I have read the manuscript "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" by Tim Coulson.
This manuscript is about the ecological and evolutionary consequences of removing a species from, or adding a species to, an interactive community. In particular the manuscript focuses on limiting resources and the possibility that adding or removing species might affect which resource becomes the most limited resource. As an illustrating example the manuscript starts out discussing how in the case of guppy communities, the presence of a predator could imply change the dominating selection pressures from being mainly determined by competition for food to being mainly determined by competition for predator-free space.
The manuscript is very well written and uses an efficient combination of theory and illustrative empirical examples to guide the reader through the many dynamical effects of biotic perturbations occurring at different levels, from birth and death processes and demography to population dynamics and evolutionary outcomes. Further the manuscript discusses how processes occurring at different levels may interact with each other and cause more or less surprising feedbacks. The paper culminates in the proposal of a modelling framework which integrates these multi-level dynamics.
I suppose the manuscript is intended as a forward-looking review or perspective article with the main aim of pointing out new research areas which becomes possible to study with an integrative approach to study eco-evolutionary responses. In its current form I think the manuscript provides many interesting thoughts, but I also think it could be improved if it would be linked more deeply to previous theory and modelling of eco-evolutionary dynamics in interacting communities.
Firstly, several papers not cited here have been devoted to the study of ecological and evolutionary consequences of species removal. These includes models which are simpler than the framework proposed here, e.g. Lotka-Volterra community models and adaptive dynamics (with much less genetic detail for example). I will provide some examples below. For this reason I think the manuscript would benefit from (A) outlining more precisely which aspects of species-removal responses require further study, and back this up with references and (B) provide more precise arguments why the study of these phenomena require the use of the rather complex model framework proposed here. I am thinking of Occam or perhaps Einsten (?):”Everything should be made as simple as possible, but not simpler”. An advantage of simpler models is that they are more transparent and often lend themselves to analytical treatments.
Secondly, and following up on point (B) above, there already exists some model frameworks (e.g. eco-genetic models, see below). which have a similar scope as the one proposed here. Thus, I think it is questionable if we actually need a new framework, or if potentially eco-genetic models (or other existing frameworks) could be used with some adaptations. If the conclusion is that existing frameworks might work equally well, then the manuscript could be shortened in this regard and perhaps end in another way, e.g. further ideas and suggestion for systems and questions that would be interesting to study.
My overall feeling however, is that the manuscript has a big point in highlighting that changes in which resource type is limiting might is likely to define eco-evolutionary responses to species loss or other perturbations. More precisely I think that most theory on evolutionary responses to environmental change in ecological communities mainly has considered adaptation to shifts in "substitutable" resources as opposed to "essential" resources. For example, quite some theory considers evolution in which species shift from one food resource to another, or shift from using one habitat to using another (substitutable resources). In contrast, a shift from food limitation to predator limitation represents imply a shift from one essential resource (food) being limiting to another essential resource (predator-free space) being limiting. Similarly, both nest holes and food are essential resources for many bird species. Shifts in which essential resource is limiting may have more profound effects than shifts in substitutable resources.
But if the manuscript would make an argument that shifts in limiting resources is a neglected theme in eco-evolutionary responses, that might need some support. Ground-breaking theory resource limitation in essential as opposed to substitutable resources by Tilman (e.g. 1980) could be cited. Some eco-evolutionary consequences (in terms of optimization and co-existence) of essential/substitutable resources are discussed by Vincent et al. (1996). A review by McGill et al (2006) which argues that community ecology has focused a bit too much on pair-wise interactions and distinct preferences (for substitutable resources) might also be relevant. A recent paper by Higginson (2017) discusses how nest sites in birds and pollinators is now becoming a more limited resource and leading to competitive exclusion in systems which were previously more structured around competition for food.
Resource limitation plays a role also in controlling the outcome of competition when resources are substitutable. For example, if two predators compete for two prey species, the predators which can supress the population abundances of the prey species to the lowest level and yet survive will win the competition. The predator can co-exist if they have different preferences however and each supress their preferred prey. This occurs in Lotka-Volterra-style food web models for example, and is fairly well studied. I suppose the manuscript is not about that, but perhaps this is worth clarifying?
Higginson, Andrew D. 2017. "Conflict over non-partitioned resources may explain between-species differences in declines: the anthropogenic competition hypothesis." Behavioral ecology and sociobiology 71.99.
