Thermal tolerance in widespread and tropical Drosophila species: does phenotypic plasticity increase with latitude?

The distribution of insects can often be related to variation in their response to thermal extremes, which in turn may reflect differences in plastic responses or innate variation in resistance. Species with widespread distributions are expected to have evolved higher levels of plasticity than those from restricted tropical areas. This study compares adult thermal limits across five widespread species and five restricted tropical species of Drosophila from eastern Australia and investigates how these limits are affected by developmental acclimation and hardening after controlling for environmental variation and phylogeny. Irrespective of acclimation, cold resistance was higher in the widespread species. Developmental cold acclimation simulating temperate conditions extended cold limits by 2°-4°C, whereas developmental heat acclimation under simulated tropical conditions increased upper thermal limits by <1°C. The response to adult heat-hardening was weak, whereas widespread species tended to have a larger cold-hardening response that increased cold tolerance by 2°-5°C. These patterns persisted after phylogenetic correction and when flies were reared under high and low constant temperatures. The results do not support the hypothesis that widely distributed species have larger phenotypic plasticity for thermal tolerance limits, and Drosophila species distributions are therefore more closely linked to differences in innate thermal tolerance limits.     

A Comparison of Inbreeding Depression in Tropical and Widespread Drosophila Species

The evolutionary history of widespread and specialized species is likely to cause a different genetic architecture of key ecological traits in the two species groups. This may affect how these two groups respond to inbreeding. Here we investigate inbreeding effects in traits related to performance in 5 widespread and 5 tropical restricted species of Drosophila with the aim of testing whether the two species groups suffered differently from inbreeding depression. The traits investigated were egg-to-adult viability, developmental time and resistance to heat, cold and desiccation. Our results showed that levels of inbreeding depression were species and trait specific and did not differ between the species groups for stress resistance traits. However, for the life history traits developmental time and egg-to adult viability, more inbreeding depression was observed in the tropical species. The results reported suggest that for life history traits tropical species of Drosophila will suffer more from inbreeding depression than widespread species in case of increases in the rate of inbreeding e.g. due to declines in population sizes.     

A Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future

The ability to respond evolutionarily to increasing temperatures is important for survival of ectotherms in a changing climate. Recent studies suggest that upper thermal limits may be evolutionary constrained. We address this hypothesis in a laboratory evolution experiment, encompassing ecologically relevant thermal regimes. To examine the potential for species to respond to climate change, we exposed replicate populations of Drosophila melanogaster to increasing temperatures (0.3 °C every generation) for 20 generations, whereas corresponding replicate control populations were held at benign thermal conditions throughout the experiment. We hypothesized that replicate populations exposed to increasing temperatures would show increased resistance to warm and dry environments compared with replicate control populations. Contrasting replicate populations held at the two thermal regimes showed (i) an increase in desiccation resistance and a decline in heat knock‐down resistance in replicate populations exposed to increasing temperatures, (ii) similar egg‐to‐adult viability and fecundity in replicate populations from the two thermal regimes, when assessed at high stressful temperatures and (iii) no difference in nucleotide diversity between thermal regimes. The limited scope for adaptive evolutionary responses shown in this study highlights the challenges faced by ectotherms under climate change.     

Complexity of the cold acclimation response in Drosophila melanogaster

Insects can increase their resistance to cold stress when they are exposed to non-lethal conditions prior to the stress; these plastic responses are normally described only in terms of immediate effects on mortality. Here we examine in Drosophila melanogaster the short- and longer-term effects of different conditions on several measures of cold resistance, but particularly chill coma recovery. Short-term exposure to sublethal temperature (cold hardening) did not decrease chill coma recovery times even though it decreased mortality. Exposure to 12 degrees C for 2 days (acclimation) decreased chill coma recovery times for a range of stressful temperatures when flies were cultured at 25 degrees C, but did not usually affect recovery times when flies were cultured at 19 degrees C. In contrast, 2-day exposure to 12 degrees C decreased mortality regardless of rearing temperature. Rearing at 19 degrees C decreased mortality and chill coma recovery time relative to rearing at 25 degrees C. Acclimation increased the eclosion rate of eggs from stressed females, but did not affect development time or size of the offspring. These results indicate that plastic responses to cold in D. melanogaster are complex when resistance is scored in different ways, and that effects can extend across generations.     

