Extreme elevational migration spurred cryptic speciation in giant hummingbirds.

The ecoevolutionary drivers of species niche expansion or contraction are critical for biodiversity but challenging to infer. Niche expansion may be promoted by local adaptation or constrained by physiological performance trade-offs. For birds, evolutionary shifts in migratory behavior permit the broadening of the climatic niche by expansion into varied, seasonal environments. Broader niches can be short-lived if diversifying selection and geography promote speciation and niche subdivision across climatic gradients. To illuminate niche breadth dynamics, we can ask how "outlier" species defy constraints. Of the 363 hummingbird species, the giant hummingbird (Patagona gigas) has the broadest climatic niche by a large margin. To test the roles of migratory behavior, performance trade-offs, and genetic structure in maintaining its exceptional niche breadth, we studied its movements, respiratory traits, and population genomics. Satellite and light-level geolocator tracks revealed an >8,300-km loop migration over the Central Andean Plateau. This migration included a 3-wk, ~4,100-m ascent punctuated by upward bursts and pauses, resembling the acclimatization routines of human mountain climbers, and accompanied by surging blood-hemoglobin concentrations. Extreme migration was accompanied by deep genomic divergence from high-elevation resident populations, with decisive postzygotic barriers to gene flow. The two forms occur side-by-side but differ almost imperceptibly in size, plumage, and respiratory traits. The high-elevation resident taxon is the world's largest hummingbird, a previously undiscovered species that we describe and name here. The giant hummingbirds demonstrate evolutionary limits on niche breadth: when the ancestral niche expanded due to evolution (or loss) of an extreme migratory behavior, speciation followed.

Fitness surfaces and local thermal adaptation in Drosophila along a latitudinal gradient.

Local adaptation is commonly cited to explain species distribution, but how fitness varies along continuous geographical gradients is not well understood. Here, we combine thermal biology and life-history theory to demonstrate that Drosophila populations along a 2500 km latitudinal cline are adapted to local conditions. We measured how heat tolerance and viability rate across eight populations varied with temperature in the laboratory and then simulated their expected cumulative Darwinian fitness employing high-resolution temperature data from their eight collection sites. Simulations indicate a trade-off between annual survival and cumulative viability, as both mortality and the recruitment of new flies are predicted to increase in warmer regions. Importantly, populations are locally adapted and exhibit the optimal combination of both traits to maximize fitness where they live. In conclusion, our method is able to reconstruct fitness surfaces employing empirical life-history estimates and reconstructs peaks representing locally adapted populations, allowing us to study geographic adaptation in silico.

Rapid turnover of a pea aphid superclone mediated by thermal endurance in central Chile.

Global change drivers are imposing novel conditions on Earth's ecosystems at an unprecedented rate. Among them, biological invasions and climate change are of critical concern. It is generally thought that strictly asexual populations will be more susceptible to rapid environmental alterations due to their lack of genetic variability and, thus, of adaptive responses. In this study, we evaluated the persistence of a widely distributed asexual lineage of the alfalfa race of the pea aphid, Acyrthosiphon pisum, along a latitudinal transect of approximately 600 km in central Chile after facing environmental change for a decade. Based on microsatellite markers, we found an almost total replacement of the original aphid superclone by a new variant. Considering the unprecedented warming that this region has experienced in recent years, we experimentally evaluated the reproductive performance of these two A. pisum lineages at different thermal regimes. The new variant exhibits higher rates of population increase at warmer temperatures, and computer simulations employing a representative temperature dataset suggest that it might competitively displace the original superclone. These results support the idea of a superclone turnover mediated by differential reproductive performance under changing temperatures.

Climate change and population persistence in a hibernating marsupial.

