It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes. Age-related division of labor in honey bee colonies, a highly derived behavioral system, involves the performance of different feeding-related tasks by different groups of individuals. Older bees acquire the colony's food by foraging for nectar and pollen, and the younger ''nurse'' bees feed larvae processed foods. The transition from hive work to foraging has been shown to be socially regulated and associated both with decreases in abdominal lipid stores and with increases in brain expression of genes implicated in feeding behavior in Drosophila melanogaster. Here we show that division of labor is influenced by a canonical regulator of food intake and energy balance in solitary species, the insulin/insulin-like growth factor signaling (IIS) pathway. Foragers had higher levels of IIS gene expression in the brain and abdomen than did nurses, despite their low lipid stores. These differences are likely nutritionally mediated because manipulations that induced low lipid stores in young bees also up-regulated these genes. Changes in IIS also causally influenced the timing of behavioral maturation: inhibition of the insulin-related target of rapamycin pathway delayed the onset of foraging in a seasonally dependent manner. In addition, pathway analyses of microarray data revealed that nurses and foragers differ in brain energy metabolism gene expression, but the differences are opposite predictions based on their insulin-signaling status. These results suggest that changes in the regulation of the IIS pathway are associated with social behavior.Apis mellifera ͉ behavioral maturation ͉ social insect ͉ nutrition ͉ foraging A n important problem in biology is to understand the molecular basis for complex behavior. It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes (1). It is well established that orthologous sets of genes regulate the development of body plans across taxa (2), but this idea has only recently begun to be tested for behavior (3,4).Age-related division of labor in honey bee colonies involves the performance of different food-related tasks by different groups of individuals. Nurse bees feed brood for the first 1-2 weeks of adult life, process and store food for another week, and then shift to foraging for nectar and pollen at Ϸ2-3 weeks of age (5). This division of labor is socially regulated; bees speed up, slow down, or reverse their maturation in response to colony needs (6). Although the mechanics of foraging in honey bees are similar to food-gathering in solitary bees, there are fundamental differences. Honey bees forage to improve the fitness of the colony rather than their own; they collect food when their colony needs it. Honey bees feed on honey before exiting the hive to fuel their foraging flights, and most of the food obtained on a foraging trip is not for their own sustenance.We hypothesized that the regulation of honey bee behavioral mat...
Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.
The varroa mite, Varroa destructor Anderson & Trueman, is a devastating pest of honey bees, Apis mellifera L., that has been primarily controlled over the last 15 yr with two in-hive miticides: the organophosphate coumaphos (Checkmite+), and the pyrethroid tau-fluvalinate (Apistan). Both coumaphos and tau-fluvalinate are lipophilic compounds that are absorbed by the wax component of the hive, where they are stable and have the potential to build up over repeated treatments such that bees could be exposed to both compounds simultaneously. Although these compounds were chosen as in-hive miticides due to their low toxicity to honey bees, that low toxicity depends, at least in part, on rapid detoxification mediated by cytochrome P450 monooxygenase enzymes (P450s). In this laboratory study, we observed a large increase in the toxicity of tau-fluvalinate to 3-d-old bees that had been treated previously with coumaphos, and a moderate increase in the toxicity of coumpahos in bees treated previously with tau-fluvalinate. The observed synergism may result from competition between miticides for access to detoxicative P450s. These results suggest that honey bee mortality may occur with the application of otherwise sublethal doses of miticide when tau-fluvalinate and coumaphos are simultaneously present in the hive.
BackgroundHoney bees are exposed to phytochemicals through the nectar, pollen and propolis consumed to sustain the colony. They may also encounter mycotoxins produced by Aspergillus fungi infesting pollen in beebread. Moreover, bees are exposed to agricultural pesticides, particularly in-hive acaricides used against the parasite Varroa destructor. They cope with these and other xenobiotics primarily through enzymatic detoxificative processes, but the regulation of detoxificative enzymes in honey bees remains largely unexplored.Methodology/Principal FindingsWe used several approaches to ascertain effects of dietary toxins on bee susceptibility to synthetic and natural xenobiotics, including the acaricide tau-fluvalinate, the agricultural pesticide imidacloprid, and the naturally occurring mycotoxin aflatoxin. We administered potential inducers of cytochrome P450 enzymes, the principal biochemical system for Phase 1 detoxification in insects, to investigate how detoxification is regulated. The drug phenobarbital induces P450s in many insects, yet feeding bees with phenobarbital had no effect on the toxicity of tau-fluvalinate, a pesticide known to be detoxified by bee P450s. Similarly, no P450 induction, as measured by tau-fluvalinate tolerance, occurred in bees fed xanthotoxin, salicylic acid, or indole-3-carbinol, all of which induce P450s in other insects. Only quercetin, a common pollen and honey constituent, reduced tau-fluvalinate toxicity. In microarray comparisons no change in detoxificative gene expression was detected in phenobarbital-treated bees. However, northern blot analyses of guts of bees fed extracts of honey, pollen and propolis showed elevated expression of three CYP6AS P450 genes. Diet did not influence tau-fluvalinate or imidacloprid toxicity in bioassays; however, aflatoxin toxicity was higher in bees consuming sucrose or high-fructose corn syrup than in bees consuming honey.Conclusions/SignificanceThese results suggest that regulation of honey bee P450s is tuned to chemicals occurring naturally in the hive environment and that, in terms of toxicological capacity, a diet of sugar is not equivalent to a diet of honey.
