Acclimation of thermal physiology in natural populations of Drosophila melanogaster : a test of an optimality model

Many organisms modify their physiological functions by acclimating to changes in their environment. Recent studies of thermal physiology have been influenced by verbal models that fail to consider the selective advantage of acclimation and thus make no predictions about variation in acclimation capacity. We used a quantitative model of optimal plasticity to generate predictions about the capacity of Drosophila melanogaster to acclimate to developmental temperature. This model predicts that the ability to acclimate thermal sensitivity should evolve when temperature varies greatly among generations. Based on the model, we expected that flies from the highly seasonal environment of New Jersey would acclimate thermal sensitivity more than would flies from the less seasonal environment of Florida. When raised at constant and fluctuating temperatures, flies from these populations failed to adjust their thermal optima in the way predicted by the model, suggesting that current assumptions about functional and genetic constraints should be reconsidered.     

A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

Evolutionary quantitative genetics of nonlinear developmental systems

In quantitative genetics, the effects of developmental relationships among traits on microevolution are generally represented by the contribution of pleiotropy to additive genetic covariances. Pleiotropic additive genetic covariances arise only from the average effects of alleles on multiple traits, and therefore the evolutionary importance of nonlinearities in development is generally neglected in quantitative genetic views on evolution. However, nonlinearities in relationships among traits at the level of whole organisms are undeniably important to biology in general, and therefore critical to understanding evolution. I outline a system for characterizing key quantitative parameters in nonlinear developmental systems, which yields expressions for quantities such as trait means and phenotypic and genetic covariance matrices. I then develop a system for quantitative prediction of evolution in nonlinear developmental systems. I apply the system to generating a new hypothesis for why direct stabilizing selection is rarely observed. Other uses will include separation of purely correlative from direct and indirect causal effects in studying mechanisms of selection, generation of predictions of medium‐term evolutionary trajectories rather than immediate predictions of evolutionary change over single generation time‐steps, and the development of efficient and biologically motivated models for separating additive from epistatic genetic variances and covariances.     

DOES ENVIRONMENTAL ROBUSTNESS PLAY A ROLE IN FLUCTUATING ENVIRONMENTS?

Fluctuating environments are expected to select for individuals that have highest geometric fitness over the experienced environments. This leads to the prediction that genetically determined environmental robustness in fitness, and average fitness across environments should be positively genetically correlated to fitness in fluctuating environments. Because quantitative genetic experiments resolving these predictions are missing, we used a full‐sib, half‐sib breeding design to estimate genetic variance for egg‐to‐adult viability in Drosophila melanogaster exposed to two constant or fluctuating temperatures that were above the species’ optimum temperature, during development. Viability in two constant environments (25°C or 30°C) was used to estimate breeding values for environmental robustness of viability (i.e., reaction norm slope) and overall viability (reaction norm elevation). These breeding values were regressed against breeding values of viability at two different fluctuating temperatures (with a mean of 25°C or 30°C). Our results based on genetic correlations show that average egg‐to‐adult viability across different constant thermal environments, and not the environmental robustness, was the most important factor for explaining the fitness in fluctuating thermal environments. Our results suggest that the role of environmental robustness in adapting to fluctuating environments might be smaller than anticipated.     

Evidence for multiple stressor interactions and effects on coral reefs

Concern is growing about the potential effects of interacting multiple stressors, especially as the global climate changes. We provide a comprehensive review of multiple stressor interactions in coral reef ecosystems, which are widely considered to be one of the most sensitive ecosystems to global change. First, we synthesized coral reef studies that examined interactions of two or more stressors, highlighting stressor interactions (where one stressor directly influences another) and potentially synergistic effects on response variables (where two stressors interact to produce an effect that is greater than purely additive). For stressor‐stressor interactions, we found 176 studies that examined at least 2 of the 13 stressors of interest. Applying network analysis to analyze relationships between stressors, we found that pathogens were exacerbated by more costressors than any other stressor, with ca. 78% of studies reporting an enhancing effect by another stressor. Sedimentation, storms, and water temperature directly affected the largest number of other stressors. Pathogens, nutrients, and crown‐of‐thorns starfish were the most‐influenced stressors. We found 187 studies that examined the effects of two or more stressors on a third dependent variable. The interaction of irradiance and temperature on corals has been the subject of more research (62 studies, 33% of the total) than any other combination of stressors, with many studies reporting a synergistic effect on coral symbiont photosynthetic performance (n = 19). Second, we performed a quantitative meta‐analysis of existing literature on this most‐studied interaction (irradiance and temperature). We found that the mean effect size of combined treatments was statistically indistinguishable from a purely additive interaction, although it should be noted that the sample size was relatively small (n = 26). Overall, although in aggregate a large body of literature examines stressor effects on coral reefs and coral organisms, considerable gaps remain for numerous stressor interactions and effects, and insufficient quantitative evidence exists to suggest that the prevailing type of stressor interaction is synergistic.     

