Metabolism, Growth, and the Energetic Definition of Fitness: A Quantitative Genetic Study in the Land SnailCornu aspersum

Abstract

Life-history evolution-the way organisms allocate time and energy to reproduction, survival, and growth-is a central question in evolutionary biology. One of its main tenets, the allocation principle, predicts that selection will reduce energy costs of maintenance in order to divert energy to survival and reproduction. The empirical support for this principle is the existence of a negative relationship between fitness and metabolic rate, which has been observed in some ectotherms. In juvenile animals, a key function affecting fitness is growth rate, since fast growers will reproduce sooner and maximize survival. In principle, design constraints dictate that growth rate cannot be reduced without affecting maintenance costs. Hence, it is predicted that juveniles will show a positive relationship between fitness (growth rate) and metabolic rate, contrarily to what has been observed in adults. Here we explored this problem using land snails (Cornu aspersum). We estimated the additive genetic variance-covariance matrix for growth and standard metabolic rate (SMR; rate of CO2 production) using 34 half-sibling families. We measured eggs, hatchlings, and juveniles in 208 offspring that were isolated right after egg laying (i.e., minimizing maternal and common environmental variance). Surprisingly, our results showed that additive genetic effects (narrow-sense heritabilities, h(2)) and additive genetic correlations (rG) were small and nonsignificant. However, the nonadditive proportion of phenotypic variances and correlations (rC) were unexpectedly large and significant. In fact, nonadditive genetic effects were positive for growth rate and SMR ([Formula: see text]; [Formula: see text]), supporting the idea that fitness (growth rate) cannot be maximized without incurring maintenance costs. Large nonadditive genetic variances could result as a consequence of selection eroding the additive genetic component, which suggests that past selection could have produced nonadditive genetic correlation. It is predicted that this correlation is reduced when adulthood is attained and selection starts to promote the reduction in metabolic rate.

Energy demand and the context-dependent effects of genetic interactions underlying metabolism

“…Genetic variants that compromises energy supply-via nutrient acquisition, storage, or conversion to ATP-may then manifest as phenotypic effects on performance and fitness under conditions where demand is high, but be masked under conditions where supplies are in excess of lower demands. The contextdependent genotype-phenotype relationships that we describe exemplify how energy allocation principles and design constraints can generate complicated environment-dependence, potentially confounding attempts to define fitness in energetic terms (e.g., Bruning et al 2013). Yet, many components of fitness are expected to depend on the pathways of metabolism, and the variable phenotypic expression of mutations in these pathways presents a dynamic and perhaps challenging context for both purifying and adaptive selection, as context-dependent mutational effects only experience selection in a fraction of possible environments (Van Dyken and Wade 2010).…”

The quantitative genetics of physiological and morphological traits in an invasive terrestrial snail: additive vs. non‐additive genetic variation

“…; Bruning et al . ). Given this, it would be reasonable to conclude that Chilean populations are special, being perhaps the result of a particular founder effect; that is, initial colonization might have occurred by a small number of individuals with little genetic variance.…”

Energy expenditure and body size are targets of natural selection across a wide geographic range, in a terrestrial invertebrate

“…On the other hand, the many versions of metabolic rate measurements such as standard metabolic rate, resting metabolic rate and maximum metabolic rate (see Lighton ) have been related to body size with different scaling exponents (Lehmann, Dickinson & Staunton ; Glazier ; Clarke, Rothery & Isaac ; Bruning et al . ). This reflects the fact that more tissue represents more energy consumption, a relationship that varies depending on the tissue involved, the organism and the environment.…”

“…It is interesting to note that C. aspersum snails appear to follow this pattern (Diego Gaitan‐Espitia & Nespolo ), which is corroborated with our results, as higher GRs, body sizes and SMR R (late in the season) were promoted in the south (Bruning et al . ; Nespolo et al . ).…”

“…; Naya, Bozinovic & Karasov ; Bruning et al . ). However, these are context‐dependent processes that depend on a number of factors that vary across the geographic range of species (see below).…”