Francisco Bozinovic

Heat freezes niche evolution

Climate change is altering phenology and distributions of many species and further changes are projected. Can species physiologically adapt to climate warming? We analyse thermal tolerances of a large number of terrestrial ectotherm (n = 697), endotherm (n = 227) and plant (n = 1816) species worldwide, and show that tolerance to heat is largely conserved across lineages, while tolerance to cold varies between and within species. This pattern, previously documented for ectotherms, is apparent for this group and for endotherms and plants, challenging the longstanding view that physiological tolerances of species change continuously across climatic gradients. An alternative view is proposed in which the thermal component of climatic niches would overlap across species more than expected. We argue that hard physiological boundaries exist that constrain evolution of tolerances of terrestrial organisms to high temperatures. In contrast, evolution of tolerances to cold should be more frequent. One consequence of conservatism of upper thermal tolerances is that estimated niches for cold-adapted species will tend to underestimate their upper thermal limits, thereby potentially inflating assessments of risk from climate change. In contrast, species whose climatic preferences are close to their upper thermal limits will unlikely evolve physiological tolerances to increased heat, thereby being predictably more affected by warming.

Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents.

Abstract Metabolic rate is a key aspect of organismal biology and the identification of selective factors that have led to species differences is a major goal of evolutionary physiology. We tested whether environmental characteristics and/or diet were significant predictors of interspecific variation in rodent metabolic rates. Mass‐specific basal metabolic rates (BMR) and maximum metabolic rates (MMR, measured during cold exposure in a He‐O2 atmosphere) were compiled from the literature. Maximum (Tmax) and minimum (Tmin) annual mean temperatures, latitude, altitude, and precipitation were obtained from field stations close to the capture sites reported for each population (N= 57). Diet and all continuous‐valued traits showed statistically significant phylogenetic signal, with the exception of mass‐corrected MMR and altitude. Therefore, results of phylogenetic analyses are emphasized. Body mass was not correlated with absolute latitude, but was positively correlated with precipitation in analyses with phylogenetically independent contrasts. Conventional multiple regressions that included body mass indicated that Tmax (best), Tmin, latitude, and diet were significant additional predictors of BMR. However, phylogenetic analyses indicated that latitude was the only significant predictor of mass‐adjusted BMR (positive partial regression coefficient, one‐tailed P = 0.0465). Conventional analyses indicated that Tmax, Tmin (best), and altitude explained significant amounts of the variation in mass‐adjusted MMR. With body mass and Tmin in the model, no additional variables were significant predictors. Phylogenetic contrasts yielded similar results. Both conventional and phylogenetic analyses indicated a highly significant positive correlation between residual BMR and MMR (as has also been reported for birds), which is consistent with a key assumption of the aerobic capacity model for the evolution of vertebrate energetics (assuming that MMR and exercise‐induced maximal oxygen consumption are positively functionally related). Our results support the hypothesis that variation in environmental factors leads to variation in the selective regime for metabolic rates of rodents. However, the causes of a positive association between BMR and latitude remain obscure. Moreover, an important area for future research will be experiments in all taxa are raised under common conditions to allow definitive tests of climatic adaptation in endotherm metabolic rates and to elucidate the extent of adaptive phenotypic plasticity.

Maximum Metabolic Rate of Rodents: Physiological and Ecological Consequences on Distributional Limits

In this work we determine the maximum metabolic effort of rodents under extreme thermal conditions. We expected that species living under cold conditions would show higher maximum metabolic capabilities than species inhabiting tropical and intermediate habitats. Maximum weight-specific metabolic rate for temperature regulation (MMR) of rodents decreases allometrically with body size (W) but with a different slope than that for basal rate (-0 338 vs -0 25). Deviations from the MMR/W curve are apparently associated with the thermal climate of the species. Analogous species from climatically extreme environments present maximum (body-ambient) thermal differentials (ATM) and weight-specific values that depart from the A TM/Wcurve. Convergence of both MMR and ATM values was found among species with similar climatic/geographic ranges. Maximum energetic capabilities and geographic distribution appear to be correlated. Key-words: Maximum metabolic rate, rodents, thermal climate, lower lethal temperature, distributional limits

The Mean and Variance of Environmental Temperature Interact to Determine Physiological Tolerance and Fitness

