Coadapted changes in energy metabolites and body color phenotypes for resistance to starvation and desiccation in latitudinal populations of D. melanogaster

In D. melanogaster, resistance to starvation and desiccation vary in opposite directions across a geographical gradient in India but there is lack of such clinal variation on other continents. However, it is not clear whether these resistance traits or other correlated traits are the target of natural selection. For resistance to starvation or desiccation in D. melanogaster, we tested the hypothesis whether body color phenotypes and energy metabolites show correlated selection response. Our results are interesting in several respects. First, based on within population analysis, assorted darker and lighter flies from a given population showed that darker flies store higher amount of trehalose and confer greater desiccation resistance as compared with lighter flies. By contrast, lighter flies store higher lipids content and confer increased starvation tolerance. Thus, there is a trade-off for energy metabolites as well as body color phenotypes for starvation and desiccation stress. Further, trait associations within populations reflect similar patterns in geographical populations. Second, we found opposite clines for trehalose and body lipids. Third, coadapated phenotypes have evolved under contrasting climatic conditions i.e. drier and colder northern localities select darker flies with higher trehalose as well as desiccation resistance while hot and humid localities favor lighter flies with higher lipids level and greater starvation tolerance. Thus, the evolution of coadapated phenotypes associated with starvation and desiccation resistance might have resulted due to specific ecological conditions i.e. humidity changes on the Indian subcontinent.     

Starvation Resistance in a Stenothermal Species from the Indian Subcontinent: Mechanistic Basis of Clinal Variation

Parallel clines for starvation resistance and lipid content are well documented among drosophilids on the Indian subcontinent. However, the mechanistic basis of these clines has not been investigated so far. Here, we investigate the utilization of lipids during starvation as a function of duration of stress in D. ananassae. We found higher lipid content responsible for high starvation resistance at lower latitudes. Lipids were utilized during starvation only; not during any other climatic stresses like desiccation or thermal stresses. We also found a cline for consumption of total body lipids; as more content (out of total amount of lipids) was utilized by flies at lower latitudes and lesser at higher latitudes. But, there was no latitudinal cline for threshold lipid amount in the case of females while for males there was a positive cline. Lastly, parallel clines have evolved under contrasting climatic conditions i.e. drier and colder northern localities have flies with lower lipid and reduced starvation resistance while hot and humid localities favor flies with higher lipid levels and greater starvation tolerance. Thus, the evolution of clines associated with starvation and lipid content might have resulted due to specific ecological conditions i.e. humidity gradient on the Indian subcontinent.     

Changes in cuticular lipids, water loss and desiccation resistance in a tropical drosophilid: analysis of variation between and within populations

We investigated within as well as between population variability in desiccation resistance, cuticular lipid mass per fly and cuticular water loss in nine geographical populations of a tropical drosophilid, Zaprionus indianus. Interestingly, the amount of cuticular lipids and desiccation resistance in this non-melanic species are significantly higher as compared with melanic Drosophila melanogaster. On the basis of isofemale line analysis, within population trait variability in cuticular lipid mass per fly is positively correlated with desiccation resistance and negatively correlated with cuticular water loss but show lack of correlation with body size. We observed geographical variation in the amount of cuticular lipid mass per fly in Zaprionus indianus but no such divergence was found in D.melanogaster. In both the species, geographical variations in desiccation resistance are negatively correlated with cuticular water loss but the underlying mechanisms for changes in cuticular permeability are quite different. Thus, we may suggest that body melanisation and cuticular lipids may represent alternative strategies for coping with dehydration stress in melanic versus non-melanic drosophilids. For both the species, desiccation resistance and cuticular water loss are correlated with regular increase in aridity in the northern subtropical localities as compared with southern peninsular humid tropical localities. The role of climatic selection is evident from multiple regression analysis with seasonal changes in temperature and humidity (Tcv and RHcv) of the sites of origin of populations of Zaprionus indianus along latitude.     

The effect of selection for desiccation resistance on cold tolerance of Drosophila melanogaster

Abstract.  Low temperature and desiccation stress are thought to be mechanistically similar in insects, and several studies indicate that there is a degree of cross-tolerance between them, such that increased cold tolerance results in greater desiccation tolerance and vice versa . This assertion is tested at an evolutionary scale by examining basal cold tolerance, rapid cold-hardening (RCH) and chill coma recovery in replicate populations of Drosophila melanogaster selected for desiccation resistance (with controls for both selection and concomitant starvation) for over 50 generations. All of the populations display a RCH response, and there is no effect of selection regime on RCH or basal cold tolerance, although there are differences in basal cold tolerance between sampling dates, apparently related to inter-individual variation in development time. Flies selected for desiccation tolerance recover from chill coma slightly, but significantly, faster than control and starvation-control flies. These findings provide little support for cross-tolerance between survival of near-lethal cold and desiccation stress in D. melanogaster .     

