Hot and dry conditions predict shorter nestling telomeres in an endangered songbird: Implications for population persistence

Abstract

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens (Malurus coronatus), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

Keywords: climate change; early life; fitness; telomere.

Fig. 1.

Higher air temperatures in conditions of low water availability are associated with shorter early-life TL. Shown are (A) the interaction effect between season and average daily maximum temperature during the nestling period (T_max) and (B) the interaction effect between rainfall during the nestling period and T_max, predicting early-life TL. Data represent TL values z-score transformed. The regression lines and confidence intervals are based on model estimates.

Fig. 2.

For both intermediate and high warming scenarios, the change in mean fitness over a generation is negative in most simulations (59%) but overwhelmingly positive when assuming TL evolution. Model and simulations are those described in Box 1. (A and B) An intermediate warming scenario (RCP4.5) and (C and D) a high rate of warming (RCP8.5) are assumed. (A and C) Outcomes of models without adaptive evolution of TL (zero heritability) and (B and D) model outcomes assuming TL is an adaptive trait (based on estimated links to fitness and heritability). Models take into account uncertainty in parameter estimates; dashed lines represent the values predicted using point estimates of the parameters with red for negative values and blue for positive values.

Fig. 3.

Modeling the effect of climate warming across the full range of potential water availability conditions reveals a bias toward population decline. Simulations were based on predicted changes in mean fitness under any rate of warming and without evolution. For presentation purposes, the four environmental conditions (500,000 random parameter sets for p₁, p₂, p₃, and p₄) were combined into three categories: low water availability = dry season nestlings without rainfall (p₁); high water availability = wet season nestlings with rainfall (p₄); and intermediate water availability = wet season nestlings without rainfall and dry season with rainfall (p₂ + p₃). The scale represents the percentage of simulated populations that declined (0% dark blue, 100% yellow). The red-filled circle shows the prediction based on the current water availability conditions, which corresponds to declines for 59% of simulated populations (Fig. 2 A and C). The open red circle represents the most likely future water availability conditions that nestlings will encounter based on rainfall projections for the region (36) (SI Appendix, Table S3).