Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird

Abstract

Telomere length is associated with cellular senescence, lifestyle and ageing. Short telomeres indicate poor health in humans and reduced life expectancy in several bird species, but little is known about telomeres in relation to phenotypic quality in wild animals. We investigated telomere lengths in erythrocytes of known-age common terns (Sterna hirundo), a migratory seabird, in relation to arrival date and reproductive performance. Cross-sectional data revealed that, independent of age, individuals with short telomeres performed better: they arrived and reproduced earlier in the season and had more chicks in the nest. The latter effect was stronger the older the brood and stronger in males, which do most of the chick provisioning. Longitudinal data confirmed this pattern: compared with birds that lost their brood, birds that raised chicks beyond the 10th nestling day experienced higher telomere attrition from one year to the next. However, more detailed analysis revealed that the least and most successful individuals lost the fewest base pairs compared with birds with intermediate success. Our results suggest that reproductive success is achieved at the expense of telomeres, but that individual heterogeneity in susceptibility to such detrimental effects is important, as indicated by low telomere loss in the most successful birds.

Figure 1.

Residual telomere length (corrected for age, gel and bird identity) in relation to arrival date (mean of 2007 and 2008) at the breeding site (females: open circles, n = 98 samples; males: filled circles, n = 83 samples; b = 0.23). Arrival date increased the r² of the model by 3.1%. See table 1 for other statistics.

Figure 2.

Slopes (±s.e.) of the relationship between telomere length and reproductive success (brood size) decreased with increasing brood age (females: open circles, n = 122 samples; males: filled circles, n = 117 samples; for statistics see table 2).

Figure 3.

Telomere length in 2007 plotted against telomere length in 2008 (n = 50 individuals). The dotted line represents the function y = x. The solid lines represent the slopes of individuals with (lower line) or without (upper line) chicks in the nest at brood age 10 days. Individuals with chicks at day 10 lost more base pairs (filled circle: no chicks left at brood age 10 days; open circle: 1–3 chicks at brood age 10 days). For statistics see table 3(a).

Figure 4.

Change in telomere length between two consecutive years in relation to brood size at the 10th nestling day in the first year (n = 50 individuals—for distribution see n bottom of graph). Boxes show the median, and the 25th and 75th percentiles (box limits); whiskers represent the 5th and 95th percentiles. For statistics see table 3(b).