Tilman, D. (1980) Resources: a graphical-mechanistic approach to competition and predation. Am. Nat. 116, 362–393
Vincent, T. L. S., et al. 1996 Trade-offs and coexistence in consumer-resource models: it all depends on what and where you eat. The American Naturalist 148:1038-1058.
Mcgill, B. J., Enquist, B. J., Weiher, E., & Westoby, M. (2006). Rebuilding community ecology from functional traits. TRENDS in Ecology and Evolution, 21: 178-185.
MORE SPECIFIC POINTS
Following up my points above I will provide some specific suggestions below regarding literature which I think the manuscript should be related to and which is some cases may require some larger adjustments of the text. The manuscript already has a lot of references, which is natural since it covers so many areas. I do not suggest all the below references needs to be cited. Rather, I hope that these suggestions would help defining the novelty in the manuscript a bit more and make it possible to shorten sections where previous work has been done.
- Eco-genetic modeling and individual based eco-evolutionary models
The so called “eco-genetic” model framework presented by Dunlop et al (2009) bears many similarities with the framework proposed here (Fig. 5). Similar to here that model describes processes at many scales. Specific building blocks includes: evolving traits, inheritance model, individual growth model, density dependence, environmental variation, phenotypic plasticity, sex structure, mating systems and more. I have not done a detailed comparison, but it seems to me that the proposed framework in principle corresponds to such an eco-genetic model. Potentially the genotype-phenotype mapping is not included in the Dunlop et al framework, but on the other hand that framework includes a nice take on plasticity (via reaction norms) which seems generic and not discussed here. In Dunlop et al there are further references to applications of eco-genetic models (in fisheries). These studies give some idea of the strengths and potential weaknesses of this approach.
A recent review of individual-based eco-evolutionary models of different complexity is further provided by Romero-Mujalli et al. 2019.
Dunlop ES, Heino M & Dieckmann U (2009). Eco-genetic modeling of contemporary life-history evolution. Ecological Applications 19: 1815–1834
Romero-Mujalli, Daniel et al. 2018 Individual-based modeling of eco-evolutionary dynamics: state of the art and future directions. Regional Environmental Change 1:1-12.
- Evolution in species interactions
The manuscript discusses evolution in species interactions (e.g. last para on page 22 to top of page 24 and page 30). There are relatively few citations here in spite of this being a huge research area, especially within the field of adaptive dynamics, and addresses many issues including community evolution, speciation and diversification (see refs below). I think this should be acknowledged, however I also think it might be possible to argue that there has been little focus on resource limitations and essential resources here (I think, but I am not 100%). Another reason to link the manuscript more to the field of adaptive dynamics and related frameworks is that the manuscript once published then could become more easily accessed to a broader modelling community, which I think will be inspired by the ideas in this manuscript.
Loeuille, N. and Loreau, M. 2005. Evolutionary emergence of size-structured food webs. Proc. Natl. Acad. Sci. USA, 102: 5761–5766.
Dieckmann U & Doebeli M (1999). On the origin of species by sympatric speciation. Nature 400: 354–357
Van Dooren, TJM, M Durinx and I Demon 2004 Sexual dimorphism or evolutionary branching? Evolutionary Ecology Research 6: 857-871.
Abrams P. A. 2001. Modelling the adaptive dynamics of traits involved in inter- and intraspecific interactions: An assessment of three methods. Ecology Letters 4:166-175.
Ripa J., L. Storlind, P. Lundberg & J. S. Brown. 2009. Niche co-evolution in consumer-resource dynamics. Evol. Ecol. Res. 11: 305-323.
Brännström Å et al. 2012. Modeling the ecology and evolution of communities: A review of past achievements, current efforts, and future promises. Evolutionary Ecology Research 14: 601–625
- Theory regarding ecological and evolutionary consequences of species removal
The ecological consequences of species removal from an interactive community has been studied quite a lot. The classic study by Paine (1966) could be cited as it identifies keystone species, i.e. species which if removed have a large impact on the community structure, relevant for present manuscript. Theoretical studies have tried to identify keystone species in model food webs. One interesting phenomena which may occur when removing species from a community is “community closure”, i.e. once you have removed some species they cannot reinvade again, i.e. the community has changed irreversibly (Lundberg et al. 2000). That in turn links to the idea of “alternative stable states” and “attraction domains” in ecological systems where removal of species can lead to irreversible changes and trophic cascades (i.e. when a significant perturbation or removal of important (keystone) species moves the system from one domain of attraction to another).
