Coexistence Theory for Microbial Ecology, and Vice Versa

Abstract

Classical models from theoretical ecology are seeing increasing uptake in microbial ecology, but there remains rich potential for closer cross-pollination. Here we explore opportunities for stronger integration of ecological theory into microbial research (and vice versa) through the lens of so-called "modern" coexistence theory. Coexistence theory can be used to disentangle the contributions different mechanisms (e.g., resource partitioning, environmental variability) make to species coexistence. We begin with a short primer on the fundamental concepts of coexistence theory, with an emphasis on the relevance to microbial communities. We next present a systematic review, which highlights the paucity of empirical applications of coexistence theory in microbial systems. In light of this gap, we then identify and discuss ways in which: (i) coexistence theory can help to answer fundamental and applied questions in microbial ecology, particularly in spatio-temporally heterogeneous environments, and (ii) experimental microbial systems can be leveraged to validate and advance coexistence theory. Finally, we address several unique but often surmountable empirical challenges posed by microbial systems, as well as some conceptual limitations. Nevertheless, thoughtful integration of coexistence theory into microbial ecology presents a wealth of opportunities for the advancement of both theoretical and microbial ecology.

Keywords: invasion analysis; microbial ecology; modern coexistence theory; synthesis; theoretical ecology.

FIGURE 1

Experimental approaches that can be used to acquire the necessary data for coexistence theory (A–C) and the two threads of coexistence theory that can be used to analyse the data (D, E). The arrows between panels show the number of studies in our systematic review that used that combination of empirical and analytical approaches. The numbers in superscripts refer to row numbers of Table 1. (A) Response surface designs, which can not always be applied in microbial systems (see Empirical challenges), manipulate species' densities to parameterize population models. Alternatively, competitive factors (e.g., resource concentrations) can be manipulated to parameterize mechanistic models (e.g., consumer‐resource models). (B) Invasion tests can be performed to test the mutual invasion criterion (i.e., coexistence predicted if all species can invade the community from low densities). (C) Timeseries datasets can be used to parameterize population dynamics models or to test coexistence theory predictions. (D) The most common analytical approach for applying coexistence theory is quantifying niche and fitness differences, either directly from the data through model‐agnostic approaches or from parameterized population models using mathematical approaches. Communities can then be placed in a “coexistence plane” with axes defined by niche and fitness differences where different regions indicate either competitive exclusion (pale grey zones on top and bottom), stable coexistence (mid grey zone on the right), or priority effects (dark grey zone on the left). (E) Coexistence theory can also be used to partition the effects of different coexistence mechanisms either using analytical techniques or using simulation‐based approaches. In this hypothetical example, there is stable coexistence between the blue and yellow species (both have positive invasion growth rates) primarily due to large contributions from fluctuation‐dependent mechanisms.