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The Life History of Damaraland Mole-Rats Fukomys Damarensis: Growth, Ageing and Behaviour

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The Life History of Damaraland Mole-Rats Fukomys Damarensis: Growth, Ageing and Behaviour The Life History of Damaraland Mole-rats Fukomys damarensis: Growth, Ageing and Behaviour Jack Thorley A thesis submitted to the University of Cambridge in application for the degree of Doctor of Philosophy Jesus College July 2018 i ii The Life History of Damaraland Mole-rats Fukomys damarensis: Growth, Ageing and Behaviour Jack Thorley SUMMARY The social mole-rats have often been typecast as extreme examples of mammalian sociality. With their pronounced reproductive skew, status-related contrasts in lifespan and morphology, and the suggestion of a division of labour amongst helpers, mole-rat societies have repeatedly been likened to the structurally complex societies of some eusocial insects. However, because few studies of mole-rats have quantified individual variation in growth and behaviour across long periods of development, it has remained unclear the extent to which mole-rat societies, and the features of individuals within them, should be considered unique amongst social vertebrates. In this thesis, I examine life history variation in Damaraland mole-rats Fukomys damarensis from three perspectives- growth, behaviour, and ageing- to explore how individual developmental trajectories contribute to, and are influenced by, the structure of mole-rat societies. First, I use a large longitudinal dataset to test for the presence of behavioural specialisation in non-breeding mole-rat helpers. I find no indication of individual specialisation in cooperative activities. Instead, individual differences in helping behaviour are largely the result of age-related changes in the extent to which individuals commit to all forms of helping (Chapter 3); refuting the notion of helper castes. I then focus on the variation in growth across non-breeders, developing a novel biphasic model to accurately quantify sex differences in growth and explore the influence of social effects on growth trajectories (Chapter 4). Despite the proposition of intense intrasexual competition in mole-rat societies, there was no clear signature of sex-specific competition on helper growth trajectories. A more conspicuous form of socially-mediated growth in mole-rats is the secondary growth spurt displayed by females that have acquired the dominant breeding position, causing them to become larger and more elongated. By experimentally controlling reproduction in age-matched siblings, I show that rather than being stimulated by the removal from reproductive suppression, this adaptive morphological divergence is achieved through a lengthening of the lumbar vertebrae when breeding is commenced (Chapter 5). With i contrasts in size and shape following the acquisition of the breeding role, this status-related growth pattern shares similarities with growth in naked mole-rats and other social vertebrates. Breeders also show a twofold greater lifespan than non-breeders in Fukomys mole- rats, prompting the suggestion that the transition to dominance also sets individuals onto a slower ageing trajectory. To date, there is little evidence to support a physiological basis to lifespan extension in breeders. This assertion is bolstered by the absence of longer telomeres or slower rates of telomere attrition in breeding females compared to non-breeding females residing in groups (Chapter 6), each of which might be expected if breeders age more slowly. I argue that previous studies exploring status-related ageing in captive Fukomys mole-rats have overlooked the importance of demographic processes (and associated behavioural influences) on mortality schedules. Irrespective of the proximate basis of the longer lifespan of breeders, at an interspecific level the social mole-rats are unusually long-lived for their size. A recent large-scale comparative analysis concluded that prolonged lifespan is a general characteristic of all mammalian cooperative breeders, but this conclusion is premature, as in most of the major clades containing both cooperative and non-cooperative species there is no consistent trend towards lifespan extension in cooperative species (Chapter 7). In the case of mole-rats, it seems more likely that their exceptional longevity arises principally from their subterranean habits and related reductions in extrinsic mortality. Overall, these findings demonstrate that cooperative breeding has important consequences for individual life histories, but there is no strong basis for the claim that Damaraland mole-rat societies are markedly different in form than other cooperative breeding societies. ii PREFACE This thesis is the result of my own work, and contains no work done in collaboration except where stated at the commencement of each chapter. The text does not exceed 60,000 words. No part of this thesis has been submitted to any other university in application for a higher degree. Jack Thorley July 2018 iii PAPERS ARISING FROM THESIS Thorley, J., Mendonça, R., Vullioud, P., Torrents-Ticó, M, Zöttl, M., Gaynor, D., and T. Clutton-Brock. 