Global climate change poses one of the greatest threats to biodiversity. Most analyses of the potential biological impacts have focused on changes in mean temperature, but changes in thermal variance will also impact organisms and populations. We assessed the combined effects of the mean and variance of temperature on thermal tolerances, organismal survival, and population growth in Drosophila melanogaster. Because the performance of ectotherms relates nonlinearly to temperature, we predicted that responses to thermal variation (±0° or ±5°C) would depend on the mean temperature (17° or 24°C). Consistent with our prediction, thermal variation enhanced the rate of population growth (rmax) at a low mean temperature but depressed this rate at a high mean temperature. The interactive effect on fitness occurred despite the fact that flies improved their heat and cold tolerances through acclimation to thermal conditions. Flies exposed to a high mean and a high variance of temperature recovered from heat coma faster and survived heat exposure better than did flies that developed at other conditions. Relatively high survival following heat exposure was associated with low survival following cold exposure. Recovery from chill coma was affected primarily by the mean temperature; flies acclimated to a low mean temperature recovered much faster than did flies acclimated to a high mean temperature. To develop more realistic predictions about the biological impacts of climate change, one must consider the interactions between the mean environmental temperature and the variance of environmental temperature.

Dietary and Digestive Constraints on Basal Energy Metabolism in a Small Herbivorous Rodent

McNab (1986, 1988) has hypothesized that mammals using food with low energy content should exhibit basal metabolic rates (BMR) lower than those expected on the basis of their body mass (mb). That is, those species that exploit food with low energy content and/or high cost of digestion tend to have low, mass-independent metabolic rates. To date there is not an experimental test of this pattern. The aim of this work was to examine experimentally the effect of diet quality on BMR, digestive efficiency, and the relationship between digestion and energy expenditure in a small herbivorous mammal. We used as a model the herbivorous caviomorph burrowing rodent Octodon degus (mb nearly 200 g), an inhabitant of semi-arid and mediterranean communities of northern and central Chile. Individuals maintained during 27 wk with a diet high in dietary fiber showed significantly lower BMRs (28%) than those feeding on low fiber. Daily food intake and ingestion rates (energy and dry matter) of individuals under a high-fiber diet were significantly higher than animals maintained with a low-fiber diet. The same pattern was obtained for total feces production and rate of feces production. The total intake and rate of ingestion of proteins were not significantly different between treatments. However, a significantly higher amount of protein was excreted by the individuals exposed to a high-fiber diet. Apparent digestibility of dry matter, energy, and protein were consistently lower in individuals maintained with high fiber. However, nonsignificant differences were observed between gut contents in the two treatments (P > .58), but a significantly higher digesta turnover rate was observed in animals exposed to a high-fiber diet (P < .05). A significant correlation was found between digestibility and the basal metabolic rate of individuals (r, = 0.781, P < .01), suggesting that elevated digestibilities on high-quality diets allow increased basal rates of metabolism. We suggest that, although small mammals like degus may select sparsely distributed plants of high quality in their habitat, their capability to drop their metabolic demands may help them meet their nutritional and energy requirements when nutritional conditions in the environment deteriorate.

Intrapopulational variation in the standard metabolic rate of insects: repeatability, thermal dependence and sensitivity (Q10) of oxygen consumption in a cricket.

SUMMARY Studies focusing on physiological variation among individuals, and its possible evolutionary consequences, are scarce. A trait can only be a target of natural selection if it is consistent over time, that is, a trait must be repeatable. In ectotherms it has been suggested that standard metabolic rate (MR) is related to Darwinian fitness, since it reflects energy usage and expenditure. The metabolic rate of the cricket Hophlosphyrum griseus was determined at three ambient temperatures. Repeatability of MR was estimated by product–moment correlation on residuals of body mass, as well as the thermal sensitivity of MR on an individual basis (individual Q10). The MR of H. griseus was significantly repeatable (r=0.53) and highly dependent on ambient temperature, and its sensitivity (Q10) was dependent on the temperature range. Our estimation of MR repeatability was high in comparison to published studies in vertebrates. Ours is the second report of repeatability (i.e. consistency over time of an individuals performance ranking within a population) of any aspect of energy metabolism in an insect, and also the first study to report significant repeatability of MR. Individual Q10 values revealed important interindividual variation, which reflects the existence of intrapopulational variability in the thermal sensitivity of MR. In addition, individual Q10 values were negatively correlated between temperature ranges. This means that crickets having low Q10 at low temperatures, presented high Q10 at high temperatures, and vice versa. Our results suggest that MR could be of selective value in insects, showing consistency over time and intrapopulational variability in its thermal dependence. Nevertheless, its heritability remains to be determined.

