Causes and consequences of telomere lengthening in a wild vertebrate population

Telomeres have been advocated to be important markers of biological age in
evolutionary and ecological studies. Telomeres usually shorten with age,
and shortening is frequently associated with environmental stressors and
increased subsequent mortality. Telomere lengthening – an apparent
increase in telomere length between repeated samples from the same
individual – also occurs. However, the exact circumstances, and
consequences, of telomere lengthening are poorly understood. Using
longitudinal data from the Seychelles warbler (Acrocephalus sechellensis),
we tested whether telomere lengthening – which occurs in adults of this
species – is associated with specific stressors (reproductive effort, food
availability, malarial infection and cooperative breeding) and predicts
subsequent survival. In females, telomere shortening was observed under
greater stress (i.e. low food availability, malaria infection), while
telomere lengthening was observed in females experiencing lower stress
(i.e. high food availability, assisted by helpers, without malaria). The
telomere dynamics of males were not associated with the key stressors
tested. These results indicate that, at least for females, telomere
lengthening occurs in circumstances more conducive to self-maintenance.
Importantly, both females and males with lengthened telomeres had improved
subsequent survival relative to individuals that displayed unchanged, or
shortened, telomeres – indicating that telomere lengthening is associated
with individual fitness. These results demonstrate that telomere dynamics
are bidirectionally responsive to the level of stress that an individual
faces, but may poorly reflect the accumulation of stress over the
lifetime. This study challenges how we think of telomeres as a marker of
biological age.