Abstract

While sex requires two parents, there is no obvious need for them to be differentiated into distinct mating types or sexes. Yet this is the predominate state of nature. Here, we argue that mating types could play a decisive role because they prevent the apparent inevitability of self-stimulation during sexual signalling. We rigorously assess this hypothesis by developing a model for signaller–detector dynamics based on chemical diffusion, chemotaxis and cell movement. Our model examines the conditions under which chemotaxis improves partner finding. Varying parameter values within ranges typical of protists and their environments, we show that simultaneous secretion and detection of a single chemoattractant can cause a multifold movement impediment and severely hinder mate finding. Mutually exclusive roles result in faster pair formation, even when cells conferring the same roles cannot pair up. This arrangement also allows the separate mating types to optimize their signalling or detecting roles, which is effectively impossible for cells that are both secretors and detectors. Our findings suggest that asymmetric roles in sexual chemotaxis (and possibly other forms of sexual signalling) are crucial, even without morphological differences, and may underlie the evolution of gametic differentiation among both mating types and sexes.

Highlights

  • The evolution and persistence of different sexes and mating types has received remarkably little attention compared with that lavished on the value of sexual reproduction [1]

  • The forces leading to incompatible mating types is a distinct and fundamental question to address in understanding the origins of gametic differentiation

  • The relative advantage of sexual chemotaxis is assessed by contrasting three cases: (i) all cells in the population can mate with one another and are non-chemotactic (NC), (ii) all cells in the population can mate with one another and are both signallers and detectors (SD), and (iii) half of the cells are signallers (S) and half are detectors (D)

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Summary

Introduction

The evolution and persistence of different sexes and mating types has received remarkably little attention compared with that lavished on the value of sexual reproduction [1]. The difference between sexes manifests itself in morphological and functional asymmetry at the gametic and organism level. This is most obviously seen among multicellular organisms, but extends back to unicellular eukaryotic forms. Many protists retain morphologically identical gametes (isogamy), typically associated with little dimorphism at the organismal or vegetative stage. Despite this apparent similarity, only gametes of different mating types can fuse, with unions between gametes of the same mating type being very rare. While sex requires two gametes, there is no obvious necessity that these are from different mating types, without any seeming morphological or behavioural differences.

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