Trade-off of energy metabolites as well as body color phenotypes for starvation and desiccation resistance in montane populations of Drosophila melanogaster

Storage of energy metabolites has been investigated in different sets of laboratory selected desiccation or starvation resistant lines but few studies have examined such changes in wild-caught populations of Drosophila melanogaster. In contrast to parallel selection of desiccation and starvation tolerance under laboratory selection experiments, opposite clines were observed in wild populations of D. melanogaster. If resistance to desiccation and starvation occurs in opposite directions under field conditions, we may expect a trade-off for energy metabolites but such correlated changes are largely unknown. We tested whether there is a trade-off for storage as well as actual utilization of carbohydrates (trehalose and glycogen), lipids and proteins in D. melanogaster populations collected from different altitudes (512-2500 m). For desiccation resistance, darker flies (> 50% body melanization) store more body water content and endure greater loss of water (higher dehydration tolerance) as compared to lighter flies (< 30% body melanization). Based on within population analysis, we found evidence for coadapted phenotypes i.e. darker flies store and actually utilize more carbohydrates to confer greater desiccation resistance. In contrast, higher starvation resistance in lighter flies is associated with storage and actual utilization of greater lipid amount. However, darker and lighter flies did not vary in the rate of utilization of carbohydrates under desiccation stress; and of lipids under starvation stress. Thus, we did not find support for the hypothesis that a lower rate of utilization of energy metabolites may contribute to greater stress resistance. Further, for increased desiccation resistance of darker flies, about two-third of total energy budget is provided by carbohydrates. By contrast, lighter flies derive about 66% of total energy content from lipids which sustain higher starvation tolerance. Our results support evolutionary trade-off for storage as well as utilization of energy metabolites for desiccation versus starvation resistance in D. melanogaster.     

Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster

Wild caught samples of Drosophila melanogaster from five highland localities showed parallel changes in melanisation and desiccation resistance in darker versus lighter phenotypes, i.e. darker flies (>45% melanisation) showed significantly higher desiccation resistance than lighter flies (<30% melanisation). In order to find an association between body melanisation and desiccation resistance, highland and lowland populations from tropical and subtropical regions (11.15-31.06 degrees N) of the Indian subcontinent were raised and investigated at 21 degrees C for four physiological traits, i.e. per cent body melanisation, desiccation resistance, rate of water loss and rate of water absorption. On the basis of mother-offspring regression, body melanisation and desiccation resistance showed higher heritability (0.58-0.68) and thus these traits are suitable for laboratory analyses. Significantly higher melanisation as well as desiccation resistance were observed in highland populations as compared with lowland populations. The rates of water loss as well as absorption were negatively correlated with body melanisation, i.e. darker flies from highlands showed a reduced rate of water loss as well as a lower rate of water absorption while the reverse trend was observed in lighter flies from lowlands. On the basis of multiple regressions, significant effects due to combined altitude and latitude were observed for all the four physiological traits. Local climatic conditions (i.e. annual average temperature and relative humidity) helped in explaining parallel changes in body melanisation and desiccation resistance in D. melanogaster.     

Desiccation tolerance and starvation resistance exhibit opposite latitudinal clines in Indian geographical populations of Drosophila kikkawai

Abstract. 1. Desiccation tolerance and starvation resistance demonstrated significant differentiation among seven Indian geographical populations of Drosophila kikkawai, collected along a latitudinal range of 12.6–32.7 °N. Lack of significant differences in two successive generations suggested that these physiological traits were genetically controlled. 2. North Indian populations of D. kikkawai displayed significantly higher desiccation tolerance than southern populations, whereas there was a reverse trend for starvation tolerance (r > 0.90). Regression slope values indicated an increase of 0.61 h for desiccation and a decrease of 1.71 h per degree latitude for starvation tolerance at 17 °C. The traits evidenced opposite latitudinal clines, and such data also matched thermal climatic conditions on the Indian subcontinent. The survival duration for such traits was significantly higher at 17 than at 25 °C. 3. Significantly higher starvation tolerance in south Indian populations might be due to large population size, species interactions, and higher metabolic rates in the humid tropical environments. In contrast, prolonged unfavourable colder climatic conditions are known to favour starvation tolerance in temperate regions. Thus, the causes of desiccation and starvation tolerance seem quite different under tropical and temperate conditions. 4. Starvation tolerance was correlated negatively with body weight and ovariole number, which might be due to a trade-off in favour of greater allocation to non-lipidic reserves for sustaining starvation tolerance in the tropics. Reduction in metabolic rate may not be applicable for observed higher starvation tolerance in the tropical populations. 5. Multiple regression analysis demonstrated a major effect of coefficient of variation of mean monthly temperature for both the traits of ecological significance. Thus, Indian geographical populations of D. kikkawai provided evidence of independent genetic divergence for starvation and desiccation tolerance under natural conditions.     

