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The Biological Importance of Individual Variation in Metabolic Responses in Animals Facing Direct Ecological Pressures in a Controlled Environment

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The Biological Importance of Individual Variation in Metabolic Responses in Animals Facing Direct Ecological Pressures in a Controlled Environment The biological importance of individual variation in metabolic responses to environmental conditions by Elle J. D. McDonald A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Hawkesbury Institute for the Environment, Western Sydney University September 2019 STATEMENT OF AUTHENTICATION The work presented in this thesis is, to the best of my knowledge and belief, original except as acknowledged in the text. I hereby declare that I have not submitted this material, either in full or in part, for a degree at this or any other institution. - - - - - - - - - - - - - - - - - - i ABSTRACT Life-history theory was established to help understand the large diversity in life-history strategies among-species. Fundamentally, a trade-off between survival and reproduction underlies the evolution of different life-histories along the slow – fast life-history continuum. The pace-of-life syndrome (POLS) hypothesis expands on life-history theory to help explain variation in life-histories at the population and individual levels. The POLS hypothesis proposes that variation in life-histories can only be completely understood when integrated with a suite of physiological and behavioural traits that have co-evolved to maximise fitness according to the life-history idiosyncrasies of different species and populations. Indeed, within populations, individuals differ considerably in their phenotypic expression of many important physiological and behavioural traits. Energy expenditure, for instance, is an important physiological trait of animals that drives ecological patterns and processes at individual to community levels. A primary area of research in animal physiology and evolutionary biology focuses on understanding the fitness consequences of among-individual variation in energy expenditure. Individual variation in basal metabolic rate (BMR) is by far the most common index of energy expenditure. Variation in BMR is often is assumed to reflect variation in other components of metabolism and energy expenditure and is expected to have fitness consequences. However, BMR excludes important ways in which metabolic rate can be adjusted in response to environmental conditions (e.g. air temperature and food availability). Therefore, BMR cannot incorporate how these responses might differ among individuals, nor predict their relative contribution to energy expenditure and their probable influence on fitness. Metabolic rate varies within- and among-individuals in response to environmental change. As such, quantifying among-individual variation in metabolic responses to ii environmental conditions could expand our current understanding of the fitness consequences of among-individual variation in energy expenditure. Therefore, the principal aim of this thesis was to examine the relationships among various measures of energy expenditure and determine whether metabolic responses to environmental conditions can be consistent and important individual traits. The first chapter of this thesis reviews the literature on life-history theory and the POLS hypothesis and highlights the current limitations faced by animal physiologists and evolutionary biologists, both theoretically and practically, when seeking to integrate metabolism with other physiological, behavioural and life-history traits in endothermic animals. The second, third, fourth and fifth chapters of this thesis describe empirical research undertaken to address the main aim of this thesis and provide novel insights into how consistent among-individual variation in metabolic responses to environmental conditions relates to behaviour and reproductive fitness. The research questions were addressed using a Diversity Outbred strain of laboratory mouse that was developed by crossing eight different strains of Mus musculus subspecies. The Diversity Outbred line was bred to contain a wide range of genotypic and phenotypic diversity. The sixth and final chapter summarises the main results of this thesis and provides new perspectives that will help future research to examine the ecological consequences of individual variation in energy expenditure. The second chapter provides a detailed evaluation of the factors that are correlated with variation in metabolism and energy expenditure at the species and population levels. The second chapter also critiques the current methods used by ecologists, physiologists and evolutionary biologists to characterise individual metabolic phenotypes in studies wishing to determine how energy expenditure interacts with other key physiological, behavioural and life-history traits and proposes that using metabolic responses to environmental conditions could provide a more ecologically relevant way to characterise individual metabolic iii phenotypes. Furthermore, chapter two outlines the experimental approach that was used to estimate the effects that air temperature (Ta) and food availability have on metabolism at the individual level in a small endothermic mammal. In chapter two, a reaction norm approach was used to quantify baseline metabolism and metabolic responses to Ta (31 and 15 °C) and food availability in 97 Diversity Outbred laboratory mice. Responses were measured up to three times over a one-year period, allowing for estimates of repeatability to be calculated. The most important result that was identified in chapter two is that although individuals exhibit large differences in their baseline metabolism and energy expenditure, they exhibit even larger differences in their metabolic responses to Ta and starvation. Moreover, average metabolic responses to starvation were highly repeatable over a one-year period, far beyond the expected lifespan for wild Mus musculus. Individual variation in baseline levels of resting metabolic rate (RMR) at 15 °C and the response of RMR at 15 °C to starvation were highly informative of individual variation in daily energy expenditure, considerably more so than RMR measured at 31 °C. The results described in chapter two suggest that measuring individual metabolic reaction norms to ecologically relevant environmental conditions is indeed a valuable way to characterise important aspects of individual variation in energy expenditure that might be relevant to fitness. The third chapter examines possible correlations between consistent individual differences (CIDs) in different components of metabolism (e.g. including metabolic responses to Ta and food availability) and behavioural responses to an open-field test (i.e. indices of boldness, exploration and activity). Diversity Outbred mice were found to exhibit CIDs in their baseline metabolism, metabolic responses to environmental conditions and behavioural traits. Indeed, behavioural responses were correlated such that individuals exhibited variation in behavioural syndromes along a proactive – reactive continuum. Despite large among-individual variation in both metabolic phenotypes and behavioural traits, no iv evidence was found to suggest that they were correlated. The lack of any correlation under laboratory conditions (i.e. in a controlled environment) suggests that variation in metabolism and behaviour are not correlated through shared physiological pathways (e.g. a shared hormonal basis). The fourth chapter evaluated the possible fitness consequences of among-individual variation in metabolic responses to environmental conditions and revealed some novel results. Two indices of reproductive fitness: litter size and offspring growth rate; and individual metabolic responses to Ta and food availability were measured in a sample of 77 Diversity Outbred mice. The first important result in chapter two was that CIDs in the slope of the mother’s metabolic response to temperature were negatively correlated with offspring growth rate from birth to 16 days old (i.e. when offspring are completely reliant on their mother’s milk), and from birth to weaning (i.e. 31 days old). Furthermore, CIDs in the father’s RMR31 (i.e. reaction norm intercept) and RMR31 and RMR15 in response to starvation (i.e. reaction norm slopes) were correlated with offspring growth rate from birth to weaning. The results found in chapter two have shown that among-individual variation in different components of metabolism in adult Mus musculus are correlated with offspring growth rate in different ways at different stages of postanal growth via either developmental (i.e. maternal effects), behavioural (i.e. maternal investment based on perceived quality of their mate) or physiological mechanisms (i.e. genetic or epigenetic effects). The fifth chapter examined variation in organ mass as possible proximate mechanism underlying variation in metabolic responses to environmental conditions. Correlations were quantified between individual variation in metabolic responses to environmental conditions and the residual dry mass of several metabolically active organs in a sample of 43 Diversity Outbred mice. It was found that the masses of different organs were correlated with different components of metabolism. For instance, the residual dry mass of the heart was positively v correlated with DEE indicating that a larger heart might facilitate higher rates of average energy expenditure. Whereas the residual dry mass of the kidneys was positively correlated with individual differences in the metabolic response to Ta and negatively correlated with RMR at 15 °C indicating that the kidneys could be involved in thermoregulation at cold Ta’s. The results of this thesis provided a test of the ecological relevance
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