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

Abstract

Interactions at all levels of ecology are influenced by the rate at which energy is obtained, converted, and allocated. Tradeoffs in energy allocation within individuals in turn form the basis for life-history theory. Here we describe tests of the influences of temperature, developmental environment, and genetic background on measures of growth efficiency and resting metabolic rate in an ectothermic vertebrate, the western terrestrial garter snake (Thamnophis elegans). After raising captive-born snakes from divergent life-history ecotypes on thermal regimes mimicking natural habitat differences (2 # 2 experimental design of ecotype and thermal environment), we measured oxygen consumption rate at temperatures spanning the activity range of this species. We found ecotypic differences in the reaction norms of snakes across the measured range of temperatures and a temperature-dependent allometric relationship between mass and metabolic rate predicted by the metabolic-level boundaries hypothesis. Additionally, we present evidence of within-individual trade-offs between growth efficiency and resting metabolic rate, as predicted by classic lifehistory theory. These observations help illuminate the ultimate and proximate factors that underlie variation in these interrelated physiological and life-history traits.

Hormonal and metabolic responses to upper temperature extremes in divergent life-history ecotypes of a garter snake

“…Male snakes from the L-fast ecotype had higher mass-independent oxygen consumption rates across a range of non-stressful temperatures (15-32°C; Bronikowski and Vleck, 2010). Second, studies in laboratory-born offspring from these two ecotypes indicate no difference in oxygen consumption rates between neonates at 28°C (Robert and Bronikowski, 2010), but identified ecotype-specific thermal response curves in older snakes (Gangloff et al, 2015), suggesting that genetic background exerts developmental effects on resting metabolic rates. Captiveborn snakes from both ecotypes have similar CORT thermal response curves, but differ in their responses to high ambient temperatures for both liver mitochondrial H 2 O 2 production and erythrocyte superoxide concentration, two measures related to mitochondrial respiration (Schwartz and Bronikowski, 2013).…”

“…With the exception of the temperature × ecotype interaction, which is of biological interest and influences metabolic rate in this species (Gangloff et al, 2015), we removed non-significant interactions from final models. Because the ecotypes differed in mass (L-fast snakes are larger; t-test, P<0.0001), we accounted for mass by first normalizing the log 10 -tranformed mass to a mean of zero and unit variance within each ecotype so that we could test for the effect of different sizes without confounding this with ecotype.…”

“…For example, metabolic rate can be temperature insensitive within a range (Aleksiuk, 1971;Seidel and Lindeborg, 1973), be dependent on ecological role (e.g. foraging strategy; Andrews and Pough, 1985;Angilletta, 2001;Beaupre, 1993;Sears, 2005;Taylor and Davies, 1981;Zaidan, 2003;Zari, 2013) or exhibit temperature-dependent scaling with body size (Buikema and Armitage, 1969;Dmi'el, 1972;Gangloff et al, 2015;Vinegar et al, 1970). Both the standard effect of temperature to increase metabolic rate and the capacity of organisms to adjust that relationship (for example, via the effects of glucocorticoids) will determine the energetic cost of high-temperature exposure.…”

Geographic variation in thermal sensitivity of early life traits in a widespread reptile

“…All biochemical reactions are thermally dependent, but ectotherms are well known for having an inordinate fraction of their biology linked to prevailing thermal conditions (Angilletta 2009). Many of their demographic vital rates and life-history traits are influenced by temperature-dependent physiological processes, for example, metabolic rates and digestive efficiency (Huey, 1982;Peterson, Gibson, & Dorcas, 1993;White, Phillips, & Seymour, 2006), behavior (Keogh & DeSerto, 1994;Mori & Burghardt, 2001;Schieffelin & de Queiroz, 1991), and development (Birchard & Deeming, 2004;Bronikowski, 2000;Gangloff, Vleck, & Bronikowski, 2015), including temperature-dependent sex determination (TSD) in some species (Bull, 1983;Harrington, 1967;Holleley et al., 2015;Janzen & Paukstis, 1991). In many cases, freeliving adult ectotherms alter habitat use to achieve improved thermal conditions for these traits (e.g., Sunday et al, 2014).…”

Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

“…To address our second question, we quantify the influence of birth body condition and mass on growth and survival to ages four months and one year. Furthermore, we test how maternal investment might be mediated through environmental conditions by raising offspring in two different thermal regimes designed to mimic potential variation in natural habitats (Bronikowski 2000, Gangloff et al 2015. Finally, we discuss how these results may provide a potential mechanism by which phenotypic polymorphisms may be maintained in stochastic environments by fluctuating correlated selection.…”