Johansson & Dieckmann (2009) introduces the Evolutionary Domain of Attraction (EDA) as an evolutionary analogue to the ecological concept. The idea there is that if you perturb an evolutionarily stable community (an ESS community), for example by temporarily subject it to a new selection regime, ensuing evolutionary responses may or may not restore the original community after the perturbation. Some ESS communities may have a large EDA meaning that it will return to the original ESS also after large perturbations. In some cases, a system may have multiple possible evolutionary equilibria (several locally stable ESS solutions). In such systems a perturbation may cause a transition from one ESS to another. The guppy system discussed in this manuscript could be thought of as a system with two evolutionarily stable states. The addition/removal of predators causes the evolutionary transition from one ESS to another. It is conceivable that the removal of a guppy prey species instead would not cause such drastic changes. Perhaps the lost prey species may over time be replaced by a similar one, by speciation or invasion and the original system be restored. Such a perturbation would hence not cause a transition to another ESS: the community would stay within the evolutionary domain of attraction of the original ESS community and be restored after the perturbation.
There is also a connection between the guppy discussion and the concept of “evolutionary keystones” introduced by Brown and Vincent (1992). In their model, removal of the predator caused evolutionary convergence in the niche positions of their prey, resulting in competitive exclusions. Hence the presence of the predator was key to maintain coexistence among the prey. Similarly, Johansson & Dieckmann studied the removal predator species from a slightly more complex food web of 5 species including two predators. After removal of one of the predators, the original system is restored, but when removing the other triggers evolutionary responses which collapses the food web. In this system there are thus two alternative evolutionary stable states. An evolutionary keystone species can thus be seen as one which if removed causes the system to enter another evolutionary domain of attraction.
For the section of trophic cascades caused by evolutionary change, it might be relevant to cite theoretical work dealing with the issue of evolutionary change in one species causing severe changes in population densities of other species. One model studied by Bronstein et al (2004) considers co-evolutionary extinction cascades in mutualistic networks. Another theoretical study (Georgelin et al 2015) considers plant-pollinator-herbivore communities and shows that evolutionary changes in herbivores triggered by environmental change (pesticide use) may cause extinctions among pollinator species.
These studies are generally based on more minimalistic models than the framework proposed in the present manuscript. Many of them consist of Lotka-Volterra population dynamic models where the interaction coefficients are trait-dependent and selection gradients derived directly from the population dynamic models. Therefore, they cannot make predictions regarding for example population structure. They nevertheless show that many aspects of eco-evolutionary responses to species removal can be studied using relatively simple approaches.
Bronstein, Judith L., Ulf Dieckmann, and Régis Ferrière. "Coevolutionary dynamics and the conservation of mutualisms." (2004).
Brown J. S. & T. L. Vincent. 1992. Organization of predator-prey communities as an evolutionary game. Evolution 46:1269-1283
Georgelin, E et al 2015 Eco-Evolutionary Dynamics of Plant–Insect Communities Facing Disturbances: Implications for Community Maintenance and Agricultural Management. Advances in Ecological Research. 52: 91-114.
Lundberg, Per, E. Ranta, and V. Kaitala. 2000. Species loss leads to community closure." Ecology Letters 3: 465-468.
Johansson, J., & Dieckmann, U. (2009). Evolutionary responses of communities to extinctions. Evolutionary Ecology Research, 561–588.
Paine, R. 1966. Food web complexity and species diversity. Am. Nat. 100: 65-75.
Solé, R.V., Montoya, J.M. and Erwin, D.H. 2002. Recovery after mass extinction: evolutionary assembly in large–scale biosphere dynamics. Philos. T. Roy. Soc. B. 357: 697-707.
Page 4, middle
"Obviously, when a = 0, E(lambdat)=VE."
This is not really obvious from the approximation a = log(lambdat)-VE.
If one linearizes log(lambdat) one gets log(lambdat) approximately equal to lambda_t - 1.
Perhaps I am missing something.
"More generally, in such cases some heritable phenotypes will have long-run stochastic population growth rates that are greater than 0, others will necessarily have rates that are less than zero, but the average long-run stochastic growth rates across competing phenotypes will be 0."
