Many Paths to Intermediate Symbiont Prevalence

Lead author Marion Donald discusses her recently published Journal of Ecology article: Context-dependent variability in the population prevalence and individual fitness effects of plant-fungal symbiosis.

Find out more about about this investigation into intermediate symbiont prevalence.

Microbial symbionts are common partners of nearly every macro-organism on Earth. While some symbioses are deeply integrated, rendering them effectively obligate, others are more flexible in their associations. In both cases, some of these microbial partners can be passed directly from parent to offspring. For microbial symbionts that are beneficial, theory predicts that positive fitness feedbacks between the host and symbiont should drive the symbiont to fixation within the host population. However, contrary to this clear expectation, heritable symbionts are often observed at intermediate prevalence within a wide variety of bacterial-arthropod and fungal-grass symbioses.

We addressed three competing hypotheses that could explain this puzzle of intermediate prevalence. First, in the absence of symbiont-conferred fitness effects on hosts, prevalence may drift neutrally, tracking the prevalence of the previous year. Second, intermediate prevalence may be a snapshot of heritable mutualists within a system trending toward symbiont fixation. Third, intermediate prevalence may be a stable outcome reflecting strong positive fitness effects and imperfect vertical transmission. Population level prevalence should arise from individual-level outcomes, which are notoriously context-dependent.

Study system of winter bent grass (Agrostis hyemalis) and its heritable fungal endophyte (Epichloë amarillans). The arrow points out the endophytic hyphae weaving amongst the stained blue cells of the seed. Photo by J. Fowler. Grass image by USDA.

To test these hypotheses, we established experimental populations of winter bent grass (Agrostis hyemalis) across a range of prevalence of its heritable fungal endophyte (Epichloë amarillans) under two environmental contexts – ambient and elevated precipitations – in Texas. Across two annual transitions, we tracked demographic individuals for survival, flowering, reproduction, and recruitment, and vertical transmission. Using hierarchical Bayesian models, we inferred long-run equilibria and found support for all three proposed mechanisms for intermediate prevalence across the two transition years.

Linking these population-level outcomes with individual-level effects, we found that symbiont-conferred recruitment benefits outweighed reproductive costs resulting in the long-run fixation of symbiont prevalence under drought conditions, while elevated precipitation tempered these effects (2014-2015). In the second transition year (2015-2016), we found that a balance between symbiont-conferred benefits and imperfect vertical transition likely allowed low-prevalence populations to increase and high-prevalence populations to decrease, resulting in an inferred stable intermediate prevalence across both treatments.

Prevalence estimates for individual populations (points) across two transition years (2014-2015 and 2015-2016). Variation in final symbiont prevalence was plotted against prevalence in the preceding year with thick lines showing fitted relationships. Posterior distributions of equilibrium symbiont prevalence in host populations are overlaid and visualized as density distributions. Arrows indicate support for each of the three hypotheses.

To conclude, our study shows that intermediate prevalence of heritable microbial symbionts, which is widely documented across plant and animal host populations, is likely to reflect some combination of neutral, transient, and stable mechanisms, and the context-dependent fluctuations among them. Exciting avenues of future work are to combine geographic surveys of symbiont prevalence with geographically distributed experiments – similar to the one described here – to quantify the distance between observed symbiont prevalence and environmentally determined equilibria.

Marion Donald Rice University, Houston, Texas, USA.

You can read the full paper online: Context-dependent variability in the population prevalence and individual fitness effects of plant-fungal symbiosis

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