types exist, yet they lack an explanation for how many are possible and in which species to expect high numbers. Here, we present a theoretical null model that explains the distribution of mating type numbers using just three biological parameters: mutation rate, population size and the rate of sex. If the number of mating types results from a mutation–extinction balance, the rate of sexual reproduction plays a crucial role. If sex is facultative and rare (a very common combination in isogamous species), mating type diversity will remain low. In this rare sex regime, small fitness differences between the mating types lead to more frequent extinctions, further lowering mating type diversity. We also show that the empirical literature supports the role of drift and facultativeness of sex as a determinant of mating type dynamics.

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Fig. 1: Visualization of the model illustrating three types of potential event: sexual reproduction, asexual reproduction and mutation.
Fig. 2: Dynamics of mating type frequency with three initial mating types (M0 = 3).
Fig. 3: Dynamics of the mating type number, M, with M0 = 2 for various parameters under different modelling assumptions.
Fig. 4: Bounds on the expected number of mating types predicted by the model as a function of the population size, N, and the per-generation mutation rate, mg, when there are no selective differences between the mating types (σ = 0).

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Acknowledgements

We thank J. Christie, L. Turner and the audience of the seminar series at the Milner Centre for Evolution for useful discussions and input. G.W.A.C. thanks the Finnish Center for Excellence in Biological Interactions and Leverhulme Early Career Fellowship provided by the Leverhulme Trust for funding. H.K. thanks the Swiss National Science Foundation and Academy of Finland for funding.

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G.W.A.C. designed the project and conducted the mathematical analysis. G.W.A.C. and H.K. developed the model and wrote the paper.

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Correspondence to George W. A. Constable.

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Constable, G.W.A., Kokko, H. The rate of facultative sex governs the number of expected mating types in isogamous species. Nat Ecol Evol 2, 1168–1175 (2018). https://doi.org/10.1038/s41559-018-0580-9

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