Climate change has physiological consequences on organisms, ecosystems and human societies, surpassing the pace of organismal adaptation. Hibernating mammals are particularly vulnerable as winter survival is determined by short-term physiological changes triggered by temperature. In these animals, winter temperatures cannot surpass a certain threshold, above which hibernators arouse from torpor, increasing several fold their energy needs when food is unavailable. Here, we parameterized a numerical model predicting energy consumption in heterothermic species and modelled winter survival at different climate change scenarios. As a model species, we used the arboreal marsupial monito del monte (genus Dromiciops), which is recognized as one of the few South American hibernators. We modelled four climate change scenarios (from optimistic to pessimistic) based on IPCC projections, predicting that northern and coastal populations (Dromiciops bozinovici) will decline because the minimum number of cold days needed to survive the winter will not be attained. These populations are also the most affected by habitat fragmentation and changes in land use. Conversely, Andean and other highland populations, in cooler environments, are predicted to persist and thrive. Given the widespread presence of hibernating mammals around the world, models based on simple physiological parameters, such as this one, are becoming essential for predicting species responses to warming in the short term.

Temperature adaptation and its impact on the shape of performance curves in Drosophila populations.

Understanding how species adapt to different temperatures is crucial to predict their response to global warming, and thermal performance curves (TPCs) have been employed recurrently to study this topic. Nevertheless, fundamental questions regarding how thermodynamic constraints and evolution interact to shape TPCs in lineages inhabiting different environments remain unanswered. Here, we study Drosophila simulans along a latitudinal gradient spanning 3000 km to test opposing hypotheses based on thermodynamic constrains (hotter-is-better) versus biochemical adaptation (jack-of-all-temperatures) as primary determinants of TPCs variation across populations. We compare thermal responses in metabolic rate and the egg-to-adult survival as descriptors of organismal performance and fitness, respectively, and show that different descriptors of TPCs vary in tandem with mean environmental temperatures, providing strong support to hotter-is-better. Thermodynamic constraints also resulted in a strong negative association between maximum performance and thermal breadth. Lastly, we show that descriptors of TPCs for metabolism and egg-to-adult survival are highly correlated, providing evidence of co-adaptation, and that curves for egg-to-adult survival are systematically narrower and displaced toward lower temperatures. Taken together, our results support the pervasive role of thermodynamics constraining thermal responses in Drosophila populations along a latitudinal gradient, that are only partly compensated by evolutionary adaptation.

Phenotypic specialization of the pea aphid in its southern limit of distribution.

The success of biological invasions ultimately relies on phenotypic traits of the invasive species. Aphids, which include many important pests worldwide, may have been successful invading new environments partly because they can maximize reproductive output by becoming parthenogenetic and losing the sexual phase of their reproductive cycle. However, invasive populations of aphids invading wide ranges can face contrasting environmental conditions and requiring different phenotypic strategies. Besides transitions in their reproductive cycle, it is only partially known which phenotypic traits might be associated to the invasion success of aphid populations in extended novel ranges. Here, we used four genotypes of the pea aphid Acyrthosiphon pisum from two localities in Chile to test for phenotypic specialization that might explain their establishment and spread in habitats exhibiting contrasting environmental conditions. We show that lineages living at a higher latitude with low temperatures show, in addition to facultative sexual reproduction, smaller body sizes, lower metabolic rates and a higher tolerance to the cold than the obligate asexual lineages living in a mild weather, at the expense of fecundity. Conversely, at higher temperatures only asexual lineages were found, which exhibit larger body sizes, higher reproductive outputs and consequently enhanced demographic ability. As a result, in conjunction with the reproductive mode, lineage specialization in physiological and life-history traits could be taken into account as an important strategy for populations of pea aphid to effectively invade extended novel ranges comprising different climatic conditions.

Age-Dependent Behavioral and Synaptic Dysfunction Impairment Are Improved with Long-Term Andrographolide Administration in Long-Lived Female Degus (Octodon degus).

