Note from Jeremy: this is a guest post from Christopher Moore. Thank you Chris for writing such a fun and meaty post!
I went to graduate school because I was curiously captivated by a species interaction between plants and animals that disperse their seeds. This interaction is mutualistic; that is, both species directly interact and reciprocally increase each other’s fitness. The animals benefit from the nutrient reward from the plant (e.g., fruit pulp or nut endosperm) and the sessile plants benefit by having the animals do the work of dispersing their seeds across the landscape.
My first semester of graduate school I took one of the best courses of my life, “Advances in theoretical ecology,” whose readings were a mix of current papers and classic papers mostly from Foundations of Ecology by Brown and Real. Although it was an amazing course, I was really surprised that neither the course readings nor the text mentioned mutualism a single time. But what did I know? I was a first-semester graduate student and I thought this was surely an anomalous experience. I thought as I continued my studies I would surely learn more of the theoretical foundations of mutualism.
As graduate school continued, however, this experience was repeated over and over again: I’d go to the library and check out a book or I’d buy a new book with theoretical foci on species interactions, and mutualism would be missing. As examples, I bought Scheiner and Willig’s The Theory of Ecology (2011) the moment it came out (I love the framework of their ’05 paper that preceded it), and despite chapters on competition and enemy-victim interactions (predator-prey, herbivore-plant, host-parasite, etc.), there was no analogous chapter or even a mention of mutualism. I acquired Hastings and Gross’ remarkable 848-page tome Encyclopedia of Theoretical Ecology my final year in grad school. Of the 129 topics there are substantial entries on various species interactions, but not a single mention of mutualism in the entire book.
One day as a postdoc (circa 2016) I was preparing for a talk and decided I wanted a slide to show the lack of attention of mutualism in theoretical textbooks, so I decided to pull some of these books off my shelf to have a visual and some data. The books I owned would, of course, be biased towards including mutualism. But, if the data weren’t too biased, I thought, maybe I’d see a difference between how much attention mutualism receives compared with other species interactions. I haphazardly grabbed 16 and summed the number of pages with the word “mutualism” or synonyms. Here’re the books and data:
Despite expecting a difference, I still found this to be striking. This small, biased sample of texts shows that mutualism is most often mentioned 0 times, and on average it’s mentioned 1 time. This singular mention is always when it’s listed as one of the six types of species interactions. Additionally, if you look at representation of mutualism over time, there seems to be a slight increase in pages and presence of chapters, but nothing that substantially deviates from the figure above.
The number of pages is just one way of assessing how much attention mutualism has received in theoretical texts. We can also look at how authors were discussing mutualism. Allow me to briefly take you through a chronological tour of what the authors have said about mutualism by those that gave at least some space to it:
Christiansen & Fenchel (1973) is a rarity of the ’70s with some text on mutualism:
Mutualism, however, is a special quality of interaction which has rarely been considered from the point of view of theoretical ecology. This is regrettable since a vast number of such relationships, many of which are still incompletely understood, are known from nature.
May (1975, 1st ed. of Theoretical Ecology):
Most contemporary ecology books have chapters, complete with simple mathematical models, on competition and prey-predator. Analogous chapters on mutualism are usually absent. I think the reasons for this are partly historical (Lotka and Volterra studies models for competition and prey-predator, but not for mutualism), and partly because mutualism is a relatively inconspicuous feature in temperate zone ecosystems. Be this as it may, mutualism is a conspicuous and ecologically important factor in most tropical communities, and I hope that the next generation of ecology texts will treat all three types of pairwise interaction between species on a roughly equal footing. . .
Following my admonition in the opening paragraph of this section, I would have liked to include a chapter, along the lines of chapters 6, 7, 8, on mutualism. But I think that neither the theoretical nor empirical aspects of the subject are sufficiently developed to justify this. Many insightful field studies are currently being done, and they should soon provide the basis for such a synthesis
May (1981, 2nd ed. of Theoretical Ecology, with a slight change to the 2nd ed. paragraph from above):
Following my admonition in the opening paragraph of this section, I would have liked to include a chapter, along the lines of chapters 6, 7, 8, on mutualism. But I think that neither the empirical nor theoretical aspects of the subject are yet developed to the point where such a synthetic overview is possible. There are, however, many insightful recent field studies, which shed increasing light on the interplay between the long sweep of evolution and the immediate dynamical effects of populations interactions; it is possible that my laziness is the real reason why such a chapter does not appear in this second edition.
For the record, I deeply appreciate May’s #OverlyHonestMethods here. And to add two notes on subsequent editions: the third edition (May and McLean 2007) only mentions mutualism once (w.r.t. climate change), but the fresh-off-the-press fourth edition edited by McCann and Gellner (2020) has a whole chapter on mutualistic networks (!)
