Thinking about theorizing ...

My inspiration for this blog has been the eminent microbial ecologist Jim Prosser. Jim has written a series of thoughtful pieces on the philosophy of microbial ecology over the past 17 years. That first article was entitled “The role of ecological theory in microbial ecology” in which he and his coauthors said that the underdevelopment of theory had stunted progress in microbial ecology and that an important factor was “cultural, in that the tools and disciplines of ecological theory are not part of the contemporary mindset in microbiology.” That article has certainly been widely read --it has been cited more than 700 times. However, as I reflect on the current state of microbial ecology research I cannot unequivocally assert that this cultural barrier has been overcome.

This barrier contrasts with macrobe ecology, which has a long and deep history of theory development (as well as continuing disagreements between empiricists and theoreticians on the role of each other’s approaches). My current opinion is that microbial ecology need not develop theories unique to itself but can build upon and enrich macrobe ecology theory. Theory can provide a framework to develop testable hypotheses. A weakness in macrobe ecology theories is the difficulty in testing them at the appropriate time and space scales and with adequate replication. I think there is enough congruence between the ecology of microbes and macrobes that the advantages of microbial systems can be exploited to rigorously test these theories.

However, the application of ecological and evolutionary theory to microbiome community dynamics is complicated by features of the microbiome, including horizontal gene transfer, rapid evolution and the production of public goods and antimicrobial compounds

The hierarchy of theory

I read a book edited by Scheiner and Willig (SW), The Theory of Ecology, published in 2011 that was very illuminating regarding a philosophical basis for theorizing. SW define theories as “hierarchical frameworks that connect broad general principles to highly specific models.” They propose three (loose) tiers: general theory, constitutive theories and models. In their view, general theory sets a broad framework of principles upon which constitutive theories are developed. These generate propositions (relationship or causation) to explain specific phenomena. Models are the level where Popper’s exhortation to generate ‘risky hypotheses’ and test them is fundamental. The tests may entail field experiments but may also be statistical or mathematical models. A good example of the latter was Robert May’s seminal work on the diversity vs stability debate (May, 1973). He carried out linear stability analysis of randomly constructed communities with random interaction strengths and found that diversity destabilizes community dynamics when perturbed. This was puzzling to ecologists and at odds with some empirical results. However, the controversy stimulated efforts to understand how authentic communities may not be random and what kinds of interaction structures promote persistence.

General theory of ecology

SW have put forward their proposal for a general theory that consists of 8 principles. I reproduce them here.

Eight fundamental principles of the general theory of ecology

1. Organisms are distributed in space and time in a heterogeneous manner.

2. Organisms interact with their abiotic and biotic environments.

3. Variation in the characteristics of organisms results in heterogeneity of ecological patterns and processes.

4. The distributions of organisms and their interactions depend on contingencies.

5. Environmental conditions as perceived by organisms are heterogeneous in space and time.

6. Resources as perceived by organisms are finite and heterogeneous in space and time.

7. Birth rates and death rates are a consequence of interactions with the abiotic and biotic environment.

8. The ecological properties of species are the result of evolution.

SW anticipate your immediate assessment: “The reaction of many to confirmed generalizations is, “Well, isn’t that obvious?” In reality, the answer is no. Often such generalizations are obvious only after their explication.”

On reflection, I see that the principles I set out in Big questions in (microbial) ecology for the most part fit within this framework. If there is something missing from a microbial perspective, it might be the fundamental importance of thermodynamics.

Constitutent theories

Superficially, ecology looks to be theory-rich. Marquet et al. (2014) identified 78 theories in the ecological literature, although some might better fit as ‘models’ than constituent theories. Furthermore, a few are rather specific for plants or animals (e.g., life history theory) that they are not very meaningful for microbial ecology.

I did a Web of Science survey of microbial ecology papers published since 2000 (about 78,000) – only 2,000 contained “theory” as a Topic. Those most commonly mentioned were related to two of Vellend’s ecological processes that determine community composition: selection among species and dispersal. These papers rarely tested Vellend’s theory but rather used the processes as a context for their molecular censuses of microbial community composition. The metabolic theory of ecology and game theory were the next most commonly cited.

