The Evolution of Metabolic Rate in Terrestrial Ectotherms Taryn Stephanie Crispin Bmarst (Hons)

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The Evolution of Metabolic Rate in Terrestrial Ectotherms Taryn Stephanie Crispin Bmarst (Hons) The evolution of metabolic rate in terrestrial ectotherms Taryn Stephanie Crispin BMarSt (Hons) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2014 School of Biological Sciences ABSTRACT Metabolic rate (MR) is the rate of all biochemical processes that underlie an animal’s demand to sustain life. In a complex environment with interactions between abiotic and biotic factors, the MR of an animal also represents the physiological cost of adaptation and survival. The MR within and between species varies considerably, even after the effects of body mass are accounted for. For terrestrial ectotherms (animals which do not regulate body temperature using metabolically- produced heat), much of the variation in MR is directly attributable to variation in body temperature, which influences the rates of energy turnover from the molecular level to the level of the whole animal. Given the pervasive effect of temperature on metabolic processes, elucidating the selection pressures that environmental temperature and other key environmental factors place on the evolution of ectotherm MR is thus important for understanding the evolution of ectotherm life histories, physiology and behaviour. The goal of this thesis was to explore the hypothesis that variation in environmental factors explains variation in terrestrial ectotherm MR. There are many mechanistic species-level studies that examine variation in ectotherm MR, however, uncovering the evolutionary causes for variation among species requires a broad-scale comparative approach. Examination of the current scientific literature suggests that large-scale comparative investigations into variation in terrestrial ectotherm MR are rare; this thesis addresses this issue by presenting findings from a series of studies that seek correlations between MR in terrestrial ectotherms (reptiles, amphibians and insects) and habitat temperature, precipitation and net primary productivity (NPP), whilst accounting for the effects of body mass, measurement temperature, and phylogenetic affiliations. This thesis does not, however, neglect the importance of a mechanistic, small-scale approach, and also presents the findings of a small-scale study that examines variation in MR, rates of water loss, and desiccation tolerance of a fruit fly species, Drosophila serrata, along a latitudinal gradient. Using a broad-scale comparative approach, I found no significant correlation between reptile RMR with any of the examined environmental parameters. Reptile MMR, however, exhibited a significant negative association with coefficients of variation in precipitation. It is possible that behavioural adaptation may have moderated the detectability of any potential correlation between reptile RMR and an environmental factor. Conversely, I conclude that it is possible that reptile aerobic MMR, a trait for which behaviour cannot buffer environmental sources of selection, is more likely to correlate with environmental factors. i Variation in amphibian and insect MR is strongly associated with habitat temperature; this finding agrees with the general scientific consensus that variations in characteristics of temperature are often the key explanatory factors for differences in ectotherm MR. I show that amphibian RMR correlates negatively with mean annual temperature, and aerobic MMR correlates positively with coefficients of variation in temperature. The metabolic cold adaptation (MCA) hypothesis predicts that, when compared at the same body temperature, ectotherms from cold environments should have higher MRs than those from warm environments. Because amphibian RMR and MMR both positively correlated with colder and thermally variable climates, I argue that this finding supports the MCA hypothesis. Similarly, a negative relationship was found between both insect RMR and insect MMR and mean annual temperature, and a positive association was observed between the two MR levels examined and coefficients of variation in temperature, suggesting that natural selection tends to favour a higher MR in insect populations inhabiting the colder environments with greater coefficients for variation in temperature. Thus, this thesis provides the first phylogenetically-informed support for MCA in insects. I found a weak negative correlation between amphibian aerobic MMR and NPP, and no correlation between amphibian RMR or MMR with coefficients of variation in precipitation. Further, I found no support for a relationship between the two levels of insect MR and coefficients of variation in precipitation, but a negative relationship was detected between insect RMR and NPP, though not between MMR and NPP. The potential for environmental productivity to act as a driver of terrestrial ectotherm MR remains to be further resolved, as correlations between NPP and amphibian and insect MR are negative and difficult to interpret given the lack of a definition of the type of selection that an annual estimate of NPP represents. A positive phenotypic association between MR and water loss was detected in D. serrata, yet there was no clinal variation in these traits when treated either independently or in association. There was, however, a strong pattern of clinal variation in dehydration tolerance, suggesting that sub- tropical populations are more desiccation tolerant, and a positive phenotypic and genetic association was found between dehydration tolerance and survival time under chronic desiccation stress. This association between dehydration tolerance and survival time did not, however, exhibit any clinal pattern to suggest adaptation to environmental aridity. I conclude that there is no evidence to suggest that variation in MR is a consequence of adaptation to desiccation stress along a tropical to subtropical latitudinal gradient for D. serrata, and suggest that aridity-driven selection may favour desiccation tolerance traits, rather than resistance traits, at these latitudes. 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, 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 research higher degree 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 General Award Rules of The University of Queensland, immediately made available for research and study in accordance with the Copyright Act 1968. 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. iii Publications during candidature No publications. Publications included in this thesis No publications included. iv Contributions by others to the thesis Craig White and I were jointly responsible for the conception and design of this thesis in its entirety. I was responsible for 90% of study design, 90% of drafting and writing, 100% data collation and collection, 100% construction of informal phylogenetic supertrees, 90% of statistical analysis and interpretation and 90% of drafting and writing for all chapters included in this thesis. Craig White provided critical feedback and suggestions, and was responsible for 10% of study design, 10% of statistical analysis and interpretation and 10% of drafting and writing for this thesis. Statement of parts of the thesis submitted to qualify for the award of another degree None. v ACKNOWLEDGEMENTS The completion of this thesis would not have been possible without the discussions, support and humour from the many remarkable people that I know and have encountered. I am very grateful that of these people, one of the most remarkable I have ever known was also my supervisor, Craig White. Craig, your selfless time and care were sometimes all that kept me going, and my academic and personal growth was inspired by your example. I will forever be indebted to you for this. If I can even remotely resemble what you embody as a supervisor, a colleague, and a friend, I will consider my lifetime a success. A sincere thanks is extended to my co-supervisor Craig Franklin for the discussions that helped focus and refine my approach to scientific research. I am also greatly indebted to David Booth for his thorough critiques and interest in the research I have undertaken, and to Robbie Wilson for the encouragement brought to each discussion on my progress. Steve Chenoweth and the Chenoweth laboratory group are gratefully acknowledged for their expertise and contribution of animals for the experimental component of this thesis, and thanks are extended to Katrina McGuigan, Mark Blows and the Blows laboratory group for their helpful guidance and
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