In Octodon degus, the aging process is not equivalent between sexes and worsens for females. To determine the beginning of detrimental features in females and the ways in which to improve them, we compared adult females (36 months old) and aged females (72 months old) treated with Andrographolide (ANDRO), the primary ingredient in Andrographis paniculata. Our behavioral data demonstrated that age does not affect recognition memory and preference for novel experiences, but ANDRO increases these at both ages. Sociability was also not affected by age; however, social recognition and long-term memory were lower in the aged females than adults but were restored with ANDRO. The synaptic physiology data from brain slices showed that adults have more basal synaptic efficiency than aged degus; however, ANDRO reduced basal activity in adults, while it increased long-term potentiation (LTP). Instead, ANDRO increased the basal synaptic activity and LTP in aged females. Age-dependent changes were also observed in synaptic proteins, where aged females have higher synaptotagmin (SYT) and lower postsynaptic density protein-95 (PSD95) levels than adults. ANDRO increased the N-methyl D-aspartate receptor subtype 2B (NR2B) at both ages and the PSD95 and Homer1 only in the aged. Thus, females exposed to long-term ANDRO administration show improved complex behaviors related to age-detrimental effects, modulating mechanisms of synaptic transmission, and proteins.

Why bears hibernate? Redefining the scaling energetics of hibernation.

Hibernation is a natural state of suspended animation that many mammals experience and has been interpreted as an adaptive strategy for saving energy. However, the actual amount of savings that hibernation represents, and particularly its dependence on body mass (the 'scaling') has not been calculated properly. Here, we estimated the scaling of daily energy expenditure of hibernation (DEEH), covering a range of five orders of magnitude in mass. We found that DEEH scales isometrically with mass, which means that a gram of hibernating bat has a similar metabolism to that of a gram of bear, 20 000 times larger. Given that metabolic rate of active animals scales allometrically, the point where these scaling curves intersect with DEEH represents the mass where energy savings by hibernation are zero. For BMR, these zero savings are attained for a relatively small bear (approx. 75 kg). Calculated on a per cell basis, the cellular metabolic power of hibernation was estimated to be 1.3 × 10-12 ± 2.6 × 10-13 W cell-1, which is lower than the minimum metabolism of isolated mammalian cells. This supports the idea of the existence of a minimum metabolism that permits cells to survive under a combination of cold and hypoxia.

Communal nesting is the optimal strategy for heat conservation in a social marsupial: lessons from biophysical models.

Endothermy, understood as the maintenance of continuous and high body temperatures owing to the combination of metabolic heat production and an insulative cover, is severely challenged in small endotherms inhabiting cold environments. As a response, social clustering combined with nest use (=communal nesting) is a common strategy for heat conservation. To quantify the actual amount of energy that is saved by this strategy, we studied the social marsupial Dromiciops gliroides (monito del monte), an endemic species of the cold forests of southern South America. It is hypothesized that sociability in this marsupial was driven by cold conditions, but evidence supporting this hypothesis is unclear. Here, we used taxidermic models ('mannequins') to experimentally test the energetic benefits of clustering combined with nest use. To do this, we fitted and compared cooling curves of solitary and grouped mannequins, within and outside of a nest, at the typical winter ambient temperatures of their habitat (5°C). We found that the strategy that minimized euthermic cost of maintenance was the combination of nest use and clustering, thus supporting communal nesting as a social adaptation to cope with the cold. Considering the basal metabolic rate of monitos, our estimates suggest that the savings represents almost half of energy consumption per day (in resting conditions). This study shows how simple biophysical models could help to evaluate bioenergetic hypotheses for social behavior in cold-adapted endotherms.

Thermal tolerance in Drosophila: Repercussions for distribution, community coexistence and responses to climate change.

Here we combined controlled experiments and field surveys to determine if estimates of heat tolerance predict distributional ranges and phenology of different Drosophila species in southern South America. We contrasted thermal death time curves, which consider both magnitude and duration of the challenge to estimate heat tolerance, against the thermal range where populations are viable based on field surveys in an 8-year longitudinal study. We observed a strong correspondence of the physiological limits, the thermal niche for population growth, and the geographic ranges across studied species, which suggests that the thermal biology of different species provides a common currency to understand how species will respond to warming temperatures both at a local level and throughout their distribution range. Our approach represents a novel analytical toolbox to anticipate how natural communities of ectothermic organisms will respond to global warming.

