On the Evolutionary Physiology of Metabolic Allometry
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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 animal, 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 scaling and growth rate has a genetic basis, with growth rate being strongly negatively correlated with the scaling slope, and strongly positively correlated with the scaling intercept. In other words, genotypes that grow more quickly have higher mass-specific metabolic rate at small sizes early in development, but then have a steeper decline in mass-specific metabolic rate with increasing size compared to genotypes with slower growth rates. Hence, selection on growth rate will cause a correlated evolutionary response in ontogenetic metabolic scaling, and vice versa. Since energy expenditure is functionally and genetically linked to growth, the optimisation of multivariate physiological and life-history variation with respect to fitness will shape rates of energy expenditure and growth over development and, therefore, will shape ontogenetic metabolic scaling. There is still much that remains unknown about how multivariate selection has shaped the covariation between metabolic rate and body size and progress in this area stands to illuminate the mechanistic basis of variation in life-history and fitness. Furthermore, understanding the physiological and ecological consequences of the genetic constraints on covariation in growth and metabolic scaling relationships remain essentially an unexplored area of research. There is now an opportunity to integrate evolutionary and metabolic theory to accommodate the evolutionary lability of the covariance between mass and metabolic rate within and among species. Genetic approaches provide a framework for integrating evolutionary and metabolic theory. Such approaches have already been used to understand the evolutionary constraints on growth curves and reaction norms, and have advanced the understanding of life-history and phenotypic plasticity. Evolutionary genetic approaches could therefore be readily adapted to understand the evolution of metabolic allometry, such that the evolution of metabolic allometry, life history and phenotypic plasticity could be incorporated into metabolic theory. Evolutionary genetics and metabolic ecology are both quantitative and predictive frameworks, and combining them would enable more accurate predictions of how contemporary environmental change will alter ecological processes and communities in the future. II Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. III Publications included in this thesis Julian E. Beaman, Craig R. White, Frank Seebacher (2016) Evolution of plasticity: mechanistic link between developmental and reversible acclimation. Trends in Ecology and Evolution, 31:237-249. Submitted manuscripts included in this thesis No other chapters have been submitted for publication. Other publications during candidature Craig R. White, Dustin J. Marshall, Lesley A. Alton, Pieter A. Arnold, Julian E. Beaman, Candice L. Bywater, Catriona Condon, Taryn S. Crispin, Aidan Janetzki, Elia Pirtle (2019) The origin and maintenance of metabolic allometry in animals. Nature Ecology and Evolution, 3: 598-603. Frank Seebacher, Julian E. Beaman, Alexander G. Little (2014) Regulation of thermal acclimation varies between generations of the short-lived mosquitofish that developed in different environmental conditions. Functional Ecology, 28: 137-148. IV Contributions by others to the thesis Name Contribution Chapter Advised on conceptualisation, experimental design, Craig R. White respirometry, data extraction, data analysis, edited All manuscript, funding Advised on conceptualisation, experimental design Daniel Ortiz-Barrientos 2, 4 and data analysis, edited manuscript Advised on conceptualisation, data interpretation, Frank Seebacher 4, 5 edited manuscript Matthew Hall Feedback on data analysis, edited manuscript 2 Feedback on conceptualisation, experimental design Mark Blows 2, general and analysis Robbie Wilson Feedback on conceptualisation General Keyne Monro Feedback on data analysis 2 Evatt Chirgwin Feedback on