Life-history evolution under a production constraint

Abstract

The recently formulated metabolic theory of ecology has profound implications for the evolution of life histories. Metabolic rate constrains the scaling of production with body mass, so that larger organisms have lower rates of production on a mass-specific basis than smaller ones. Here, we explore the implications of this constraint for life-history evolution. We show that for a range of very simple life histories, Darwinian fitness is equal to birth rate minus death rate. So, natural selection maximizes birth and production rates and minimizes death rates. This implies that decreased body size will generally be favored because it increases production, so long as mortality is unaffected. Alternatively, increased body size will be favored only if it decreases mortality or enhances reproductive success sufficiently to override the preexisting production constraint. Adaptations that may favor evolution of larger size include niche shifts that decrease mortality by escaping predation or that increase fecundity by exploiting new abundant food sources. These principles can be generalized to better understand the intimate relationship between the genetic currency of evolution and the metabolic currency of ecology.allometry ͉ life-history theory ͉ metabolic ecology T he recently formulated metabolic theory of ecology (1) predicts that many attributes of individuals, populations, communities, and ecosystems should be relatively straightforward consequences of the metabolic processes of the relevant organisms. Specifically, many rate processes should scale with body size and temperature in the same way as mass-specific metabolic rate:where R is the rate of some biological process, R 0 is a normalization constant, the M Ϫ1/4 term gives the power-function dependence on body mass M, and the e ϪE/kT term or Boltzmann factor gives the exponential temperature dependence in terms of an ''activation energy'', E, Boltzmann's constant, k, and temperature, T, in Kelvin. This very general relationship holds both within and between species. It can be applied to the rate of production of biomass per unit mass, which is predicted to scale as M Ϫ1/4 (e.g., refs. 2-4). If we ignore temperature or assume for the moment that it does not vary, the Boltzmann factor is a constant. Then, taking logarithms of Eq. 1 we have log (mass-specific production rate) log (body mass). [2]This prediction appears to be generally supported, although for some traits, the empirically measured scaling exponents appear to deviate from the predicted Ϫ1͞4, sometimes being closer to Ϫ1͞3 (e.g., ref. 5). For our argument here, however, the exact value of the exponent is not an issue; what is important is that it is negative. The consequence of the negative exponent is that in a log-log plot, mass-specific production rate is a declining straight-line function of body mass, as shown schematically by the solid black line in Fig. 2 A. We take this to be a fundamental causal constraint limiting life-history options as suggested by metabolic theory. The result is that sm...

Metabolic rate links density to demography in Tetrahymena pyriformis

“…The relationship was linear, which is consistent with Fenchel and Finlay's (1983) observation that production is linearly related to metabolic rate in protists. As expected, as metabolism fuels production (Brown and Sibly, 2006), individuals had the highest metabolic rates and highest division rates at low densities. Our estimated death rate function indicated that deaths were negligible until metabolic rates were highly suppressed (Figure 3).…”

“…From the point of view of population regulation, variation in resource supply should lead to altered metabolic rates and changes in the allocation of energy and resources to growth, reproduction or survival, driving changes in population growth rate (Tonn et al, 1994;Lewis et al, 2001;Schmoker and Hernandez-Leon, 2003;Forrester et al, 2006). As metabolism fuels production (Brown and Sibly, 2006), a reduction in metabolic rate should decrease the rate at which offspring can be produced. Similarly, survival should be enhanced when metabolism can be allocated to cell maintenance or other defense mechanisms, such as avoidance of predation.…”

The natural selection of metabolism and mass selects lifeforms from viruses to multicellular animals

“…The differential of the profile ($\mathit{\partial }{r}_i/\mathit{\partial }{w}_{ifalse|w_i=w}=1/w-c$) at the limit of the average variant ( w ) is the selection gradient (Figure 1b) that describes selection as a function of the average body mass. And the evolutionary equilibrium ($w^{\ast \ast }=1/c$) is the optimum of the selection integral [$\int \left(\mathrm{italic\partial }{r}_{i}false/\mathrm{italic\partial }{w}_{i|w_i=w}\right)\mathrm{d}w$; Figure 1c] that integrates the selection gradient across the potential evolution in the average mass of the population.The more recent approach of metabolic ecology (Brown & Sibly, 2006) assumes, somewhat contrary to evidence, that the variation in the intraspecific birth rate ($b_i\propto w_i^{-1/4}$) follows the interspecific allometry for biotic periods, with an intraspecific birth rate that declines with mass instead of increasing as often observed. Large species may then evolve by a survival rate that increases with mass.…”

“…The more recent approach of metabolic ecology (Brown & Sibly, 2006) assumes, somewhat contrary to evidence, that the variation in the intraspecific birth rate ($b_i\propto w_i^{-1/4}$) follows the interspecific allometry for biotic periods, with an intraspecific birth rate that declines with mass instead of increasing as often observed. Large species may then evolve by a survival rate that increases with mass.…”

Why Is Living Fast Dangerous? Disentangling the Roles of Resistance and Tolerance of Disease

“…Compared to large-bodied animals, small-bodied animals often have shorter life spans and lower antibodybased adaptive immunity but greater metabolic, developmental, and reproduction rates (Sheldon and Verhulst 1996;Ricklefs and Wikelski 2002;Brown et al 2004;Brown and Sibly 2006;Lee 2006;Lee et al 2008;Johnson et al 2012). Plants fall along a similar continuum based on traits of their leaves (Reich 2001;Enquist et al 2007;Cronin et al 2010b).…”