Leonardo D. Bacigalupe

HERITABILITY OF ENERGETICS IN A WILD MAMMAL, THE LEAF-EARED MOUSE (PHYLLOTIS DARWINI)

Abstract.— As a first examination of the additive genetic variance of thermoregulatory traits in a natural population of endotherms, we studied the quantitative genetics of key physiological ecology traits in the leaf‐eared mouse, Phyllotis darwini. We measured basal metabolic rate (BMR), nonshivering thermogenesis (NST), maximum metabolic rate for thermoregulation (MMR), thermal conductance (CT), body temperature (Tb), and factorial aerobic scope (FAS) in individuals acclimated to cold and warm conditions. For comparability with previous studies, we included the following morphological traits: foot length (FL), total length (TL), body mass (mb, at birth, sexual maturity, 6 months, and 8 months). Variance components were obtained from two different procedures: the expected variance component in an ANOVA Type III sum of squares and an animal model approach using restricted maximum likelihood. Results suggest the presence of additive genetic variance in FL(h2= 0.47, P = 0.045), CT of cold‐acclimated animals (h2= 0.66, P = 0.041), and night body temperature, measured in cold‐acclimated animals (h2= 0.68, P = 0.080). Heritabilities of mb were near zero at all ages, but maternal effects and common environment effects were high and significant. We found no evidence of additive genetic variance in BMR, NST, MMR, or FAS (i.e., estimates were not significantly different from zero for all tests). Our results are in general agreement with previous studies of mammals that reported low heritability for: (1) BMR and MMR; (2) daytime body temperature; and (3) body mass for wild, but not laboratory or domestic, populations.

QUANTITATIVE GENETICS OF BIOENERGETICS AND GROWTH-RELATED TRAITS IN THE WILD MAMMAL, PHYLLOTIS DARWINI

Abstract We studied the potential for response to selection in typical physiological‐thermoregulatory traits of mammals such as maximum metabolic rate (MMR), nonshivering thermogenesis (NST) and basal metabolic rate (BMR) on cold‐acclimated animals. We used an animal model approach to estimate both narrow‐sense heritabilities (h2) and genetic correlations between physiological and growth‐related traits. Univariate analyses showed that MMR presented high, significant heritability (h2= 0.69±0.35, asymptotic standard error), suggesting the potential for microevolution in this variable. However, NST and presented low, nonsignificant h2, and NST showed large maternal/common environmental/nonadditive effects (c2 0.34 ± 0.17). Heritabilities were large and significant (h2 > 0.5) for all growth‐related traits (birth mass, growth rate, weaning mass). The only significant genetic correlations we found between a physiological trait and a growth‐related trait was between NST and birth mass (r= ‐0.74; P < 0.05). Overall, these results suggest that additive genetic variance is present in several bioenergetic traits, and that genetic correlations could be present between those different kinds of traits.

When Nonshivering Thermogenesis Equals Maximum Metabolic Rate: Thermal Acclimation and Phenotypic Plasticity of Fossorial Spalacopus cyanus (Rodentia)

Many small mammals inhabiting fluctuating and cold environments display enhanced capacity for seasonal changes in nonshivering thermogenesis (NST) and thermoregulatory maximum metabolic rate (MMR). However, it is not known how this plasticity remains in a mammal that rarely experiences extreme thermal fluctuations. In order to answer this question, we determined body mass (mb), basal metabolic rate (BMR), NST, MMR, and minimum thermal conductance (C) on a Chilean fossorial caviomorph (Spalacopus cyanus) from a coastal population, acclimated to cold (15°C) and warm (30°C) conditions. NST was measured as the maximum response of metabolic rate (NSTmax) after injection of norepinephrine (NE) in thermoneutrality minus BMR. Maximum metabolic rate was assessed in animals exposed to enhanced heat‐loss atmosphere (He‐O2) connected with an open‐flow respirometer. Body mass and metabolic variables increased significantly after cold acclimation with respect to warm acclimation but to a low extent (BMR, 26%; NST, 10%; and MMR, 12%). However, aerobic scope (MMR/BMR), calculated shivering thermogenesis (ST), and C did not change with acclimation regime. Our data suggest that physiological plasticity of S. cyanus is relatively low, which is in accordance with a fossorial mode of life. Although little is known about MMR and NST in fossorial mammals, S. cyanus has remarkably high NST; low MMR; and surprisingly, a nil capacity of ST when compared with other rodents.

THE QUANTITATIVE GENETICS OF SUSTAINED ENERGY BUDGET IN A WILD MOUSE

Abstract We explored how morphological and physiological traits associated with energy expenditure over long periods of cold exposure would be integrated in a potential response to natural selection in a wild mammal, Phyllotis darwini. In particular, we studied sustained energy expenditure (SusMR), the rate of expenditure fueled by concurrent energy intake, basal metabolic rate (BMR), and sustained metabolic scope (SusMS = SusMR/BMR), a measure of the reserve for sustained work. We included the masses of different central processing organs as an underlying factor that could have a mechanistic link with whole animal traits. Only the liver had heritability statistically different from zero (0.73). Physiological and morphological traits had high levels of specific environmental variance (average 70%) and postnatal common environmental variance (average 30%) which could explain the low heritabilities estimates. Our results, (1) are in accordance with previous studies in mammals that report low heritabilities for metabolic traits (SusMR, BMR, SusMS), (2) but not completely with previous ones that report high heritabilities for morphological traits (masses of central organs), and (3) provide important evidence of the relevance of postnatal common environmental variance to sustained energy expenditure.