Trait‐specific consequences of inbreeding on adaptive phenotypic plasticity

Environmental changes may stress organisms and stimulate an adaptive phenotypic response. Effects of inbreeding often interact with the environment and can decrease fitness of inbred individuals exposed to stress more so than that of outbred individuals. Such an interaction may stem from a reduced ability of inbred individuals to respond plastically to environmental stress; however, this hypothesis has rarely been tested. In this study, we mimicked the genetic constitution of natural inbred populations by rearing replicate Drosophila melanogaster populations for 25 generations at a reduced population size (10 individuals). The replicate inbred populations, as well as control populations reared at a population size of 500, were exposed to a benign developmental temperature and two developmental temperatures at the lower and upper margins of their viable range. Flies developed at the three temperatures were assessed for traits known to vary across temperatures, namely abdominal pigmentation, wing size, and wing shape. We found no significant difference in phenotypic plasticity in pigmentation or in wing size between inbred and control populations, but a significantly higher plasticity in wing shape across temperatures in inbred compared to control populations. Given that the norms of reaction for the noninbred control populations are adaptive, we conclude that a reduced ability to induce an adaptive phenotypic response to temperature changes is not a general consequence of inbreeding and thus not a general explanation of inbreeding–environment interaction effects on fitness components.     

Thermal sensitivity does not determine acclimation capacity for a tropical reef fish

1. Short-term measures of metabolic responses to warmer environments are expected to indicate the sensitivity of species to regional warming. However, given time, species may be able to acclimate to increasing temperature. Thus, it is useful to determine if short-term responses provide a good predictor for long-term acclimation ability. 2. The tropical reef fish Acanthochromis polyacanthus was used to test whether the ability for developmental thermal acclimation of two populations was indicated by their short-term metabolic response to temperature. 3. While both populations exhibited similar short-term responses of resting metabolic rate (RMR) to temperature, fish from the higher-latitude population were able to fully acclimate RMR, while the lower-latitude population could only partially compensate RMR at the warmest temperature. These differences in acclimation ability are most likely due to genetic differences between the populations rather than differences in thermal regimes. 4. This research indicates that acclimation ability may vary greatly between populations and that understanding such variation will be critical for predicting the impacts of warming environmental temperatures. Moreover, the thermal metabolic reaction norm does not appear to be a good predictor of long-term acclimation ability.     

Sensitivity to thermal extremes in Australian Drosophila implies similar impacts of climate change on the distribution of widespread and tropical species

Climatic factors influence the distribution of ectotherms, raising the possibility that distributions of many species will shift rapidly under climate change and/or that species will become locally extinct. Recent studies have compared performance curves of species from different climate zones and suggested that tropical species may be more susceptible to climate change than those from temperate environments. However, in other comparisons involving responses to thermal extremes it has been suggested that mid‐latitude populations are more susceptible. Using a group of 10 closely related Drosophila species with known tropical or widespread distribution, we undertake a detailed investigation of their growth performance curves and their tolerance to thermal extremes. Thermal sensitivity of life history traits (fecundity, developmental success, and developmental time) and adult heat resistance were similar in tropical and widespread species groups, while widespread species had higher adult cold tolerance under all acclimation regimes. Laboratory measurements of either population growth capacity or acute tolerance to heat and cold extremes were compared to daily air temperature under current (2002–2007) and future (2100) conditions to investigate if these traits could explain current distributions and, therefore, also forecast future effects of climate change. Life history traits examining the thermal sensitivity of population growth proved to be a poor predictor of current species distributions. In contrast, we validate that adult tolerance to thermal extremes provides a good correlate of current distributions. Thus, in their current distribution range, most of the examined species experience heat exposure close to, but rarely above, the functional heat resistance limit. Similarly, adult functional cold resistance proved a good predictor of species distribution in cooler climates. When using the species’ functional tolerance limits under a global warming scenario, we find that both tropical and widespread Drosophila species will face a similar proportional reduction in distribution range under future warming.     

