Temperature and clinal variation in larval growth efficiency in Drosophila melanogaster

Geographic clines in ectotherm species including Drosophila melanogaster have been found throughout the world, with genetically larger body size and shorter development time occurring at high latitudes. Temperature is thought to play a major role in the evolution of this clinal variation. Laboratory thermal selection has effects similar to those seen in geographical clines. Evolution at low temperatures results in more rapid development to larger adult flies. This study investigated the effects of geographical origin and experimental temperature on larval growth efficiency in D. melanogaster. Larvae from populations that had evolved at high latitudes were found to use limited food more efficiently, so that the overall adult body size achieved was larger. Larvae reared at a lower experimental temperature (18 °C) used food more efficiently than those reared at a higher temperature (25 °C). The increases in growth efficiency found in populations from high latitudes could explain their increased body size and more rapid development.     

Plastic and Genetic Variation in Wing Loading as a Function of Temperature Within and Among Parallel Clines in Drosophila subobscura

Drosophila subobscura is a European (EU) species that was introducedinto South America (SA) approximately 25 years ago. Previousstudies have found rapid clinal evolution in wing size and inchromosome inversion frequency in the SA colonists, and theseclines parallel those found among the ancestral EU populations.Here we examine thermoplastic changes in wing length in fliesreared at 15, 20, and 25°C from 10 populations on each continent.Wings are plastically largest in flies reared at 15°C (thecoldest temperature) and genetically largest from populationsthat experience cooler temperatures on both continents. We hypothesizethat flies living in cold temperatures benefit from reducedwing loading: ectotherms with cold muscles generate less powerper wing beat, and hence larger wings and/or a smaller masswould facilitate fight. We develop a simple null model, basedon isometric growth, to test our hypothesis. We find that bothEU and SA flies exhibit adaptive plasticity in wing loading:flies reared at 15°C generally have lower wing loadingsthan do flies reared at 20°C or 25°C. Clinal patterns,however, are strikingly different. The ancestral EU populationsshow adaptive clinal variation at rearing a temperature of 15°C:flies from cool climates have lower wing loadings. In the colonizingpopulations from SA, however, we cannot reject the null model:wing loading increases with decreasing clinal temperatures.Our data suggest that selective factors other than flight havefavored the rapid evolution of large overall size at low environmentaltemperatures. However, selection for increased flight abilityin such environments may secondarily favor reduced body mass.     

Indirect selection of thermal tolerance during experimental evolution of Drosophila melanogaster

Natural selection alters the distribution of a trait in a population and indirectly alters the distribution of genetically correlated traits. Long‐standing models of thermal adaptation assume that trade‐offs exist between fitness at different temperatures; however, experimental evolution often fails to reveal such trade‐offs. Here, we show that adaptation to benign temperatures in experimental populations of Drosophila melanogaster resulted in correlated responses at the boundaries of the thermal niche. Specifically, adaptation to fluctuating temperatures (16–25°C) decreased tolerance of extreme heat. Surprisingly, flies adapted to a constant temperature of 25°C had greater cold tolerance than did flies adapted to other thermal conditions, including a constant temperature of 16°C. As our populations were never exposed to extreme temperatures during selection, divergence of thermal tolerance likely reflects indirect selection of standing genetic variation via linkage or pleiotropy. We found no relationship between heat and cold tolerances in these populations. Our results show that the thermal niche evolves by direct and indirect selection, in ways that are more complicated than assumed by theoretical models.     

Investigating thermal acclimation effects before and after a cold shock in Drosophila melanogaster using behavioural assays

Acclimation to environmental change can impose both costs and benefits to organisms. In this study we explored to what extent locomotor behaviour of Drosophila melanogaster is influenced by developmental temperature and adult temperature in both the laboratory and the field. Following development at 15, 25, or 31 °C, adult flies were tested for locomotor activity at all developmental temperatures in the laboratory before and after exposure to a cold shock and in the field for their ability to locate resources after a cold shock. Both test (15, 25, and 31 °C) and developmental temperatures strongly affected locomoter activity, with flies developed at 25 °C having the highest activity at all three test temperatures before the cold shock. After the cold shock flies developed at 15 °C had higher activity compared with flies developed at 25 and 31 °C when tested at 15 and 25 °C, and flies developed at 25 °C had the highest activity when tested at 31 °C. Furthermore, flies developed at 31 °C showed longer recovery times following the cold shock at test temperatures of 15 and 25 °C. However, flies acclimated at 15 °C during development did not recover faster at 15 and 25 °C compared with flies developed at 25 °C. There were no significant correlations between recovery time and locomotor activity at any of the test temperatures. Flies developed at 15 °C and exposed to a cold shock before release in the field were much more successful in locating a resource at low field temperatures compared with flies developed at 25 and 31 °C. Our results provide support for both the beneficial acclimation hypothesis and the optimal developmental temperature hypothesis, but the results are highly context dependent and change with the temperature experienced by the individual during its lifetime.     

