Age-related sex differences in body condition and telomere dynamics of red-sided garter snakes

Abstract

Life-history strategies vary dramatically between the sexes, which may drive divergence in sex-specific senescence and mortality rates. Telomeres are tandem nucleotide repeats that protect the ends of chromosomes from erosion during cell division. Telomeres have been implicated in senescence and mortality because they tend to shorten with stress, growth and age. We investigated age-specific telomere length in female and male red-sided garter snakes, We hypothesized that age-specific telomere length would differ between males and females given their divergent reproductive strategies. Male garter snakes emerge from hibernation with high levels of corticosterone, which facilitates energy mobilization to fuel mate-searching, courtship and mating behaviours during a two to four week aphagous breeding period at the den site. Conversely, females remain at the dens for only about 4 days and seem to invest more energy in growth and cellular maintenance, as they usually reproduce biennially. As male investment in reproduction involves a yearly bout of physiologically stressful activities, while females prioritize self-maintenance, we predicted male snakes would experience more age-specific telomere loss than females. We investigated this prediction using skeletochronology to determine the ages of individuals and qPCR to determine telomere length in a cross-sectional study. For both sexes, telomere length was positively related to body condition. Telomere length decreased with age in male garter snakes, but remained stable in female snakes. There was no correlation between telomere length and growth in either sex, suggesting that our results are a consequence of divergent selection on life histories of males and females. Different selection on the sexes may be the physiological consequence of the sexual dimorphism and mating system dynamics displayed by this species.

Evolutionary ecology of telomeres: a review

“…We predicted that telomere erosion would be more pronounced in males than females for these reasons, and this indeed proved to be correct; males have a (negative) quadratic telomere decline with age, whereas females maintain their telomeres without noticeable attrition (Fig. A–D) . Thus, identical methods used for both sexes (qPCR) by the same person (Nicky Rollings) strongly suggest that these results are robust.…”

“…Furthermore, male size does not seem to affect male mating success (and therefore age, as snakes have indeterminate growth). This may generate very different selection scenarios for males and females favoring longevity and somatic maintenance in females, as suggested by their lack of telomere attrition . Although they did not find sex‐specific effects, a similar argument, based on enhanced reproductive output in older animals, has been evoked to explain cross‐sectional patterns of telomere length increases with age in edible dormouse ( Glis glis ; using qPCR).…”

“…RTL of yellow males was significantly higher than red and blue males (B and C from Ref. ; see text) (© CRF).…”

Dynamics of telomere length in captive Siamese cobra (Naja kaouthia) related to age and sex

“…This process of gradual telomere length attrition has been linked to aging (Blackburn, 1991). Telomeres are known to shorten with increasing age in humans, some birds, and male garter snakes (Benetos et al, 2001;Bronikowski, 2008;Hausmann et al, 2003;Rollings et al, 2017). Telomeres behave as biomarkers of somatic redundancy and represent effects of other biological processes on aging (Boonekamp, Simons, Hemerik, & Verhulst, 2013;Young, 2018).…”

“…Snakes mostly exhibit genotypic sex determination for ZZ/ZW type (Laopichienpong, Muangmai, et al, 2017;Laopichienpong, Tawichasri, et al, 2017;Tawichasri et al, 2017), and telomere dynamics have been characterized in snake species including water pythons (Liasis fuscus), garter snakes (Thamnophis elegans), and red-sided garter snakes (Thamnophis sirtalis parietalis) (Bronikowski, 2008;Rollings et al, 2017;Ujvari & Madsen, 2009). The present study makes use of precise individual age records from actively maintained populations of Siamese cobra (Naja kaouthia) to improve our understanding of age-and sex-related telomere dynamics in ZZ/ ZW species.…”