Does cold tolerance plasticity correlate with the thermal environment and metabolic profiles of a parasitoid wasp?

Tolerance of ectotherm species to cold stress is highly plastic according to thermal conditions experienced prior to cold stress. In this study, we investigated how cold tolerance varies with developmental temperature (at 17, 25 and 30 °C) and whether developmental temperature induces different metabolic profiles. Experiments were conducted on the two populations of the parasitoid wasp, Venturia canescens, undergoing contrasting thermal regimes in their respective preferential habitat (thermally variable vs. buffered). We predicted the following: i) development at low temperatures improves the cold tolerance of parasitoid wasps, ii) the shape of the cold tolerance reaction norm differs between the two populations, and iii) these phenotypic variations are correlated with their metabolic profiles. Our results showed that habitat origin and developmental acclimation interact to determine cold tolerance and metabolic profiles of the parasitoid wasps. Cold tolerance was promoted when developmental temperatures declined and population originating from variable habitat presented a higher cold tolerance. Cold tolerance increases through the accumulation of metabolites with an assumed cryoprotective function and the depression of metabolites involved in energy metabolism. Our data provide an original example of how intraspecific cold acclimation variations correlate with metabolic response to developmental temperature.     

Temperature and photoperiod affect stress resistance traits in Drosophila melanogaster

The long‐term survival of species and populations depends on their ability to adjust phenotypic values to environmental conditions. In particular, the capability of dealing with environmental stress to buffer detrimental effects on fitness is considered to be of pivotal importance. Resistance traits are readily modulated by a wide range of environmental factors. In the present study, Drosophila melanogaster Meigen is used to investigate plastic responses to temperature and photoperiod in stress resistance traits. The results reveal that stress resistance traits (cold, heat, starvation and desiccation resistance) are affected by the factors temperature and sex predominantly. Cooler temperatures compared with warmer temperatures increase cold tolerance, desiccation and starvation resistance, whereas they reduce heat tolerance. Except for heat resistance, females are more stress‐resistant than males. Stress resistance traits are also affected by photoperiod. Shorter photoperiods decrease cold tolerance, whereas longer photoperiods enhance desiccation resistance. Overall, thermal effects are pervasive throughout all measured resistance traits, whereas photoperiodic effects are of limited importance in the directly developing (i.e. nondiapausing) flies used here, suggesting that pronounced photoperiodic effects on stress resistance traits may be largely limited to, and triggered by, diapause‐inducing effects.     

Variation in resistance and acclimation to low-temperature stress among three geographical strains of Drosophila melanogaster

Variation in cold resistance was examined in cold acclimated and non-acclimated Drosophila melanogaster from three geographical strains representing Morocco, France and Finland. Resistance was estimated as survival of adults at 0°C; the acclimation treatment involved a long-term exposure to 11°C starting from the late pupal stage and continuing with adults. After the cold stress, two fitness traits, percentage of fertile individuals and the number of adult progeny, were scored in both acclimated and non-acclimated flies. Acclimation dramatically increased survival in all strains, but did not affect the pattern of geographic variation in cold resistance. The European flies tended to be more resistant than the African ones and the ranking from most to least resistant strain was France>Finland>Morocco. In the absence of acclimation, females showed a higher survival than males. Percentage of fertile males in all strains and the number of progeny in the Finnish and French strains were decreased after acclimation. Without cold acclimation, the number of progeny was higher in the European flies as compared with the African ones. The results suggest that populations of D. melanogaster from cold climates are better adapted to low stressful temperatures and among-population variation in cold resistance may be due to non-plastic rather than plastic genetic changes. The deleterious effects of cold pretreatment on the life-history parameters indicate a possibility for acclimation costs in reproduction.     