Adaptation to fluctuating environments in a selection experiment with Drosophila melanogaster

A fundamental question in life‐history evolution is how organisms cope with fluctuating environments, including variation between stressful and benign conditions. For short‐lived organisms, environments commonly vary between generations. Using a novel experimental design, we exposed wild‐derived Drosophila melanogaster to three different selection regimes: one where generations alternated between starvation and benign conditions, and starvation was always preceded by early exposure to cold; another where starvation and benign conditions alternated in the same way, but cold shock sometimes preceded starvation and sometimes benign conditions; and a third where conditions were always benign. Using six replicate populations per selection regime, we found that selected flies increased their starvation resistance, most strongly for the regime where cold and starvation were reliably combined, and this occurred without decreased fecundity or extended developmental time. The selected flies became stress resistant, displayed a pronounced increase in early life food intake and resource storage. In contrast to previous experiments selecting for increased starvation resistance in D. melanogaster, we did not find increased storage of lipids as the main response, but instead that, in particular for females, storage of carbohydrates was more pronounced. We argue that faster mobilization of carbohydrates is advantageous in fluctuating environments and conclude that the phenotype that evolved in our experiment corresponds to a compromise between the requirements of stressful and benign environments.     

TEMPORAL VARIATION FAVORS THE EVOLUTION OF GENERALISTS IN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade‐offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments.     

Escherichia coli populations adapt to complex,unpredictable fluctuations by minimizing trade‐offs across environments

In nature, organisms are simultaneously exposed to multiple stresses (i.e. complex environments) that often fluctuate unpredictably. Although both these factors have been studied in isolation, the interaction of the two remains poorly explored. To address this issue, we selected laboratory populations of Escherichia coli under complex (i.e. stressful combinations of pH, H₂O₂ and NaCl) unpredictably fluctuating environments for ~900 generations. We compared the growth rates and the corresponding trade‐off patterns of these populations to those that were selected under constant values of the component stresses (i.e. pH, H₂O₂ and NaCl) for the same duration. The fluctuation‐selected populations had greater mean growth rate and lower variation for growth rate over all the selection environments experienced. However, whereas the populations selected under constant stresses experienced trade‐offs in the environments other than those in which they were selected, the fluctuation‐selected populations could bypass the across‐environment trade‐offs almost entirely. Interestingly, trade‐offs were found between growth rates and carrying capacities. The results suggest that complexity and fluctuations can strongly affect the underlying trade‐off structure in evolving populations.     

SEX ALLOCATION BASED ON RELATIVE AND ABSOLUTE CONDITION

Traditional models predict that organisms should allocate to sex based on their condition relative to the condition of their competitors, tracking shifts in mean condition in fluctuating environments, and maintaining an equilibrium sex ratio. In contrast, when individuals are constrained to define their condition absolutely, environmental fluctuations induce fluctuating sex ratios and the evolutionary loss of condition‐dependent sex allocation in short‐lived organisms. Here, we present a simulation model of temperature‐dependent sex determination (TSD) in fluctuating environments that specifically examines the importance of relativity in defining individual condition. When relativity in condition is allowed to evolve, short‐lived organisms evolve switchlike TSD reaction norms and define their condition relative to the annual temperature distribution, thus preventing biased cohort sex ratios in extreme years. Long‐lived organisms also evolve switchlike reaction norms, but define condition less relatively and experience biased cohort sex ratios. The predictions are supported by data from painted turtles, where TSD reaction norms exhibit pivotal temperatures of sex determination that partially track mean annual temperature. Examining relativity in amniotic vertebrates provides a conceptual framework for multifactorial sex determination and suggests new ways of exploring adaptive hypotheses of sex allocation by focusing on the importance of frequency‐dependent selection on sex.     