The Relationship between Diet Quality and Basal Metabolic Rate in Endotherms: Insights from Intraspecific Analysis

In this article, we review intraspecific studies of basal metabolic rate (BMR) that address the correlation between diet quality and BMR. The “food‐habit hypothesis” stands as one of the most striking and often‐mentioned interspecific patterns to emerge from studies of endothermic energetics. Our main emphasis is the explicit empirical comparison of predictions derived from interspecific studies with data gathered from within‐species studies in order to explore the mechanisms and functional significance of the putative adaptive responses encapsulated by the food‐habit hypothesis. We suggest that, in addition to concentrating on the relationship among diet quality, internal morphology, and BMR, new studies should also attempt to unravel alternative mechanisms that shape the interaction between diet and BMR, such as enzymatic plasticity, and the use of energy‐saving mechanisms, such as torpor. Another avenue for future study is the measurement of the effects of diet quality on other components of the energy budget, such as maximum thermogenic and sustainable metabolic rates. It is possible that the effects of diet quality operate on such components rather than directly on BMR, which might then push or pull along changes in these traits. Results from intraspecific studies suggest that the factors responsible for the association between diet and BMR at an ecological timescale might not be the same as those that promoted the evolution of this correlation. Further analyses should consider how much of a role the proximate and ultimate processes have played in the evolution of BMR.

Seasonal Changes in Energy Expenditure and Digestive Tract of Abrothrix andinus (Cricetidae) in the Andes Range

The South American field mouse Abrothrix andinus (Rodentia: Cricetidae) is a small mammal active throughout the year in the Andes, despite substantial seasonal environmental changes. Body mass exhibited a significant decrease during winter, and maximum metabolic rate for thermoregulation increased by 36.6%. In absolute terms, the maximum thermal differential between body and environmental temperatures increased 44° C during winter. On the other hand, body temperature and thermal conductance did not show significant changes through the year; however, mass-independent conductance decreased in winter. Parallel to these changes, the length and dry mass of the total digestive tract changed significantly with wintertime; at the same time the length and mass of the small intestine and the length of the large intestine also showed significance. Significant differences in gastrointestinal morphology between males andfemales were found only during the reproductive season (summer).

Dietary Flexibility and Intestinal Plasticity in Birds: A Field and Laboratory Study

The adaptive modulation hypothesis posits that the expression of digestive proteins should be modulated in response to intake of their respective substrates. A corollary of this hypothesis suggests that dietary flexibility and digestive plasticity should be correlated. We examined these two hypotheses in two gra‐nivorous Chilean birds (Zonotrichia capensis and Diuca diuca) that differ in dietary breadth. D. diuca is a strict granivore, whereas Z. capensis also eats insects. In field‐caught birds, the activity of the intestinal dipeptidase aminopeptidase‐N was positively correlated with intake of insects in Z. capensis but not in D. diuca. This is the first field documentation of modulation of intestinal enzymes by diet in birds. Intestinal maltase and sucrase activities were not correlated with seed (vs. insect) intake in either species. In the laboratory, captive birds of both species exhibited similar modulation of membrane‐bound intestinal hydrolases when fed on synthetic diets of contrasting carbohydrate and protein composition. Maltase, sucrase, and aminopeptidase‐N activities were significantly higher in birds fed on the carbohydrate‐free than those on the carbohydrate‐containing diet. Activities of the three enzymes were positively correlated. Therefore, this increase probably resulted from nonspecific increases of all enzymes resulting from intake of the carbohydrate‐free diet. Principal components analysis separating the effect of diet on specific and on nonspecific modulation revealed that diet had a strong effect on nonspecific activity of intestinal enzymes in both Z. capensis and D. diuca. Diet also significantly affected aminopeptidase‐N activities when the effect of diet on nonspecific modulation was removed. Birds fed on the carbohydrate‐free, high‐protein diet had significantly higher specific aminopeptidase‐N activities than those fed on the carbohydrate‐containing diet. Our results cast doubts on the notion that dietary flexibility and the plasticity of the guts enzymes are necessarily correlated and on the general validity of the adaptive modulation hypothesis.

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.