Rapid within‐ and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

Phenotypic plasticity may increase the performance and fitness and allow organisms to cope with variable environmental conditions. We studied within‐generation plasticity and transgenerational effects of thermal conditions on temperature tolerance and demographic parameters in Drosophila melanogaster. We employed a fully factorial design, in which both parental (P) and offspring generations (F1) were reared in a constant or a variable thermal environment. Thermal variability during ontogeny increased heat tolerance in P, but with demographic cost as this treatment resulted in substantially lower survival, fecundity, and net reproductive rate. The adverse effects of thermal variability (V) on demographic parameters were less drastic in flies from the F1, which exhibited higher net reproductive rates than their parents. These compensatory responses could not totally overcome the challenges of the thermally variable regime, contrasting with the offspring of flies raised in a constant temperature (C) that showed no reduction in fitness with thermal variation. Thus, the parental thermal environment had effects on thermal tolerance and demographic parameters in fruit fly. These results demonstrate how transgenerational effects of environmental conditions on heat tolerance, as well as their potential costs on other fitness components, can have a major impact on populations’ resilience to warming temperatures and more frequent thermal extremes.     

Transgenerational and within‐generation plasticity shape thermal performance curves

Thermal performance curves (TPCs) compute the effects of temperature on the performance of ectotherms and are frequently used to predict the effect of environmental conditions and currently, climate change, on organismal vulnerability and sensitivity. Using Drosophila melanogaster as an animal model, we examined how different thermal environments affected the shape of the performance curve and their parameters. We measured the climbing speed as a measure of locomotor performance in adult flies and tested the ontogenetic and transgenerational effects of thermal environment on TPC shape. Parents and offspring were reared at 28 ± 0ºC (28C), 28 ± 4ºC (28V), and 30 ± 0ºC (30C). We found that both, environmental thermal variability (28V) and high temperature (30C) experienced during early ontogeny shaped the fruit fly TPC sensitivity. Flies reared at variable thermal environments shifted the TPC to the right and increased heat tolerance. Flies held at high and constant temperature exhibited lower maximum performance than flies reared at the variable thermal environment. Furthermore, these effects were extended to the next generation. The parental thermal environment had a significative effect on TPC and its parameters. Indeed, flies reared at 28V whose parents were held at a high and constant temperature (30C) had a lower heat tolerance than F1 of flies reared at 28C or 28V. Also, offspring of flies reared at variable thermal environment (28V) reached the maximum performance at a higher temperature than offspring of flies reared at 28C or 30C. Consequently, since TPC parameters are not fixed, we suggest cautiousness when using TPCs to predict the impact of climate change on natural populations.     

Fluctuating thermal environments and time‐dependent effects on fruit fly egg‐hatching performance

Organismal performance in a changing environment is dependent on temporal patterns and duration of exposure to thermal variability. We experimentally assessed the time‐dependent effects of thermal variability (i.e., patterns of thermal exposure) on the hatching performance of Drosophila melanogaster. Flies were collected in central Chile and maintained for four generations in laboratory conditions. Fourth generation eggs were acclimated to different thermal fluctuation cycles until hatching occurred. Our results show that the frequency of extreme thermal events has a significant effect on hatching success. Eggs exposed to 24 hr cycles of thermal fluctuation had a higher proportion of eggs that hatched than those acclimated to shorter (6 and 12 hr) and longer cycles (48 hr). Furthermore, eggs subjected to frequent thermal fluctuations hatched earlier than those acclimated to less frequent thermal fluctuations. Overall, we show that, egg‐to‐adult viability is dependent on the pattern of thermal fluctuations experienced during ontogeny; thus, the pattern of thermal fluctuation experienced by flies has a significant and until now unappreciated impact on fitness.     

