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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G. Phd, Mphil, Dclinpsychol) at the University of Edinburgh This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Experimental and Comparative Analyses of Maternal Age and Senescence Edward R. Ivimey-Cook Thesis submitted for the degree of Doctor of Philosophy School of Biological Sciences The University of Edinburgh 2019 Contents ABSTRACT ............................................................................................................. 3 LAY SUMMARY ..................................................................................................... 5 DECLARATION ...................................................................................................... 7 ACKNOWLEDGEMENTS ...................................................................................... 8 CHAPTER 1: GENERAL INTRODUCTION ....................................................... 11 1.1 SENESCENCE ........................................................................................................................ 12 1.2 EVOLUTIONARY THEORIES OF AGEING ................................................................................ 16 1.3 LIFE HISTORY THEORY ......................................................................................................... 19 1.4 CROSS-FOSTERING EXPERIMENTS ........................................................................................ 22 1.5 THE BURYING BEETLE, NICROPHORUS VESPILLOIDES ......................................................... 23 1.6 THESIS AIMS ........................................................................................................................ 26 CHAPTER 2: DISENTANGLING PRE- AND POSTNATAL MATERNAL AGE EFFECTS ON OFFSPRING PERFORMANCE IN AN INSECT WITH ELABORATE MATERNAL CARE ...................................................................... 29 2.1 INTRODUCTION .................................................................................................................... 30 2.2 MATERIALS AND METHODS ................................................................................................. 33 2.3 RESULTS............................................................................................................................... 41 2.4 DISCUSSION .......................................................................................................................... 50 2.5 CONCLUSION ........................................................................................................................ 57 CHAPTER 3: EVALUATING THE DIVERSITY OF MATERNAL AGE EFFECTS UPON NEONATAL SURVIVAL ACROSS ANIMAL SPECIES ........ 58 3.1 INTRODUCTION .................................................................................................................... 59 3.2 MATERIALS AND METHODS ................................................................................................. 63 3.3 RESULTS............................................................................................................................... 71 3.4 DISCUSSION .......................................................................................................................... 78 3.5 CONCLUSION ........................................................................................................................ 83 1 CHAPTER 4: WHAT CAN NATURAL SELECTION TELL US ABOUT DIVERSITY OF AGEING PATTERNS ACROSS SPECIES? ............................. 85 4.1 INTRODUCTION .................................................................................................................... 86 4.2 MATERIALS AND METHODS ................................................................................................. 91 4.3 RESULTS............................................................................................................................... 98 4.4 DISCUSSION ........................................................................................................................ 111 4.5 CONCLUSION ...................................................................................................................... 117 CHAPTER 5: GENERAL DISCUSSION ............................................................ 119 5.1 THESIS OVERVIEW ............................................................................................................. 120 5.2 KEY FINDINGS ................................................................................................................... 121 5.3 IMPLICATIONS AND FUTURE DIRECTIONS.......................................................................... 124 5.4 CONCLUDING REMARKS ..................................................................................................... 126 REFERENCES ..................................................................................................... 127 APPENDICES ..................................................................................................... 157 SUPPLEMENTARY MATERIAL FROM: “DISENTANGLING PRE- AND POSTNATAL MATERNAL AGE EFFECTS ON OFFSPRING PERFORMANCE IN AN INSECT WITH ELABORATE MATERNAL CARE” 157 SUPPLEMENTARY MATERIAL FROM: “EVALUATING THE DIVERSITY OF MATERNAL AGE EFFECTS UPON NEONATAL SURVIVAL ACROSS ANIMAL SPECIES” ............................................ 181 SUPPLEMENTARY MATERIAL FROM: “WHAT CAN NATURAL SELECTION TELL US ABOUT DIVERSITY OF AGEING RATES ACROSS SPECIES?” .................................................................... 255 2 Abstract Senescence is often described as an age-related physiological deterioration accompanied with declining fertility and increasing mortality, and it is believed to be the result of declining forces of natural selection. A manifestation of senescence that has attracted much recent interest is the detrimental effect of increasing maternal age acting on offspring traits. However, uncertainty arises when attempting to describe the prevalence and ubiquity of this third form of ageing and the evolutionary causes for diversity in ageing trajectories. Here I address the following questions: (1) How are maternal age effects distributed across taxa? And (2) Can an evolutionary perspective help us to understand the observed diversity in maternal age effects and demographic senescence? I addressed these through (i) a cross-fostering ageing experiment using a laboratory population of burying beetle, Nicrophorus vespilloides to decouple the separate effects of increasing pre- and postnatal maternal age, whilst accounting for the potential bias of selective disappearance. I found no evidence for maternal age effects or effects deriving from selective disappearance. These results suggest that current theory may be insufficient to account for the true diversity in ageing patterns. (ii) A meta-analytical review of maternal effect senescence to investigate the prevalence and diversity of maternal effect ageing patterns and the performance of an evolutionary model to predict observed patterns. We found taxa-wide evidence for maternal age effects on offspring survival. However the direction of these effects was based on phylogenetic constraints with laboratory and natural-mammal species showing a decline, but natural-bird species 3 showing an ambiguous effect of maternal age. The evolutionary model was shown to improve in performance compared to evolution-agnostic demographic models when describing maternal effect ageing in natural populations. This result suggests an evolutionary cause to maternal effect senescence. (iii) Lastly, I performed a comparative analysis of vital rate selection across the tree of life. Using extensive existing databases of life history data coupled with predictions from two evolutionary theories, I derived correlations between predicted and observed vital rates across multiple animal species. I found that whilst natural selection had weak predictive power when describing patterns of mortality, age-specific fertility patterns showed extensive departures from evolutionary predictions. Additionally, I found that several biological processes were readily contributing to non-conformance of Hamilton-like ageing. Taken together, we provide convincing evidence to suggest that both natural selection and biological processes have helped shape the vast diversity of observed ageing rates that exist across the tree of life. 4 Lay Summary Ageing is often accompanied with a decrease in fertility and survival, and is believed to be the result of declining forces of natural selection. One form of ageing that has attracted much recent interest is the harmful effect of increasing maternal age acting on offspring traits. However, there is uncertainty when attempting to describe the distribution of this form of ageing and the evolutionary causes for diversity in ageing patterns
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