I don’t have a theoretical ecology text from the ’90s with anything about mutualism to quote. May, Roughgarden, and Levin’s Perspectives on Ecological Theory (1989) is almost the ’90s and has chapters on interspecific interactions, but nothing on mutualism. Gotelli’s Primer of Ecology (1995) is another excellent text, but it has no mention of mutualism. Maybe the ’90s were just too angsty to publish then?
Kot (2001) has an entire chapter on mutualism:
Mutualism is an interaction in which species help one another. Mutualism has seldom received the attention of predation and competition. This neglect is quite surprising, given the ubiquity of mutualism.
Vandermeer & Goldberg (2003, 1st ed. has some pages on mutualism in the competition chapter):
That is, as pointed out several times in the past (e.g., Rich and Boucher 1976), mutualism in its various forms is probably the dominant form of interaction in the world yet received the least attention in ecology textbooks. The reason for such a bias eludes ecologists. We follow the traditional orthodoxy of pretending that predation and competition are the dominant forms of interactions, or at least the ones most worthy of the development of theory.
Vandermeer & Goldberg (2013, the 2nd ed. has a chapter on mutualism):
Despite the ubiquitousness of mutualism, no central body of theory of their population dynamics has emerged in the way that it has for predator-prey systems or for competition . . .
To add another line of evidence of underrepresentation of mutualism in theoretical textbooks we can have a look at what is perhaps the most influential monograph series in our field, Princeton Monographs in Population Biology (MPB). Of the > 60 MPBs, only one is focused on mutualism (Bascompte and Jordano’s 2013 Mutualistic Networks). Of the 31 MPBs on my shelf, here is a rough estimate of the number of pages ordered through the series:
I show mutualism (blue) with the one MPB on mutualism (solid) and without (dashed). I don’t think I have to interpret these data because the pattern is clear. Although, I will add that I’m aware of at least 2 MPBs in the works that will have substantial parts on mutualism by M. McPeek and M. Frederickson, so stay tuned.
The pages in theoretical texts, quotes from theoretical texts, and pages in MPB have hopefully convinced you to some extent that mutualism is largely missing from theoretical textbooks. But I also hope that you gained the sense from the quotes that there seems to be a passing of the mutualism buck as you read through the years, where the importance of mutualism will be acknowledged but not given much, if any, attention. And it’s strange because theoretical work on mutualism has been developed and it has been synthesized since the ’70s. Yes, not nearly to the same extent as competition and enemy-victim interactions, but it’s there, and it’s solid work.
I later learned that my observations—or lack of observing mutualism, in this case—were not new. Ecologists have documented this lack of attention for almost 50 years. As early as 1976, Risch and Boucher surveyed 12 textbooks and noted the neglect of mutualism, with 718 pages devoted to interspecific interactions, and 35, roughly 5%, of those were devoted to mutualism. If you’re interested in the history of studies of mutualism, have a look at the first two chapters in the only two general books on mutualism: Mutualism by Bronstein (2015) and The Biology of Mutualism by Boucher (1985) for brief historical accounts.
At this point you’re probably wondering: what is the deal? You may be asking yourself, for instance, if mutualism could not be included in theoretical texts because its ecology is fundamentally different than other species interactions? Is it different? Let’s consider a bit of the ecology of mutualism that might matter for theoretical models:
- Some mutualisms occur between organisms with large differences in generation times or body sizes: this is true of other species interactions
- Mutualism sometimes involves species beyond simplified two-species motifs: this is also true of other species interactions
- Some mutualisms are behaviorally mediated with no direct contact: yup, this happens in other species interactions, too
- In some mutualisms the effects on fitness is delayed: uh-huh, this is also true of other species interactions
- Mutualism has costs and benefit: definitely true of other species interactions
- Mutualism is dependent on ecological context: which is, yet again, true of other species interactions
- Mutualistic interactions are facultative or obligate: TOOSI (True Of Other Species Interactions)
- Mutualistic interactions span specialized and generalized: TOOSI
- Some mutualistic interactions are consumer-resource interactions: #TOOSI
- And so on
It seems like maybe that mutualism might not be that different after all? . . . If we are willing to view other species interactions as simplified spherical cows and massless horses in our simple theoretical models, then we ought to be consistent by also allowing the mutualistic llamas to be frictionless in vacuums and have other simplified properties for the sake of educating readers of textbooks and theoretical development. Also, thank you for bearing through my stretching the spherical-cow metaphor across the ungulate and physics axes 🙂
Another reason that mutualism might not be included in theoretical texts is because of the spectre of unbounded growth. The late Robert May famously described mutualism as “an orgy of mutual benefaction.” This comes from the simple two-species Lotka-Volterra model of mutualism developed by Guase and Witt in the ’30s by switching the sign of the competition model from – to +. In this model, if the mutualistic benefit is greater than intraspecific competition, then the populations grow exponentially without bound. This seems to be the central focus of this model—but perhaps it shouldn’t be. Unbounded growth shouldn’t be the central focus of the Lotka-Volterra mutualism model because it is a theoretical inconvenience and a consequence of the model structure; unbounded growth is not a feature of real populations. We should therefore not ignore mutualism because the model we chose to use produces silly results. Instead we should focus on the facts like that even in the overly-simplified, general Lotka-Volterra mutualism model, we find that mutualism increases species’ abundances at equilibrium(!) and increases population growth rates(!). It even seems like showing how mutualistic interactions are kept from unbounded growth would be a good transition in textbooks between 2 to 3-n species models or as a way to introduce nonlinear functions or numerical solutions.