Ontogenetic stage-dependent effect of temperature on developmental and metabolic rates in a holometabolous insect

Different hypotheses attempt to explain how different stages of organisms with complex life cycles respond to environmental changes. Most studies have focused at the among-species level showing similar responses to temperature throughout ontogeny. However, there is no agreement about the pattern expected at the intraspecific scale where a strong selective effect is expected. In this paper, we studied the effects of thermal treatments on a life history trait (developmental rate) and a physiological trait (metabolic rate) during development in the fruitfly Drosophila buzzatii. First, we estimated the rate of development during larval life (LDR) and the pupal stage (PDR) in flies derived from two natural populations exposed to several thermal treatments. Our results showed that the developmental rate ratio, LDR/PDR, did not vary between populations, and that the effects of thermal treatments were stage specific. Second, we studied the relationship between developmental rate (DR) and metabolic rate (MR) in each life cycle stage. We found that allometric relationships between DR and MR varied throughout ontogeny, a pattern that shed light on the mechanisms responsible for thermal plasticity. We conclude that, although different populations may show developmental rate isomorphy; larvae and pupae may choose alternative “decisions” in terms of life-history evolution and physiological traits when confronted to different thermal environments.     

Strong responses of Drosophila melanogaster microbiota to developmental temperature

Physiological responses to changes in environmental conditions such as temperature may partly arise from the resident microbial community that integrates a wide range of bio-physiological aspects of the host. In the present study, we assessed the effect of developmental temperature on the thermal tolerance and microbial community of Drosophila melanogaster. We also developed a bacterial transplantation protocol in order to examine the possibility of reshaping the host bacterial composition and assessed its influence on the thermotolerance phenotype. We found that the temperature during development affected thermal tolerance and the microbial composition of male D. melanogaster. Flies that developed at low temperature (13°C) were the most cold resistant and showed the highest abundance of Wolbachia, while flies that developed at high temperature (31°C) were the most heat tolerant and had the highest abundance of Acetobacter. In addition, feeding newly eclosed flies with bacterial suspensions from intestines of flies developed at low temperatures changed the heat tolerance of recipient flies. However, we were not able to link this directly to a change in the host bacterial composition.     

Niche evolution and thermal adaptation in the temperate species Drosophila americana

The study of ecological niche evolution is fundamental for understanding how the environment influences species' geographical distributions and their adaptation to divergent environments. Here, we present a study of the ecological niche, demographic history and thermal performance (locomotor activity, developmental time and fertility/viability) of the temperate species Drosophila americana and its two chromosomal forms. Temperature is the environmental factor that contributes most to the species' and chromosomal forms' ecological niches, although precipitation is also important in the model of the southern populations. The past distribution model of the species predicts a drastic reduction in the suitable area for the distribution of the species during the last glacial maximum (LGM), suggesting a strong bottleneck. However, DNA analyses did not detect a bottleneck signature during the LGM. These contrasting results could indicate that D. americana niche preference evolves with environmental change, and thus, there is no evidence to support niche conservatism in this species. Thermal performance experiments show no difference in the locomotor activity across a temperature range of 15 to 38 °C between flies from the north and the south of its distribution. However, we found significant differences in developmental time and fertility/viability between the two chromosomal forms at the model's optimal temperatures for the two forms. However, results do not indicate that they perform better for the traits studied here in their respective optimal niche temperatures. This suggests that behaviour plays an important role in thermoregulation, supporting the capacity of this species to adapt to different climatic conditions across its latitudinal distribution.     

Seasonal morphotypes of Drosophila suzukii differ in key life‐history traits during and after a prolonged period of cold exposure

Seasonal polyphenism in Drosophila suzukii manifests itself in two discrete adult morphotypes, the “winter morph” (WM) and the “summer morph” (SM). These morphotypes are known to differ in thermal stress tolerance, and they co‐occur during parts of the year. In this study, we aimed to estimate morph‐specific survival and fecundity in laboratory settings simulating field conditions. We specifically analyzed how WM and SM D. suzukii differed in mortality and reproduction during and after a period of cold exposure resembling winter and spring conditions in temperate climates. The median lifespan of D. suzukii varied around 5 months for the WM flies and around 7 months for the SM flies. WM flies showed higher survival during the cold‐exposure period compared with SM flies, and especially SM males suffered high mortality under these conditions. In contrast, SM flies had lower mortality rates than WM flies under spring‐like conditions. Intriguingly, reproductive status (virgin or mated) did not impact the fly survival, either during the cold exposure or during spring‐like conditions. Even though the reproductive potential of WM flies was greatly reduced compared with SM flies, both WM and SM females that had mated before the cold exposure were able to continuously produce viable offspring for 5 months under spring‐like conditions. Finally, the fertility of the overwintered WM males was almost zero, while the surviving SM males did not suffer reduced fertility. Combined with other studies on D. suzukii monitoring and overwintering behavior, these results suggest that overwintered flies of both morphotypes could live long enough to infest the first commercial crops of the season. The high mortality of SM males and the low fertility of WM males after prolonged cold exposure also highlight the necessity for females to store sperm over winter to be able to start reproducing early in the following spring.     

