Causes and consequences of variation in early-life telomere length in a bird metapopulation

Abstract

Environmental conditions during early-life development can have lasting effects shaping individual heterogeneity in fitness and fitness-related traits. The length of telomeres, the DNA sequences protecting chromosome ends, may be affected by early-life conditions, and telomere length (TL) has been associated with individual performance within some wild animal populations. Thus, knowledge of the mechanisms that generate variation in TL, and the relationship between TL and fitness, is important in understanding the role of telomeres in ecology and life-history evolution. Here, we investigate how environmental conditions and morphological traits are associated with early-life blood TL and if TL predicts natal dispersal probability or components of fitness in 2746 wild house sparrow (Passer domesticus) nestlings from two populations sampled across 20 years (1994-2013). We retrieved weather data and we monitored population fluctuations, individual survival, and reproductive output using field observations and genetic pedigrees. We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non-dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success. Our study showed how early-life TL is shaped by effects of growth, weather conditions, and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, shorter telomeres may be associated with a faster pace-of-life, as individuals with higher dispersal rates and annual reproduction tended to have shorter early-life TL.

Keywords: demography; dispersal; early‐life; individual heterogeneity; life‐history; pace‐of‐life; stress; telomere dynamics.

FIGURE 1

Juvenile house sparrow (Passer domesticus), Helgeland, Norway. Photo by P.S. Ranke.

FIGURE 2

Map of the house sparrow metapopulation study area in northern Norway. We measured early‐life telomere lengths in sparrows hatched on the islands of Hestmannøy and Træna. Mist netting and observations took place regularly on the black islands, which are the main inhabited islands within the monitored study area (red dotted line). Human settlements on the mainland coast east of the study area were visited in autumn and spring to search for dispersers. Weather data was retrieved from a meteorological station at the island of Myken.

FIGURE 3

The effect of population density (mean centered) on log₁₀‐transformed early‐life telomere length (TL) in (a) the Træna population (negative association) and (b) in the Hestmannøy population (no association), see Tables 1 and 2. (c) The negative quadratic association between early‐life TL and the best weather variable predictor (max. NAO index during incubation) from a sliding window analysis (Tables S2 and S3).

FIGURE 4

Binomial logistic regression of successful natal dispersal probability predicted by early‐life telomere length (TL, n = 455). The highest ranked models (Table S4) suggested a weak negative association between dispersal probability and TL (black regression line). One of these top models suggested that there was a stronger negative association between TL and dispersal probability among males born on Hestmannøy (n = 167, green regression line with 95% confidence intervals in gray areas).

FIGURE 5

Relationship between first‐year survival (recruitment) probability in two populations of house sparrows (n = 2462, gray: Træna, black: Hestmannøy) and (a) fledgling tarsus length (negative quadratic association) and (b) fledgling telomere length (no evidence for any associations). The logistic regression lines are from the top models shown in Table S6 including tarsus length (model ranked 1) and telomere length (model ranked 4). There was no evidence for differences in first‐year survival probability between the two populations.

FIGURE 6

Mortality risk measured as hazard ratio in two populations of house sparrows (n = 2462, gray: Træna, black: Hestmannøy) as a function of (a) fledgling tarsus length (positive quadratic association) and (b) fledgling telomere length (no evidence for any associations). The simulated regression lines (black) show the modeled effect from the top models in Table S7 with 95% and 50% confidence intervals in light gray and dark gray, respectively.

FIGURE 7

The associations between annual recruit production (ARS: annual reproductive success, n = 709 annual reproductive events of n = 396 individuals) and (a) fledgling tarsus length and (b) fledgling telomere length. The regressions lines (black, with 95% confidence intervals in gray) show the non‐significant tendencies (see the main text) predicted from the top models in Table S8.