Stasis and the phenotypic gambit
Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework
The preprint "Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework" by Coulson (2020) presents a general framework for evolutionary ecology, useful to interpret patterns of selection and evolutionary responses to environmental transitions. The paper is written in an accessible and intuitive manner. It reviews important concepts which are at the heart of evolutionary ecology. Together, they serve as a worldview which you can carry with you to interpret patterns in data or observations in nature. I very much appreciate it that Coulson (2020) presents his personal intuition laid bare, the framework he uses for his research and how several strong concepts from theoretical ecology fit in there. Overviews as presented in this paper are important to understand how we as researchers put the pieces together.
A main message of the paper is that resource detection and acquisition traits, broadly called "resource accrual traits" are at the core of evolutionary dynamics. These traits and the processes they are involved in often urge some degree of individual specialization. Not all traits are resource accrual traits all the time. Guppies are cited as an example, which have traits in high predation environments that make foraging easier for them, such as being less conspicuous to predators. In the absence of predators, these same traits might be neutral. Their colour pattern might then contribute much less to the odds of obtaining resources.
"Resource accrual" reminds me of discussions of resource holding potential (Parker 1974), which can be for example the capacity to remain on a bird feeder without being dislodged. However, the idea is much broader and aggression does not need to be important for the acquisition of resources. Evolutionary success is reserved for those steadily obtaining resources. This recalls the pessimization principle of Metz et al. (2008), which applies in a restricted set of situations and where the strategy which persists at the lowest resource levels systematically wins evolutionary contests. If this principle would apply universally, the world then inherently become the worst possible. Resources determine energy budgets and different life history strategies allocate these differently to maximize fitness. The fine grain of environments and the filtration by individual histories generate a lot of variation in outcomes. However, constraint-centered approaches (Kempes et al. 2019, Kooijman 2010) are mentioned but are not at the core of this preprint. Evolution is rather seen as dynamic programming optimization with interactions within and between species. Coulson thus extends life history studies such as for example Tonnabel et al. (2012) with eco-evolutionary feedbacks. Examples used are guppies, algae-rotifer interactions and others. Altogether, this makes for an optimistic paper pushing back the pessimization principle.
Populations are expected to spend most of the time in quasi-equilibrium states where the long run stochastic growth rate is close to zero for all genotypes, alleles or other chosen classes. In the preprint, attention is given to reproductive value calculus, another strong tool in evolutionary dynamics (Grafen 2006, Engen et al. 2009), which tells us how classes within a population contribute to population composition in the distant future. The expected asymptotic fitness of an individual is equated to its expected reproductive value, but this might require particular ways of calculating reproductive values (Coulson 2020). Life history strategies can also be described by per generation measures such as R0 (currently on everyone's radar due to the coronavirus pandemic), generation time etc. Here I might disagree because I believe that this focus in per generation measures can lead to an incomplete characterization of plastic and other strategies involved in strategies such as bet-hedging. A property at quasi-equilibrium states is precise enough to serve as a null hypothesis which can be falsified: all types must in the long run leave equal numbers of descendants. If there is any property in evolutionary ecology which is useful it is this one and it rightfully merits attention.
However, at quasi-equilibrium states, directional selection has been observed, often without the expected evolutionary response. The preprint aims to explain this and puts forward the presence of non-additive gene action as a mechanism. I don't believe that it is the absence of clonal inheritance which matters very much in itself (Van Dooren 2006) unless genes with major effect are present in protected polymorphisms. The preprint remains a bit unclear on how additive gene action is broken, and here I add from the sphere in which I operate. Non-additive gene action can be linked to non-linear genotype-phenotype maps (Van Dooren 2000, Gilchrist and Nijhout 2001) and if these maps are non-linear enough to create constraints on phenotype determination, by means of maximum or minimum phenotypes which cannot be surpassed for any combination of the underlying traits, then they create additional evolutionary quasi-equilibrium states, with directional selection on a phenotype such as body size. I believe Coulson hints at this option (Coulson et al. 2006), but also at a different one: if body size is mostly determined by variation in resource accrual traits, then the resource accrual traits can be under stabilizing selection while body size is not. This requires that all resource accrual traits affect other phenotypic or demographic properties next to body size. In both cases, microevolutionary outcomes cannot be inferred from inspecting body sizes alone, either resource accrual traits need to be included explicitly, or non-linearities, or both when the map between resource accrual and body size is non-linear (Van Dooren 2000).
