Density dependent environments can select for extremes of body size

Abstract

Body size variation is an enigma. We do not understand why species achieve the sizes they do, and this means we also do not understand the circumstances under which gigantism or dwarfism is selected. We develop size-structured integral projection models to explore evolution of body size and life history speed. We make few assumptions and keep models simple: all functions remain constant across models except for the one that describes development of body size with age. We set sexual maturity to occur when size attains 80% of the asymptotic size, which is typical of a large mammal, and allow negative density dependence to only affect either reproduction or juvenile survival. Fitness -the quantity that is maximized by adaptive evolution -is carrying capacity in our models, and we are consequently interested in how it changes with size at sexual maturity, and how this association varies with development rate. The simple models generate complex dynamics while providing insight into the circumstances when extremes of body size evolve. The direction of selection leading to either gigantism or dwarfism crucially depends on the proportion of the population that is sexually mature, which in turn depends on how the development function determines the survivorship schedule. The developmental trajectories consequently interact with size-specific survival or reproductive rates to determine the best life history and the optimal body size emerges from that interaction. These dynamics result in trade-offs between different components of the life history, with the form of the trade-off that emerges depending upon where in the life history density dependence operates most strongly. Empirical application of the approach we develop has potential to help explain the enigma of body size variation across the tree of life.

Density-Dependent Selection

“…Density-dependent selection has certainly not been neglected. Recent theoretical work has offered new insights (Lande et al 2009, Engen et al 2020, Coulson et al 2022, and recent work in natural populations has demonstrated density-dependent selection for life-history traits (Saether et al 2016, Reznick et al 2019, Kentie et al 2020, color morphs (Kvalnes et al 2022), and phenotypic plasticity (Donohue et al 2000). Our argument is that density-dependent selection demands even more investigation.…”

“…It also prompted a renewed focus on understanding the mechanisms of density dependence. On the theoretical side, this meant building demographic models of births and deaths in limiting environments (Charlesworth 1994, Lande et al 2009, de Roos 2021, Coulson et al 2022. These models led to a renewed interest in density-dependent selection, the driver of adaptation to a limiting environment.…”

Evolving to stay the same: life history evolution and tradeoffs in response to high and low total food

“…Such a scenario could be tested for using reciprocal transplant experiments, where we would expect that high‐food lineages should underperform relative to low‐food lineages in a low‐food environment. Alternatively, adult size and early reproduction may tradeoff independently of longevity, mediated by the benefits of larger size at sexual maturity for adults against the costs of delayed maturity for juveniles (Coulson et al 2022). That is, delayed reproduction in low‐food lineages may have some mitigating effect such that fitness would have been lower if maturation happened earlier at the expense of adult size or condition.…”

“…Life histories evolve as a function of when and how selection acts on the life cycle (Stearns 1992). A venerable line of theory has explored the role of food as an agent of selection in life history evolution, from classic r/K and competitive‐stress tolerant‐ruderal (C‐S‐R) life history strategies (Pianka 1970, Grime 1974) to contemporary demographic models (Parker and Begon 1986, Winemiller and Rose 1993, Day and Rowe 2002, Coulson et al 2022). Older models such as r/K selection emphasised the role of per capita (or relative) food abundance in life history evolution, while the effects of total (at the population‐level) food abundance have received limited theoretical attention (Grether et al 2001, Reznick et al 2002).…”

“…Unlike common depictions of simple spectra (such as r/K), life history tradeoffs along food gradients can be complex and non-uniform (Felmy et al 2022). IPMs can also identify such nuances, for example by perturbing trait values and evaluating which life history components show the highest sensitivities of fitness (Coulson et al 2022). Using these tools, we dig deeper into previous work in copepods (Blake and Marshall 2023) to obtain a fuller picture of life history tradeoffs under different food regimes across the whole life cycle.…”