Maternal glucocorticoids promote offspring growth without inducing oxidative stress or shortening telomeres in wild red squirrels

Abstract

Elevations in glucocorticoid levels (GCs) in breeding females may induce adaptive shifts in offspring life histories. Offspring produced by mothers with elevated GCs may be better prepared to face harsh environments where a faster pace of life is beneficial. We examined how experimentally elevated GCs in pregnant or lactating North American red squirrels (Tamiasciurus hudsonicus) affected offspring postnatal growth, structural size, oxidative stress levels (two antioxidants and oxidative protein damage) in three different tissues (blood, heart, liver), and liver telomere lengths. We predicted that offspring from mothers treated with GCs would grow faster but would also have higher levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring from mothers treated with GCs during pregnancy were 8.3% lighter around birth but grew (in body mass) 17.0% faster than those from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% slower than those from controls and did not differ in body mass around birth. Treating mothers with GCs during pregnancy or lactation did not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring from any of the treatment groups did not have higher oxidative stress levels or shorter telomere lengths, indicating that offspring that grew faster early in life did not exhibit oxidative costs after this period of growth. Our results indicate that elevations in maternal GCs may induce plasticity in offspring growth without long-term oxidative costs to the offspring that might result in a shortened lifespan.

Decoupling the effects of food and density on life‐history plasticity of wild animals using field experiments: Insights from the steward who sits in the shadow of its tail, the North American red squirrel

“…Crucially, the elevation in GCs was within their natural physiological range such that this was not a supraphysiological or unnatural increase in circulating GCs (van Kesteren et al, 2019). Females that were treated with exogenous GCs also produced faster growing offspring, but only if they were treated with GCs during pregnancy and not during lactation (Dantzer, van Kesteren, et al, 2020). Females with experimentally elevated GCs during lactation tended to produce slower growing offspring, which is consistent with some studies of laboratory rodents (Nephew & Bridges, 2011).…”

“…How pregnant females with elevated GCs produced faster growing offspring is not yet clear, but a reduction in litter size or a change in litter sex ratio do not appear to be the cause as experimental (fed GCs) and control females had similar litter sizes and similar litter sex ratios (Dantzer, van Kesteren, et al, 2020;Dantzer et al, 2013).…”

Parental age does not influence offspring telomeres during early life in common gulls (Larus canus)

“…This could in turn activate the production of reactive oxygen species (ROS), as well as decrease telomerase activity in the offspring (Haussmann & Heidinger, 2015), potentially leading to telomere erosion. While there are now a number of studies linking pre-natal stress to offspring telomeres (reviewed for example, in Dantzer et al 2020;Haussmann & Heidinger;, Heidinger & Young, 2020, none have included parental age in this equation. Third route are post-natal effects, as age-related variation in parental care and the characteristics of the post-birth environment could also be important mediators of offspring telomere dynamic (Tarry-Adkins et al 2009).…”

Short-term elevations in glucocorticoids do not alter telomere lengths: A systematic review and meta-analysis of non-primate vertebrate studies

“…The empirical evidence for a relationship between CORT and telomere length is mixed, with some studies showing that telomere shortening is directly related to CORT levels, and other studies finding no relationship. For example, CORT influences telomere dynamics in wild roe deer and great tits [59][60], but not in red squirrels or magellanic penguins [61][62]. These results suggest that the relationship between CORT and telomere length is species-specific.…”

“…In adult zebra finches, telomere length in red blood cells is correlated with telomere length in the spleen, liver and brain, but not muscle or heart [74]. While avian studies in our meta-analysis used red blood cells for telomere measurement, telomere length was measured in tail muscle and liver in mammals and amphibians, which could lead to discrepancies when comparing among studies [61,[75][76].…”