Climate Change and Thermoregulatory Consequences of Activity Time in Mammals.

Activity times structure the thermal environments experienced by organisms. In mammals, species shift from being nocturnal to diurnal and vice versa, but the thermal consequences of variable activity patterns remain largely unexplored. Here we used theoretical thermoregulatory polygons bounded by estimates of basal metabolic rates (BMR), maximum metabolic rates (MMR), and thermal conductance (C) in small mammals to explore the metabolic consequences of exposure to global-scale daytime and nighttime temperatures. Model predictions indicated higher metabolic scope for activity for nocturnal species at low latitudes and that reduced minimum C and larger body size increased the geographic range in which nocturnality was advantageous. Consistent with predictions, within rodents nocturnal species have low C. However, nocturnal mammals tend to be smaller than diurnal species, likely reflecting the importance of additional factors driving body size. Projections of warming impacts on small mammals suggest that diurnal species could lose habitable space globally. Conversely, warming could lift cool temperature constraints on nocturnal species and increase habitable space, suggesting that a shift toward nocturnal niches might be favored in a warming world. Taken together, these findings demonstrate the importance of energetic considerations for endotherms in managing global change impacts on nocturnal and diurnal species.

Thermal effects vary predictably across levels of organization: empirical results and theoretical basis.

Thermal performance curves have provided a common framework to study the impact of temperature in biological systems. However, few generalities have emerged to date. Here, we combine an experimental approach with theoretical analyses to demonstrate that performance curves are expected to vary predictably with the levels of biological organization. We measured rates of enzymatic reactions, organismal performance and population viability in Drosophila acclimated to different thermal conditions and show that performance curves become narrower with thermal optima shifting towards lower temperatures at higher levels or organization. We then explain these results on theoretical grounds, showing that this pattern reflects the cumulative impact of asymmetric thermal effects that piles up with complexity. These results and the proposed framework are important to understand how organisms, populations and ecological communities might respond to changing thermal conditions.

The interplay between ambient temperature and salt intake affects oxidative status and immune responses in a ubiquitous Neotropical passerine, the rufous-collared sparrow.

Physiological traits associated with maintenance, growth, and reproduction demand a large amount of energy and thus directly influence an animal's energy budget, which is also regulated by environmental conditions. In this study, we evaluated the interplay between ambient temperature and salinity of drinking water on energy budgets and physiological responses in adult Rufous-collared sparrow (Zonotrichia capensis), an omnivorous passerine that is ubiquitous in Chile and inhabits a wide range of environments. We acclimated birds to 30 days at two ambient temperatures (27 °C and 17 °C) and drinking water salinity (200 mM NaCl and fresh water) conditions. We evaluated: 1) the aerobic scope and the activities of mitochondrial metabolic enzymes, 2) osmoregulatory parameters, 3) the skin-swelling immune response to an antigen, 4) oxidative status, and 5) the length of telomeres of red blood cells. Our results confirm that Z. capensis tolerates the chronic consumption of moderate levels of salt, maintaining body mass but increasing their basal metabolic rates consistent with expected osmoregulatory costs. Additionally, the factorial aerobic scope was higher in birds acclimated to fresh (tap) water at both 17° and 27 °C. Drinking water salinity and low ambient temperatures negatively impacted inflammatory response, and we observed an increase in lipid peroxidation and high levels of circulating antioxidants at low temperatures. Finally, telomere length was not affected by osmo- and thermoregulatory stress. Our results did not support the existence of an interplay between environmental temperature and drinking water salinity on most physiological and biochemical traits in Z. capensis, but the negative effect of these two factors on the inflammatory immune response suggests the existence of an energetic trade-off between biological functions that act in parallel to control immune function.

A functional transcriptomic analysis in the relict marsupial Dromiciops gliroides reveals adaptive regulation of protective functions during hibernation.

