Genetic and Environmental Responses to Temperature of Drosophila Melanogaster from a Latitudinal Cline

Field-collected Drosophila melanogaster from 19 populations in Eastern Australia were measured for body size traits, and the measurements were compared with similar ones on flies from the same populations reared under standard laboratory conditions. Wild caught flies were smaller, and latitudinal trends in size were greater. Reduced size was caused by fewer cells in the wing, and the steeper cline by greater variation in cell area. The reduction in size in field-collected flies may therefore have been caused by reduced nutrition, and the steeper cline may have been caused by an environmental response to latitudinal variation in temperature. No evidence was found for evolution of size traits in response to laboratory culture. The magnitude of phenotypic plasticity in response to temperature of development time, body size, cell size and cell number was examined for six of the populations, to test for latitudinal variation in plasticity. All characters were plastic in response to temperature. Total development time showed no significant latitudinal variation in plasticity, although larval development time showed a marginally significant effect, with most latitudinal variation at intermediate rearing temperatures. Neither thorax length nor wing size and its cellular components showed significant latitudinal variation in plasticity.     

Latitudinal and temperature-dependent variation in embryonic development and growth in Rana temporaria

Variation in seasonal time constraints and temperature along latitudinal gradients are expected to select for life history trait differentiation, but information about the relative importance of these factors in shaping patterns of divergence in embryonic traits remains sparse. We studied embryonic survival, growth and development rates in the common frog (Rana temporaria) along a 1,400-km latitudinal gradient across Sweden by raising embryos from four populations in the laboratory at seven temperatures (9 degrees C, 12 degrees C, 15 degrees C, 18 degrees C, 21 degrees C, 24 degrees C, 27 degrees C). We found significant differences in mean values of all traits between the populations and temperature treatments, but this variation was not latitudinally ordered. In general, embryonic survival decreased at the two highest temperatures in all populations, but less so in the southernmost as compared to the other populations. The northernmost population developed slowest at the lowest temperature, while the two mid-latitude populations were slowest at the other temperatures. Hatchling size increased with increasing temperature especially in the two northern populations, whereas the two southern populations showed peak hatchling size at 15 degrees C. Analyses of within-population genetic variation with a half-sib design revealed that there was significant additive genetic variation in all traits, and egg size-related maternal effects were important in the case of hatchling size. Overall, our results indicate that unlike larval growth and development, variation in embryonic development and growth in R. temporaria cannot be explained in terms of a latitudinal gradient in season length. While adaptation to a latitudinal variation in temperature might have contributed to the observed differentiation in embryonic performance, the effects of other, perhaps more local environmental factors, seem to have overridden them in importance.     

Body size patterns in Drosophila inhabiting a mesocosm: interactive effects of spatial variation in temperature and abundance

Body size is a major component of fitness. However, the relative contributions of different factors to optimal size, and the determinants of spatial and temporal variation in size, have not been fully established empirically. Here, we use a mesocosm of a Drosophilidae assemblage inhabiting decaying nectarines to investigate the influence of spatial variation in temperature on adult body size in Drosophila simulans Sturtevant. Two treatments were established; one in the sun where developing larvae were exposed to high temperatures and the other in the shade where temperature conditions were milder. The simple developmental effects of temperature differences (i.e. larger flies are likely to emerge from cooler environments), or the simple effects of stressful temperatures (i.e. high temperatures yield wing abnormalities and smaller flies), were overridden by interactive effects between temperature and larval density. Emergences were lower in the sun than shade, probably as a result of temperature-induced mortality. However, flies attained the same final sizes in the shade and sun. In addition, abnormally winged flies were clustered in the shaded treatments. In the shade treatments, where emergences were higher than in the sun, stressful conditions as a result of high larval density likely resulted in wing abnormalities and small size. Consequently, there was little spatial variation in size across the mesocosm, but substantial spatial variation in abundance. Under natural conditions both mortality and non-lethal effects of temperature and/or crowding are likely to play a role in the evolution of body size.     

Latitudinal variation in wild populations of Drosophila melanogaster: heritabilities and reaction norms

Large amounts of genetic variation for wing length and wing area were demonstrated both within and between Drosophila melanogaster populations along a latitudinal gradient in South America. Wing length and wing area showed a strong positive correlation with latitude in both wild flies and laboratory-raised descendants. Large population differences were observed for heritability and coefficient of variation of these two traits, whereas relatively small population differences were found for development time, viability, pupal mortality, sex ratio and their norms of reaction to four developmental temperatures. No clear-cut latitudinal clines were established for these life-history characters. These results are discussed in the light of Bergmann's Rule and the relation between larval development and adult body size.     

Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster

Genetic variation of body size along latitudinal clines is found globally in Drosophila melanogaster, with larger individuals encountered at higher latitudes. Temperature has been implicated as a selective agent for these clines, because the body size of laboratory populations allowed to evolve in culture at lower temperatures is larger. In this study, we investigated the hypothesis that larger size is favoured at lower temperature through natural selection on adult males. We measured life‐span and age‐specific fertility of males from lines of flies artificially selected for body size at two different experimental temperatures. There was an interaction between experimental temperature and body size selection for male fitness; large‐line males were fitter than controls at both temperatures, but the difference in fitness was greater at the lower experimental temperature. Smaller males did not perform significantly differently from control males at either experimental temperature. The results imply that thermal selection for larger adult males is at least in part responsible for the evolution of larger body size at lower temperatures in this species. The responsible mechanisms require further investigation.     

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.     

The influence of host fruit and temperature on the body size of adult Ceratitis capitata (Diptera: Tephritidae) under laboratory and field conditions

The adult body size of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), varies in natural conditions. Body size is an important fitness indicator in the Mediterranean fruit fly; larger individuals are more competitive at mating and have a greater dispersion capacity and fertility. Both temperature during larval development and host fruit quality have been cited as possible causes for this variation. We studied the influence of host fruit and temperature during larval development on adult body size (wing area) in the laboratory, and determined body size variation in field populations of the Mediterannean fruit fly in eastern Spain. Field flies measured had two origins: 1) flies periodically collected throughout the year in field traps from 32 citrus groves, during the period 2003-2007; and 2) flies evolved from different fruit species collected between June and December in 2003 and 2004. In the lab, wing area of male and female adults varied significantly with temperature during larval development, being larger at the lowest temperature. Adult size also was significantly different depending on the host fruit in which larvae developed. The size of the flies captured at the field, either from traps or from fruits, varied seasonally showing a gradual pattern of change along the year. The largest individuals were obtained during winter and early spring and the smallest during late summer. In field conditions, the size of the adult Mediterannean fruit fly seems apparently more related with air temperature than with host fruit. The implications of this adult size pattern on the biology of C. capitata and on the application of the sterile insect technique are discussed.     

Reproductive characteristics of the flower breeding Drosophila hibisci Bock (Drosophilidae) along a latitudinal gradient in eastern Australia: relation to flower and habitat features

For many insect species, egg and larval substrate characteristics are significantly correlated with interspecific differences in female reproductive allocation and egg size-number tradeoffs. We tested the hypothesis that a similar pattern occurred within the Australian drosophilid, Drosophila hibisci, that is restricted throughout its life cycle to flowers of species in the genus Hibiscus. These plants occur as small, isolated, normally monospecific stands that should facilitate differentiation of the fly populations in relation to specific oviposition and larval substrates. Data from 38 sites ranging from 20.8̀ to 34.4̀ S latitude in eastern Australia indicated no relationship between female body size, egg size, or ovariole numbers and floral size or mass among four species of Hibiscus. However, the flies did show a latitudinal cline in ovariole number that was independent of floral variation. Females averaged 15–20 ovarioles per female in the south (32–34̀ S latitude) and 10–12 ovarioles in the north (21–22̀ S latitude). The increase in ovariole number with latitude was due to divergence in the ovariole number of the largest females. In contrast, small females in the north and south had the same number of ovarioles. Reproductive allocation of female flies in the northern region was less than females in the southern region. The latitudinal divergence in ovariole number was not associated with habitat differences (density of trees, density of flies and beetles), nor with differences in floral characteristics (flower weight, petal length, yeast species present). Short term weather patterns in daily temperature and rainfall preceding collections pardy explain the variation in ovariole number. These observations in conjunction with preliminary genetic results suggest the cline is associated with genetic differences that interact with environmental determinants such as the temperature during larval development.     

Ecology of body size in Drosophila buzzatii: untangling the effects of temperature and nutrition

Abstract.

• 1 A method of separating the effects of two important determinants of body size in natural populations, temperature of larval development and level of larval nutrition, by making measurements of thorax length and wing length of adult flies is investigated.
• 2 I show that at any given time variation in body size of Drosophila buzzatii from two sites in eastern Australia is determined primarily by variation in the quality of nutrition available to larvae.
• 3 Throughout the year adult flies are consistently at least 25% smaller in volume than predicted for optimal nutrition at their predicted temperature of larval development.
• 4 Nutritional stress is therefore a year-round problem for these flies.
• 5 Measurements of adult flies emerging from individual breeding substrates (rotting cactus cladodes) show that there is substantial variation among these substrates in the nutrition available to larvae.
• 6 This method will allow study of spatial and temporal variation in the temperature of larval substrates and in the nutritional resources available to flies in natural populations.