Here you could cite Ripa & Dieckman 2013 who considers evolution in stochastic environments (both for clonal and sexual (diploid) heritance)
Ripa, J., & Dieckmann, U. (2013). Mutant invasions and adaptive dynamics in variable environments. Evolution, 67(5), 1279–1290. http://doi.org/10.1111/evo.12046
"This is most easily achieved by assuming that competing strategies are clonally inherited with (near) perfect fidelity (Metz et al. 1995). For sexually reproducing species this assumption is violated."
With sexually reproducing species it becomes trickier to study evolution of competing strategies. But the adaptive dynamics approach (i.e. Metz et al. 1995) has been extended to sexually reproducing species and can thus be used in this context:
Metz J. A. J. & C. G. F. de Kovel. 2013. The canonical equation of adaptive dynamics for Mendelian diploids and haplo-diploids. Interface Focus 3: 20130025.
See also Ripa & Dieckmann above.
"A third route to large body size is the ability to access resources that may be unavailable to smaller individuals."
Perhaps trees fit in here as well? Evolutionary arms race to access light and suppress competitors. I am just curious.
" Such a process will occur in systems where resources are limiting, where density- and frequency-dependent selection operates, or where coevolution is observed (Roughgarden 1971, Thompson 1999). "
Here is a good place to cite adaptive dynamics papers mentioned above, because most of them considers frequency and density dependent selection.
It would be good with worded titles of the top panels, just like in the bottom panels and the mathematical symbol in the top panel looks odd. What = 1.046?
Perhaps also colour the population dynamics in B with red to get a consistent coloring scheme which can be immediately appreciated from the figure.
Here I think it would be good with some more details about the simulations (for reproducibility). It seems like the original distribution of traits (the z_i:s) are drawn from a normal distribution. How are the offspring generated?
Review on ‘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’ by Coulson T
This manuscript describes the case how structural models can aid in understanding ecological population dynamics and natural selection – particularly Integrative Population Models and Individual Based models. The manuscripts first describes well in detail the components of life-history-fitness linkages and how these may be implemented in a modelling framework. In particular, the author discusses the role of various sources of ‘resource limitation’ in driving fitness and selection. For most parts the manuscript is clear and pleasant read and would be a valuable contribution.
However, the sections (starting page 31) on how to implement these models, left me wanting. I would like to see a discussion how we can better integrate empirical data collection with implementing such models – as it seems that some of the short comings of our ability to use these in natural populations come from lack of right kind of temporal population size, demographic and life-history/trait data, and data on the key limiting resources in any given system. Currently it would seem to be possible to apply such models to a limited number of model systems. I think the field would progress more if we could aim to collect more of relevant long-term data in nature (in addition perhaps to implementing similar data on more controlled but manipulative systems on organisms with sufficiently fast generation times). Would be great if the ‘data needed’ aspect was explicitly covered and the non-modeller readers among us would be advised on what type of data would be useful to collect for increasing inferential power and rigour of such structured models – so that they could be implemented on a wider range of natural systems.
Sometimes the use of references is insufficient, and the manuscript is rather long and could be shortened somewhat – I make some suggestion below to this end. I hope my comments help to improve it further, as I think it would be a useful paper for many evolutionary ecologists.
Specific comments that I hope help to increase readability & value further:
P2: I found the start of the introduction, using the empirical guppy example a bit lengthy – before coming to the main goal of the manuscript. It is nice to illustrate with an empirical case the biological relevance, but I think the first 2 paragraphs could be condensed to essential. Particularly since the guppy example is repeatedly returned to in different places. In fact, it might work best if the guppy system, to the parts relevant to the topic at hand, was described in a separate box – to which one could refer to in the text. (The first 3 lines on page 3 “The guppies….factors that limit the population’s growth” could in fact be moved earlier on, for a sharper start)
P5: As a non-modeller I had to check the word ‘moments’ used in this context. Might be useful (if also empiricists are targeted) to clarify such jargon.
P5: I found the reasoning for the use of clonal versus sexually reproducing species in different aspects a bit confusing. May be useful to explicitly state why in some place clonal reproduction and in other sexual reproduction is assumed (= why is not one or the other used for the different section – or more interestingly both compared).
P6-1st line P7: I would like to see clear mentioning of the caveats of making inferences about historical determinants of selection – else this statement seems rather trivial, at least for within species comparisons.
