Mothers Matter Most: Maternal, but Not Paternal, Age and Inbreeding Affect Nestling Telomere Length in a Wild Passerine

Abstract

Early-life telomere length can be an integrated and accessible biomarker of lifetime fitness. Telomere length can result from complex interactions between heritable genetic variation, inherited gametic variation and accumulated environmental effects acting on individuals and parents. Consequently, to understand early-life telomere length and its fitness consequences, both offspring traits and intergenerational effects resulting from parental traits need to be studied simultaneously. This is, particularly, true for inbreeding as poor performance or impaired telomere maintenance in offspring as well as poor parental reproductive effort or changes in gametic telomeres can reduce telomere length of offspring. Here, we explore the effects of individual inbreeding, parental inbreeding and parental age in a large dataset (n = 679) of nestling telomere length in a long-term studied wild population of purple-crowned fairy-wrens (Malurus coronatus coronatus) with multigenerational ecological and environmental data. We find no effect of nestling inbreeding on telomere length, even in adverse (hot and dry) climatic conditions. Offspring telomere length was not associated with paternal inbreeding or age (neither within- nor between-fathers). However, nestling telomere length declined with maternal inbreeding and with increasing maternal age. Combined, these results do not support inherited gametic effects but rather suggest that effects of inbreeding and ageing on the mother's phenotypic state may affect pre- and/or post-natal reproductive investment. Offspring from older and more inbred mothers, with shorter telomeres, will suffer reduced lifetime fitness. Moreover, inheritance of shorter telomeres could lead to population-level changes in performance.