Increased temperature reduces herbivore host‐plant quality

Globally increasing temperatures may strongly affect insect herbivore performance, as their growth and development is directly linked to ambient temperature as well as host‐plant quality. In contrast to direct effects of temperature on herbivores, indirect effects mediated via thermal effects on host‐plant quality are only poorly understood, despite having the potential to substantially impact performance and thereby to alter responses to the changing climatic conditions. We here use a full‐factorial design to explore the direct (larvae were reared at 17 °C or 25 °C) and indirect effects (host plants were reared at 17 °C or 25 °C) of temperature on larval growth and life‐history traits in the temperate‐zone butterfly Pieris napi. Direct temperature effects reflected the common pattern of prolonged development and increased body mass at lower temperatures. At the higher temperature, efficiency of converting food into body matter was much reduced being accompanied by an increased food intake, suggesting compensatory feeding. Indirect temperature effects were apparent as reduced body mass, longer development time, an increased food intake, and a reduced efficiency of converting food into body matter in larvae feeding on plants grown at the higher temperature, thus indicating poor host‐plant quality. The effects of host‐plant quality were more pronounced at the higher temperature, at which compensatory feeding was much less efficient. Our results highlight that temperature‐mediated changes in host‐plant quality are a significant, but largely overlooked source of variation in herbivore performance. Such effects may exaggerate negative effects of global warming, which should be considered when trying to forecast species' responses to climate change.     

Effects of temperature on biology and life table parameters of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae)

The development, survivorship, longevity, reproduction, and life table parameters of the Asian citrus psyllid, Diaphorina citri Kuwayama were evaluated at 10°C, 15°C, 20°C, 25°C, 28°C, 30°C and 33°C. The populations reared at 10°C and 33°C failed to develop. Between 15°C and 30°C, mean developmental period from egg to adult varied from 49.3 days at 15°C to 14.1 days at 28°C. The low‐temperature developmental thresholds for 1st through 5th instars were estimated at 11.7°C, 10.7°C, 10.1°C, 10.5°C and 10.9°C, respectively. A modified Logan model was used to describe the relationship between developmental rate and temperature. The survival of the 3rd through 5th nymphal instars at 15–28°C was essentially the same. The mean longevity of females increased with decreasing temperature within 15–30°C. The maximal longevity of individual females was recorded 117, 60, 56, 52 and 51 days at 15°C, 20°C, 25°C, 28°C and 30°C, respectively. The average number of eggs produced per female significantly increased with increasing temperature and reached a maximum of 748.3 eggs at 28°C (P<0.001). The population reared at 28°C had the highest intrinsic rate of increased (0.199) and net reproductive rate (292.2); and the shortest population doubling time (3.5 days) and mean generation time (28.6 days) compared with populations reared at 15–25°C. The optimum range of temperatures for D. citri population growth was 25–28°C.     

Consequences of outbreeding on phenotypic plasticity in Drosophila mercatorum wings

A multivariate morphometric investigation was conducted on wings of two parthenogenetic Drosophila mercatorum strains and offspring (F1) of crosses between these parthenogenetic strains with highly inbred sexual individuals of the same species. The parental flies and F1 offspring were reared at three different temperatures: 20, 25, or 28°C. This design allows a comparison of completely homozygous individuals (parental generation) with identical heterozygote offspring (F1), which makes an analysis of phenotypic plasticity of morphometric traits possible, without a potentially confounding effect of genotype-environment interactions, which can increase the phenotypic variability. The same pattern of phenotypic plasticity of wing size between the homozygous parental strains and the heterozygous offspring was found in both strains with an apparent heterotic effect for wing size in the F1 at 25°C. At 20 and 28°C flies from the parental generation had the biggest wings. Phenotypic plasticity of shape was found to be strain dependent. A reduced level of developmental instability (DI) was found in the F1 as compared to the parental strain only in strain 1 reared at 20°C for the wing size and 25°C for the wing shape. For all the other treatments higher DI was found in the F1 when the difference was significant, which is suggestive of outbreeding depression. These findings are difficult to interpret since an apparent heterotic effect of size at 25°C is accompanied by higher DI (though not significant in strain 2) and complex changes in wing shape. Hence, we cannot conclude whether outbreeding lowers or increases the capacity to respond to environmental change via plastic responses and via changes of the level of DI. The degree of change of phenotypic plasticity and DI is trait specific, depending on the environment and on the genotypes which are hybridizing. Kristian Krag and Hans Thomsen have contributed equally.     