The discussion of the phenotypic gambit (Grafen 1984) leads to another long-standing issue in evolutionary biology. Can predictions of adaptation be made by inspecting and modelling individual phenotypes alone? I agree that with strongly non-linear genotype-phenotype maps they cannot and for multivariate sets of traits, genetic and phenotypic correlations can be very different (Hadfield et al. 2007). However, has the phenotypic gambit ever claimed to be valid globally or should it rather be used locally for relatively small amounts of variation? Grafen (1984) already contained caveats which are repeated here. As a first approximation, additivity might produce quite correct predictions and thus make the gambit operational in many instances. When important individual traits are omitted, it may just be misspecified. I am interested to see cases where the framework Coulson (2020) proposes is used for very large numbers of phenotypic and genotypic attributes. In the end, these highly dimensional trait distributions might basically collapse to a few major axes of variation due to constraints on resource accrual.
I highly recommend reading this preprint and I am looking forward to the discussion it will generate.
 Coulson, T. (2020) Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework. bioRxiv, 509067, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/509067
 Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X., and Kendall, B. E. (2006). Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evolutionary Ecology Research, 8(7), 1155-1171.
 Engen, S., Lande, R., Sæther, B. E. and Dobson, F. S. (2009) Reproductive value and the stochastic demography of age-structured populations. The American Naturalist 174: 795-804. doi: 10.1086/647930
 Gilchrist, M. A. and Nijhout, H. F. (2001). Nonlinear developmental processes as sources of dominance. Genetics, 159(1), 423-432.
 Grafen, A. (1984) Natural selection, kin selection and group selection. In: Behavioural Ecology: An Evolutionary Approach,2nd edn (JR Krebs & NB Davies eds), pp. 62–84. Blackwell Scientific, Oxford.
 Grafen, A. (2006). A theory of Fisher's reproductive value. Journal of mathematical biology, 53(1), 15-60. doi: 10.1007/s00285-006-0376-4
 Hadfield, J. D., Nutall, A., Osorio, D. and Owens, I. P. F. (2007). Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of evolutionary biology, 20(2), 549-557. doi: 10.1111/j.1420-9101.2006.01262.x
 Kempes, C. P., West, G. B., and Koehl, M. (2019). The scales that limit: the physical boundaries of evolution. Frontiers in Ecology and Evolution, 7, 242. doi: 10.3389/fevo.2019.00242
 Kooijman, S. A. L. M. (2010) Dynamic Energy Budget theory for metabolic organisation. University Press, third edition.
 Metz, J. A. J., Mylius, S.D. and Diekman, O. (2008) When does evolution optimize?. Evolutionary Ecology Research 10: 629-654.
 Parker, G. A. (1974). Assessment strategy and the evolution of fighting behaviour. Journal of theoretical Biology, 47(1), 223-243. doi: 10.1016/0022-5193(74)90111-8
 Tonnabel, J., Van Dooren, T. J. M., Midgley, J., Haccou, P., Mignot, A., Ronce, O., and Olivieri, I. (2012). Optimal resource allocation in a serotinous non‐resprouting plant species under different fire regimes. Journal of Ecology, 100(6), 1464-1474. doi: 10.1111/j.1365-2745.2012.02023.x
 Van Dooren, T. J. M. (2000). The evolutionary dynamics of direct phenotypic overdominance: emergence possible, loss probable. Evolution, 54(6), 1899-1914. doi: 10.1111/j.0014-3820.2000.tb01236.x
 Van Dooren, T. J. M. (2006). Protected polymorphism and evolutionary stability in pleiotropic models with trait‐specific dominance. Evolution, 60(10), 1991-2003. doi: 10.1111/j.0014-3820.2006.tb01837.x
Tom Van Dooren (2020) Stasis and the phenotypic gambit. Peer Community in Ecology, 100053. 10.24072/pci.ecology.100053
Evaluation round #2
DOI or URL of the preprint: 10.1101/509067
Version of the preprint: 1
Author's Reply, 20 Apr 2020
Decision by Tom Van Dooren, 16 Apr 2020
This manuscript by Coulson previously called "Causes Of Death And Failures To Reproduce, Limiting Resources, Ecological Dynamics, And Selection: How To Evolve A Low Predation Guppy, And Cause A Trophic Cascade", presents a thorough revision which addresses most of the previous comments by two reviewers and myself adequately. The two reviewers have a number of remaining remarks, which in my view can almost all be addressed with some rewording or the addition of references.