Patterns of environmental variability influence coral‐associated bacterial and algal communities on the Mesoamerican Barrier Reef

A coral's capacity to alter its microbial symbionts may enhance its fitness in the face of climate change. Recent work predicts exposure to high environmental variability may increase coral resilience and adaptability to future climate conditions. However, how this heightened environmental variability impacts coral‐associated microbial communities remains largely unexplored. Here, we examined the bacterial and algal symbionts associated with two coral species of the genus Siderastrea with distinct life history strategies from three reef sites on the Belize Mesoamerican Barrier Reef System with low or high environmental variability. Our results reveal bacterial community structure, as well as alpha‐ and beta‐diversity patterns, vary by host species. Differences in bacterial communities between host species were partially explained by high abundance of Deltaproteobacteria and Rhodospirillales and high bacterial diversity in Siderastrea radians. Our findings also suggest Siderastrea spp. have dynamic core bacterial communities that likely drive differences observed in the entire bacterial community, which may play a critical role in rapid acclimatization to environmental change. Unlike the bacterial community, Symbiodiniaceae composition was only distinct between host species at high thermal variability sites, suggesting that different factors shape bacterial versus algal communities within the coral holobiont. Our findings shed light on how domain‐specific shifts in dynamic microbiomes may allow for unique methods of enhanced host fitness.     

Climate change reduces offspring fitness in littoral spawners: a study integrating organismic response and long‐term time‐series

Integrating long‐term ecological observations with experimental findings on species response and tolerance to environmental stress supports an understanding of climate effects on population dynamics. Here, we combine the two approaches, laboratory experiments and analysis of multi‐decadal time‐series, to understand the consequences of climate anomalies and ongoing change for the population dynamics of a eurythermal littoral species, Carcinus aestuarii. For the generation of cause and effect hypotheses we investigated the thermal response of crab embryos at four developmental stages. We first measured metabolic rate variations in embryos following acute warming (16–24 °C) and after incubation at 20 and 24 °C for limited periods. All experiments consistently revealed differential thermal responses depending on the developmental stage. Temperature‐induced changes in metabolic activity of early embryonic stages of blastula and gastrula suggested the onset of abnormal development. In contrast, later developmental stages, characterized by tissue and organ differentiation, were marginally affected by temperature anomalies, indicating enhanced resilience to thermal stress. Then, we extended these findings to a larger, population scale, by analyzing a time‐series of C. aestuarii landings in the Venice lagoon from 1945 to 2010 (ripe crabs were recorded separately) in relation to temperature. Landings and extreme climatic events showed marked long‐term and short‐term variations. We found negative relationships between landings and thermal stress indices on both timescales, with time lags consistent with an impact on crab early life stages. When quantitatively evaluating the influence of thermal stress on population dynamics, we found that it has a comparable effect to that of the biomass of spawners. This work provides strong evidence that physiological responses to climatic anomalies translate into population‐level changes and that apparently tolerant species may be impacted before the ontogeny of eurythermy. These ontogenetic bottlenecks markedly shape population dynamics and require study to assess the effects of global change.     

Host ontogeny determines parasitoid use of a forest caterpillar

For most organisms, patterns of natural enemy‐mediated mortality change over the course of development. Shifts in enemy pressure are particularly relevant for organisms that exhibit exponential growth during development, such as juvenile insects that increase their mass by several orders of magnitude. As one of the dominant groups of insect herbivores in most terrestrial plant communities, larval lepidopterans (caterpillars) are host to a diverse array of parasitoids. Previous research has described how the frequency of herbivore parasitism varies among host plants or habitats, but much less is known about how parasitism pressure changes during host development. To test whether the two major parasitoid taxa, wasps and flies, differentially attack shared hosts based on host developmental stage, we simultaneously exposed early‐ and late‐instar Euclea delphinii Boisduval (Lepidoptera: Limacodidae) caterpillars to parasitism in the field. We found strong evidence that parasitoids partition hosts by size; adult female wasps preferentially parasitized small caterpillars, whereas adult female flies preferred to attack large caterpillars. Our results demonstrate that host ontogeny is a major determinant of parasitoid host selection. Documenting how shifts in enemy pressure vary with development is important to understanding both the population biology and evolutionary ecology of prey species and their enemies.     

