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. 2020 Feb 12;287(1920):20192754.
doi: 10.1098/rspb.2019.2754. Epub 2020 Feb 12.

Host-microbiome Coevolution Can Promote Cooperation in a Rock-Paper-Scissors Dynamics

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Free PMC article

Host-microbiome Coevolution Can Promote Cooperation in a Rock-Paper-Scissors Dynamics

Ohad Lewin-Epstein et al. Proc Biol Sci. .
Free PMC article

Abstract

Cooperation is a fundamental behaviour observed in all forms of life. The evolution of cooperation has been widely studied, but almost all theories focused on the cooperating individual and its genes. We suggest a different approach, taking into account the microbes carried by the interacting individuals. Accumulating evidence reveals that microbes can affect their host's well-being and behaviour, yet hosts can evolve mechanisms to resist the manipulations of their microbes. We thus propose that coevolution of microbes with their hosts may favour microbes that induce their host to cooperate. Using computational modelling, we show that microbe-induced cooperation can evolve and be maintained in a wide range of conditions, including when facing hosts' resistance to the microbial effect. We find that host-microbe coevolution leads the population to a rock-paper-scissors dynamics that enables maintenance of cooperation in a polymorphic state. Our results suggest a mechanism for the evolution and maintenance of cooperation that may be relevant to a wide variety of organisms, including cases that are difficult to explain by current theories. This study provides a new perspective on the coevolution of hosts and their microbiome, emphasizing the potential role of microbes in shaping their host's behaviour.

Keywords: altruism; coevolution; cooperation; evolution; host–microbiome; mathematical model.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Model illustration. Each individual hosts one type of microbe, either α (inducing cooperation) or β (no effect), and one allele, either S (susceptible to the microbial effect) or R (resistant). Thus, only αS hosts are cooperators. Carrying allele R also confers a fitness cost of δ. During interactions αS hosts cooperate: they pay a fitness cost of 0 < c < 1, and their partners receive a fitness benefit b > c. Additionally, horizontal transmission of microbes may occur during interactions, regardless of the alleles that the hosts possess. We denote by Tα the probability of microbes of type α being transmitted to the other host, establishing and replacing the resident microbes, and similarly with Tβ. (a) Fitness matrix showing the fitness of each host, according to its allele, microbe, and interaction partner, when considering one interaction per host per generation. (b) Possible interactions that yield fitness change, microbe transmission, or both. In brackets are the fitness costs for the hosts: −δ for hosts with allele R, and −c for cooperators (αS hosts). Black arrows represent the fitness benefit (+b) that cooperators provide to their partners. Coloured arrows (red and green) represent the probability for microbial horizontal transmission during interactions.
Figure 2.
Figure 2.
Cooperation can be maintained at intermediate levels even in the presence of host resistance to the microbial effect. (a,b) The expected proportion of cooperative hosts (αS; colour coded), as a function of b/c (y-axis) and δ (x-axis) for c = 0.05, Tβ = 0.25, and (a) Tα = 0.75 · Tβ, (b) Tα = 0.9 · Tβ. Cooperation goes extinct when below the horizontal line representing condition (2.1) (area I, white). Above that threshold, cooperation can either go to fixation (when δ > c, area II, black), or be maintained at intermediate levels (when δ < c, area III). The expected proportions of all four host types are shown in electronic supplementary material, figure S3. (c) Rock–paper–scissors game of cooperation. Illustrated are the conditions that allow the invasion of a rare type to a population dominated by another type, based on invasion analysis (electronic supplementary material, S2). For example, if δ < c, then αR hosts can invade αS populations, and if Tα < Tβ then αR populations can be invaded by βR hosts. Altogether, cooperation will be maintained as long as all the conditions represented by black arrows are satisfied, in addition to at least one of the conditions represented by dashed blue arrows.
Figure 3.
Figure 3.
Oscillations of cooperation can either converge or diverge. We plot the frequencies of the four host types in the population with time (a, c) and in a three-dimensional plane (b,d) for c = 0.05, δ = 0.03, Tβ = 0.25, Tα = 0.9Tβ (based on iterations of equations (S1–S4) of electronic supplementary material, S1). (a,b) b/c = 6. The population spirals and converges to the polymorphic equilibrium. (c,d) b/c = 10. The population oscillates and diverges. The red dots in panels (b,d) represent the initial state of the population, with equal proportions of the four host types, and the blue dots represent the system's polymorphic equilibrium.
Figure 4.
Figure 4.
Mutations and spatial structure help maintain cooperation in the face of host resistance in finite populations. The proportion of cooperators after up to 5000 generations is plotted as a function of the b/c ratio on the y-axis and δ on the x-axis. The colour of each square represents the average of 200 stochastic simulation runs. Panels (a,c) show the results of fully mixed populations, while panels (b,d) show the results of spatially structured populations. Panels (a,b) show the results without mutations, while panels (c,d) show the results with mutation rates of μ = 10−4 in all directions (αβ and S ↔ R). Consistent with the analytic results, we find that cooperation goes extinct if (2.1) is not maintained, and cooperation fixates if (2.1) is satisfied and δ > c. Both mutations and spatial structure significantly widen the parameter range allowing the maintenance of cooperation in polymorphism. Simulation parameters: Tβ = 0.25, Tα = 0.9Tβ, c = 0.05. All simulations used one interaction per generation, perfect vertical transmission of both alleles and microbes, and were initialized with equal proportions of the four host types. The results were robust to different mutation rates of μ = 10−3 and μ = 10−5 (electronic supplementary material, figure S6). The presented intermediate averages in area III usually represent population polymorphisms, apart from panel (a) (electronic supplementary material, figure S7). Stopping criteria is detailed in electronic supplementary material, S4.1. The results were robust to an alternative stopping threshold of 10 000 generations (electronic supplementary material, figure S8).

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