Maternal telomere length inheritance in the king penguin

Abstract

Telomeres are emerging as a biomarker for ageing and survival, and are likely important in shaping life-history trade-offs. In particular, telomere length with which one starts in life has been linked to lifelong survival, suggesting that early telomere dynamics are somehow related to life-history trajectories. This result highlights the importance of determining the extent to which telomere length is inherited, as a crucial factor determining early life telomere length. Given the scarcity of species for which telomere length inheritance has been studied, it is pressing to assess the generality of telomere length inheritance patterns. Further, information on how this pattern changes over the course of growth in individuals living under natural conditions should provide some insight on the extent to which environmental constraints also shape telomere dynamics. To fill this gap partly, we followed telomere inheritance in a population of king penguins (Aptenodytes patagonicus). We tested for paternal and maternal influence on chick initial telomere length (10 days old after hatching), and how these relationships changed with chick age (at 70, 200 and 300 days old). Based on a correlative approach, offspring telomere length was positively associated with maternal telomere length early in life (at 10 days old). However, this relationship was not significant at older ages. These data suggest that telomere length in birds is maternally inherited. Nonetheless, the influence of environmental conditions during growth remained an important factor shaping telomere length, as the maternal link disappeared with chicks' age.

Mother–offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers

“…Previously reported heritability estimates of telomere length range between 0.44 and 0.78 for humans [11][12][13][14] and between 0.18 and 1.23 for other vertebrates [15][16][17][18][19][20]. This suggests that there is a large amount of variation in the degree to which telomere length is heritable, with our estimate being at the lower end of the spectrum.…”

“…Although unlike some other methods, qPCR does not discriminate between chromosome ends and interstitial telomeric sequences, qPCR-based telomere measurements have been widely used, including in a number of bird species (e.g. [4,5,15,18,19,41]). We discuss the potential implications of this limitation of the qPCR method in some detail in the Discussion.…”

“…[13,[15][16][17][18]31,32]). For example, several of the studies investigating telomere length inheritance in non-human animals (birds and lizards) have found either maternal inheritance [15,16,18] or a much higher son-father than daughtermother resemblance [17].…”

“…[13,[15][16][17][18]31,32]). For example, several of the studies investigating telomere length inheritance in non-human animals (birds and lizards) have found either maternal inheritance [15,16,18] or a much higher son-father than daughtermother resemblance [17]. Indeed, sex-specific patterns appear to be the rule rather than the exception and suggested mechanisms include parent-specific imprinting, hormonal regulation and sex-chromosome linkage, either acting independently or jointly [13,16,17,32].…”

Reduced fitness in progeny from old parents in a natural population

“…Short telomeres are strongly associated with cellular senescence, shortened lifespan, and reduced future reproductive success (20). Although long telomeres are maintained in the germ line through replenishment during meiosis, there is some evidence that telomere length is heritable and that such inheritance is sex specific (21)(22)(23) in birds, potentially resulting in daughters of older mothers having shorter telomeres (24)(25)(26), and, in turn, reduced fitness (27). The cellular consequences of aging and stress are similar, because both lead to oxidative damage that causes telomeres to shorten (20,28).…”