2018. No task specialisation among helpers in Damaraland mole-rats. Animal Behaviour 143: 9-24. doi: 10.1098/rspb.2018.0897 Thorley, J., Katlein, N., Goddard, K., Zöttl, M., and T. Clutton-Brock. 2018. Reproduction triggers adaptive increases in body size in female mole-rats. Proceeding of the Royal Society of London B 285: 20180897. doi: 10.1098/rspb.2018.0897 OTHER RELATED CONTRIBUTIONS Zöttl, M., Thorley, J., Gaynor, D., Bennett, N.C., and T. Clutton-Brock. 2016. Variation in growth of Damaraland mole-rats is explained by competition rather than by functional specialization for different tasks. Biology Letters 12: 20160820. doi: /10.1098/rsbl.2016.0820 Thorley, J., and T. Clutton-Brock. 2017 Kalahari vulture declines, through the eyes of meerkats. Ostrich: Journal of African Ornithology. Ostrich 88(2): 177-181. doi: 10.2989/00306525.2016.1257516 iv ACKNOWLEDGEMENTS My first thanks go to my supervisor, Professor Tim Clutton-Brock, for providing me with a stimulating environment in which to conduct my PhD, in Cambridge and in the Kalahari. I admire Tim a great deal for the intellectual contributions he has made to behavioural ecology, and it has been a pleasure to be a member of the ‘Large Animal Research Group’. From him I have learnt a great deal about the method of scientific enquiry into the natural world, and the importance of clarity and precision in formulating hypotheses and constructing arguments. Above all, he has instilled in me the importance of iterations to the writing process. A result I hope to have eradicated the “streams of consciousness” that pervaded earlier versions of my thesis to leave an insightful body of work. In LARG, I have been fortunate to work as part of a close-knit community of researchers- the LARGies. It would be over-indulgent to write something about each of them, but I am nonetheless grateful to AJ, Arik, Chris, Corina, Constance, Dieter, Dom, Mark, Monica, Peter and Teja for the insightful chats at lunch, and the less coherent chats in pubs throughout my tenure. All have had an instructive role in my learning and contributed to my enjoyment in Cambridge. I reserve special mention for Markus and Philippe, members of the mole-rat team with whom I have worked closely. Along with Rute Mendonça, they have invested much time and energy into the mole-rat project to ensure that is runs as smoothly as possible. Coordinating a project from 9,000km away is always a challenging and thankless task, but where it can be thanked it should. For a brief period in my thesis I was based in Glasgow to undertake telomere work in the lab of Pat Monaghan. Pat was a wonderful host and I am thankful to her lab for the warm environment they provided to me. While there, Rob Gillespie was a fantastic mentor and source of much entertainment through the hours of pipetting. My telomeres would have shortened exceptionally fast without his help. Whilst Cambridge has been a wonderful base for a PhD, it is the time spent in the South Africa that I will remember most vividly and cherish most fondly. As Niko Tinbergen notes in his Curious Naturalists “it is only natural for a man to have occasional doubts about the value of what he is doing”. Such doubts have certainly surfaced in me from time to time throughout my studies. But to return to the Kalahari each time was to feel refreshed and reinvigorated. It is a mesmerising place, beautiful in its harshness and deeply affecting in its enormity. Each visit to the Kalahari would reaffirm my decision to pursue an ecologically-oriented career. The intellectual gains provided some validation, but more fundamental is that feeling of intense kinship with a place that comes with extended fieldwork, living not with the landscape, but in it. The nights trapping mole-rats under a quicksilver milky way; the early morning hoar frosts; the metallic chattering of the sparrow-weavers; the blood-stained sunsets; the calms before the storms. I have been immensely lucky and will miss it all. v Yet for all its remoteness, the desert was a place of friendships, and there are many people at the Kalahari Meerkat Project who I am fortunate to have met. Many afforded me their time and patience, their skills, their jokes. Some indulged me with their cookery skills, and one even gave me their affection. In particular, I would like to thank Dave Gaynor for his hospitality and infectious enthusiasm for the natural world. He was a great sounding board and I would always enjoy nipping up to the ‘dog-house’ for a coffee. Nanine, for her warmth, and Bracken for his optimism and boundless energy- I’m sorry I never found that Lego piece you were missing. Tim Vink was always of great help with his technological and mechanical wizardry, second only to his skills at Braaing. And to the scores of meerkat volunteers with which I shared the place, Baie Danke. Looking back at the earliest photos now it is alarming just how many people I met across my PhD.
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