Sperm telomere length correlates with blood telomeres and body size in red‐sided garter snakes, Thamnophis sirtalis parietalis

Abstract

Telomeres, tandem repeats of TTAGGG at the ends of chromosomes, are highly dynamic structures that shorten in response to a variety of factors, including organismal stress and tissue‐specific growth rates. Cell turnover rates are frequently linked to their functions, resource availability and telomere dynamics. Using male red‐sided garter snakes, Thamnophis sirtalis parietalis, as a model, we investigated the relationship between telomere length in sperm cells, blood cells telomere length and a growth proxy (age‐adjusted body length and mass). This relationship is interesting because snakes exhibit indeterminate growth and because these garter snakes have a dissociated reproductive cycle where spermatogenesis occurs months prior to the mating season. In this study, we determined sperm telomere length (STL) and male age using qPCR and skeletochronology, respectively. Sperm telomere length correlated positively with snout–vent length (SVL) and with age‐adjusted SVL as a proxy for growth rate (residuals of size against age regression, hereafter growth), but not with age. Although an individual’s STL is correlated with blood telomere length (BTL), sperm telomeres are 60% longer than blood telomeres. In previous work, we have shown that BTL is shorter in older males and unrelated to SVL or any growth rate proxies. We hypothesized that STL is related to growth and SVL because growth and sperm production both occur during summer when resources are most abundant and stress lowest. This study is the first to compare telomere dynamics between cell types in a snake and supports growing evidence that telomere dynamics may be highly tissue‐specific and driven by the life‐history strategy of an organism.

Ectothermic telomeres: it's time they came in from the cold

“…Thus, high-level ornamentation seems to be costly and condition-dependent. In the red-sided garter snake, telomere length was positively correlated with body condition in both sexes, but overall males had much lower body condition than females and it decreased with age in males, a pattern that was mirrored in telomere loss [44].…”

“…Male and female red-sided garter snakes also differ in their corticosterone levels (higher in males) following hibernation, with males having costly mating behaviours while females have a much more passive role and reproduce biennially. Telomere erosion is predicted to be more pronounced in males than females, and this indeed proved to be the case; males had a (negative) quadratic telomere length decline with age, whereas females maintained their telomeres without noticeable attrition ( [44]; figure 3).…”

“…Ongoing differential selection on body size between the sexes, and corresponding selection in the wild on telomere length, have been demonstrated in a (correlative) quantitative genetics field study of sand lizards [40]. Such selection processes could lead to the evolution of the drastically different life-history strategies in the sexually size-dimorphic red-sided garter snake (Thamnophis sirtalis parietalis; [44]), where females grow much larger and live longer than males. Male and female red-sided garter snakes also differ in their corticosterone levels (higher in males) following hibernation, with males having costly mating behaviours while females have a much more passive role and reproduce biennially.…”

Somatic growth and telomere dynamics in vertebrates: relationships, mechanisms and consequences

“…Many ectotherms continue to grow throughout life, and also show somatic telomerase activity throughout life. This may explain why in red-sided garter snakes Thamnophis sirtalis for example [122], no relationship between telomere length and age has been found in either sex, and no difference between young and adult animals in leather-backed turtles Dermochelys coriacea [123]. In zebra fish Danio rerio, there is also apparently no telomere loss with age [124], but in other fish species such as the Atlantic salmon, age-related loss does occur [77] presumably because the telomerase activity cannot fully compensate for the telomere loss.…”

Climate change and ageing in ectotherms

“…Although telomere lengths seem to correlate among tissues (e.g. in reptiles: Rollings et al., 2019, 2020), differences in cell division and turnover rate, together with the possible tissue‐specific expression of buffering mechanisms, may imply divergent responses in ageing‐related mechanisms at the tissue level. Evidence from mammals suggests that telomere attrition rates are similar across tissues in adults, but not necessarily so in early life (Daniali et al, 2013; Sabharwal et al., 2018), so the life stage at which the temperature effects occur could be important.…”