The multigenerational effects of water contamination and endocrine disrupting chemicals on the fitness of Drosophila melanogaster

Water pollution due to human activities produces sedimentation, excessive nutrients, and toxic chemicals, and this, in turn, has an effect on the normal endocrine functioning of living beings. Overall, water pollution may affect some components of the fitness of organisms (e.g., developmental time and fertility). Some toxic compounds found in polluted waters are known as endocrine disruptors (ED), and among these are nonhalogenated phenolic chemicals such as bisphenol A and nonylphenol. To evaluate the effect of nonhalogenated phenolic chemicals on the endocrine system, we subjected two generations (F0 and F1) of Drosophila melanogaster to different concentrations of ED. Specifically, treatments involved wastewater, which had the highest level of ED (bisphenol A and nonylphenol) and treated wastewater from a constructed Heliconia psittacorum wetland with horizontal subsurface water flow (He); the treated wastewater was the treatment with the lowest level of ED. We evaluated the development time from egg to pupa and from pupa to adult as well as fertility. The results show that for individuals exposed to treated wastewater, the developmental time from egg to pupae was shorter in individuals of the F1 generation than in the F0 generation. Additionally, the time from pupae to adult was longer for flies growing in the H. psittacorum treated wastewater. Furthermore, fertility was lower in the F1 generation than in the F0 generation. Although different concentrations of bisphenol A and nonylphenol had no significant effect on the components of fitness of D. melanogaster (developmental time and fertility), there was a trend across generations, likely as a result of selection imposed on the flies. It is possible that the flies developed different strategies to avoid the effects of the various environmental stressors.     

Summer aridity rather than management shapes fitness‐related functional traits of the threatened mountain plant Arnica montana

Semi‐natural mountain grasslands are increasingly exposed to environmental stress under climate change. However, which are the environmental factors that limit plants in these grasslands? Also, is the present management effective against these changes? Fitness‐related functional traits may offer a way to detect changes in performance and provide new insights into their vulnerability to climate change. We investigated changes in performance and variability of functional traits of the mountain grassland target species Arnica montana along a climate gradient in Central German low mountain ranges. This gradient represents at its lower end climate conditions that are expected at its upper end under future climate change. We measured vegetative, generative, and physiological traits to account for multiple ways of plant responses to the environment. Using mixed effects and multivariate models, we evaluated changes in trait values among individuals as well as the variability of their populations in order to assess performance under changing summer aridity and different management regimes. Fitness‐related performance of most traits showed strongly positive associations with reduced summer aridity at higher elevations, while only specific leaf area and leaf dry matter content showed no association. This suggests a higher performance level at less arid montane sites and that the physiological traits are less sensitive to this climate change factor. The coefficient of variation of almost all traits declined steadily with decreasing site aridity. We suggest that this reduced variability indicates a lower environmental stress level for A. montana toward its environmental optimum at montane elevations, especially because the trait performance increased simultaneously. Surprisingly, management factors and habitat characteristics had only low influence on both trait performance and variability. In summary, summer aridity had a stronger effect to shape the trait performance and variability of A. montana under increased environmental stress than management and other habitat characteristics.     

Flies evolved small bodies and cells at high or fluctuating temperatures

Recent theory predicts that the sizes of cells will evolve according to fluctuations in body temperature. Smaller cells speed metabolism during periods of warming but require more energy to maintain and repair. To evaluate this theory, we studied the evolution of cell size in populations of Drosophila melanogaster held at either a constant temperature (16°C or 25°C) or fluctuating temperatures (16 and 25°C). Populations that evolved at fluctuating temperatures or a constant 25°C developed smaller thoraxes, wings, and cells than did flies exposed to a constant 16°C. The cells of flies from fluctuating environments were intermediate in size to those of flies from constant environments. Most genetic variation in cell size was independent of variation in wing size, suggesting that cell size was a target of selection. These evolutionary patterns accord with patterns of developmental plasticity documented previously. Future studies should focus on the mechanisms that underlie the selective advantage of small cells at high or fluctuating temperatures.     

