Longer telomeres during early life predict higher lifetime reproductive success in females but not males

Abstract

The mechanisms that contribute to variation in lifetime reproductive success are not well understood. One possibility is that telomeres, conserved DNA sequences at chromosome ends that often shorten with age and stress exposures, may reflect differences in vital processes or influence fitness. Telomere length often predicts longevity, but longevity is only one component of fitness and little is known about how lifetime reproductive success is related to telomere dynamics in wild populations. We examined the relationships between telomere length beginning in early life, telomere loss into adulthood and lifetime reproductive success in free-living house sparrows (Passer domesticus). We found that females, but not males, with longer telomeres during early life had higher lifetime reproductive success, owing to associations with longevity and not reproduction per year or attempt. Telomeres decreased with age in both sexes, but telomere loss was not associated with lifetime reproductive success. In this species, telomeres may reflect differences in quality or condition rather than the pace of life, but only in females. Sexually discordant selection on telomeres is expected to influence the stability and maintenance of within population variation in telomere dynamics and suggests that any role telomeres play in mediating life-history trade-offs may be sex specific.

Keywords: house sparrow; lifetime reproductive success; longevity; pace-of-life hypothesis; quality hypothesis; stressors.

Figure 1.

Plot of 250 individual linear trajectories (shaded differently) of relative telomere length sampled from nestling house sparrows at 10 days post-hatch (age = 0 years) and again one to three times later in life, with age at sampling indicated in years. Mixed model analysis (see text) revealed significant intercept and slope variation.

Figure 2.

The relationship between early-life telomere length (at 10 days post-hatching) and (a) longevity (months seen alive), and (b) lifetime reproductive success (total offspring produced across the lifetimes) of 104 house sparrows (Passer domesticus) who bred at least once. The sexes are separated by colour (48 females are red and 56 males are black) and their separate linear regressions indicated with solid lines and 95% confidence limits by the shaded areas. Significance (see text) in (a) was assessed using a Cox regression and in (b) using a GLM with a negative binomial distribution. (Online version in colour.)