There certainly are a lot of ecological theories that could be tested using microbes– either natural or model systems. Some of the more obvious ones (based on Marquet et al.’s list) include:

Drivers of community composition:

1. Biological Invasion Theory

2. Community Assembly / Species Diversity Theory

3. Competition / Coexistence / Competitive Exclusion / Niche Theory

4. (Intermediate) Disturbance Theory

5. Insular Biogeography Theory

6. Landscape / Metacommunity / Macroecological Theories

7. Neutral Theory of Biodiversity

“Life history” strategies

1. C-S-R Triangle / Metabolic Theory

2. Dynamic Energy Budget Theory

3. Ecological Stoichiometry / Resource Ratio Theory

4. Optimal Foraging Theory

5. Trait-based Theory

Ecosystem / larger scales

1. Ecological Network Theory

2. Information Theory (see RE Ulanowicz)

3. Diversity-Stability Theory

4. Succession Theory

Another very important area to which I will devote a future blog post is Evolutionary ecology theory. This area became discernible in macrobe ecology during the 1960s to investigate the environmental factors that drive species adaptation. However, many questions remain outstanding. I think microbes can play a special role here, given the strong selective pressures that can be applied at a small spatial scale, their relatively rapid rate of growth which can fix advantageous mutations and their added capacity for horizontal gene transfer.

Models

The third tier of SW’s hierarchy are Models. They will be the most specific of the tiers and may be pertinent to a particular mechanism or system. They may very well be conceptual or abstract, and comprise statistical, analytical or computational approaches. The intent is to generate predictions that can be empirically tested. These models are not a description of reality but rather our assumptions about reality. Hence, it is appropriate that the model evolves as it is empirically tested.

Per some of Jim Prosser’s comments over the years, the effort required to take your study-of-interest and tune its experimental details to test a hypothesis/model that falls underneath a constitutive model is not enormous and would markedly enhance the impact of your work.

An example: Diversity-stability theory.

The question whether biological diversity confers stability has been a contentious one for decades. A significant part of the problem are the diverse ways in which ‘stability’ has been defined and measured (Donohue et al., 2016). Here I take as my conceptual model that higher microbial diversity (and in particular functional redundancy) will result in greater stability of ecosystem function (measured as key process rates such as primary production or degradation of organic matter), observed as resilience to or recovery from environmental perturbations.

The tests and limits of this model could entail natural systems in which there are environmental gradients of physicochemical factors such as temperature, pH or salinity – hot spring mat communities provide a good example for temperature. Alternatively, natural communities can be diluted to reduce diversity (this will tend to selectively exclude ecotypes found in low relative abundance) and then reinoculated into a sterilized natural sample or a synthetic analog of the habitat. Lastly, synthetic communities of differing diversities could be constructed from cultures sourced from the habitat of interest.

In my ‘dream’ world, there is the capacity to continuously monitor system function (for example, an oxygen microelectrode in a phototrophic microbial mat) but at least occasional assays for activity would be necessary to monitor the effects of and recovery from the perturbation. Of course, during and after recovery a microbial census can be done to determine changes in diversity or community composition.

The natural systems that have environmental ‘edge’ effects with likely changes in diversity are soils <pH 5 (Rousk et al., 2010) and hot spring mats where oxygenic photosynthesis wanes at temperatures above 65-70° C. Manipulating diversity within a natural sample can be a tricky business, as the extracted and manipulated community has to be reintroduced into a sterilized version of the system. This has been done employing a ‘model soil’ (Domeignoz-Horta et al., 2020). A laboratory-based model system has merits in terms of experimental control but certainly strays far from ‘realism’ and is dependent upon those microbes that have been cultured.

References

Domeignoz-Horta, LA et al. (2020) Microbial diversity drives carbon use efficiency in a model soil. Nature Comm 11: 3684

Donohue I et al. (2016) Navigating the complexity of ecological stability. Ecol Lett 19:1172-85. doi: 10.1111/ele.12648.

Li Z et al.(2025) A powerful but frequently overlooked role of thermodynamics in environmental microbiology: inspirations from anammox. Appl Environ Microbiol 91:e01668-24. https://doi.org/10.1128/aem.01668-24

Marquet PA et al. (2014) On Theory in Ecolog. BioScience, 64:701–710, https://doi.org/10.1093/biosci/biu098

May, R. M. Stability and complexity in model ecosystems (Princeton Univ. Press, 1973).

Prosser, JI et al. (2007) The role of ecological theory in microbial ecology

Nat Rev Microbiol 5: 384–392

Rousk J et al. (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4:1340-51. doi: 10.1038/ismej.2010.58.

Scheiner, S. M., & Willig, M. R. (Eds.). (2011). The theory of ecology. University of Chicago Press.

I am going to take a hiatus from thinking philosophically about microbes for the next three weeks – we are travelling to Patagonia tomorrow. Most of the time will be on a ship going around Cape Horn and up the west coast of Chile admiring the fjords. I am looking forward to indulging my photographic instincts there …

Today’s Moment of Zen

I have lived in Maryland for about 6 months now, and it has been great seeing my family much more often and taking advantage of the arts scene here (sorry E Washington State!). However, I do get wistful about having those mountains so close by