Age-Related Telomere Dynamics in Bats

Understanding the mechanisms underpinning ageing and exceptional longevity remains one of the central challenges in biology. Much of what is currently known about the ageing process has been derived from short-lived, model organisms. However, recent years have seen an expansion of studies involving wild, non-model species. Bats make up over 20% of all living mammals and possess extraordinary adaptations including laryngeal echolocation, powered flight, and a unique immune system that enables them to tolerate viral infections typically lethal in other mammals. Bats also exhibit extreme longevity given their body size with most species living far longer than similarly sized mammals. As a result, bats have emerged as a new model organism for ageing research. Telomeres, the nucleotide repeats that protect chromosome ends, are a key hallmark of cellular ageing and have been widely studied in both laboratory and wild species. However, telomere biology in bats remains underexplored. This thesis presents the most extensive comparative analysis of telomere dynamics in bats to date, encompassing >3400 bats across five species. In Chapter 2, I focus on early-life telomere dynamics in Myotis myotis, a long-lived, insectivorous bat. Using qPCR-based telomere length measures from 500 juvenile bats, I identify spring rainfall as the strongest predictor of telomere length in pups, with wetter conditions associated with longer telomeres. Despite this environmental sensitivity, early-life telomere length did not predict survival to the first year or longer-term survival. These findings suggest that while telomere length in M. myotis is environmentally plastic during development, it may not translate to fitness differences in a species capable of strong telomere maintenance. In Chapter 3, I present the first telomere study on Molossus molossus, a fast-flying tropical, insectivorous bat previously considered short-lived. Fieldwork in Panama involving multi-year mark-recapture sampling revealed a new longevity record of at least 13 years. I found no consistent evidence for age-related telomere shortening in this species. These findings parallel those in M. myotis, suggesting that telomere maintenance may be a convergent trait among potentially long-lived bat species despite their ecological differences. In Chapter 4, I conduct the largest comparative telomere study in bats to date, investigating the relationship between telomere length and age in >2900 bats across five species of differing lifespans, ecologies and life histories: M. myotis, Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, and M. molossus. Results here reveal dramatic interspecific variation in telomere dynamics. While M. myotis and M. molossus showed no correlation between telomere attrition and age, R. ferrumequinum and P. discolor exhibited clear age-related telomere shortening. R. aegyptiacus displayed a non-linear trajectory, with telomere length increasing in early life before declining. Additionally I investigate sex differences, finding that patterns varied across species, with no universal male or female bias. Finally, I explore potential molecular mechanisms underlying telomere maintenance through a comparative transcriptomic analysis across species. Expression profiling revealed upregulation of shelterin complex genes and DNA repair pathways (e.g., homologous recombination and ALT-like mechanisms) in species which display telomere maintenance with age. In Chapter 5, I synthesise the findings across all chapters and highlight their implications for ageing research. The data presented in this thesis demonstrate that telomere shortening with age is not a universal feature of mammals, and that bats possess diverse, species-specific strategies to regulate telomere dynamics. The integration of field-based mark-recapture methods with molecular and transcriptomic approaches offers a powerful framework for studying ageing in the wild.