Trait specific consequences of fast and slow inbreeding: lessons from captive populations of <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

The increased homozygosity due to inbreeding leads to expression of deleterious recessive alleles, which may cause inbreeding depression in small populations. The severity of inbreeding depression has been suggested to depend on the rate of inbreeding, with slower inbreeding being more effective in purging deleterious alleles of smaller effect. The effectiveness of purging is however dependent on various factors such as the effect of the deleterious, recessive alleles, the genetic background of inbreeding depression and the environment in which purging occurs. Investigations have shown inconclusive results as to whether purging efficiently diminish inbreeding depression. Here we used an ecologically relevant inbreeding coefficient (f ≈ 0.25) and generated ten slow and ten fast inbred lines of Drosophila melanogaster by keeping the effective population size constant at respectively 32 and 2 for 19 or 2 generations. These inbred lines were contrasted to non-inbred control lines. We investigated the effect of inbreeding and inbreeding rate in traits associated with fitness including heat, cold and desiccation stress resistance, egg-to-adult viability, development time, productivity, metabolic rate and wet weight under laboratory conditions. The results showed highly trait specific consequences of inbreeding and generally no support for the hypothesis that slow inbreeding is less deleterious than fast inbreeding. Egg-to-adult viability and development time were investigated under both benign and heat stress conditions. Reduced viability and increased developmental time were observed at stressful temperatures and inbreeding depression was on average more severe at stressful compared to benign temperatures.     

Beneficial developmental acclimation in reproductive performance under cold but not heat stress

Thermal plasticity can help organisms coping with climate change. In this study, we analyse how laboratory populations of the ectotherm species Drosophila subobscura, originally from two distinct latitudes and evolving for several generations in a stable thermal environment (18 °C), respond plastically to new thermal challenges. We measured adult performance (fecundity traits as a fitness proxy) of the experimental populations when exposed to five thermal regimes, three with the same temperature during development and adulthood (15-15 °C, 18-18 °C, 25-25 °C), and two where flies developed at 18 °C and were exposed, during adulthood, to either 15 °C or 25 °C. Here, we test whether (1) flies undergo stress at the two more extreme temperatures; (2) development at a given temperature enhances adult performance at such temperature (i.e. acclimation), and (3) populations with different biogeographical history show plasticity differences. Our findings show (1) an optimal performance at 18 °C only if flies were subjected to the same temperature as juveniles and adults; (2) the occurrence of developmental acclimation at lower temperatures; (3) detrimental effects of higher developmental temperature on adult performance; and (4) a minor impact of historical background on thermal response. Our study indicates that thermal plasticity during development may have a limited role in helping adults cope with warmer - though not colder - temperatures, with a potential negative impact on population persistence under climate change. It also emphasizes the importance of analysing the impact of temperature on all stages of the life cycle to better characterize the thermal limits.     

Environmental effects on temperature stress resistance in the tropical butterfly Bicyclus anynana

Background

The ability to withstand thermal stress is considered to be of crucial importance for individual fitness and species'' survival. Thus, organisms need to employ effective mechanisms to ensure survival under stressful thermal conditions, among which phenotypic plasticity is considered a particularly quick and effective one.

Methodology/Principal Findings

In a series of experiments we here investigate phenotypic adjustment in temperature stress resistance following environmental manipulations in the butterfly Bicyclus anynana. Cooler compared to warmer acclimation temperatures generally increased cold but decreased heat stress resistance and vice versa. In contrast, short-time hardening responses revealed more complex patterns, with, e.g., cold stress resistance being highest at intermediate hardening temperatures. Adult food stress had a negative effect on heat but not on cold stress resistance. Additionally, larval feeding treatment showed interactive effects with adult feeding for heat but not for cold stress resistance, indicating that nitrogenous larval resources may set an upper limit to performance under heat stress. In contrast to expectations, cold resistance slightly increased during the first eight days of adult life. Light cycle had marginal effects on temperature stress resistance only, with cold resistance tending to be higher during daytime and thus active periods.