Phenotypic plasticity,but not adaptive tracking,underlies seasonal variation in post‐cold hardening freeze tolerance of Drosophila melanogaster

In temperate regions, an organism's ability to rapidly adapt to seasonally varying environments is essential for its survival. In response to seasonal changes in selection pressure caused by variation in temperature, humidity, and food availability, some organisms exhibit plastic changes in phenotype. In other cases, seasonal variation in selection pressure can rapidly increase the frequency of genotypes that offer survival or reproductive advantages under the current conditions. Little is known about the relative influences of plastic and genetic changes in short‐lived organisms experiencing seasonal environmental fluctuations. Cold hardening is a seasonally relevant plastic response in which exposure to cool, but nonlethal, temperatures significantly increases the organism's ability to later survive at freezing temperatures. In the present study, we demonstrate seasonal variation in cold hardening in Drosophila melanogaster and test the extent to which plasticity and adaptive tracking underlie that seasonal variation. We measured the post‐cold hardening freeze tolerance of flies from outdoor mesocosms over the summer, fall, and winter. We bred outdoor mesocosm‐caught flies for two generations in the laboratory and matched each outdoor cohort to an indoor control cohort of similar genetic background. We cold hardened all flies under controlled laboratory conditions and then measured their post‐cold hardening freeze tolerance. Comparing indoor and field‐caught flies and their laboratory‐reared G1 and G2 progeny allowed us to determine the roles of seasonal environmental plasticity, parental effects, and genetic changes on cold hardening. We also tested the relationship between cold hardening and other factors, including age, developmental density, food substrate, presence of antimicrobials, and supplementation with live yeast. We found strong plastic responses to a variety of field‐ and laboratory‐based environmental effects, but no evidence of seasonally varying parental or genetic effects on cold hardening. We therefore conclude that seasonal variation in post‐cold hardening freeze tolerance results from environmental influences and not genetic changes.     

Life history evolution and cellular mechanisms associated with increased size in high‐altitude Drosophila

Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.     

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.     

Ontogenetic changes in the carapace shape of the non-marine ostracod Eucypris virens (Jurine)

Developmental changes in carapace form (size+shape) during ontogeny have been explored in Eucypris virens (Crustacea, Ostracoda) using elliptic Fourier analysis. Clones from different geographic localities raised under controlled constant conditions (temperature and photoperiod) were used to characterize developmental pathways in the species. A larger data set including field populations and laboratory populations cultured under a range of environmental conditions were used to infer influence of environmental factors on carapace shape changes during ontogeny. Size changes between consecutive juvenile stages support empirical laws describing the doubling of ostracod volume at each moult. Ontogenetic changes point out the remarkable influence of environmental conditions on carapace shape.     

Seasonal polyphenism of spotted‐wing Drosophila is affected by variation in local abiotic conditions within its invaded range,likely influencing survival and regional population dynamics

1. Overwintering Drosophila often display adaptive phenotypic differences beneficial for survival at low temperatures. However, it is unclear which morphological traits are the best estimators of abiotic conditions, how those traits are correlated with functional outcomes in cold tolerance, and whether there are regional differences in trait expression.
2. We used a combination of controlled laboratory assays, and collaborative field collections of invasive Drosophila suzukii in different areas of the United States, to study the factors affecting phenotype variability of this temperate fruit pest now found globally.
3. Laboratory studies demonstrated that winter morph (WM) trait expression is continuous within the developmental temperature niche of this species (10–25°C) and that wing length and abdominal melanization are the best predictors of the larval abiotic environment.
4. However, the duration and timing of cold exposure also produced significant variation in development time, morphology, and survival at cold temperatures. During a stress test assay conducted at ?5°C, although cold tolerance was greater among WM flies, long‐term exposure to cold temperatures as adults significantly improved summer morph (SM) survival, indicating that these traits are not controlled by a single mechanism.
5. Among wild D. suzukii populations, we found that regional variation in abiotic conditions differentially affects the expression of morphological traits, although further research is needed to determine whether these differences are genetic or environmental in origin and whether thermal susceptibility thresholds differ among populations within its invaded range.