Organisms vary widely in size from microbes weighing 0.1 picograms to trees weighing thousands of megagrams, a 10 21-fold range similar to the difference in mass between an elephant and the Earth. Mass has a pervasive influence on biological processes but the effect is usually non-proportional; for example, a 10-fold increase in mass is typically accompanied by just a 4-to-7-fold increase in metabolic rate. Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns. We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds, and mammals. We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.
Summary1. Environmental variability and perturbations can influence population persistence. It is therefore important to understand whether and how animals can compensate for environmental variability and thereby increase resilience of natural populations. Evolutionary theory predicts that in fluctuating environments, selection should favour developmental modifiers that reduce phenotypic expression of genetic variation. The expected result is that phenotypes are buffered from environmental variation across generations. 2. Our aim was to determine whether phenotypes of mosquitofish (Gambusia holbrooki) remain stable across generations in which individuals were born into different thermal environments. We predicted that the spring generation (cool environment) would acclimate by increasing the concentration of regulatory transcription factor mRNA and activities of rate-limiting enzymes (hierarchical regulation) to compensate for the negative thermodynamic effects of lower temperatures on metabolic and locomotor performance. In contrast, the summer-born generation (warm environment) would show less capacity for acclimation and hierarchical regulation. 3. We show that fish from both generations acclimated, but that there were significant differences in the phenotypic consequences of acclimation. The overall result was that burst performance, metabolic scope, and the activities of cytochrome c oxidase and lactate dehydrogenase were buffered from environmental change and did not differ between spring and summer fish at their natural water temperatures of 15°C and 25°C, respectively. However, there were differences between generations in sustained swimming performance and citrate synthase activity. 4. We used metabolic control analysis to show that modes of regulation of metabolic scope and locomotor performance differed between generations. Spring-born fish relied to a greater extent on rate-limiting enzymes and transcriptional regulator (PGC-1a and b) mRNA concentrations than summer-born fish. 5. We suggest that developmental modifiers are favoured in fluctuating environments to maximize phenotypic fitness of each generation. We show that the interaction between developmental and reversible acclimation can increase the resilience of physiological performance in a natural population to climate variation.
Anthropogenic climate change and invasive species are two of the greatest threats to biodiversity, affecting the survival, fitness and distribution of many species around the globe. Invasive species are often expected to have broad thermal tolerances, be highly plastic, or have high adaptive potential when faced with novel environments. Tropical island ectotherms are expected to be vulnerable to climate change as they often have narrow thermal tolerances and limited plasticity. In Fiji, only one species of endemic bee, Homalictus fijiensis, is commonly found in the lowland regions, but two invasive bee species, Braunsapis puangensis and Ceratina dentipes, have recently been introduced to Fiji. These introduced species pollinate invasive plants and might compete with H. fijiensis and other native pollinators for resources. To test whether certain performance traits promote invasiveness of some species, and to determine which species are the most vulnerable to climate change, we compared the thermal tolerance, desiccation resistance, metabolic rate, and seasonal performance adjustments of endemic and invasive bees in Fiji. The two invasive species tended to be more resistant to thermal and desiccation stress than H. fijiensis, while H. fijiensis had greater capacity to adjust their CTMAX with season, and H. fijiensis females tended to have higher metabolic rates, than B. puangensis females. These findings provide mixed support for current hypotheses for the functional basis of the success of invasive species, however, we expect the invasive bees in Fiji to be more resilient to climate change due to their increased thermal tolerance and desiccation resistance.
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