Growing old, yet staying young: The role of telomeres in bats’ exceptional longevity

Abstract

Understanding aging is a grand challenge in biology. Exceptionally long-lived animals have mechanisms that underpin extreme longevity. Telomeres are protective nucleotide repeats on chromosome tips that shorten with cell division, potentially limiting life span. Bats are the longest-lived mammals for their size, but it is unknown whether their telomeres shorten. Using >60 years of cumulative mark-recapture field data, we show that telomeres shorten with age in <i>Rhinolophus ferrumequinum</i> and <i>Miniopterus schreibersii</i>, but not in the bat genus with greatest longevity, <i>Myotis</i>. As in humans, telomerase is not expressed in <i>Myotis myotis</i> blood or fibroblasts. Selection tests on telomere maintenance genes show that <i>ATM</i> and <i>SETX</i>, which repair and prevent DNA damage, potentially mediate telomere dynamics in <i>Myotis</i> bats. Twenty-one telomere maintenance genes are differentially expressed in <i>Myotis</i>, of which 14 are enriched for DNA repair, and 5 for alternative telomere-lengthening mechanisms. We demonstrate how telomeres, telomerase, and DNA repair genes have contributed to the evolution of exceptional longevity in <i>Myotis</i> bats, advancing our understanding of healthy aging.