Physiological dynamics, reproduction-maintenance allocations, and life history evolution

Abstract

Allocation of resources to competing processes of growth, maintenance, or reproduction is arguably a key process driving the physiology of life history trade-offs and has been shown to affect immune defenses, the evolution of aging, and the evolutionary ecology of offspring quality. Here, we develop a framework to investigate the evolutionary consequences of physiological dynamics by developing theory linking reproductive cell dynamics and components of fitness associated with costly resource allocation decisions to broader life history consequences. We scale these reproductive cell allocation decisions to population-level survival and fecundity using a life history approach and explore the effects of investment in reproduction or tissue-specific repair (somatic or reproductive) on the force of selection, reproductive effort, and resource allocation decisions. At the cellular level, we show that investment in protecting reproductive cells increases fitness when reproductive cell maturation rate is high or reproductive cell death is high. At the population level, life history fitness measures show that cellular protection increases reproductive value by differential investment in somatic or reproductive cells and the optimal allocation of resources to reproduction is moulded by this level of investment. Our model provides a framework to understand the evolutionary consequences of physiological processes underlying trade-offs and highlights the insights to be gained from considering fitness at multiple levels, from cell dynamics through to population growth.

Keywords: Euler–Lotka; force of selection; levels of fitness; reproductive value; theoretical evolutionary ecology.

Figure 1

Model formulation. Schematic outline of (A) the general framework for the life history model. Resources are allocated to somatic or reproductive cells, somatic cells produce defenses that protect somatic, or precursor reproductive cells. (B) Dynamics of reproductive cell maturation from precursor to functional cells

Figure 2

Effects of cell mortality, maturation rate, and defense investment on reproductive cell fitness. Fitness ($\lambda$) is expressed in terms of maturation rate (${\gamma }_0$) and investment in precursor cell protection ($b$) for different levels of precursor cell death rate (${\mu }_0$). (A) Under low cell death rates (${\mu }_0=0.01$) investment in defense has positive fitness benefits when reproductive cell precursor maturation rate is low. (B) When cell death rate is high (${\mu }_0=0.1$) high investment in protection increases fitness across a range of maturation rates. [Other parameters: $R=100$, $q=0.5$]

Figure 3

Effects of investment in protecting somatic and/or precursor reproductive cells on reproductive value in (A–B) increasing ($r=1.1$) or (C–D) decreasing ($r=-1.1$) populations under different rates of reproductive cell maturation (slow maturation: panels A,C ${\gamma }_0=0.75$; high maturation: panels B,D ${\gamma }_0=2.0$). Lines represent different allocation strategies: (red line: low $a=0.1$, high $b=0.9$. green line: high $a=0.9$, low $b=0.1$. blue line: low $a=0.1$, low $b=0.1$) [Other parameters: $q=0.5$, ${\mu }_0=0.1$, ${\mu }_n=0.1$, $\psi =1.0$]

Figure 4

Lifetime fitness as a function of resource allocation ($q$) to cellular protection and maintenance for different allocations to protecting somatic cells ($a$) and reproductive cells ($b$) [$a=b$ (red line); $a>b$ (yellow line); $a<b$ (orange line)] under different resource use functions as the organism ages [(A–C) linear decline in resources, (D–F) accelerating (exponential) decline in resources, (G‐I) decelerating (1‐/exp(‐x)) decline in resources] and physiological demand increase [A,D,G: 1 ‐ (a + b) = 0; B,E,H: 1 ‐ (a + b) = 0.2; C,F,I: 1 ‐ (a + b) = 0.4]. Increasing physiological demand constrains fitness and leads to nonextreme fitness values [Other parameters ${\gamma }_0=0.1$, $\psi =0.01$, ${\mu }_0=0.1$, ${\mu }_n=0.1$]