The evolutionary ecology of telomere variation in an exceptionally long-lived mammal, the greater horseshoe bat (Rhinolophus ferrumequinum).

Over 20% of all living mammals are bats who possess extraordinary adaptations including powered flight, laryngeal echolocation and the ability to tolerate a diversity of viral infections without presenting clinical disease symptoms. Significant physiological and ecological diversity occurs across the order and they also exhibit extreme longevity given their body size. Telomeres, TTAGGG repeats located at the ends of eukaryotic chromosomes, were initially framed as a biomarker of ageing. Research on bat TL has focused primarily on relationships with age and there is a lack of studies exploring within-individual change of TLs in bats across key life-history stages (early-life, reproduction and hibernation) and little work on tissue-specific TL patterns in bats. Chapter 1: I detail current knowledge on bat TL and how these relate to ecology, longevity and life-history strategies. An overview of methods for measuring TL is given with an introduction to the focal bat species of this thesis, Rhinolophus ferrumequinum. Chapter 2: I present an exploration into bat tissue-specific dynamics in a closely-related species, Rousettus aegyptiacus. This chapter reveals that wing, a rapid and minimally non-invasive tissue collection method, is representative of global tissue TL dynamics in bats. In particular, wing tissue TLs were highly repeatable when measured multiple times within individuals. This chapter details patterns of tissue TLs in bats for the first time and supports the use of wing tissue for measurement of TLs in bats as a proxy for other tissues that are otherwise difficult to obtain. Chapter 3: I measured TL during hibernation in R. ferrumequinum. These analyses show that TL appears to be preserved during hibernation, with within-individual increases occurring across the hibernation period. TLs reflected seasonal stressors, with warm, wet and windy conditions resulting in overall shorter TL, yet patterns of increases remained. I show that torpor confers a protective effect on bat TL and TLs are sensitive to climatic extremes that potentially disrupt hibernation patterns. Chapter 4: TL were measured in reproductive female R. ferrumequinum to investigate if costs of reproduction can be detected. I show with longitudinal data that patterns of TL shortening occur as found in a previous cross-sectional study. In reproductive females, females with shorter TL disappeared more quickly from the study population. Moreover, costs of reproduction on TL were complex with only short-term patterns uncovered, highlighting lactation as a stressful reproductive event for bats.. For the first time, I show age at first reproduction effects on TL, with earlier breeders showing shorter TL than their counterparts that defer breeding. This chapter highlights the complexity of reproductive patterns on TL in bats. Chapter 5: I explored the effects of early-life using a novel dataset of TL from greater horseshoe bat pups, mostly taken during their first week of life. Here environmental factors play a crucial role, with an optimum range of environmental conditions resulting in longer juvenile TLs. While TLs decreased with a rapid period of growth, increases could be observed from 40 days of age onwards indicating recovery mechanisms after stressful conditions. Yet early-life TL did not predict survival to the next year. Sex-specific transgenerational effects were found, with mothers producing sons with shorter TL as they aged while older fathers produced sons with longer TL. When expanding the dataset, repeatability and heritability of TL was found to be low, with strong effects across years. This further highlights environmental conditions as key in shaping TL in R. ferrumequinum. Chapter 6: I discuss the impact of these results in relation to advancing knowledge of TL variation and life-history trade-offs and propose future directions for telomere research in bats with additional comments on ways to overcome limitations when studying bats.