The influence of temperature and photoperiod on the reproductive diapause and cold tolerance of spotted‐wing drosophila,Drosophila suzukii

Knowledge regarding the reproductive status of spotted‐wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), is of critical importance in predicting potential infestations of this invasive pest, as eggs are laid in ripe or ripening fruit of several commercially important small‐fruit crops. Token environmental stimuli for the induction of reproductive diapause and improved cold tolerance were identified for D. suzukii. Diapause induction was evaluated by assessing, via dissection, the number of mature eggs carried by field‐captured D. suzukii and laboratory‐reared D. suzukii held under various temperature and photoperiod regimes. Egg load decreased over time in females trapped from July to December at sites in Benton County, OR, and Ontario County, NY, both USA, and reached zero eggs by December at all sites. Photoperiods below 14 h of day length led to reduced egg maturation in laboratory‐reared flies held at moderate temperatures (15 or 20 °C). Whereas very few mature eggs were found in females held at 10 °C under short‐ or long‐day photoperiods for several weeks after eclosion, a spontaneous return to ovarian maturity was observed in short‐day‐entrained females after 7 weeks. Diapause termination was investigated by evaluating fecundity in diapausing females returned to optimal environmental conditions. Whereas long‐day‐entrained flies began producing offspring immediately upon return to optimal conditions, short‐day‐entrained flies returned after 1 and 6 weeks at 10 °C were slower to produce offspring than colony flies or short‐day‐entrained flies returned after 7 weeks. Cold tolerance was evaluated by observing chill coma recovery rates after 24 h exposure to ?1 °C. Cold‐acclimated (diapausing) females recovered from chill coma faster than cold‐hardened or unacclimated females.     

Effects of food type, feeding frequency, and temperature on juvenile survival and growth of Marisa cornuarietis (Mollusca: Gastropoda)

Abstract. The present experiments are part of a larger study designed to investigate the influence of husbandry parameters on the life history of the ramshorn snail, Marisa cornuarietis, in order to identify suitable husbandry conditions for maintaining multi‐generation populations in the laboratory for use in ecotoxicological testing. In this paper we focus on the effects of a combination of food types and feeding frequencies (i.e., the frequency with which the snails were offered food) on juvenile growth and survival at different temperatures. Offspring produced in the laboratory by wild specimens of M. cornuarietis, from Puerto Rico, were used to test the effects of three types of food (lettuce, alginate with fish food, alginate with snail mix) fed at three frequencies (given ad libitum on 4/4, 2/4, or 1/4 d) on juvenile survival and growth. The 4‐d feeding regimens were repeated four times, giving a total of 16 d for the experiments. The experiments were conducted at two temperatures (22° and 25°C) under a 12 h light:12 h dark photoperiod. Juvenile growth rates increased with increasing feeding frequency for all food types. The most rapid growth rates occurred in the high‐frequency lettuce treatments and the slowest growth rates in the low‐frequency lettuce and alginate with snail mix treatments. Juvenile snails grew faster at 25° than at 22°C, and mortality was about twice as high at the lower temperature. Growth rates were used to provide a rough estimate of time to maturity, which was determined to take about twice as long at 22° than at 25°C. The results showed that lettuce is the best food if supplied in abundance, but effects on growth are very dependent on feeding frequency and temperature. We conclude that 25°C is a more appropriate temperature for maintaining populations than 22°C, that lettuce provides a suitable food source, and that food should be supplied continuously for husbandry and toxicity testing of populations of M. cornuarietis.     

Temporal relationships between leaving food, ecdysone release, mucoprotein extrusion and puparium formation in Drosophila virilis

The time sequence of various developmental processes at the end of larval life in Drosophila virilis larvae is reported. If reared at 25·3°C the larvae leave their food about 140 hr after oviposition; 6·6 hr later ecdysone release occurs, while 8·5 to 9 hr after leaving food the mucoprotein, synthesized and stored in the salivary gland cells, is extruded into the lumen of the gland. Puparium formation takes place 11·2 hr after leaving food. Changes in the puffing activity are correlated with these processes.     