In my view, this manuscript in a way provides a generalization of the concept of "resource holding power" to a broader eco-evolutionary context. On line 555 the manuscript cites a redefinition of fitness in terms of energy, but there are usually several resources required to complete a life cycle and as L561 states, there can be several primary causes of death and failure to breed. I would appreciate it if the manuscript could give a bit more attention to situations where there are several primary causes or limiting resources, or stress the conditionality of an argumentation on there being a single primary cause or limiting resource when that is the case.
Best regards, Tom Van Dooren
Reviewed by Katja Räsänen, 24 Mar 2020
Reviewed by Jacob Johansson, 05 Apr 2020
Evaluation round #1
DOI or URL of the preprint: doi: https://doi.org/10.1101/509067
Author's Reply, 11 Feb 2020
Decision by Tom Van Dooren, 25 Feb 2019
Coulson proposes a framework to investigate what happens when a change in community composition alters the dominant cause of death (or of failure to reproduce) by changing the limiting resource. This is a topical issue. Immediately, it bears relevance to studies of context-dependent specialization of species, of potential effects of ecosystems going trough bifurcations (tipping points), although neither is treated. The manuscript is accessible and reads well. However it is for a large part a very lengthy description of required components of any realistic eco-evolutionary model that would be able to produce predictions for a particular system. These components are rather cursorily covered, none of the equations proposed are linked into a real model. Two reviewers and myself believe that this manuscript presents a relevant topic and that it is potentially worth recommending. However, a number of issues have to be addressed before we can make such a recommendation on behalf of PCI Ecology. Next to the points raised by the reviewers, I want to point out the following:
The guppy example leads us very easily into the issues addressed and I appreciate it very much. However, I believe the manuscript currently has too much focus on removing predators (or consumers, for plants), i.e., on community changes on a different trophic level than a focal species (the guppy). In another relevant scenario, coexisting competitors might each specialize on a different resource, becoming limiting for each of them. A removal of one competitor could then alter the eco-evolutionary feedback drastically.
Here is my most important remark: the manuscript lacks any definition of what a limiting resource is or of a key factor limiting population growth, and how one should define and determine "the dominant cause of death" or a factor controlling reproduction. This needs to be added. When these characteristics are not defined, they cannot be used to generate or assess predictions. I believe the author refers to a method like λ‐contribution analysis, but this is not made explicit, so we can't assess whether that approach is entirely defensible for the intended purpose.
Recently, a special issue has appeared in Functional Ecology on eco-evolutionary dynamics https://besjournals.onlinelibrary.wiley.com/toc/13652435/2019/33/1 with much attention for community effects of feedback loops in models and empirical systems. Coulson presents a mix of results on age-structured models, of modelling population and evolutionary dynamics in fluctuating environments, mostly using IPM's. Often the presentation does not do justice to the true origin of a concept. For example evolutionary suicide is not due to Rankin and Lopez-Sepulcre, but to Ferriere, Gyllenberg and Parvinen. Several modelling frameworks are just omitted (physiologically structured population modelling, epidemiological modelling using ODE's). I believe it is undoable to treat them all well. On the other hand, the bias towards IPM's has no obvious merit either. I would therefore prefer that the description of all model ingredients is drastically shortened to bring the focus back on the main issue: predict what happens when a sudden species change in an assemblage or community alters the eco-evolutionary feedback drastically.
The manuscript stays a bit unclear on what the timescale is where limiting resources will usually change. Is adaptation really relevant if species composition changes often? How often does a switch in key-factor occur? What with organisms that have a metamorphosis?
The manuscript treats the specialization of traits to environmental conditions. However, there is no mention of trade-offs. They need to be discussed, the focus is too much on single traits now (such as body size).
I believe the statement on p. 35 that no model combines all ingredients of Figure 5 is an overstatement. Please consult for example the models by Gavrilets and coworkers in the group of papers called "CASE STUDIES AND MATHEMATICAL MODELS OF ECOLOGICAL SPECIATION". I believe the link between the issue treated here and such models is strong and insufficiently treated. Consider Rundle and Schluter (2004. Natural selection and ecological speciation in sticklebacks), box 9.5: They use results of eco-evolutionary modelling to predict scenarios where speciation does not occur, but repeated invasions instead. The same trick can be applied for species removals. Hence I believe much of the framework needed exists and has been used to predict effects of changes in community composition, with results maybe needing a different interpretation in view of the questions asked here.
The Emu example: I would use it to propose colonization and evolution on islands as a general scenario where changes in limiting factor are relevant. For an overview of patterns of selection on small and large body size, please consult Blanckenhorn, W. U. (2000). The evolution of body size: what keeps organisms small?. The Quarterly review of biology, 75(4), 385-407.
Best regards, Tom Van Dooren