Between‐family variation and quantitative genetics of developmental instability of long bones in rabbit foetuses

The genetic basis of developmental instability (DI) remains largely unknown as a result of its morphological expression, fluctuating asymmetry (FA), poorly reflecting DI, especially if few traits are studied. The typically low values of heritability of FA (h²_FA) can be translated into higher values of DI (h²_DI) by the hypothetical repeatability, yet leading to wide confidence intervals. Thus, high sample sizes and/or several traits are indispensible for reaching meaningful conclusions. To obtain more insights into quantitative genetic variation of DI, we investigated between‐family variance in DI in six long bones of 1126 foetuses of the New Zealand white rabbit from a full‐sib experiment. We applied different approaches to obtain genetic parameters for DI. Heritabilities and the coefficients of between‐family variation (CVB) were calculated for six individual traits and composite indices. The results obtained, despite a likely upward bias as a result of maternal and non‐additive effects, lend support to the presence of moderate additive genetic variance for DI. It is suggested that, in foetal traits, the environmental variance was minimal, leading to a high likelihood of detecting genetic variation in DI, thus creating an ideal model system for studying the genetic basis of DI. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 33–42.     

Experimentally Manipulated Growth Rate in Threespine Sticklebacks: Assessing Trade Offs with Developmental Stability

The evolution of adaptive growth rate and its influence on how other life history traits evolve is a neglected topic in biology. Growth rate influences life history because size strongly influences age-specific survival and fecundity, and because growth rate defines the relationship between age and size. Improved predictions about the evolution of life history traits may be possible with a greater understanding of the factors that influence the evolution of growth rate. We experimentally tested the hypothesis that a trade off may exist between growth rate and developmental stability in freshwater threespine sticklebacks, Gasterosteus aculeatus. We compared the degree of developmental instability (measured as fluctuating asymmetry = FA) in four lateral plate and two fin traits of fish reared under a high vs. low growth regime in response to food ration and temperature. We found evidence that symmetry was reduced (FA increased) in fast growing compared to slow growing fish, suggesting that a trade off between developmental stability and growth is possible. FA plausibly reflected developmental instability because of significant associations between rank FA levels across traits in individuals. These results are preliminary because of the possible confounding effects of temperature and food ration on asymmetry, and because we do not know if this trade off has fitness or other life history consequences. Our results also do not support the hypothesis of honest signaling sometimes invoked in studies of sexual selection because greater symmetry was found under poorer rather than better resource levels.     

Temperature‐dependent development of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae) at seven constant temperatures

Abstract The effect of seven constant temperatures of 15, 20, 25, 27, 30, 35 and 37°C on developmental time of Neoseiulus barkeri Hughes were determined in laboratory conditions under 65%± 5% RH and a photoperiod of 12 : 12 (L : D) h on nymphal stages of Tetranychus urticae Koch. Total developmental time of females (from egg to adult emergence) at the above‐mentioned temperatures was 26.59, 14.43, 6.32, 5.64, 4.59, 3.98 and 4.67 days, respectively. Developmental rate of the N. barkeri increased as temperature increased from 15 to 35°C, but declined at 37°C. A linear and two nonlinear models were fitted to developmental rate of immature stages of N. barkeri to predict the developmental rate as a function of temperature, as well as to estimate the thermal constant (K) and critical temperatures (i.e., T_min, T_opt and T_max). The estimated values of the T_min and K for total developmental time using the linear model were 12.07°C and 86.20 degree‐days (DD), respectively. The T_min and T_max estimated by the Sharpe‐Schoolfield‐Ikemoto (SSI) model were 11.90°C and 37.41°C, respectively. The estimated T_opt for overall immature stage development of N. barkeri by the Lactin and SSI models were 33.89°C and 24.51°C, respectively. Based on the biological criteria of model evaluation, the linear and SSI models were found to be the best models for describing the developmental rate of overall immature stages of N. barkeri and estimating the temperature thresholds.     