     

Covariation of larval gene expression and adult body size in natural populations of Drosophila melanogaster

Understanding adaptive phenotypic variation is one of the most fundamental problems in evolutionary biology. Genes involved in adaptation are most likely those that affect traits most intimately connected to fitness: life-history traits. The genetics of quantitative trait variation (including life histories) is still poorly understood, but several studies suggest that (1) quantitative variation might be the result of variation in gene expression, rather than protein evolution, and (2) natural variation in gene expression underlies adaptation. The next step in studying the genetics of adaptive phenotypic variation is therefore an analysis of naturally occuring covariation of global gene expression and a life-history trait. Here, we report a microarray study addressing the covariation in larval gene expression and adult body weight, a life-history trait involved in adaptation. Natural populations of Drosophila melanogaster show adaptive geographic variation in adult body size, with larger animals at higher latitudes. Conditions during larval development also affect adult size with larger flies emerging at lower temperatures. We found statistically significant differences in normalized larval gene expression between geographic populations at one temperature (genetic variation) and within geographic populations between temperatures (developmental plasticity). Moreover, larval gene expression correlated highly with adult weight, explaining 81% of its natural variation. Of the genes that show a correlation of gene expression with adult weight, most are involved in cell growth or cell maintenance or are associated with growth pathways.     

Temperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster

Geographical variation in Drosophila melanogaster body size is a long-standing problem of life-history evolution. Adaptation to a cold climate invariably produces large individuals, whereas evolution in tropical regions result in small individuals. The proximate mechanism was suggested to involve thermal evolution of resource processing by the developing larvae. In this study an attempt is made to merge proximate explanations, featuring temperature sensitivity of larval resource processing, and ultimate approaches focusing on adult and pre-adult life-history traits. To address the issue of temperature dependent resource allocation to adult size vs. larval survival, feeding was stopped at several stages during the larval development. Under these conditions of food deprivation, two temperate and two tropical populations reared at high and low temperatures produced different adult body sizes coinciding with different probabilities to reach the adult stage. In all cases a phenotypic trade-off between larval survival and adult size was observed. However, the underlying pattern of larval resource allocation differed between the geographical populations. In the temperate populations larval age but not weight predicted survival. Temperate larvae did not invest accumulated resources in survival, instead they preserved larval biomass to benefit adult weight. In other words, larvae from temperate populations failed to re-allocate accumulated resources to facilitate their survival. A low percentage of the larvae survived to adulthood but produced relatively large flies. Conversely, in tropical populations larval weight but not age determined the probability to reach adulthood. Tropical larvae did not invest in adult size, but facilitated their own survival. Most larvae succeeded in pupating but then produced small adults. The underlying physiological mechanism seemed to be an evolved difference in the accessibility of glycogen reserves as a result of thermal adaptation. At low rearing temperatures and in the temperate populations, glycogen levels tended to correlate positively with adult size but negatively with pupation probability. The data presented here offer an explanation of geographical variation in body size by showing that thermal evolution of resource allocation, specifically the ability to access glycogen storage, is the proximate mechanism responsible for the life-history trade-off between larval survival and adult size.     

Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations

The duration of Drosophila melanogaster larval and pupal periods was measured in laboratory thermal lines and in populations collected along a latitudinal transect in eastern Australia. In replicated laboratory lines kept for 9 years at 16.5° C or 25° C the duration of larval development had continued to diverge compared with 4 and 5 years previously, with more rapid larval development, and hence reduced total duration of pre-adult development, in the low temperature lines at both experimental temperatures. After 4 years of separate evolution, lines derived from the 25° C lines and subsequently cultured at 29° C showed no evidence of significant divergence in the duration of any part of the pre-adult period. The geographic populations showed a decrease in the duration of larval development, and hence of the total pre-adult period, with increasing latitude. In both laboratory and field populations, evolution at lower temperature was associated with more rapid larval development to a larger adult body size, the opposite genetic correlation between these traits to that found within a single temperature. The indications are that lower temperatures may be permissive of more efficient growth in D. melanogaster. It will be important to discover if evolution in response to temperature induces similar correlations in other ectotherms.     

