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

Significance

Heat waves are becoming more frequent, and we find that high air temperatures under dry conditions are associated with shorter telomere length in wild nestling purple-crowned fairy-wrens. Furthermore, impacts of heat exposure in nestlings may carry over into adulthood, as shorter early-life telomeres are associated with reduced lifetime fitness. Models using telomere data, fitness estimates, and climate change projections suggest that temperature-mediated telomere shortening could lead to population decline. However, the evolution of increased telomere length potentially counteracts these negative effects of warming and maintains population viability. For wildlife, increased early-life heat exposure from a warming climate may affect later life history with implications for population persistence and conservation.

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.