Non-linear interaction dynamics of grasses and vertically transmitted fungal symbionts

Background/Question/Methods

Vertically transmitted microbial symbionts have played keys roles in major evolutionary transitions and can modify the dynamics of populations, communities, and ecosystems. Given their fundamental ecological and evolutionary significance, understanding the factors that determine the persistence and frequency of symbionts within host populations merits high importance. Theoretical work highlights two key processes in driving symbiont dynamics: effects on host fitness and the efficiency of vertical transmission. Existing theory assumes that these processes operate linearly with respect to population density and symbiont frequency (i.e., they are constants). We integrated experiments and mathematical modeling to test for non-linearity in host-symbiont interactions and evaluate its dynamical consequences. Our empirical work focused on the native grass Agrostis hyemalis and its vertically transmitted fungal endophyte, Epichlöe amarillans. In a greenhouse experiment, we simultaneously varied initial host plant density and symbiont frequency across 275 population replicates. We quantified seed production and symbiont frequency in the next generation, and fit demographic models to identify non-linear responses in interaction parameters. Finally, we used the best-fit model to predict long-term dynamics of this system and quantify the contributions of non-linear feedbacks. 

Results/Conclusions

There was a strong influence of density dependence on host population dynamics, but there was no clear evidence that fungal endophytes modified the nature of density dependence in the host population. However, host population density significantly modified endophyte dynamics. Endophytes increased in frequency more rapidly under lower host population densities, suggesting that their beneficial effect was stronger under low host density and / or that the vertical transmission rate was reduced at higher host densities. We also found nonlinear, negative frequency-dependent feedbacks in the symbiont population: endophytes increased rapidly from low initial frequencies but tended to decrease from high initial frequencies. Using parameterized models, we show how these non-linear feedbacks lead to predictions for host and symbiont dynamics that differ markedly from expectations based on mean rates of host demography and symbiont transmission. Our results provide, to our knowledge, the first empirical evidence for non-linear feedbacks in host-symbiont interactions and their long-term effects at the population level. Non-linear dynamics are widely recognized to play a central role in competitive and consumer-resource interactions. We argue that non-linearities can have similarly important but under-studied effects in host-symbiont interactions, and that greater attention to these effect can promote synthesis of symbiosis research with broader ecological theory of species interactions.