The small South American marsupial, Dromiciops gliroides, known as the missing link between the American and the Australian marsupials, is one of the few South American mammals known to hibernate. Expressing both daily torpor and seasonal hibernation, this species may provide crucial information about the mechanisms and the evolutionary origins of marsupial hibernation. Here, we compared torpid and active individuals, applying high-throughput sequencing technologies (RNA-seq) to profile gene expression in three D. gliroides tissues and determine whether hibernation induces tissue-specific differential gene expression. We found 566 transcripts that were significantly up-regulated during hibernation (369 in brain, 147 in liver and 50 in skeletal muscle) and 339 that were down-regulated (225 in brain, 79 in liver and 35 in muscle). The proteins encoded by these differentially expressed genes orchestrate multiple metabolic changes during hibernation, such as inhibition of angiogenesis, prevention of muscle disuse atrophy, fuel switch from carbohydrate to lipid metabolism, protection against reactive oxygen species and repair of damaged DNA. According to the global enrichment analysis, brain cells seem to differentially regulate a complex array of biological functions (e.g., cold sensitivity, circadian perception, stress response), whereas liver and muscle cells prioritize fuel switch and heat production for rewarming. Interestingly, transcripts of thioredoxin-interacting protein (TXNIP), a potent antioxidant, were significantly over-expressed during torpor in all three tissues. These results suggest that marsupial hibernation is a controlled process where selected metabolic pathways show adaptive modulation that can help to maintain homeostasis and enhance cytoprotection in the hypometabolic state.

Terrestrial birds in coastal environments: metabolic rate and oxidative status varies with the use of marine resources.

Life in saline environments represents a major physiological challenge for birds, particularly for passerines that lack nasal salt glands and hence are forced to live in environments that do not contain salty resources. Increased energy costs associated with increased salt intake, which in turn increases the production of reactive oxygen species, is likely a major selection pressure for why passerines are largely absent from brackish and marine environments. Here we measured basal metabolic rates (BMR) and oxidative status of free-ranging individuals of three species of Cinclodes, a group of passerine birds that inhabit marine and freshwater habitats in Chile. We used a combination of carbon, nitrogen, and hydrogen isotope data from metabolically active (blood) and inert (feathers) tissues to estimate seasonal changes in marine resource use and infer altitudinal migration. Contrary to our expectations, the consumption of marine resources did not result in higher BMR values and higher oxidative stress. Specifically, the marine specialist C. nigrofumosus had lower BMR than the other two species (C. fuscus and C. oustaleti), which seasonally switch between terrestrial and marine resources. C. fuscus had significantly higher total antioxidant capacity than the other two species (C. nigrofumosus and C. oustaleti) that consumed a relatively high proportion of marine resources. Nearly all studies examining the effects of salt consumption have focused on intraspecific acclimation via controlled experiments in the laboratory. The mixed results obtained from field- and lab-based studies reflect our poor understanding of the mechanistic link among hydric-salt balance, BMR, and oxidative stress in birds.

Mitochondrial phenotype during torpor: Modulation of mitochondrial electron transport system in the Chilean mouse-opossum Thylamys elegans.

Mammalian torpor is a phenotype characterized by a controlled decline of metabolic rate, generally followed by a reduction in body temperature. During arousal from torpor, both metabolic rate and body temperature rapidly returns to resting levels. Metabolic rate reduction experienced by torpid animals is triggered by active suppression of mitochondrial respiration, which is rapidly reversed during rewarming process. In this study, we analyzed the changes in the maximal activity of key enzymes related to electron transport system (complexes I, III and IV) in six tissues of torpid, arousing and euthermic Chilean mouse-opossums (Thylamys elegans). We observed higher maximal activities of complexes I and IV during torpor in brain, heart and liver, the most metabolically active organs in mammals. On the contrary, higher enzymatic activities of complexes III were observed during torpor in kidneys and lungs. Moreover, skeletal muscle was the only tissue without significant differences among stages in all complexes evaluated, suggesting no modulation of oxidative capacities of electron transport system components in this thermogenic tissue. In overall, our data suggest that complexes I and IV activity plays a major role in initiation and maintenance of metabolic suppression during torpor in Chilean mouse-opossum, whereas improvement of oxidative capacities in complex III might be critical to sustain metabolic machinery in organs that remains metabolically active during torpor.