P7, last 3 lines: The relevance of comparing the scenario of two different equilibria, with both a = 0, is not clear. Perhaps provide empirical example to illustrate this. Neither is it clear why the shift between the two equilibria is expected to last only a few generations. Is there a basis for this?
P13, 2nd paragraph. This paragraph seems to me to be linked to traits that allow adjustments to buffer against environmental variation = phenotypic plasticity in physiology, behaviour, morphology etc. Does this refer to phenotypic plasticity only or are there other forms of traits that allow resilience in face of environmental variation? Or does it not matter for how selection operates whether the ‘resilience increasing’ traits are plastic?
P14, 1st paragraph: I would imagine that in several empirical study systems, it would be possible to compete the different life-history strategies against each other empirically also. Would be useful to state (for those who work on such malleable systems) how this could be empirically directly tested (also to confirm results of simulations). Also, state more explicitly why this assumption is violated for sexually reproducing species and what difference it makes. Can we only test clonally reproducing species? If so, how strong are our inferences?
P14, 2nd paragraph: you mean variation in developmental plasticity / ontogeny? Would be useful to clarify and exemplify.
P15: I think this is a bit thin argument for what we can do (and should do) to build better genotype-phenotype-fitness maps, such as could be achieved by investing G-P maps in more detail and via high throughput phenotyping (e.g. Houle et al. 2010 review on Phenomics) and accounting for gene-phenotype network structure.
P17, 3rd paragraph, line 3: this would seem to me to assume that the food source productivity (e.g. grass or algal production) is stable and does not evolve in response (which in many cases of biotic interactions of herbivory or predator-prey does not hold). How does the scenario change in eco-evolutionary feedbacks where the food source may evolve? Same holds for p 18, 2nd paragraph: failure could also be if assumed that the food does not evolve in response to consumption?
P18-19. I found the heading of ‘Inheritance – genetic and otherwise’ intriguing but the content somewhat disappointingly not covering the recent discussions on non-genetic inheritance. How this matters for our inferences on evolution, for example via cross-generational effects of resource limitation, would be a useful addition. Right now the content covers standard population genetic/quantitative genetic (Va) based inferences. P19: earlier in the text evolution was defined as either allele frequency change or heritable phenotypic change. Here only allele frequency changes are covered primarily and the linkages with different inferences based on heritable phenotypic change could be better covered.
P21, 1st paragraph. The forms of non-genetic inheritance is rather poorly covered here. It would be useful to more explicitly state the main types, as well as how (if) it affects our inferences about ecological and evolutionary processes. The recent book by Bonduriansky and Day on “Extended heredity” could be a useful reference here. And perhaps at least briefly touch on under the structural models section how these could be implemented and what information is needed for us to be able to infer the relevant contribution of different modes of inheritance on direction and magnitude of eco-evo feedbacks.
P22: how does the within species variance (rather than mean distance) affect our inferences and predictions on co-evolution? Also P23: The concept of individual specialization and how it links to eco-evolutionary feedbacks could be better covered here.
P26: I could not quite follow from all that was written earlier, why we now focus on body size – comes abit out of the blue- Of course body size is a key life-history trait and typically a strong fitness determinant, as well as intimately linked to resource mediated selection (via metabolic requirements) – but this could be made more explicit to make clear why body size receives this extended treatment in the manuscript. References for metabolic theory of ecology should be better covered in here.
P27, 2nd paragraph: the island rule comes out of the blue and relevance is not clear for the general goal of the manuscript. Seems to take away attention from the core. In general, I find the body size evolution section in need of streamlining and condensing. It just seems to bring different alternatives for body size evolution and some seem rather peripheral – yet is not explicit enough how this will help us with those structural models…and evolution of life-histories / eco-evo feedbacks in general. Would be good to streamline this and link better to the goal of the manuscript.
P30: In general, unless we are talking of population dynamics (of one focal species or of two interacting species) I am not sure we expect the dynamics to continue ‘ad infinitum’. I think such continuous process takes place under certain assumptions (the same factors feeding back on each other, the continued ability of the target species to evolve etc…).
P30: 2nd paragraph, line 5: It would be perhaps useful to consider the potential for indirect eco-evolutionary feedbacks – that may be much harder to both track. Also, how predictable would we expect such feedbacks to be (i.e. when the ecological selective agent and the phenotype determining fitness may not influence each other directly) ?