Influence of rearing temperature on triacylglycerol storage in the pea aphid,Acyrthosiphon pisum

Total fatty acids in the pea aphid reared at low temperatures increased significantly compared to that at high rearing temperatures. This change is reflected in a large increase of myristic acid, which occurs exclusively in triacylglycerols. When aphids were moved from 25°C to a lower rearing temperature at 10°C, saturated fatty acids accumulated over time, reaching a maximum at 16th day. When aphids were moved to 4°C, a temperature below the developmental threshold, those aphids did not accumulate saturated fatty acids. Similar results were observed when aphids were exposed to sequential decrease in rearing temperature. However, both total fatty acids and myristic acid in the aphids from the treatments of sequential decreasing rearing temperature were significantly higher compared to those in the aphids from the treatments of sudden decreasing rearing temperature. This result, therefore, supports the hypothesis that cold‐adapted aphids can survive under threshold temperature for a longer period of time than noncold‐adapted aphids. Acetyl‐CoA carboxylase activity in the aphids at 25°C was twofold higher than that in the aphids at 10°C, whereas fatty acid synthase activities in the aphids reared at 25 and 10°C are similar. Aphids reared at 10°C showed a threefold reduction in reproduction rates. This reduced production of new nymphs reduces energy demand and would allow for accumulation of energy in the form of triacylglycerols. Therefore, the increased level of saturated fatty acids in aphids reared at low temperature is probably related to lower utilization of fatty acids rather than increased rates of biosynthesis.     

HERITABLE VARIATION FOR FECUNDITY IN FIELD-COLLECTED DROSOPHILA MELANOGASTER AND THEIR OFFSPRING REARED UNDER DIFFERENT ENVIRONMENTAL TEMPERATURES

Heritable variation for fitness components is normally measured under favorable laboratory conditions, but organisms in the field experience variable conditions that are often stressful and may affect the expression of heritable variation. We examined heritable variation for early fecundity in three samples of Drosophila melanogaster from the field. Flies were obtained from a rotting fruit pile in summer, autumn, and spring, and progeny were reared under laboratory conditions. Field parents were tested for fecundity at 14°C or 28°C depending on ambient temperatures. Wing/thorax length ratios measured on flies from the spring collection suggested that flies had developed at around 20°C. Progeny were reared and tested at 14°C, 25°C, and 28°C. In the summer collection, parent-offspring regression coefficients were high and significant, compared to nonsignificant values obtained in two of three autumn comparisons. In the spring collection, parent-offspring regressions were negative regardless of testing temperature, suggesting that field females with a high fecundity produced offspring with low scores. Comparisons of F₁ and F₂ laboratory generations indicated intermediate heritabilities for fecundity in the laboratory. The lower bound heritability estimate for fecundity in field individuals was 37% in summer and 59% in autumn. Estimates of field heritability and evolvability for wing length measured in the spring collection were lower than in the laboratory. The results indicate that heritabilities and additive genetic variances for fecundity can be high in field-reared flies, but that results may vary between field collections.     

The effects of inbreeding and heat stress on male sterility in Drosophila melanogaster

Understanding the consequences of inbreeding in combination with stress is important for the persistence of small endangered populations in a changing environment. Inbreeding and stress can influence the population at all stages of the life cycle, and in the last two decades a number of studies have demonstrated inbreeding depression for most life‐cycle components, both in laboratory populations and in the wild. Although male fertility is known to be sensitive to temperature extremes, few studies have focused on this life‐cycle component. We studied the effects of inbreeding on male sterility in benign and stressful environments using Drosophila melanogaster as a model organism. Male sterility was compared in 21 inbred lines and five non‐inbred control lines at 25.0 and 29.0 °C. The effect of inbreeding on sterility was significant only at 29.0 °C. This stress‐induced increase in sterility indicates an interaction between the effects of inbreeding and high‐temperature stress on male sterility. In addition, the stress‐induced temporary and permanent sterility showed significant positive correlation, as did stress‐induced sterility and the decrease in egg‐to‐adult viability. This suggests that the observed stress‐induced decline in fitness could result from conditionally expressed, recessive deleterious alleles affecting both sterility and viability simultaneously. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 432–442.     

