Evolutionary maintenance of genomic diversity within arbuscular mycorrhizal fungi

Abstract

Most organisms are built from a single genome. In striking contrast, arbuscular mycorrhizal fungi appear to maintain genomic variation within an individual fungal network. Arbuscular mycorrhizal fungi dwell in the soil, form mutualistic networks with plants, and bear multiple, potentially genetically diverse nuclei within a network. We explore, from a theoretical perspective, why such genetic diversity might be maintained within individuals. We consider selection acting within and between individual fungal networks. We show that genetic diversity could provide a benefit at the level of the individual, by improving growth in variable environments, and that this can stabilize genetic diversity even in the presence of nuclear conflict. Arbuscular mycorrhizal fungi complicate our understanding of organismality, but our findings offer a way of understanding such biological anomalies.

Keywords: arbuscular mycorrhizal fungi; chimera; genetic conflict; individuality; intraorganismal genetic heterogeneity; levels of selection; modular organisms; mosaic; mycorrhizal networks; organismality.

Figure 1

Effect of environmental variability (p) and the curvature of specialization returns (α) on genomic diversity. Both parts show the level of genomic diversity at evolutionary equilibrium (E[z*]) in the absence of nuclear replicative differences. The y‐axis is the shape of the relationship between fitness and nucleus proportion (α), where α > 1 reflects accelerating returns to specialization and α < 1 reflects diminishing returns. The x‐axis is the proportion of plant species one (p), relative to plant species two (1‐p). Part (a) shows the analytically derived ESS of the Competing Individuals model, and part (b) shows the results of our individual‐based simulation (n = 2000, f = 0.005, d = 0.5, m = 0). The results of our ESS model and our simulation are quantitatively equivalent, showing that genomic diversity is stabilized, for diminishing returns to specialization (α → 0) and mixed environments (p → 0.5), in the absence of replicative differences between nuclei

Figure 2

Simulation lifecycle. (a) The population of individuals (green box) is patch structured (circles containing plants). (b) Type 1 nuclei (red) replicate faster than type 2 nuclei (blue). (c) Fusion (anastomosis) is pairwise, with nuclei shared evenly between individuals via the formation then lesion of a large fused individual. (d) Individuals with dispersing offspring are orange, and compete with each other globally. Individuals with non‐dispersing offspring are beige, and compete with each other locally on their native patch (green circles). (dii) Individuals with higher fitness (smile) are more likely to reproduce (gray solid lines) into free spots. (diii) Offspring that have dispersed (orange) are sorted at random back into patches (green circles). (e) An offspring's genotype deviates stochastically from its asexual parent's genotype

Figure 3

Nuclear diversity within and between individuals. The within‐individual genomic diversity (a), and between‐individual variation in nuclear proportion (b), is plotted against the nuclear replicative advantage of type 1 nuclei (r₁–r₂/r₂) (α = 0.8, p = 0.5, d = 0.5, r₂ = 0.3, r₁ is varied). The different lines represent different degrees of fusion (no fusion m = 0; fusion: m = 0.05) and different spore sizes (large: f = 0.005; small: f = 0.01). Fusion between lines (higher m) leads to an effectively complete loss of variation between individuals, which reduces the strength of between‐individual selection, and hence leads to a faster rate of loss of within‐individual genomic diversity. Smaller spores (higher f = 0.01) lead to an increased sporulation stochasticity, which increases between‐individual variation, resulting in a slower rate of loss of within‐individual genomic diversity. The plots represent the average results taken across 10 trials. Error bars, where plotted, show one standard deviation above and below the mean across these 10 trials

Figure 4

Maintenance of genomic diversity for different between‐individual selection pressures. The results of the AM Fungi Simulation model are plotted, showing the level of genomic diversity maintained within individuals at equilibrium (E[z*]). The heat maps plot the full range of between‐individual selection, from decelerating to accelerating returns on plant specialization (α, y‐axis), and from a plant 2 to a plant 1 dominated environment (p, x‐axis). Nucleus 1 has a replicative advantage (r ₁ = 0.305, r ₂ = 0.3), meaning (a) genomic diversity is favored in environments that are slightly dominated by plant 2, which the slower replicating nucleus is specialized on (m = 0, f = 0.005). (b) As sporulation stochasticity is increased (small spores), more genomic diversity is stable across the between‐individual selection parameter space (f = 0.01). (c) Fusion of individuals destabilizes genomic diversity over most of the parameter space at equilibrium (m = 0.05). (d) The counteracting effects of fusion and sporulation stochasticity can cancel each other out (f = 0.01, m = 0.05). These results assumed n = 2,000 (population size), d = 0.5 (dispersal)