P31, 2nd paragraph: I am convinced that we would require significant amounts of data – much more, and much more detailed, than is available for most empirical systems. However, not stating how we could overcome this challenge, seems a bit unsatisfactory. Also, that we are not able to measure eco-evo feedbacks in many systems with currently available data, does not mean that they do not occur in nature. Hence the last statement could be modified to something ‘Although it is empirically difficult to demonstrate eco-evolutionary dynamics in nature, in some cases eco-evo feedbacks have the potential to generate pronounced eco-evo dynamics’. I would like to see a clear definition for eco-evo feedbacks versus eco-evo dynamics, references to empirical work that has been able to show such consequences, as well as suggestions (if possible to make) under which situations we expect eco-evo feedbacks to lead to dynamics. (I think that for the field to advance, we should be more consistent in separating feedbacks and dynamics, although other seems to put all under the umbrella of dynamics.)
P31, ‘Tying strands together’.
- I would have liked to see a lead here to the complexity of the real world (see also Hendry 2019 ‘Critique of eco-evolutionary dynamics’, Functional Ecology Special Issue), the type of data needed to do so, and how making sense/tracking the dynamics can be aided by understanding the processes and models laid out in this manuscript.
- The importance of mating system could be made more explicit and be an interesting part of the discussion in context of eco-evo dynamics
P33: I found the set-up of the paragraphs for the different functions somewhat confusing – yet these components (functions of survival, reproduction, development, inheritance) are really important for predictions of eco-evolutionary feedbacks as well as understanding the models. Would be good to structure the text for clarity (perhaps also numbering the functions by 1,2, 3, 4 would be helpful for the reader, see minor comments below).
As to function 3 (development) – this seems to me reflecting plasticity (including developmental plasticity) of the phenotype. This could be more explicitly stated. In general, I think we need more attention to this component in understanding eco-evolutionary feedbacks (e.g. given that the plastic components of the phenotype can be an important determinant of speed and magnitude of ecological change, and these can change over the course of the ontogeny or life-time of the organisms).
P34. To me the treatment of the inheritance function is rather narrow. Most standard approaches to eco-evo feedbacks only consider additive genetic effects, whereas non-genetic inheritance, or genetically determined parental (typically maternal) effects can strongly affect evolutionary speed and direction – and on the same token, we would expect also effects on eco-evo feedbacks. Any detailed treatment to this end is not needed for the current manuscript, but I think it would be useful to make the point explicit that these other forms of cross-generational effects may alter the scenarios based on additive genetic inheritance.
P35-36: 2nd paragraph. As noted in my general comment above, it would be useful to state what we (empiricists) need to do to be able to use these models – more explicitly state the type of data needed. Which ecologically relevant eco-evo model systems are possibly suitable for this? I find the long list of different models conducted a bit too abstract to be useful – it does illustrate the many different aspects, but perhaps would work better as an overview table? Can we say something more about when each type of model is best used or how they can be integrated - to create that ‘single model’ that captures better the organization of the different components influencing eco-evo processes? Do we not need the data that allows building the details of these models?
P38, 1st paragraph. Saying that such models are ‘frequently not analytically tractable’ begs the question of what should we do then? Can we overcome this? Or what do we do with the models at all if they are not tractable?? Perhaps the last paragraph – using models that do not have to capture all feedbacks, but still can be informative about core processes, is meant to be one solution. Which is fine, but could be better stated.
P39. ‘What can we say without models’ section was rather uninformative. It basically seems to present what empiricists can do by hard work and conducting a lot of well-designed field studies and experimental manipulations. What I would like to see is how we best can take the power of both worlds, integrating the models with empirical work to inform each approach of the best way to tackle the core questions at hand (e.g. which life-stage is the most important in mediating eco-evo feedbacks, how does sexual selection influence eco-evo feedbacks in contrasting ecological environments, which species interactions in a foodweb are likely to result in eco-evo-dynamics, how does the mode of inheritance influence direction an magnitude of eco-evo feedbacks, etc etc).
the case of the guppy. Is the most interesting question to be addressed really ‘why low predation environments result in parallel evolution of phenotypes’? Wouldn’t the simple answer be there is parallel divergent selection (loss of predators’? Wouldn’t it be more interesting to understand HOW this parallel selection operates (the eco-to-evo pathway in the feedbacks) and how do these parallel phenotypic changes influence eco-evo feedbacks ? Again, some of this text is rather repetitive and adding a box with the guppy system as an example case would help making just the case of relevant points without the need to repeat the text in other places of the manuscript.