Examining physiological traits across large spatial scales can shed light on the environmental factors driving physiological variation. For endotherms, flexibility in aerobic metabolism is especially important for coping with thermally challenging environments and recent research has shown that aerobic metabolic scope [the difference between maximum thermogenic capacity (Msum) and basal metabolic rate (BMR)] increases with latitude in mammals. One explanation for this pattern is the climatic variability hypothesis, which predicts that flexibility in aerobic metabolism should increase as a function of local temperature variability. An alternative explanation is the cold adaptation hypothesis, which predicts that cold temperature extremes may also be an important driver of variation in metabolic scope. To determine the thermal drivers of aerobic metabolic flexibility in birds, we combined data on metabolic scope from 40 bird species sampled across a range of environments with several indices of local ambient temperature. Using phylogenetically‐informed analyses, we found that minimum winter temperature was the best predictor of variation in avian metabolic scope, outperforming all other thermal variables. Additionally, Msum was a better predictor of latitudinal patterns of metabolic scope than BMR, with species inhabiting colder environments exhibiting increased Msum over their counterparts in warmer environments. Taken together, these results suggest that cold temperature extremes drive latitudinal patterns of metabolic scope via selection for enhanced thermogenic performance in cold environments, supporting the cold adaptation hypothesis. Temperature extremes may therefore be an important selective pressure driving macrophysiological trends of aerobic performance in endotherms.
1. Characterizing heat tolerance is critical for predicting an organism's vulnerability to climate warming. Recent studies of ectotherms report that impacts of climate warming are expected to be greater in the tropics, where ectotherms tend to have lower heat tolerances and experience air temperatures closer to their heat tolerance limits than their temperate counterparts. However, similar comparisons of heat tolerance are largely lacking for endotherms, and it remains an open question whether climate warming will also disproportionately affect tropical endotherms. 2. To address this empirical gap, we measured thermoregulatory responses to acute heat stress in 81 bird species (23 temperate, 58 tropical), assembling the largest comparative dataset of endothermic heat tolerances to date. 3. After controlling for body mass and experimental chamber humidity, temperate species had significantly higher heat tolerance limits (ΔHTL = 2.2°C; 45.2 vs. 43.0°C) and upper critical temperatures (ΔUCT = 1.1°C; 38.7 vs. 37.6°C) on average than tropical species. Importantly, however, these differences do not appear to impact vulnerability to climate warming, as neither thermal safety margins [i.e. the difference between upper critical temperature (UCT) and maximum air temperature, T max ] nor warming tolerances [the difference between heat tolerance limit (HTL) and T max ] differed between temperate and tropical species. We also observed substantial variation in heat tolerance among avian orders, with pigeons and doves (Columbiformes) being among the most heat tolerant species in our dataset. 4. Overall, our results suggest that, from a physiological standpoint, tropical birds may not be systematically more susceptible to climate warming than temperate birds, contrasting previous studies of ectotherms. Furthermore, we show that certain avian clades may be more resilient to warming irrespective of local climate. However, because we only sampled at one temperate and one tropical site, we caution that replication from other habitats and localities are needed to evaluate the generality of our findings.
Active flight requires the ability to efficiently fuel bursts of costly locomotion while maximizing energy conservation during non-flying times. We took a multi-faceted approach to estimate how fruit-eating bats (Uroderma bilobatum) manage a high-energy lifestyle fueled primarily by fig juice. Miniaturized heart rate telemetry shows that they use a novel, cyclic, bradycardic state that reduces daily energetic expenditure by 10% and counteracts heart rates as high as 900 bpm during flight. Uroderma bilobatum support flight with some of the fastest metabolic incorporation rates and dynamic circulating cortisol in vertebrates. These bats will exchange fat reserves within 24 hr, meaning that they must survive on the food of the day and are at daily risk of starvation. Energetic flexibly in U. bilobatum highlights the fundamental role of ecological pressures on integrative energetic networks and the still poorly understood energetic strategies of animals in the tropics.
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