On the evolutionary physiology of metabolic allometry

Julian Edward Beaman

Bachelor Arts & Sciences (Honours I)

A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2019 School of Biological Sciences

Abstract

All organisms rely on metabolism – a complex system of biochemical reactions that either release or absorb energy – to sustain life. Organisms expend energy to develop, grow, survive and reproduce. The total energy expenditure of an , as indicated by their metabolic rate, increases as organisms get larger. Metabolic rate, however, scales disproportionately (allometrically) with body mass, such that – on a gram for gram basis – smaller organisms have a higher mass-specific metabolic rate than larger organisms. This observation has puzzled biologists for over 150 years, but progress has been made in the past few decades in explaining the origin and maintenance of metabolic allometry. The scaling relationship between mass and metabolic rate can be observed at different levels of biological organisation including over development (ontogenetic scaling), among individuals of the same developmental stage (static scaling), and among species (interspecific scaling). Importantly, there is variation in the scaling relationship between and within each of these levels and this variation has implications for the way energy flows through organisms and ecosystems, as described by metabolic theories of ecology, and for the evolution of metabolic rate and body size across the tree of life. Existing hypotheses for the variation in metabolic scaling revolve around the idea that there are universal physical constraints on the transport of metabolic inputs and outputs through circulatory networks and across tissue surfaces. The contention is that these physical constraints are quantitative rather than absolute allowing individual and species-level peculiarities of physiology and ecology to generate small deviations around the average pattern. Phenotypic and environmental sources of variation in metabolic scaling are thought to derive from the energy demands of processes like growth, activity and lifestyle, as well as the effects of temperature, food availability and predation. Yet while much attention has been given to the proximate causes of variation in metabolic scaling, ultimate explanations for the evolution of metabolic allometry remain to be thoroughly explored. In this thesis, I take an evolutionary physiological approach to investigate the evolutionary consequences and physiological drivers of variation in metabolic allometry. From an evolutionary perspective, identifying the genetic basis of the covariation between mass and metabolic rate is a prerequisite for understanding the evolution of metabolic allometry. In Chapter 2, I focused on ontogenetic scaling and discovered that there is heritable genetic variation in ontogenetic scaling relationships within and among species. In other words, individuals exhibit heritable differences in the way mass-specific metabolic rate changes with age and size over development. The implication is that ontogenetic allometries have the potential to be shaped by evolutionary responses to correlational selection favouring particular combinations of age- and mass-specific metabolic rate over development (e.g. high mass-specific metabolic rate early in

I development and low mass-specific metabolic rate later in development, or vice versa). The variation in ontogenetic scaling exponents in different species also has a heritable component, which raises the question of whether differences among taxa have been driven by responses to correlational selection on mass and metabolic rate within species. In this thesis I also show that the energetic costs of growth and maintenance over development are drivers of ontogenetic metabolic scaling and that variation in growth rate is associated with variation in metabolic allometry. Importantly, the covariation between metabolic