How a thermal dichotomy in nesting environments influences offspring of the world's most northerly oviparous snake,Natrix natrix (Colubridae)

Temperature has a major influence on the rate of embryonic development in ectothermic organisms. While incubation experiments unambiguously show that constant high temperature accelerates development and shortens embryonic life, studies on the effect of fluctuating temperatures have generated contradictory results. Grass snakes (Natrix natrix) occur at latitudes and altitudes that are unusually cool for an oviparous reptile. In these cool climates females typically lay their eggs in heat‐generating anthropogenic microhabitats that provide either a highly fluctuating (compost piles) or a relatively constant (manure heaps) thermal nesting environment. A laboratory experiment with fluctuating and constant incubation temperatures mimicking those recorded in such nests in the field showed that this nest‐site dichotomy influences the development of the embryos, and the morphology and locomotor performance of the hatchlings. The incubation period increased at fluctuating temperatures and the fact that the rate of embryonic development showed a decelerating pattern with temperature suggests that periods of low temperature had a relatively larger influence on average development than periods of high temperature. Our study demonstrates how a dichotomy in the nesting environments available to female grass snakes in cool climates can affect variation in the duration of the incubation period and offspring phenotypes in ways that may have consequences for fitness. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Influence of temperature and photoperiod on embryonic development in the dragonfly Sympetrum striolatum (Odonata: Libellulidae)

Temperature and photoperiod play major roles in insect ecology. Many insect species have fixed degree‐days for embryogenesis, with minimum and maximum temperature thresholds for egg and larval development and hatching. Often, photoperiodic changes trigger the transfer into the next life‐cycle stadium. However, it is not known whether this distinct pattern also exist in a species with a high level of phenotypic plasticity in life‐history traits. In the present study, eggs of the dragonfly Sympetrum striolatum Charpentier (Odonata: Libellulidae) are reared under different constant and fluctuating temperatures and photoperiodic conditions in several laboratory and field experiments. In general, and as expected, higher temperatures cause faster egg development. However, no general temperature or light‐days for eyespot development and hatching are found. The minimum temperature thresholds are distinguished for survival (2 °C), embryogenesis (6 °C) and larval hatching (above 6 °C). Low winter temperatures synchronize hatching. Above 36 °C, no eyespots are visible and no larvae hatch. In laboratory experiments, light is neither necessary for eyespot development, nor for hatching. By contrast to the laboratory experiments, the field experiment show that naturally changing temperature and photoperiod play a significant role in the seasonal regulation of embryonic development. The post‐eyespot development is more variable and influenced by temperature and photoperiod than the pre‐eyespot development. This developmental plasticity at the end of the embryogenesis might be a general pattern in the Libellulidae, helping them to cope with variation in environmental conditions.     

DEVELOPMENTAL STABILITY OF RAINBOW TROUT HYBRIDS: GENOMIC COADAPTATION OR HETEROZYGOSITY?

I compare the developmental stability of first generation hybrids between hatchery strains of rainbow trout (Salmo gairdneri) to that of the three pure parental strains raised in a common environment. Two of three reciprocal hybrid pairs show significantly less fluctuating asymmetry of four meristic characters than is found in parental strains. In contrast, the third hybrid pair shows reduced but not significantly lower developmental stability compared to pure strains. These hybrids had previously been found to develop slower than their maternal parental strains, indicating divergence of parental regulatory mechanisms controlling early ontogeny. A significant positive association between the degree of relative delay in hybrid developmental rate and their degree of developmental instability supports this view. For example, the only hybrid pair with decreased developmental stability also had the largest relative delay in development time of all hybrids. Neither absolute developmental rate nor enzyme heterozygosity at 42 loci alone can explain the degree of fluctuating asymmetry in these hybrids. The developmental stability of hybrids is apparently a result of the interaction between the developmental divergence between parental strains and their genomic heterozygosity due to hybridization.     