ACTIVITY AND SPACE USE BY DEGUS: A TRADE-OFF BETWEEN THERMAL CONDITIONS AND FOOD AVAILABILITY?

Abstract We analyzed the influence of environmental temperature (open versus shaded habitat) and experimental food availability on surface activity of the degu (Octodon degus), a day-active herbivorous rodent that inhabits central Chile. We manipulated food availability and compared open and shaded study plots to determine the influence of thermal conditions on aboveground activity. Degus displayed a bimodal pattern of daily activity during relatively warmer thermal conditions in the austral autumn, whereas activity was unimodal during colder conditions in winter. However, they had a unimodal activity pattern under warm conditions in the shade when food availability was artificially enhanced in autumn. We observed more animals active in the plots where food was supplemented under all conditions. Our results illustrate spatial and temporal shifts in activity of degus involving a trade-off based on avoidance of exposure to heat and the search for food.

Ambient temperature limits above-ground activity of the subterranean rodent Spalacopus cyanus

Abstract We studied daily activity patterns of the subterranean rodent Spalacopus cyanus , in the field during summer and winter, and under laboratory conditions at two different temperatures, 15°C and 30°C. This rodent exhibited nocturnal activity in the laboratory, but diurnal above-ground activity in the field. We suggest that this discrepancy between field and laboratory results is a consequence of differential space-use inside burrows during the day, and that low external ambient temperatures appear to constrain activity of S. cyanus outside their burrows during the night in summer and winter. In contrast, we hypothesize that high summer temperatures constrain above-ground activity at midday.

The influence of heat increment of feeding on basal metabolic rate in Phyllotis darwini (Muridae)

One of the most important prerequisites for obtaining a reliable measure of basal metabolic rate (BMR) in endotherms is that the animal must be in a post-absorptive condition. However, because of the diversity of nutrition and digestion modes in vertebrates, it is not simple to generalize a standard procedure for BMR measurement. Thus, information in this regard must be experimentally obtained by measuring the heat increment of feeding (HIF). We used a repeated-measures design to test for the effects of HIF on BMR in Phyllotis darwini, a granivorous rodent. Our results suggest that, in this species, feeding induces an elevation in O(2) consumption that can persist up to 4 h after the last meal. In addition, and irrespective of the fasting period, measures made with less than 2 h of fasting yield BMR values that are significantly higher than measurements after longer fasting periods (i.e. 3 and 4 h).

Dynamic digestive responses to increased energy demands in the leaf-eared mouse (Phyllotis darwini)

A major area of interest in comparative physiology has been to understand how animals cope with changing environmental demands in time and space. The digestive system has been identified as one of the more sensitive systems to changes in environmental conditions. However, most research on this topic has evaluated these effects during peak energetic demands, which do not allow for evaluation of the dynamics of the digestive response along a more natural continuous gradient of environmental conditions. We examined phenotypic flexibility in digestive responses of the leaf-eared mouse Phyllotis darwini to increments in total energy demands (via sequential exposure to 26, 12 and 0°C). Additionally, we evaluated the effect of a moderate energy demand (12°C) over three different time periods (7, 17 and 27xa0days) on digestive traits. Moderate increases in energy demand were associated with changes in the distribution of digesta in the gut, whereas higher increases in energy demand involved increases in the tissue mass of digestive organs. Time-course analysis showed that at 12°C practically all digestive variables reached stable values within 7xa0days, which is in agreement with empirical data and theoretical deductions from cellular turnover rates. We conclude that although the input of energy and nutrients into the digestive tract is typically periodic, many aspects of digestive physiology are likely to be flexible in response to environmental variability over both short-term (daily) and long-term (seasonal) time scales.

Phenotypic Flexibility in a Novel Thermal Environment: Phylogenetic Inertia in Thermogenic Capacity and Evolutionary Adaptation in Organ Size

The goal of our work was to understand the role of a novel thermal environment in shaping the phenotypic expression of thermogenic capacity and organ size. To examine this we compared two populations of the South American rodent Phyllotis darwini from different altitudes (Andean and valley populations), taking advantage of the fact that this genus originated at high altitude in the Andean plateau. DNA mitochondrial analysis showed that the two populations were separated and then experienced different thermal regimens for at least the last 450,000 yr. We expected the two populations of P. darwini to present more metabolic and organ size similarities if phylogenetic inertia had been an important factor. In this sense, phylogenetic inertia means that the valley population would retain evolutionary adaptations of high altitude: a greater phenotypic flexibility in both physiological and morphological traits. In general, our results indicate that the actual thermogenic capacities (magnitude and flexibility) of the valley population are a consequence of phylogenetic inertia. On the other hand, results for organ size (magnitude and flexibility) could suggest that this population would have adapted to the less seasonal central valley.

FUNCTIONAL MORPHOLOGY AND GEOGRAPHIC VARIATION IN THE DIGGING APPARATUS OF CURUROS (OCTODONTIDAE: SPALACOPUS CYANUS)

Abstract We studied morphological and functional variations in jaws of coastal and mountain populations of subterranean Spalacopus cyanus inhabiting soils with contrasting hardness. We found almost no morphological differentiation between populations in the variables we measured. However, there were clear differences in incisor resistance between them. Apparently, soil hardness did not represent a selective pressure on cururos digging apparatus. An Andean origin of this genus could explain our results.