Abstract

The gametes of unicellular eukaryotes are morphologically identical, but are nonetheless divided into distinct mating types. The number of mating types varies enormously and can reach several thousand, yet most species have only two. Why do morphologically identical gametes need to be differentiated into self-incompatible mating types, and why is two the most common number of mating types? In this work, we explore a neglected hypothesis that there is a need for asymmetric signalling interactions between mating partners. Our review shows that isogamous gametes always interact asymmetrically throughout sex and argue that this asymmetry is favoured because it enhances the efficiency of the mating process. We further develop a simple mathematical model that allows us to study the evolution of the number of mating types based on the strength of signalling interactions between gametes. Novel mating types have an advantage as they are compatible with all others and rarely meet their own type. But if existing mating types coevolve to have strong mutual interactions, this restricts the spread of novel types. Similarly, coevolution is likely to drive out less attractive mating types. These countervailing forces specify the number of mating types that are evolutionarily stable.This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

Highlights

  • This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’

  • We examined the capacity for asymmetric gamete signalling to address both of these apparent enigmas

  • This idea goes back to the pioneering work by Hoekstra in 1982 [15]. In support of this theory, we present evidence that asymmetric communication between opposite mating types is common, if not universal, throughout sexual reproduction in species with isogamous gametes

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Summary

Introduction: why have distinct mating types and how many?

While sexual reproduction requires two parents, there is no obvious need for them to be differentiated into distinct mating types or sexes. A prevalent explanation drawn from the literature on multicellular organisms suggest that mating types serve to avoid inbreeding by preventing matings between members of the same clone [3,4,5,6] Another notable hypothesis proposes that mating types evolved because different gamete types can enforce uniparental inheritance of the cytoplasm,. The same processes in the unicellular world have been barely addressed, among isogamous species lacking obvious differentiation This neglect in part reflects the popular assumption that opposite mating-type fusions exist for reasons unrelated to the signalling interaction itself (e.g. inbreeding avoidance and control of organelle inheritance, as discussed above). We develop a simple model of gamete signalling and mating-type evolution that explains why the number of mating types is so frequently restricted to two and provides conditions under which more numerous mating types are favoured

Review: gamete signalling
The role of signalling asymmetry
Pairwise gamete interactions dictate the number of mating types
Conclusion
39. Gillard J et al 2013 Metabolomics enables the
Findings
73. Heimel K et al 2010 The transcription factor rbf1 is

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