Investigating dietary preferences in two competing dipterans, Coelopa frigida and Coelopa pilipes, using stable isotope ratios of carbon and nitrogen

Two species of seaweed fly, Coelopa frigida (Fabricius) and Coelopa pilipes (Halliday) (both Diptera: Coelopidae: Coelopini), compete for resources within deposits of marine algae washed ashore on British beaches. Previous studies report that adult flies exhibit algal‐specific behaviour that may influence interspecific interactions. It is predicted that coelopid larvae may also demonstrate algal‐specific dietary preferences. Larval dietary preferences are investigated by comparing the ratios of ¹³C/¹²C and ¹⁵N/¹⁴N in both wild flies and macroalgae to those of laboratory‐reared flies. Results showed only a small difference between the stable isotope ratios of the most abundant algae, Laminaria spp. (Laminariaceae) and Fucus spp. (Fucaceae), although there were significant differences between wild adult coelopids. This result illustrates different metabolic processes in two closely related species. The stable isotope ratios of wild‐caught coelopids were found to differ significantly from laboratory‐reared coelopids. This is either the result of red algae in the diet of natural populations or a difference in bacterial communities. We suggest that experiments with laboratory‐reared flies/specimens can greatly increase the utility of stable isotope analysis in the investigation of animal food webs, even where potential diets are isotopically similar. However, this approach is dependent on re‐creations that accurately mimic natural conditions.     

Effects of temperature on growth and efficiency of food utilization in fifth-instar caterpillars of the tobacco hornworm, Manduca sexta

Fifth-instar larvae of Manduca sexta were reared from hatching on artificial diet at 15, 20, 25, 30 and 35°C. Total development time decreased with increasing temperature. Very few larvae (12%) survived at 15°C, so this temperature was not considered further. There was some mortality at 30°C (11%), and at 35°C (50%).The absolute rate of growth in the fifth instar was faster at 25 than at 20°C, but was similar at 25, 30 and 35°C. This was true both for caterpillars that were chronically exposed to experimental temperatures (i.e. since hatching) and for those acutely exposed (i.e. reared up to fifth instar at 25°C).There was a progressive decrease with higher rearing temperatures in both the initial and final sizes of chronically exposed fifth-instar larvae. Acutely exposed caterpillars matched for initial size showed smaller temperature related differences in final size. Because of these size differences there were differences in relative growth rate which did not reflect true differences in absolute growth rate.Total food consumed by chronically exposed caterpillars was greatest at the lowest temperature (20°C), and decreased progressively with increasing temperature. The absolute rate of food consumption increased from 20 to 25°C, but did not vary significantly between 25 and 35°C. Differences in the sizes of the insects at the different temperatures meant that there were differences among relative measures of consumption that did not reflect absolute food consumption.For chronically exposed caterpillars, none of the three usual indices of food conversion efficiency (AD, ECI and ECD) varied significantly with temperature between 20 and 35°C. This implies that the effects of temperature on metabolic costs are closely matched to food consumption.Oxygen consumption increased with temperature between 20 and 25°C but was temperature compensated between 25 and 35°C.These findings are discussed in terms of their implications for the optimal temperature for growth in Manduca.     

Life history parameters of two geographically separated populations of <Emphasis Type="Italic">Spalangia cameroni</Emphasis>, a microhymenopteran pupal parasitoid of muscoid flies

Spalangia cameroni Perkins (Hymenoptera: Pteromalidae) is used as a biological control agent against house flies and stable flies in livestock farms in Northern Europe. In the present study, the juvenile development, survival, and sex ratio of one Danish and one Norwegian population of S. cameroni were investigated at 15, 20, 25, 30, and 35°C to determine the best adapted strain for release programs. The Danish population developed 50 days faster at 15°C, whereas the Norwegian developed 3–4 days faster at 25°C. The difference was smaller at 20°C and 30°C. Only a few Danish female parasitoids emerged at 35°C. Both populations required 381 degree days to complete development and exhibited optimal juvenile survival at 23.7°C. The Norwegian population produced more females than the Danish population at all temperatures (average of 67.5% vs. 55.5%, respectively). The overall differences between the populations were small, but might still be important for inundative release programs.     

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.     

Acclimation of different strains of the olive fly, Dacus oleae, to low temperatures

Male and female D. oleae have similar powers of acclimation when exposed to low temperatures. Their torpor thresholds depend upon the temperature to which they have been acclimatised. During slow cooling (i.e. less than 1°C per min) they are capable of some rapid acclimation which enables them to lower their torpor threshold by almost 1°C degree, as compared with when they are chilled quickly. After abrupt transfer from 25°C to a different temperature, acclimation takes some time to be accomplished. At 15°C and above it occurs within 10 days but at temperatures below this, progressive acclimation lowers the torpor thresholds to the very low levels typical of flies overwintering under natural conditions. During this long term acclimation torpor thresholds may change by almost 0.5°C per 1°C change of acclimation temperature.No differences were observed in the ability of either flies from northern and southern Greece, or normal and γ-irradiated laboratory reared flies to acclimate to winter conditions in the field. In all cases, torpor thresholds were progressively lowered in advance of the decline in weekly minimum temperatures.