Effects of diurnal temperature range on adult size and emergence times from diapausing pupae in Papilio glaucus and P. canadensis (Papilionidae)

Abstract With recent climate warming trends, both the increase in thermal variance (i.e., diurnal temperature range; DTR) as well as increased mean temperature may impact many different organisms, especially poikilothermic invertebrates. Predictions of insect developmental rates using degree‐days (thermal unit accumulations above the developmental base threshold of the insect) are based on daily mean temperatures, regardless of DTR. However, non‐linearity and variance in the means and extremes are often ignored. The role of thermal variance (e.g., daily temperature extremes and DTR) was evaluated experimentally for two swallowtail butterfly sister species using a common day/night photoperiod of 18: 6 h photo: scoto‐phase and corresponding daytime thermophase and nighttime cryophase periods of 22: 22°C (constant 22°C), 24: 16°C, and 26: 10°C (all three treatments had the same daily mean and the same degree‐day accumulations). Although developmental rates of post‐diapause pupae were largely unaffected for both species, our results show that sizes in P. canadensis females (but not males) were smaller in the treatments with more variance (26°C: 10°C) compared to constant 22°C. Such potentially significant impacts of size reduction in P. canadensis females were not observed in P. glaucus males or females under the same series of thermo‐period treatments.     

Effects of thermophotoperiod on growth parameters of Helicoverpa armigera

The effects of photoperiod and temperature on growth parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) were investigated under laboratory conditions by exposing its larvae to fluctuating and alternating temperature regimes. Our data made evident that the interplay between photoperiod and temperature has a direct effect on growth parameter responses of H. armigera. However, the type of temperature regime (fluctuating or alternating) may enhance or diminish the effects of photoperiod. With fluctuating temperature, larval developmental time was significantly reduced with increasing photophase, irrespective of the diapause status later in the pupal stage; the lowest value was observed under continuous light conditions. With alternating temperature, larval developmental time was significantly decreased with the reduction in temperature amplitude, and with the coincidence of the thermophase with the scotophase. At both temperature regimes, no significant differences in pupal weight were observed between diapausing and non‐diapausing individuals, although, in most treatments, the diapausing pupae tended to be heavier than the non‐diapausing ones. The increased pupal weight of individuals destined for diapause is probably related to their longer larval developmental time. Knowing the effects of these factors on the variation of H. armigera growth is necessary in explaining phenomena associated with immature stages, and can lead to a more profound understanding of the potential for this insect to evolve in response to environmental changes.     

Inclusion of host quality data improves predictions of herbivore phenology

Understanding the correspondence between ambient temperature and insect development is necessary to forecast insect phenology under novel environments. In the face of climate change, both conservation and pest control efforts require accurate phenological predictions. Here, we compare a suite of degree‐day models to assess their ability to predict the phenology of a common, oligophagous butterfly, the silver‐spotted skipper, Epargyreus clarus (Cramer) (Lepidoptera: Hesperiidae). To estimate model parameters, we used development time of eggs and larvae reared in the laboratory at six constant temperatures ranging from 8 to 38 °C and on two host plants of contrasting quality (kudzu and wisteria). We employed three approaches to determine the base temperature to calculate degree days: linear regression, modified reduced major axis regression, and application of a generic base temperature value of 10 °C, which is commonly used in the absence of laboratory data. To calculate the number of degree days required to complete a developmental stage, we used data from caterpillars feeding on high‐ and low‐quality hosts, both in the field and in the laboratory. To test model accuracy, we predicted development time of seven generations of larvae reared in the field on the same host plants across 3 years (2014–2016). To compare performance among models, we regressed predicted vs. observed development time, and found that r² values were significantly larger when accounting for host plant quality. The accuracy of development time predictions varied across the season, with estimates of the first two generations being more accurate than estimates of the third generation, when ambient temperatures dropped outside the range in which development rate and temperature have a linear relationship. Overall, we show that accounting for variation in host plant quality when calculating development time in the field is more important than the choice of the base temperature for calculating degree days.     

Effect of stressful and nonstressful growth temperatures on variation of sternopleural bristle number in Drosophila melanogaster

The effect of stressful (31 degrees C) and nonstressful (25 degrees C) growth temperatures on quantitative variation and developmental stability (fluctuating asymmetry) of Drosophila melanogaster was examined in a short-term selection experiment on sternopleural bristle number. Realized heritabilities based on 10 generations of selection in an upward direction did not differ between the two temperature regimes, which indicated that additive genetic variation was not affected by a high, stressful temperature. Phenotypic variability and fluctuating asymmetry of sternopleural bristles were significantly higher under stressful conditions when averaged over generations, although most pairwise comparisons in separate generations showed nonsignificant differences between temperatures.