Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats

Abstract

Early-life adversity can affect health, survival and fitness later in life, and recent evidence suggests that telomere attrition may link early conditions with their delayed consequences. Here, we investigate the link between early-life competition and telomere length in wild meerkats. Our results show that, when multiple females breed concurrently, increases in the number of pups in the group are associated with shorter telomeres in pups. Given that pups from different litters compete for access to milk, we tested whether this effect is due to nutritional constraints on maternal milk production, by experimentally supplementing females' diets during gestation and lactation. While control pups facing high competition had shorter telomeres, the negative effects of pup number on telomere lengths were absent when maternal nutrition was experimentally improved. Shortened pup telomeres were associated with reduced survival to adulthood, suggesting that early-life competition for nutrition has detrimental fitness consequences that are reflected in telomere lengths. Dominant females commonly kill pups born to subordinates, thereby reducing competition and increasing growth rates of their own pups. Our work suggests that an additional benefit of infanticide may be that it also reduces telomere shortening caused by competition for resources, with associated benefits for offspring ageing profiles and longevity.

Keywords: Suricata suricatta; early-life adversity; early-life stress; infanticide; meerkats; telomeres.

Figure 1.

(a) The positive association between maternal age and pup telomere length at emergence from the natal burrow. The line represents the model predictions from a GLMM, with a mean pup number of 5.43. (b) The negative association between the number of competitors a pup encounters in the first weeks of life and its telomere length at emergence from the natal burrow. The line represents the model predictions from a GLMM, with an average maternal age of 4.86 years. In both figures, the points represent raw data, which are translucent for clarity. Shaded areas represent the 95% confidence intervals of each model prediction.

Figure 2.

The effect of experimental maternal feeding (during gestation and lactation) on pup telomere lengths is dependent on the number of competitor pups. In control litters (filled points and solid line), there is a negative relationship between the number of pups and telomere lengths, while in litters from mothers receiving supplementary feeding (open triangles and dashed line), this negative association disappears. Lines represent model predictions for a mean maternal age of 4.5 years, from a GLMM with telomere length as the response, and maternal age, experimental treatment and the interaction between treatment and number of pups. Shaded areas represent the model's 95% confidence intervals for each model prediction line. Points represent raw data and are jittered on the x-axis for clarity.

Figure 3.

The positive association between pup telomere length and survival to adulthood. The line represents the model predictions from a GLMM, for a pup with a dominant mother and all other significant predictors at their mean (pup weight: 230 g; maternal age: 4.8 years and group size: 19.2). The points represent raw data (jittered on the y-axis for clarity) and the shaded areas are 95% confidence intervals of the model predictions.

Figure 4.

(a) The effect of dominant female infanticidal behaviour on the probability of subordinate litters surviving their first 2 days of life. Points represent predicted means and standard errors from a binomial mixed model with dominant female infanticide risk as the only predictor. (b) The effect of infanticide by dominant females on the total number of surviving pups produced by all subordinate females in their group.