A population biological modeling approach for life history and body size evolution
Density dependent environments can select for extremes of body size
Recommendation: posted 13 August 2022, validated 24 August 2022
Body size evolution is a central theme in evolutionary biology. Particularly the question of when and how smaller body sizes can evolve continues to interest evolutionary ecologists, because most life history models, and the empirical evidence, document that large body size is favoured by natural and sexual selection in most (even small) organisms and environments at most times. How, then, can such a large range of body size and life history syndromes evolve and coexist in nature?
The paper by Coulson et al. lifts this question to the level of the population, a relatively novel approach using so-called integral projection (simulation) models (IPMs) (as opposed to individual-based or game theoretical models). As is well outlined by (anonymous) Reviewer 1, and following earlier papers spearheading this approach in other life history contexts, the authors use the well-known carrying capacity (K) of population biology as the ultimate fitness parameter to be maximized or optimized (rather than body size per se), to ultimately identify factors and conditions promoting the evolution of extreme body sizes in nature. They vary (individual or population) size-structured growth trajectories to observe age and size at maturity, surivorship and fecundity/fertility schedules upon evaluating K (see their Fig. 1). Importantly, trade-offs are introduced via density-dependence, either for adult reproduction or for juvenile survival, in two (of several conceivable) basic scenarios (see their Table 2). All other relevant standard life history variables (see their Table 1) are assumed density-independent, held constant or zero (as e.g. the heritability of body size).
The authors obtain evidence for disruptive selection on body size in both scenarios, with small size and a fast life history evolving below a threshold size at maturity (at the lowest K) and large size and a slow life history beyond this threshold (see their Fig. 2). Which strategy wins ultimately depends on the fitness benefits of delaying sexual maturity (at larger size and longer lifespan) at the adult stage relative to the preceeding juvenile mortality costs, in agreement with classic life history theory (Roff 1992, Stearns 1992). The modeling approach can be altered and refined to be applied to other key life history parameters and environments. These results can ultimately explain the evolution of smaller body sizes from large body sizes, or vice versa, and their corresponding life history syndromes, depending on the precise environmental circumstances.
All reviewers agreed that the approach taken is technically sound (as far as it could be evaluated), and that the results are interesting and worthy of publication. In a first round of reviews various clarifications of the manuscript were suggested by the reviewers. The new version was substantially changed by the authors in response, to the extent that it now is a quite different but much clearer paper with a clear message palatable for the general reader. The writing is now to the point, the paper's focus becomes clear in the Introduction, Methods & Results are much less technical, the Figures illustrative, and the descriptions and interpretations in the Discussion are easy to follow.
In general any reader may of course question the choice and realism of the scenarios and underlying assumptions chosen by the authors for simplicity and clarity, for instance no heritability of body size and no cost of reproduction (other than mortality). But this is always the case in modeling work, and the authors acknowledge and in fact suggest concrete extensions and expansions of their approach in the Discussion.
Coulson T., Felmy A., Potter T., Passoni G., Montgomery R.A., Gaillard J.-M., Hudson P.J., Travis J., Bassar R.D., Tuljapurkar S., Marshall D.J., Clegg S.M. (2022) Density-dependent environments can select for extremes of body size. bioRxiv, 2022.02.17.480952, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.17.480952
Wolf Blanckenhorn (2022) A population biological modeling approach for life history and body size evolution. Peer Community in Evolutionary Biology, 100146. https://doi.org/10.24072/pci.evolbiol.100146
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.02.17.480952
Author's Reply, 22 Jul 2022
Decision by Wolf Blanckenhorn, posted 18 May 2022
Body size evolution is a central theme in evolutionary Biology. Particularly the question of when and how smaller body sizes can evolve is of continuing interest within the field evolutionary ecology, because most life history models, and the empirical evidence, document that large body size is favoured by natural and sexual selection in most organisms and environments at most times.
The paper by Coulson et al. lifts this question to the level of the population, a novel approach, by using so-called integrated projection models (IPMs). As well outlined by (anonymous) Reviewer 1, the authors assume the well-known carrying capacity (K) of population biology as the fitness parameter to be maximized (rather than body size per se), and observe density-dependent (as well as density-independent), size-structured population growth trajectories in terms of age and size at maturity (including also other standard life history traits). Importantly and interestingly, life-history trade-offs are not assumed, as happens frequently in life history models, but emerge as a property from the modelling approach taken here. The authors find that often large body size indeed evolves, but under some (not overly rare) parameter combinations small size can also evolve, while yet other combinations lead to disruptive selection on body size. These results may ultimately explain the evolution of smaller body sizes from large body sizes at least under some environmental circumstances (despite common selection favouring larger individual body sizes).
All reviewers agree that the approach taken seems technically sound (as far as it can be evaluated), and that the results are interesting and worthy of publication after some revision. Nevertheless, at various places clarification and justification of e.g. some assumptions need to be provided as suggested by the reviewers.
Criticism centers on the often too technical descriptions of the model and its assumptions, especially if the targeted readership are general evolutionary ecologists. This should be changed in a revision of the manuscript, and especially reviewers 1 & 2 have made multiple concrete suggestions. One solution is to write the entire manuscript for a more general audience, and to relegate some of the more technical descriptions and justifications for the modelling specialists to an appendix (or the Methods).
In general, and related to the previous criticism of being to technical in writing, the precise focus of the paper needs clarification in the Introduction (again referring to reviewer 1s & 2s comments).
Reviewer 2 additionally points out the necessity of connecting the action of natural selection, in terms of mechanistic selection coefficients, to this overall phenomenological approach. This would help reconcile any differences in the results between this type of population biological model and the more traditional life history models.
Finally, all reviewers made some more specific, minor suggestions on how to improve the paper even further that should be addressed in a revision.
I am looking forward to seeing a revised version of this manuscript in light of the reviewer comments.
Wolf Blanckenhorn, University of Zürich