Evolution of Senescence in Nature: Physiological Evolution in Populations of Garter Snake with Divergent Life Histories

Abstract

Evolutionary theories of aging are linked to life-history theory in that age-specific schedules of reproduction and survival determine the trajectory of age-specific mutation/selection balances across the life span and thus the rate of senescence. This is predicted to manifest at the organismal level in the evolution of energy allocation strategies of investing in somatic maintenance and robust stress responses in less hazardous envirnments in exchange for energy spent on growth and reproduction. Here we report experiments from long-studied populations of western terrestrial garter snakes (Thamnophis elegans) that reside in low and high extrinsic mortality environments, with evolved long and short life spans, respectively. Laboratory common-environment colonies of these two ecotypes were tested for a suite of physiological traits after control and stressed gestations. In offspring derived from control and corticosteronetreated dams, we measured resting metabolism; mitochondrial oxygen consumption, ATP and free radical production rates; and erythrocyte DNA damage and repair ability. We evaluated whether these aging biomarkers mirrored the evolution of life span and whether they were sensitive to stress. Neonates from the long-lived ecotype (1) were smaller, (2) consumed equal amounts of oxygen when corrected for body mass, (3) had DNA that damaged more readily but repaired more efficiently, and (4) had more efficient mitochondria and more efficient cellular antioxidant defenses than short-lived snakes. Many ecotype differences were enhanced in offspring derived from stress-treated dams, which supports the conclusion that nongenetic maternal effects may further impact the cellular stress defenses of offspring. Our findings reveal that physiological evolution underpins reptilian life histories and sheds light on the connectedness between stress response and aging pathways in wild-dwelling organisms.

Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles

“…In this sense, the plasticity of mitochondrial energy transduction efficiency strongly varies in a phylogenetic manner and in response to environmental factors, such as season, diet and temperature (Heise et al, 2003;Sokolova, 2004;Sommer and Portner, 2004;Brand, 2005;Emel'Yanova et al, 2007;Robert and Bronikowski, 2010). However, according to the above-mentioned theory of limited resources, evolutionary force should have optimized the ATP/O ratio toward better efficiency of the mitochondrial energy transduction system in order to maximize individual fitness.…”

Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter SnakeThamnophis elegans

“…Empirical studies testing the MLBH hypothesis with ectotherms across a range of temperatures have demonstrated the ecological dependence and adaptive significance of the relationship between mass and metabolic rate (Killen et al 2010;Vaca and White 2010;Ohlberger et al 2012;Carey et al 2013), but not with universal support (Gifford et al 2013). Our estimates of scaling exponents at 207C (b p 1.33) and 247C (b p 1.23) were significantly higher than those of both adult and month-old snakes from these populations (b p 0.59 [Bronikowski and Vleck 2010]; b p 0.38-0.58 [Robert and Bronikowski 2010]). At 287C (b p 0.87) and 327C (b p 0.78), our estimates are not statistically different from the estimates from these previous studies or from the average for squamate reptiles (b p 0.80; Andrews and Pough 1985).…”

“…Population nested within ecotype was included in the model, treated as a fixed effect, to account for among-population habitat heterogeneity within ecotypes (Palacios et al 2013). We also included the random effect of litter nested within population and ecotype, which accounts for among-litter variation within populations (Robert and Bronikowski 2010). The interaction between ecotype and rearing treatment was left in the model, as this interaction is of biological interest; the remaining nonsignificant interaction terms were removed from the model (all P 1 0.35).…”

“…This divergence in life-history strategies, despite significant gene flow between populations Arnold 2005, 2006), is putatively driven by differing thermal regimes (Bronikowski 2000), resource availability (Bronikowski and Arnold 1999;Miller et al 2011), and predation rates (Sparkman et al 2013). Studies in this system have demonstrated ecotypic differences in immune investment (Sparkman and Palacios 2009;Palacios et al 2011), endocrine function Palacios et al 2012), cellular repair efficiency (Robert and Bronikowski 2010), and stress response pathways (Schwartz and Bronikowski 2012). Adult L-fast snakes have higher resting metabolic rates than M-slow snakes across 157-327C (Bronikowski and Vleck 2010), but this ecotypic difference was not present in month-old snakes reared under common laboratory conditions (Robert and Bronikowski 2010), which suggests that developmental habitats have permanent effects of metabolic rate.…”

“…Studies in this system have demonstrated ecotypic differences in immune investment (Sparkman and Palacios 2009;Palacios et al 2011), endocrine function Palacios et al 2012), cellular repair efficiency (Robert and Bronikowski 2010), and stress response pathways (Schwartz and Bronikowski 2012). Adult L-fast snakes have higher resting metabolic rates than M-slow snakes across 157-327C (Bronikowski and Vleck 2010), but this ecotypic difference was not present in month-old snakes reared under common laboratory conditions (Robert and Bronikowski 2010), which suggests that developmental habitats have permanent effects of metabolic rate. Here, we test the metabolic consequences of variation in early life thermal environment, using a 2 # 2 experimental design of captive-born neonatal garter snakes of both ecotypes reared under thermal conditions designed to mimic field ecological differences.…”