Relationships between drosophilids (Diptera, Drosophilidae) and the environment in two contrasting tropical vegetations

Although natural populations of drosophilid flies have been the subject of ecological studies, the population ecology of these insects in the tropics is still poorly known. This paper discusses aspects of the relationship between drosophilids and their environment, based on 28 monthly collections made in two contrasting vegetations of the Brazilian Cerrado biome: gallery forest and savanna. Exotic species were found in both types of environment; but 14 of the 30 captured Neotropical species occurred exclusively in the gallery forests, probably because of their climatic stability and greater environmental heterogeneity. Even though some endemic species were more abundant in the dry and cold months, most populations exhibited peaks of abundance in the wet season. The species diversity indexes (H' and D), higher in the dry season, were probably affected by increased evenness at this time of year, when the populations of practically all the species are greatly reduced. As species richness in the savanna vegetation clearly decreased in the dry season, increasing again in the wet season, it is suggested that some drosophilids migrate to the forests when climatic conditions are too stressful in the savannas.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 233–247.     

Body melanization and its adaptive role in thermoregulation and tolerance against desiccating conditions in drosophilids

Melanism seems to have evolved independently through diverse mechanisms in various taxa and different ecological factors could be responsible for selective responses. Increased body melanization at higher altitudes as well as latitudes is generally considered to be adaptive for thermoregulation. Physiological traits such as body melanization and desiccation resistance have been investigated independently in diverse insect taxa at three levels: within populations, between populations and among species. A substantial number of Drosophila studies have reported clinal variations in both these traits along latitude. A possible link between these traits had remained unexplored in wild and laboratory populations of ectothermic insect taxa, including drosophilids, to date. Simultaneous analysis of these traits in assorted darker and lighter phenotypes in each population in the present study showed parallel changes for body melanization and desiccation resistance. The mechanistic basis of evolving desiccation resistance was explained on the basis of differential rates of water loss per hour in darker versus lighter phenotypes in six populations of Drosophila melanogaster from adjacent localities differing substantially in altitude all along the Indian subcontinent. Data on cuticular impermeability suggest a possible role of melanization in desiccation tolerance. However, substantial gaps remain in extending these results to other insect taxa and further exploring the physiological and molecular changes involved in melanization for conferring desiccation resistance.     

Adaptations to environmental stress in altitudinal populations of two Drosophila species

Abstract.  Opposite clinal variation for desiccation and starvation tolerance are observed in four altitudinal populations (219–2202 m), each of two sympatric and cold adapted species: Drosophila takahashii and Drosophila nepalensis from northern India. The high-altitude populations are more tolerant to desiccation than those from lower altitudes, whereas the reverse trend occurs for starvation tolerance. The magnitude of tolerances are significantly high in D. nepalensis, which is better adapted to cold conditions. During winter months (November to February), there are significant decreases in T _max, T _min and relative humidity along the altitudinal transect. Higher desiccation resistance can develop under cold conditions over short-range, altitudinally varying, geographical areas (250 km) compared with our previously reported long-range (>2000 km), latitudinal variations under tropical climatic conditions. However, significant starvation tolerances are favoured by small body size, higher dispersal rate and higher ambient temperature of the site of origin of populations. Significant correlations of two climatic factors (the mean monthly coefficients of variation of temperature and relative humidity) with these two physiological traits can best explain the observed altitudinal clinal variations under natural conditions.     

Desiccation Resistance in Four Drosophila Species: Sex and Population Effects

Desiccation resistance and body mass were measured in multiple populations of each of four species of Drosophila: two desert endemic species (D. nigrospiracula and D. mojavensis), and two with more widespread distributions (D. melanogaster and D. pseudoobscura). While flies from the desert species were more desiccation tolerant, there was, in certain cases, significant variation in desiccation resistance among populations of the same species. A significant difference in desiccation resistance was observed between the sexes, females were more resistant than males, but this relationship was reversed when taking into account body mass differences between the sexes. The degree of observed within-species variability demonstrates that studies focusing upon differences between species can produce different conclusions if they rely on observations for only single populations of a given species. Our data also suggest the existence of multiple mechanisms for desiccation resistance.     

