Context-dependent variability in the population prevalence and individual fitness effects of plant-fungal symbiosis

1. Heritable symbionts, found within a diverse array of flora and fauna,
are often observed at intermediate prevalence within host populations,
despite expectations that positive fitness feedbacks should drive
beneficial symbionts to fixation. Intermediate prevalence may reflect
neutral dynamics of symbionts with weak fitness effects, transient
dynamics of symbionts trending toward fixation (or elimination), or a
stable intermediate outcome determined by the balance of fitness effects
and failed symbiont transmission. Theory suggests these outcomes should
depend on symbiont-conferred effects and vertical transmission efficiency,
which may both depend on environmental context. 2. We tested these
alternatives by tracking temporal change in population-level symbiont
prevalence in a three-year field experiment with grasses and vertically
transmitted fungal endophytes under the context of manipulated
precipitation. Precipitation can mediate endophyte effects on host
grasses, and is a relevant context, as global climate models predict
changes in precipitation amount and seasonal distribution. 3. We found
evidence for each of the three proposed mechanisms for intermediate
symbiont prevalence, but the outcome differed qualitatively across years
and precipitation treatments. Specifically, within the first study year,
all populations under ambient precipitation trended toward symbiont
fixation, whereas elevated precipitation literally neutralized the
interaction resulting in no long-run equilibrium. The second study year
yielded a different result with long-run equilibria at an intermediate
prevalence for both ambient and elevated precipitation treatments. We
linked these population-level outcomes with individual-level symbiont
effects on grasses and showed that the benefits of symbiosis were
concentrated at the seedling stage, especially under drought stress during
the time period coinciding with recruitment. The drought stress evident
during the first year of the study was not present in the second year due
to greater ambient precipitation during this time period. Together, these
findings provide the first experimental evidence that population-level
outcomes of host-symbiont interactions, which arise from the composite
outcome of demographic vital rates and transmission, can be dynamically
stable and can fluctuate in response to shifts in spatio-temporal context.
4. Synthesis: Overall, these results indicate that intermediate prevalence
of heritable microbial symbionts likely reflects a combination of neutral,
transient, and stable mechanisms, and context-dependent fluctuations among
them.