Although the emu case (I assume the start was not an e-mail chick, Page 39, 2nd paragraph… ..) is somewhat entertaining as a heuristic thought exercise, I did not find the 1.5 page description necessary nor informative for our understanding.
Minor (RWD= reword):
At several places it seems original work is not well referenced (statements made without reference) – I indicate those below.
P6, 1st paragraph, 5th line – RWD to ‘increasing survivorship or fertility at any age…’
P6, line 6: provide the reference for the case of Elk in Yellowstone
P7, line 4: State explicitly that this refers to guppies experiencing high predation environments. (Note that this is an example case were it would work perhaps better to have the guppy system presented in a separate box). Same unclarity holds for P8, 2nd paragraph (guppy example). This refers to the case of guppies inhabiting low predation environments?
P7, line 5: RWD to ‘Many of the phenotypic…’
P7, line 19. This statement about ‘prior to removal of predators’ is confusing. Does this refer to an empirical case study with experimental removal?
P9, Line 2: allow who to survive? Check wording of this sentence for clarity.
P9, 1st paragraph, last 3 lines. It would be helpful for the naïve empirist to have a reference for selection differentials and need to understand patterns of inheritance already here (I am not that naïve reader, but I think this may be useful for others that may not be familiar with evolutionary inferences – but still may work on relevant empirical study systems).
P9, 3rd paragraph, line 7: RWD to …’ result in selection on phenotypic traits associated with detection, ….’
P9, 3rd paragraph, line 9: I think we can not assume that any population ‘will’ adapt – without making further assumption about trait heritability and lack of evolutionary constraints. RWD to something like ‘Given sufficient time, and that assumption underlying evolutionary responses (e.g. that traits are heritable), the population may adapt and express adaptive traits …’ (Else sounds rather deterministic).
P11, line 4: clarify that this means the mean fitness of the population.
P11, line 6 RWD to ‘ consequence of this is that the…’
P11, 2nd paragraph, line 6: RWD to ‘ non-zero selection differential…’
P11, last paragraph: This hole nesting bird sentence is unclear and confusing. RWD.
P12. State at first mention what the beta’s refer to (beta0 and beta1).
P12, lines 1-4: I found these sentences unclear. Why do we expect this and how is this evolutionary suicide manifested in this case ? L 3: RWD to ‘…, evolution will favour fewer, larger individuals…’. Again saying that ‘evolution will result’ sounds too deterministic.
P13: It was not clear to me what the first alternative of evolution was. RWD perhaps to ‘I now consider how evolution can proceed by reducing VE’.
P13, last paragraph: Not clear why ploidy of species matters. State more explicitly.
P16, 2nd paragraph: State for the non-expert reader what the breeding value is – or at least provide reference.
P16, 2nd paragraph, line 4-5: RWD the last sentence of gene expression and how environment can affect gene expression. (e.g. what are the ‘environmental drivers? Also sentence structure unclear). In general, this section against seems to relate to phenotypic plasticity (via gene expression) yet this link is poorly made.
P17, 2nd paragraph, line 1: you mean developmentally plastic traits – or traits that are expressed at maturity or that are impacted by senescence ? RWD.
P17, 2nd paragraph, line 10: RWD to ‘…they will have large values…’
P18, 3rd paragraph, line 4: RWD to ‘ … is that there is little competition…’
P18, 3rd paragraph, line 2: provide references for these statements about how artificial selection operates, as well as for line 7 on quantitative genetic covariances, and for evidence for these methods working well in absence of the covariances.
P20, 3rd paragraph
line 2: RWD to ‘ base pair substitutions…’, line 3: RWD to insertions..’
line 6: unclear what is meant by ‘such’ genes. Clarify.
Line 8: provide reference for this insight on mutations
P20. It would be useful to be more specific here as to which definition of epigenetic inheritance is referred to here (the narrow definition of methylation etc alteration or wider parental effects).
P21, 2nd paragraph: It would be useful for those not accustomed to think of eco-evo feedbacks to explicitly state that an important difference these biotic resources make (as opposed to non-biotic) is that they can evolve in return.
P21, last paragraph. Provide reference for interaction coefficients capturing functional responses and conversion rates.