热带地区相对湿度的季节性变化影响果蝇Drosophila jambulina体色多型性和水分平衡(英文)

在印度次大陆的亚热带地区, 秋天冷而干燥, 春天湿润。变温性果蝇所具有的抗干燥性有助于其度过较为干旱的气候条件。 Drosophila jambulina 具有体色二型性。已有研究表明, 随湿度变化, D. jambulina热带种群始终保持体色多型性, 这与热条件下体色黑化相反, 且该热带物种中体色分化频率随季节性变化, 这符合黑化 干燥假说。但是两种色型的D. jambulina产生这类气候适应的机理尚不明了。为了检验干燥相关性状生理基础的分化与对气候条件的色型特异性适应相关这一假说, 我们利用分别在17℃和25℃、 低湿（40% RH）和高湿（80% RH）条件下饲养获得的两种色型的D. jambulina, 检测了其水分平衡对相对湿度、 温度、 及温湿度相互作用的反应。我们发现, 在低相对湿度下, 两种温度下饲养的深色型果蝇的生理和脱水性状数值显著高于浅色型。对两种色型果蝇的水分收支情况进行的比较分析表明, 在低相对湿度下, 深色型果蝇的含水量较高、 水分损失率较低、 抗脱水能力较强, 使其具有更强的抗干燥性。在干燥胁迫过程中, 两种色型的果蝇均以碳水化合物作为代谢燃料, 但是在低湿条件下, 深色果蝇中贮存碳水化合物的含量明显要高。而且, 在两种湿度条件下, 这两种色型果蝇之间的总能量收支显著不同。据此认为, D. jambulina的水分平衡相关性状表现出的色型特异性分化与其对湿热生境的适应相关。     

Desiccation resistance in four Drosophila species: sex and population effects

Desiccation resistance and body mass were measured in multiple populations of each of four species of Drosophila: two desert endemic species (D. nigrospiracula and D. mojavensis), and two with more widespread distributions (D. melanogaster and D. pseudoobscura). While flies from the desert species were more desiccation tolerant, there was, in certain cases, significant variation in desiccation resistance among populations of the same species. A significant difference in desiccation resistance was observed between the sexes, females were more resistant than males, but this relationship was reversed when taking into account body mass differences between the sexes. The degree of observed within-species variability demonstrates that studies focusing upon differences between species can produce different conclusions if they rely on observations for only single populations of a given species. Our data also suggest the existence of multiple mechanisms for desiccation resistance.     

Divergence of larval resource acquisition for water conservation and starvation resistance in Drosophila melanogaster

Laboratory selection experiments have evidenced storage of energy metabolites in adult flies of desiccation and starvation resistant strains of D. melanogaster but resource acquisition during larval stages has received lesser attention. For wild populations of D. melanogaster, it is not clear whether larvae acquire similar or different energy metabolites for desiccation and starvation resistance. We tested the hypothesis whether larval acquisition of energy metabolites is consistent with divergence of desiccation and starvation resistance in darker and lighter isofemale lines of D. melanogaster. Our results are interesting in several respects. First, we found contrasting patterns of larval resource acquisition, i.e., accumulation of higher carbohydrates during 3rd instar larval stage of darker flies versus higher levels of triglycerides in 1st and 2nd larval instars of lighter flies. Second, 3rd instar larvae of darker flies showed ~40?h longer duration of development at 21°C; and greater accumulation of carbohydrates (trehalose and glycogen) in fed larvae as compared with larvae non-fed after 150?h of egg laying. Third, darker isofemale lines have shown significant increase in total water content (18%); hemolymph (86%) and dehydration tolerance (11%) as compared to lighter isofemale lines. Loss of hemolymph water under desiccation stress until death was significantly higher in darker as compared to lighter isofemale lines but tissue water loss was similar. Fourth, for larvae of darker flies, about 65% energy content is contributed by carbohydrates for conferring greater desiccation resistance while the larvae of lighter flies acquire 2/3 energy from lipids for sustaining starvation resistance; and such energy differences persist in the newly eclosed flies. Thus, larval stages of wild-caught darker and lighter flies have evolved independent physiological processes for the accumulation of energy metabolites to cope with desiccation or starvation stress.     