Phylogenetic Analysis Supports the Aerobic-Capacity Model for the Evolution of Endothermy.

The evolution of endothermy is a controversial topic in evolutionary biology, although several hypotheses have been proposed to explain it. To a great extent, the debate has centered on the aerobic-capacity model (AC model), an adaptive hypothesis involving maximum and resting rates of metabolism (MMR and RMR, respectively; hereafter "metabolic traits"). The AC model posits that MMR, a proxy of aerobic capacity and sustained activity, is the target of directional selection and that RMR is also influenced as a correlated response. Associated with this reasoning are the assumptions that (1) factorial aerobic scope (FAS; MMR/RMR) and net aerobic scope (NAS; MMR - RMR), two commonly used indexes of aerobic capacity, show different evolutionary optima and (2) the functional link between MMR and RMR is a basic design feature of vertebrates. To test these assumptions, we performed a comparative phylogenetic analysis in 176 vertebrate species, ranging from fish and amphibians to birds and mammals. Using disparity-through-time analysis, we also explored trait diversification and fitted different evolutionary models to study the evolution of metabolic traits. As predicted, we found (1) a positive phylogenetic correlation between RMR and MMR, (2) diversification of metabolic traits exceeding that of random-walk expectations, (3) that a model assuming selection fits the data better than alternative models, and (4) that a single evolutionary optimum best fits FAS data, whereas a model involving two optima (one for ectotherms and another for endotherms) is the best explanatory model for NAS. These results support the AC model and give novel information concerning the mode and tempo of physiological evolution of vertebrates.

Testing the niche variation hypothesis in a community of passerine birds.

The niche variation hypothesis (NVH) predicts that populations with broader niches should exhibit greater between-individual diet variation or individual specialization (IS) relative to populations with narrower niches. Most studies that quantify population niche widths and associated levels of IS typically focus on a single or few species, but studies examining NVH in a phylogenetically informed comparative analysis among species are lacking. Here we use nitrogen isotope (δ15 N) analysis to measure population niche widths and IS in a single bird community composed of 12 passerine species representing different foraging guilds. We found support for the NVH at the interspecific level; species with broader population niche widths were comprised of more individual specialists. Moreover, our results suggest that this relationship is influenced by foraging guild; specifically, omnivores have higher degrees of IS for a given population niche width than insectivores. Finally, the levels of IS among passerine species, in contrast to population niche width, were associated with their relatedness, suggesting that the potential phylogenetic effect on the prevalence of IS is higher than previously recognized.

Early life experience drives short-term acclimation of metabolic and osmoregulatory traits in the leaf-eared mouse.

We studied the putative effect of early life experience on the physiological flexibility of metabolic and osmoregulatory traits in the leaf-eared mouse, Phyllotis darwini, an altricial rodent inhabiting seasonal Mediterranean environments. Adult individuals were collected in central Chile and maintained in breeding pairs. Pups were isolated after weaning and acclimated to different temperatures (cold or warm) and water availability (unrestricted and restricted) until adulthood. Subsequently, individuals were re-acclimated to the opposite treatment. Rodents reared in the warm and subjected to water restriction had lower basal metabolic rate (BMR), total evaporative water loss (TEWL) and body mass (Mb) compared with those developing in the cold treatment; nevertheless, individuals subjected to warm temperatures had greater relative medullary thickness (RMT) and urine concentrating ability (UCA). Cold-reared rodents re-acclimated to warm conditions exhibited physiological flexibility of metabolic traits; however, their osmoregulatory attributes did not vary. Conversely, warm-reared rodents re-acclimated to cold had reduced RMT and UCA, but the metabolic traits of these individuals did not change. These results suggest a trade-off between metabolic performance and renal capabilities that might hinder physiological acclimation. Our results support the hypothesis of ontogenetic dependence of short-term acclimation in osmoregulatory and metabolic traits in P. darwini.