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila-Macrocheles system

Costs of resistance are expected to contribute to the maintenance of genetic variation for resistance in natural host populations. In the present study, we experimentally test for genetic trade-offs between parasite resistance and larval competitive ability expressed under varying levels of crowding and temperature. Artificial selection for increased behavioral resistance was applied against an ectoparasitic mite (Macrocheles subbadius) in replicate lines of the fruit fly Drosophila nigrospiracula. We then measured correlated responses to selection in larval competitive ability by contrasting replicate selected and control (unselected) lines in the absence of parasitism. Experiments were conducted under variable environmental conditions: two temperatures and three levels of larval density. Our results reveal a negative genetic correlation between resistance and larval-adult survival under conditions of moderate and severe intra-specific competition. At both low and high temperature, percent emergence was significantly higher among control lines than selected lines. This divergence in larval competitive ability was magnified under high levels of competition, but only at low temperature. Hence, the interaction between selection treatment and larval density was modified by temperature. As predicted, larvae experiencing medium and high levels of competition exhibited an overall reduction in female body size compared to larvae at low levels of competition. Female flies emerging from selected lines were significantly smaller than those females from control lines, but this effect was only significant under conditions of moderate to severe competition. These results provide evidence of environment-dependent trade-offs between ectoparasite resistance and larval competitive ability, a potential mechanism maintaining genetic polymorphism for resistance.     

Variation of life‐history traits of the Asian corn borer,Ostrinia furnacalis in relation to temperature and geographical latitude

Life‐history traits from four geographical populations (tropical Ledong population [LD], subtropical Guangzhou [GZ] and Yongxiu populations, and temperate Langfang population [LF]) of the Asian corn borer, Ostrinia furnacalis were investigated at a wide range of temperatures (20–32°C). The larval and pupal times were significantly decreased with increasing rearing temperature, and growth rate was positively correlated with temperature. The relationship between body weight and rearing temperature in O. furnacalis did not follow the temperature–size rule (TSR); all populations exhibited the highest pupal and adult weights at high temperatures or intermediate temperatures. However, development time, growth rate, and body weight did not show a constant latitudinal gradient. Across all populations at each temperature, female were significantly bigger than males, showing a female‐biased sexual size dimorphism (SSD). Contrary to Rensch's rule, the SSD tended to increase with rising temperature. The subtropical GZ population exhibited the largest degree of dimorphism while the temperate LF exhibited the smallest. Male pupae lose significantly more weight at metamorphosis compared to females. The proportionate weight losses of different populations were significantly different. Adult longevity was significantly decreased with increasing temperature. Between sexes, all populations exhibit a rather female‐biased adult longevity. Finally, we discuss the adaptive significance of higher temperature‐inducing high body weight in the moth's life history and why the moth exhibits the reverse TSR.     

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.     

Reproductive characteristics of Drosophila hibisci in the Northern Territory, Australia

Reproductive traits of Drosophila hibisci collected at 18 sites in the Northern Territory (NT) of Australia in May, 1998, as well as at two sites in north Queensland, in June, 1998, were compared to those from earlier work on a cline in ovariole number in D. hibisci along the east coast of Australia. The flies in the NT were considerably smaller, but had more ovarioles than comparably-sized flies on the east coast. Although the flies on the east coast showed an increasing number of ovarioles in populations at increasing distances from the equator, these new populations, both on the east coast and in the NT, reversed this trend, producing a generally U-shaped pattern of ovariole number with latitude among all populations. The northernmost and southernmost populations allocate more to ovariole numbers than populations in intermediate latitudes. Ovariole number is closely related to body size of females in all populations, but the regression coefficient is small at intermediate latitudes and increases at the northern and southern ends of the distribution. Egg volumes primarily varied with body size of the female (positive) and number of ovarioles per female (negatively), producing a generally inverted U-shaped pattern of egg volumes with latitude. Reproductive allocation patterns, but not thorax size or ovariole number, varied significantly in two samples taken 10 days apart at one NT site. This variation probably results from environmental differences across generations of developing larvae and is consistent with our earlier suggestion of substantial effects of the environment, primarily rainfall and temperature, on reproductive allocation in D. hibisci.     

