Cheating can stabilize cooperation in mutualisms

Abstract

Mutualisms present a challenge for evolutionary theory. How is cooperation maintained in the face of selection for selfishness and cheating? Both theory and data suggest that partner choice, where one species preferentially directs aid to the more cooperative members of the other species, is central to cooperation in many mutualisms. However, the theory has only so far considered the evolutionary effects of partner choice on one of the species in a mutualism in isolation. Here, we investigate the co-evolution of cooperation and choice in a choosy host and its symbiont. Our model reveals that even though choice and cooperation may be initially selected, it will often be unstable. This is because choice reduces variation in the symbiont and, therefore, tends to remove the selective incentive for its own maintenance (a scenario paralleled in the lek paradox in female choice and policing in within-species cooperation). However, we also show that when variability is reintroduced into symbionts each generation, in the form of less cooperative individuals, choice is maintained. This suggests that the presence of cheaters and cheater species in many mutualisms is central to the maintenance of partner choice and, paradoxically, cooperation itself.

Figure 1

The effect of partner choice by the species A on species B, for various values of the weighting parameter f (equation (2.3)).

Figure 2

Mutualism that is initially selected is not always stable. The four simulations illustrate the range of outcomes when partner choice carries a cost (f=0.1, g=0.1). (a) Cooperation unstable. Immigration from source population: m_B=10⁻⁵. (b) Limit cycles, m_B=10⁻⁴. (c) Cooperation stable, m_B=10⁻². (d) Cooperation stable: this simulation assumes biased mutation in species B towards less cooperation each generation, s=0.1. Axes are ‘coop. A’, mean level of cooperation in species A (ā); ‘choice A’, mean level of partner choice in species A ($\overline{c}$); ‘coop. B’, mean level of cooperation in species B ($\overline{b}$); ‘var. B’, variance in cooperation in species B. Unless stated parameters in the simulations are x=5, y=5, m_A=10⁻⁹, m_B=10⁻⁹ with starting frequency distributions defined by a_me=b_me=c_me=0, a_var=b_var=c_var=0.5. Note that these distributions are truncated at zero, which means they generate positive initial values of cooperation and choice. Positive starting values were used because without some initial level of cooperation and choice, mutualism does not evolve (§3, Foster & Wenseleers in press).

Figure 3

The effect of the cost of partner choice (f) and the level of introduced variability in species B each generation (m_B) on the stability of mutualism (see figure 2). All other parameters are as for figure 2. Note that relatively low levels of migration are required each generation to stabilize mutualism (for the colour version of this figure see the electronic supplementary material).