P22, 2nd paragraph: ‘However’ seems redundant here. Remove.
P24: It would be useful to have the subheading f ‘Trophic cascades’ here. Line 4, provide reference and definition or empirical example of trophic cascades. Last 2 lines on this page could be moved after the 1st full paragraph for easier reading.
P25, 2nd paragraph. This is to me generally a very unclear paragraph. For instance, does it mean evolution of any other species altered the dominant causes (and hence selection) of death and successful reproduction in a dominant species – or rather the evolution of the dominant species itself – or either ? RWD for clarity. RWD to ‘In such a case, the dominant species was unable…’. Also, what is meant by dominant species? Dominant in numbers? Dominant in role in ecosystem (aka keystone species)?
P25, 3rd paragraph: Again I think it would be easier to make these arguments more streamlined if the guppy case would be overviewed in a separate box.
P26, 2nd paragraph
- 3rd line: Provide reference for ‘relative metabolic rate’
- 4th line: RWD to …’than those that are smaller ‘
- Why is it key that the exponent is less than unity – for the current discussion?
P27, 2nd paragraph
- line 6: RWD to ‘For example, food-limited populations of…’
P29, Eco-Evolutionary feedbacks
- Is the reason that compelling empirical evidence is missing for eco-evo feedbacks that they are poorly defined or that they are difficult to demonstrate? I would rather think the reason is the latter (though I also agree that they are often poorly defined).
- Here again the contrast in definitions earlier on in the manuscript for evolution defined as change in allele frequencies or heritable phenotypic change. The allele frequency change is the narrowest sense, but given the increased realization that non-genetic (at least non-DNA sequence change) inheritance mechanisms appear common, I would consider these other alternatives. Especially since for ecological relevance of the eco-evo feedbacks any transgenerational effects can be important.
- Line 4: RWD to ‘…is frequently defined as the dynamics of populations, communities,…’. Or otherwise give a clearer definition (rather than how they are measured). Also: provide reference for the definitions. Line 5-6 ‘If we stick with this definition…’ seems redundant, delete.
- Line 8: I think we need the mediating effect of the phenotype for allele frequency change to have any eco-evo feedbacks.
- 2nd paragraph, line 2: you mean constant positive trait-fitness association ? I guess we would not expect exponential growth of the population if the association was negative.
- 2nd paragraph – It would be easier to follow this argumentation (biological relevance) if here the reader was reminded of what the denominator and numerator of the selection differential equation represents.
P30, 1st paragraph: The sentence on line 2-3 (‘What all this means…’) seems repetitive to what as said in the previous paragraph.
P30, 3rd paragraph. What type of ‘parameters’ do the beta’s present? Slope of relationships? Any?
P31, 1st paragraph, line 4. RWD to ‘increasingly’
P32. Would be useful to have a subheading ‘Modelling eco-evolutionary feedbacks’ –before going into the models.
P32, 3rd paragraph, line 5: I don’t understand what this really means ‘…the number of individuals within a population with each combination of components of the phenotype’ ? Be more explicit.
If these models are to be generally usable, perhaps refer to statistical packages that are available for users (if there are such)?
P33, line 3: which two functions? Which other functions? This becomes clear below but these can be tied together and made easier to read if ‘two functions (i.e. survival and reproduction) and two other (i.e. development and inheritance)...’)
P38, 1st paragraph, linen10: The sentence of ‘…have spurred on the modelling approaches I have been involved in developing’ is not very informative and can be deleted. The manuscript is lengthy as it is.
P40, last paragraph, line 8: RWD to ‘…which phenotypic trait will evolve ‘ (or which phenotype will evolve?)
P41, 2nd paragraph. Provide references for presumed predation pressure on ground feeding birds. Is the idea that emus lost the ability to fly prior to predation becoming a significant source of mortality based on phylogenetic or historical inferences or some such (in which case references would be appropriate) or only speculation ? In general, I find this emu section rather speculative and also uninformative. In particular the last paragraph could be completely be left out.
Last sentence of conclusion. I do think that the next step would be conduct studies in different populations where the limiting factor differs – or has changed recently so predictions can be made and eco-evolutionary (or ecological and evolutionary) dynamics observed. But it seems to me we generally require more data and, in particular, be able to identify the key limiting factor (which may require substantial data in most system) – to then test whether the framework proposed in this manuscript helps us to make more accurate predictions.