Ecological correlates of body size in relation to cell size and cell number: patterns in flies, fish, fruits and foliage

Body size is important to most aspects of biology and is also one of the most labile traits. Despite its importance we know remarkably little about the proximate (developmental) factors that determine body size under different circumstances. Here, I review what is known about how cell size and number contribute to phenetic and genetic variation in body size in Drosophila melanogaster, several fish, and fruits and leaves of some angiosperms. Variation in resources influences size primarily through changes in cell number while temperature acts through cell size. The difference in cellular mechanism may also explain the differences in growth trajectories resulting from food and temperature manipulations. There is, however, a poorly recognized interaction between food and temperature effects that needs further study. In addition, flies show a sexual dimorphism in temperature effects with the larger sex responding by changes in cell size and the smaller sex showing changes in both cell size and number. Leaf size is more variable than other organs, but there appears to be a consistent difference between how shade-tolerant and shade-intolerant species respond to light level. The former have larger leaves via cell size under shade, the latter via cell number in light conditions. Genetic differences, primarily from comparisons of D. melanogaster, show similar variation. Direct selection on body size alters cell number only, while temperature selection results in increased cell size and decreased cell number. Population comparisons along latitudinal clines show that larger flies have both larger cells and more cells. Use of these proximate patterns can give clues as to how selection acts in the wild. For example, the latitudinal pattern in D. melanogaster is usually assumed to be due to temperature, but the cellular pattern does not match that seen in laboratory selection at different temperatures.     

Variation in body size and metamorphic traits of Iberian spadefoot toads over a short geographic distance

Determinants of geographic variation in body size are often poorly understood, especially in organisms with complex life cycles. We examined patterns of adult body size and metamorphic traits variation in Iberian spadefoot toad ( Pelobates cultripes ) populations, which exhibit an extreme reduction in adult body size, 71.6% reduction in body mass, within just about 30 km at south-western Spain. We hypothesized that size at and time to metamorphosis would be predictive of the spatial pattern observed in adult body size. Larvae from eight populations were raised in a common garden experiment at two different larval densities that allow to differentiate whether population divergence was genetically based or was simply a reflection of environmental variation and, in addition, whether this population divergence was modulated by differing crowding larval environments. Larger adult size populations had higher larval growth rates, attaining larger sizes at metamorphosis, and exhibited higher survival than smaller-sized populations at both densities, although accentuated at a low larval density. These population differences appeared to be consistent once embryo size variation was controlled for, suggesting that this phenotypic divergence is not due to maternal effects. Our results suggest considerable genetic differentiation in metamorphic traits that parallels and may be a causal determinant of geographic variation in adult body size.     

Quantitative genetic analysis of the body size and shape of Drosophila buzzatii

Summary Body size in Drosophila is known to be closely related to a number of traits with important life history consequences, such as fecundity, dispersal ability and mating success. We examine the quantitative genetic basis of body size in three populations of the cactophilic species Drosophila buzzatii, which inhabit climatically different areas of Australia. Flies were reared individually to eliminate any common environmental component in a full-sib design with families split between two temperatures (18° and 25 °C). The means of several size measures differ significantly among populations while the genetic correlations among these traits generally do not differ, either among populations from different natural environments or between the different laboratory temperatures. This stability of correlation structure is necessary if laboratory estimates of genetic correlations are to have any connection with the expression of genetic variation in the field. The amount of variance due to genotype-by-environment interactions (family x temperature of development) varied among populations, apparently in parallel with the magnitudes of seasonal and diurnal variation in temperature experienced by the different populations. A coastal population, inhabiting a relatively thermally benign environment, showed no interaction, while two inland populations, inhabiting thermally more extreme areas, showed interaction. This interaction term is a measure of the amount of genetic variation in the degree of phenotypic plasticity of body size in response to temperature of development. Thus the inland flies vary in their ability to attain a given body size at a particular temperature while the coastal flies do not. This phenotypic plasticity is shown to be due primarily to differences among genotypes in the amount of response to the change in temperature. A possible selective basis for the maintenance of genetic variation for the levels of phenotypic plasticity is proposed.     

Evolution of increased adult longevity in Drosophila melanogaster populations selected for adaptation to larval crowding

In holometabolous animals such as Drosophila melanogaster, larval crowding can affect a wide range of larval and adult traits. Adults emerging from high larval density cultures have smaller body size and increased mean life span compared to flies emerging from low larval density cultures. Therefore, adaptation to larval crowding could potentially affect adult longevity as a correlated response. We addressed this issue by studying a set of large, outbred populations of D. melanogaster, experimentally evolved for adaptation to larval crowding for 83 generations. We assayed longevity of adult flies from both selected (MCUs) and control populations (MBs) after growing them at different larval densities. We found that MCUs have evolved increased mean longevity compared to MBs at all larval densities. The interaction between selection regime and larval density was not significant, indicating that the density dependence of mean longevity had not evolved in the MCU populations. The increase in longevity in MCUs can be partially attributed to their lower rates of ageing. It is also noteworthy that reaction norm of dry body weight, a trait probably under direct selection in our populations, has indeed evolved in MCU populations. To the best of our knowledge, this is the first report of the evolution of adult longevity as a correlated response of adaptation to larval crowding.