Pay up or die: Tradeoffs between costly telomere maintenance, somatic growth, and body condition in embryonic and adult sand lizards

Current knowledge about telomere biology relies to a very high degree on results from research on endotherms. This would not be problematic if organisms shared the same mechanisms regulating telomere length (TL) but this is not necessarily the case; e.g., most endotherms lack, or have very low levels, of telomerase (the main telomere repair enzyme) in adult somatic tissues, whereas they appear ubiquitous in ectotherms. To what extent this will bias our understanding of TL dynamics is largely unknown, since longitudinal studies of ectotherms in the wild have been exceedingly rare. Here, we analyze TL dynamics using qPCR-based analysis on a wild population of sand lizards (Lacerta agilis), with somatic telomerase, during a field and laboratory study over a decade. We show that slower-developing embryos hatch with longer TL, embryos from mothers surviving predator attacks more recently have shorter TL, and embryos that die in incubation have shorter TL than those that hatch out successfully. Hatchling TL predicts first year survival but has only a weak effect on TL in adults, which have longer and more variable TL than hatchlings. A contributing factor to this variation is that faster-growing adults have shorter TL. Adults with greater investments into TL maintenance show poorer body condition (residuals from a mass – snout-vent length regression) in both sexes, much in agreement with metabolic costs ideas underpinning TL dynamics. In conclusion, maternal stress in embryos, and nutritional budget constraints from rapid growth consistently throughout life, dampen telomere maintenance and elongation, a process that predicts a decline in mass scaled for size (body condition). Maintained telomere length above some critical threshold is under selection through its link to embryonic- and first year survival, in particular in young males.