Contrasting seasonal patterns of telomere dynamics in response to environmental conditions in the ectothermic sand lizard, Lacerta agilis

Abstract

Rollings 3 & Mats olsson 1* telomeres, the protective, terminal parts of the chromosomes erode during cell division and as a result of oxidative damage by reactive oxygen species (RoS). ectotherms rely on the ambient temperature for maintaining temperature-dependent metabolic rate, regulated through behavioural thermoregulation. their temperature-dependant metabolism, hence also the RoS production, is indirectly regulated through thermoregulation. Consequently, a potential causal chain affecting telomere length and attrition is: temperature (in particular, its deviation from a species-specific optimum)-metabolism-ROS production-anti-oxidation-telomere erosion. We measured telomere length in sand lizards (Lacerta agilis) using qPCR on blood samples from 1998-2006. Effects of climatological parameters (mean temperature and average sunshine hours) in the summer and winter preceding telomere sampling were used as predictors of telomere length in mixed model analysis. During the lizards' active period (summer), there was a largely negative effect of mean temperature and sun on telomere length, whereas a combined measure of age and size (head length) was positively related to telomere length. During the inactive period of lizards (winter), the results were largely the opposite with a positive relationship between temperature and sunshine hours and telomere length. in all four cases, thermal and age effects on telomere length appeared to be non-linear in the two sexes and seasons, with complex response surface effects on telomere length from combined age and thermal effects. Telomeres are the terminal parts of the chromosomes with simple tandem repeats ending as a single-stranded t-loop 1. They keep the chromosomes intact, protecting them from degradation and end-to-end fusion 2. Telomeres shorten during replication and may reach an unstable, critical point, which induces cell arrest and apoptosis 3. Aerobic metabolism generates highly reactive and cell-damaging reactive oxygen species (ROS) 4,5 , to which G-rich telomeres are particularly sensitive 6,7. Thermal shifts restrain the oxygen delivery system and ROS production increases during heat stress, hence telomere erosion is elevated by a rise in temperature, at least in some taxa 8. The loss of telomeric bases is counterbalanced by telomerase, which elongates telomeres with its RNA template 2 , in species-specific-, chromosomal location-specific-, and chromosomal-and telomere length-specific manners (e.g. 9,10 ,). Recent years has seen an increased focus on telomere dynamics in natural populations with a focus on links to life history, reproduction, ageing trajectories and survival (e.g. 9-13 ,). Specifically, there is much interest in the relationship between environmental conditions and telomere dynamics and their long-and short-term effects in a range of taxa, but thus far ectotherms have been poorly represented in the literature 9. As ectotherms, reptiles rely on environmental conditions for maintaining their body temperature and regulate this via behavioural th...

Individual telomere dynamics and their links to life history in a viviparous lizard

“…While this pattern was broadly consistent across both populations, the relationship between telomere change and age was site-specific, with telomere length increasing with age in the cool highland population and showing no change with age in the warm lowland population. The lengthening with age in the cool highland population suggests that these lizards are investing more energy into the maintenance of somatic telomeres and/or have better balances of cellular repair processes as per the free radical/cellular repair hypothesis for ageing [33,70], or possibly lower pathogen infections [71]. The lack of telomere elongation from birth to adulthood in the warm lowland population can be interpreted as evidence that individuals in this population invest less in telomere lengthening than those in the cool highland population.…”

“…As ectotherms experience both shortening and lengthening of telomeres over time through oxidative erosion and telomerase activity, we do not necessarily expect the same pattern seen in endotherms. Indeed, telomere changes over lifetimes vary greatly across ectothermic species, with telomere length decreasing with age [31], increasing with age [32,33] or showing no relationship with age at all [34,35]. The relationship between telomere length and age can also be sex-specific [36,37], nonlinear [38][39][40] or tissue-specific [41].…”

Climate change and ageing in ectotherms

“…Both faster growth and thermal stress can cause a detrimental impact on ageing-related mechanisms, as for example inducing telomere attrition or oxidative stress. From an eco-evolutionary point of view, a species' biology and buffering mechanisms will likely define the extent to which warming will impact on ageing both at the individual or intergenerational levels Rate of ageing in regulating ageing dynamics has not been tested yet in ectotherms, but a recent study shows that higher winter and summer temperatures impact positively and negatively, respectively, on telomere lengths in a hibernating lizard (Axelsson, Wapstra, Miller, Rollings, & Olsson, 2020).…”

“…Therefore, individuals may need to adjust their use of dormancy in response to environmental temperatures, to reduce the negative effects on ageing. The possible role of this process in regulating ageing dynamics has not been tested yet in ectotherms, but a recent study shows that higher winter and summer temperatures impact positively and negatively, respectively, on telomere lengths in a hibernating lizard (Axelsson, Wapstra, Miller, Rollings, & Olsson, 2020).…”

Wing: A suitable nonlethal tissue type for repeatable and rapid telomere length estimates in bats

“…In most studies conducted on telomeres in the fields of ecology and evolution, TL is estimated from DNA extracted from venous blood across divergent taxa such as birds, large mammals and reptiles (Axelsson et al., 2020; Fairlie et al., 2016; Graham et al., 2019; Rollings et al., 2017; Seeker et al., 2018). Birds and reptiles have nucleated erythrocytes whereas mammal erythrocytes are enucleated, and therefore telomeres measured from mammalian blood derive primarily from leucocyte DNA (Nussey et al., 2014).…”