The evolution of mutualism from reciprocal parasitism: more ecological clothes for the Prisoner’s Dilemma

Abstract

Many mutualisms involve reciprocal exploitation, such that each species in a mutualism is a consumer of a resource provided by the other. Frequently, such mutualisms are reformed each generation, and where they involve close physiological contact, such as between mycorrhizal fungi and plants, they can be considered as examples of reciprocal parasitism. Here we place such interactions in the framework of the Prisoner's Dilemma, and examine the conditions for the spread of mutualism using a population genetics model analogous to that used for understanding the genetic and numerical dynamics of hostparasite interactions. Genetic variants within each of two species determine whether the interaction is mutualistic or selfish, the latter being represented by resistance to being exploited or parasitized. We assume that there are fitness costs to resistance which are present even in the absence of the interaction. Just as in host-parasite interactions, we examine the effect of assuming that encounter rates between potential mutualists (and therefore entry into the Prisoner's Dilemma 'game') depend on the density and frequency of the different types interacting individuals. These elements of ecological realism greatly facilitate the evolution of mutualism even in the absence of spatial structure or iterative encounters. Moreover, stable genetic polymorphisms for resistant (selfish) and susceptible (mutualistic) alleles can be maintained, something that is not possible with the classical Prisoner's Dilemma formulation. The sensitivity of the outcomes to levels of densitydependence and mortality rate suggests environmental as well as genetic processes are likely to be important in determining directions in this pathway to mutualism.Electronic supplementary material The online version of this article (

Contextual organismality: Beyond pattern to process in the emergence of organisms

“…Indeed, context dependency is increasingly recognized to be a key feature driving the evolutionary dynamics of mutualism (Antonovics et al. ). However, do other more integrated units also show this characteristic?…”

“…It is straightforward to envision that loose interactions, such as interspecific mutualisms, incorporate both cooperation and conflict and are context dependent. Indeed, context dependency is increasingly recognized to be a key feature driving the evolutionary dynamics of mutualism (Antonovics et al 2015). However, do other more integrated units also show this characteristic?…”

Evolution of behavioral resistance in host-pathogen systems

“…Pair formation has been studied in the context of mating and marriage, and represents a complex problem of sampling without replacement [29,30]. Following previous work [31], we considered two forms of encounter. First, singletons could encounter one another at a constant frequency, independent of their density, as would occur when individuals seek others out to form associations.…”

“…Second, singletons could encounter others randomly, such that encounters occur at a higher rate at greater densities. These two types of group formation have parallels with frequency-dependent and density-dependent disease transmission processes [31]. Given that the two types of encounter gave qualitatively similar results, in the main text we present only the frequency-dependent case (density-dependent results are in Supplementary Information, S2).…”

On the difficult evolutionary transition from the free-living lifestyle to obligate symbiosis

“…Since symbiosis was identified as a potential for evolutionary innovation [2][3][4][5][6], the conditions that favour it and its subsequent evolutionary outcomes have received much attention. Studies include the evolution of organelles from symbiotic relationships [7,8], the maintenance of mutualism [9][10][11][12][13][14], the evolution of virulence [8,[15][16][17][18][19][20], and the transition along the parasitism-mutualism continuum (theoretical work: [21][22][23][24][25], empirical work: [26][27][28][29]).…”