Conclusions/Significance

Our results highlight that temperature-induced plasticity provides an effective tool to quickly and strongly modulate temperature stress resistance, and that such responses are readily reversible. However, resistance traits are not only affected by ambient temperature, but also by, e.g., food availability and age, making their measurement challenging. The latter effects are largely underexplored and deserve more future attention. Owing to their magnitude, plastic responses in thermal tolerance should be incorporated into models trying to forecast effects of global change on extant biodiversity.     

Stress and adaptation in conservation genetics

Stress, adaptation and evolution are major concerns in conservation biology. Stresses from pollution, climatic changes, disease etc. may affect population persistence. Further, stress typically occurs when species are placed in captivity. Threatened species are usually managed to conserve their ability to adapt to environmental changes, whilst species in captivity undergo adaptations that are deleterious upon reintroduction into the wild. In model studies using Drosophila melanogaster, we have found that; (a) inbreeding and loss of genetic variation reduced resistance to the stress of disease, (b) extinction rates under inbreeding are elevated by stress, (c) adaptive evolutionary potential in an increasingly stressful environment is reduced in small population, (d) rates of inbreeding are elevated under stressful conditions, (e) genetic adaptation to captivity reduces fitness when populations are reintroduced into the 'wild', and (f) the deleterious effects of adaptation on reintroduction success can be reduced by population fragmentation.     

Resistance to temperature extremes in sub-Antarctic weevils: interspecific variation, population differentiation and acclimation

Much of the work on the responses of terrestrial arthropods to high and low temperatures has been done on model organisms such as Drosophila . However, considerable variation in thermotolerance is partitioned at the family level and above, raising questions about the broader applicability of this work to other taxa. Here we investigate resistance to high and low temperatures, following different temperature treatments, in ten species and 31 populations of weevils found on sub-Antarctic Heard Island and Marion Island, which have substantially different climates. In these weevils there is considerable interspecific and among-population variation in critical thermal minimum (CTmin) and critical thermal maximum (CTmax), but most of this variation in critical limits can be ascribed to phenotypic plasticity. We find no relationship between CTmin and CTmax at the species level, and this is true also of populations and of responses to the temperature treatments. In general, plastic (acclimation) changes in CTmin are larger than those in CTmax. Our data therefore provide support for the idea that resistance to heat and to cold are decoupled in terrestrial arthropods. Furthermore, our results suggest that investigations of physiological limits to species borders should incorporate the effects of phenotypic plasticity on physiological capabilities.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 401–414.     

Desiccation resistance along an aridity gradient in the cactophilic fly Drosophila buzzatii: sex-specific responses to stress

Stress resistance characters are valuable tools for the study of acclimation potential, adaptive strategies and biogeographic patterns in species exposed to environmental variability. Water stress is a challenge to terrestrial arthropods because of their small size and relatively high area: volume ratio. Fruit flies have been investigated to record adaptive morphological and physiological traits, as well as to test their responses to stressful factors. In this study, we investigate the ability to cope with water stress, by examining variation in desiccation resistance in a species that lives mainly in desert lands. Specifically, we explored the genetic and ecological basis of desiccation resistance in populations of Drosophila buzzatii from Northern Argentina. We used a common garden experiment with desiccation treatments on a number of isofemale lines from four populations along an aridity gradient. Our results revealed significant among-population differentiation and substantial amounts of genetic variation for desiccation resistance. We also detected significant genotype-by-environment and genotype-by-sex interactions indicative that desiccation resistance responses of the lines assayed were environment- and sex-specific. In addition, we observed clinal variation in female desiccation resistance along gradients of altitude, temperature and humidity; that desiccation resistance is a sexually dimorphic trait, and that sexual dimorphism increased along the aridity and altitudinal gradients. Based on current evidence, we propose that the observed sex-specific responses may reflect different life history traits, and survival and reproductive strategies in different ecological scenarios.     

Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster

Recent meta-analyses conducted across a broad range of taxa have demonstrated a strong linear relationship between the change in magnitude of inbreeding depression under stress and stress level, measured as fitness loss in outbred individuals. This suggests that a general underlying response may link stress and inbreeding depression. However, this relationship is based primarily on laboratory data, and it is unknown whether natural environments with multiple stressors and fluctuating stress levels alter how stress affects inbreeding depression. To test whether the same pattern persists in the field, we investigated the effect of seasonal variation on stress level and inbreeding depression in a 3-year field study measuring the productivity of captive populations of inbred and outbred Drosophila melanogaster. We found cold winter temperatures were most stressful and induced the greatest inbreeding depression. Furthermore, these data, collected under natural field conditions, conformed to the same predictive linear relationship seen in Drosophila laboratory studies, with inbreeding depression increasing by 0.17 lethal equivalents for every 10 per cent increase in stress level. Our results suggest that under natural conditions stress level is a primary determinant of the magnitude of inbreeding depression and should be considered when assessing extinction vulnerability in small populations.     

Interactive effects of acclimation temperature and short‐term stress exposure on resistance traits in the butterfly Bicyclus anynana

The ability to buffer detrimental effects of environmental stress on fitness is of great ecological importance because, in nature, pronounced environmental variation may regularly induce stress. Furthermore, several stressors may interact in a synergistic manner. In the present study, plastic responses in cold, heat and starvation resistance are investigated in the tropical butterfly Bicyclus anynana Butler, 1879, using a full factorial design with two acclimation temperatures (20 and 27 °C) and four short‐term stress treatments (control, cold, heat, starvation). Warm‐acclimated butterflies are more heat‐ but less cold‐tolerant as expected. Short‐term cold and starvation exposure reduce cold and heat resistance, and short‐term heat exposure decreases cold but increases heat resistance. Starvation resistance is not affected by any of the short‐term treatments. Thus, the effects of short‐term stress exposure are either neutral or negative, except for a positive effect of heat exposure on heat resistance, indicating the negative effects of pre‐exposure to stress. Interestingly, significant interactions between acclimation temperature and short‐term stress exposure for heat and cold resistance are found, demonstrating that larger temperature differences incur more damage. Therefore, animals may not generally be able to benefit from pre‐exposure to stress (through ‘hardening’), depending on their previously experienced conditions. The complex interactions between environmental variation, stress and resistance are highlighted, warranting further investigations.     

Intraspecific variation in thermal acclimation and tolerance between populations of the winter ant,Prenolepis imparis

Thermal phenotypic plasticity, otherwise known as acclimation, plays an essential role in how organisms respond to short‐term temperature changes. Plasticity buffers the impact of harmful temperature changes; therefore, understanding variation in plasticity in natural populations is crucial for understanding how species will respond to the changing climate. However, very few studies have examined patterns of phenotypic plasticity among populations, especially among ant populations. Considering that this intraspecies variation can provide insight into adaptive variation in populations, the goal of this study was to quantify the short‐term acclimation ability and thermal tolerance of several populations of the winter ant, Prenolepis imparis. We tested for correlations between thermal plasticity and thermal tolerance, elevation, and body size. We characterized the thermal environment both above and below ground for several populations distributed across different elevations within California, USA. In addition, we measured the short‐term acclimation ability and thermal tolerance of those populations. To measure thermal tolerance, we used chill‐coma recovery time (CCRT) and knockdown time as indicators of cold and heat tolerance, respectively. Short‐term phenotypic plasticity was assessed by calculating acclimation capacity using CCRT and knockdown time after exposure to both high and low temperatures. We found that several populations displayed different chill‐coma recovery times and a few displayed different heat knockdown times, and that the acclimation capacities of cold and heat tolerance differed among most populations. The high‐elevation populations displayed increased tolerance to the cold (faster CCRT) and greater plasticity. For high‐temperature tolerance, we found heat tolerance was not associated with altitude; instead, greater tolerance to the heat was correlated with increased plasticity at higher temperatures. These current findings provide insight into thermal adaptation and factors that contribute to phenotypic diversity by revealing physiological variance among populations.