Mutualism, as the quoted authors above and many others contend, is ubiquitous and incredibly important for communities and ecosystems. I don’t have the space in this blog to further elaborate on the reasons why mutualism receives less attention, but again see Boucher (1985) and Bronstein (2015) for their historical treatments. In the end, to channel May, it is possible that my laziness is the real reason I why a further elaboration does not appear in this post.
For those of you looking for material on mutualism to add to your textbooks, there is a ton of great work out there, but here’re a few foundational references and several references to newer, exciting work in mutualism theory (of simple, low-dimensional systems, not the exciting explosion of literature on mutualistic networks):
A few classics:
- Vandermeer, J.H. and Boucher, D.H.,1978, Varieties of mutualistic interaction in population models. Journal of Theoretical Biology, 74(4), pp.549-558.
Introduces facultative and obligate interactions into the Lotka-Volterra mutualism model
- Wolin, C.L. and Lawlor, L.R., 1984. Models of facultative mutualism: density effects. The American Naturalist, 124(6), pp.843-862.
Considers the effects of intraspecific density in mutualistic interactions and explicit nonlinear functions (a personal favorite)
- Wright, D.H., 1989. A simple, stable model of mutualism incorporating handling time. The American Naturalist, 134(4), pp.664-667.
- Adapts Holling’s Type II functional response to mutualism
Just several (limited to 6) of many recent (last 5 years) works that I find exciting:
- Johnson, C.A. & Bronstein, J.L., 2019. Coexistence and competitive exclusion in mutualism. Ecology, 100(6), p.e02708.
Develops analogous R* rule for coexistence of mutualism
- Wu, F., Lopatkin, A.J., Needs, D.A., Lee, C.T., Mukherjee, S. & You, L., 2019. A unifying framework for interpreting and predicting mutualistic systems. Nature communications, 10(1), pp.1-10.
Derives and evaluates a simple rule for understanding mutualistic interactions
- Revilla, T.A., 2015. Numerical responses in resource-based mutualisms: a time scale approach. Journal of Theoretical Biology, 378, pp.39-46.
Explicit look at consumer-resource nature of mutualistic interactions and ecological meanings of saturating function parameters
- Hoek, T.A., Axelrod, K., Biancalani, T., Yurtsev, E.A., Liu, J. & Gore, J., 2016. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS biology, 14(8), p.e1002540.
A simple microbial cross-feeding mutualism experiment supported with a simple model
- Hale, K.R.S., Maes, D.P., & Valdovinos, F.S., 2020, The ecological theory of mutualism: Models generalizing across different mechanisms, Contributed Poster, Ecological Society of America’s Annual Meeting
Very new formulation of models specific to protection, nutritional, and dispersal (pollen and seed) mutualisms
- Nakazawa, T., 2020. A perspective on stage‐structured mutualism and its community consequences. Oikos, 129(3), pp.297-310.
Develops general theoretical framework for incorporating stage-structure and developing an ontogenetic perspective of mutualism
I also want to give a shout out to all those that have included theory of simple mutualisms (not comprehensive); e.g., DeAngelis et al. (Positive feedback in natural systems, 1986), Holland (in Mutualism, edited by Bronstein, 2015), Kot (Elements of mathematical ecology, 2001), Morin (Community ecology, 2011), Stadler and Dixon (Mutualism: ants and their insect partners, 2008), Vandermeer and Goldberg (Population ecology: first principles, 2013), and Wolin (in The biology of mutualism, edited by Boucher, 1985).
There has been so much outstanding work on theoretical aspects of mutualism ecology and evolution over the last four decades, and I’m sorry I cannot include all of it here! Perhaps you can add your favorites in the comments and add to this blog so it can be used as a resource.
Thanks to J. Bronstein and J. Dittel for comments on an earlier draft of this post.
Thank you for reading and I hope you enjoyed it!