The respiratory pattern in Drosophila melanogaster selected for desiccation resistance is not associated with the observed evolution of decreased locomotory activity

We examined spontaneous locomotory behavior and respiratory pattern in replicate outbred populations of Drosophila melanogaster selected for desiccation resistance or starvation resistance, as well as their control and ancestral populations. Use of these populations allows us to compare evolved behavioral changes in response to different stress selections. We also reasoned that previously observed changes in respiratory patterns following selection for increased desiccation resistance might be associated with or even caused by changes in locomotory behavior. We measured spontaneous locomotory behavior using video recordings and a computer-based tracking system while simultaneously measuring patterns of CO(2) release from single fruit flies. Statistically significant differences in behavior were observed to be correlated with selection regime. Reduced levels of spontaneous locomotory activity were observed in moist air in both desiccation- and starvation-selected populations compared with their controls. Interestingly, in dry air, only the desiccation-selected flies continue to show reduced spontaneous locomotory activity. No correlation was found between the level of locomotory activity of individual flies and the respiratory patterns of those flies, indicating that the reduced activity levels that have evolved in these flies did not directly cause the documented changes in their respiratory pattern.     

PHYLOGENETIC CONSTRAINTS IN KEY FUNCTIONAL TRAITS BEHIND SPECIES’ CLIMATE NICHES: PATTERNS OF DESICCATION AND COLD RESISTANCE ACROSS 95 DROSOPHILA SPECIES

Species distributions are often constrained by climatic tolerances that are ultimately determined by evolutionary history and/or adaptive capacity, but these factors have rarely been partitioned. Here, we experimentally determined two key climatic niche traits (desiccation and cold resistance) for 92–95 Drosophila species and assessed their importance for geographic distributions, while controlling for acclimation, phylogeny, and spatial autocorrelation. Employing an array of phylogenetic analyses, we documented moderate‐to‐strong phylogenetic signal in both desiccation and cold resistance. Desiccation and cold resistance were clearly linked to species distributions because significant associations between traits and climatic variables persisted even after controlling for phylogeny. We used different methods to untangle whether phylogenetic signal reflected phylogenetically related species adapted to similar environments or alternatively phylogenetic inertia. For desiccation resistance, weak phylogenetic inertia was detected; ancestral trait reconstruction, however, revealed a deep divergence that could be traced back to the genus level. Despite drosophilids’ high evolutionary potential related to short generation times and high population sizes, cold resistance was found to have a moderate‐to‐high level of phylogenetic inertia, suggesting that evolutionary responses are likely to be slow. Together these findings suggest species distributions are governed by evolutionarily conservative climate responses, with limited scope for rapid adaptive responses to future climate change.     

CHILL-COMA TOLERANCE, A MAJOR CLIMATIC ADAPTATION AMONG DROSOPHILA SPECIES

Abstract.— Most drosophilid species can be classified either as temperate or tropical. Adults of species were submitted to a cold treatment (0°C) and then brought back to ambient temperature. They generally exhibited a chill coma and the time needed to recover was measured. We found in a set of 26 temperate species that recovery was rapid (average 1.8 min, range 0.15–4.9). In contrast, a long recovery time (average 56 min, range 24–120) was observed for 48 tropical species. A few species, like Drosophila melanogaster, are cosmopolitan and can proliferate under temperate and tropical climates. In 9 of 10 such species, slight genetic differences were found: a shorter recovery in temperate than in tropical populations. Comparing physiological data to phylogeny suggests that chill‐coma tolerance has been a recurrent adaptation that is selected for in cold climates but tends to disappear under a permanently warm environment. This major climatic adaptation, evidenced in drosophilids, seems to occur in other insect groups also.     

Climatic adaptations of body melanisation in Drosophila melanogaster from Western Himalayas

We investigated population divergence in body melanisation in wild samples of Drosophila melanogaster across an elevational gradient (512 - 2202m) in the Western Himalayas. Wild populations are characterized by higher phenotypic variability as compared with laboratory populations. Significant differences in elevational slope values for three posterior abdominal segments (5th, 6th and 7th) in wild versus laboratory populations suggest plastic effects. However, elevational slope values do not differ for the three anterior abdominal segments (2nd, 3rd and 4th). Thus, elevational changes in melanisation include genetic as well as plastic effects. Fitness consequences of within population variability were analyzed on the basis of assorted darker and lighter flies from two highland as well as from two lowland localities. There is lack of correlation of melanisation with body size as well as ovariole number in assorted darker and lighter flies. For each population, darker flies showed higher desiccation resistance, lower rate of water loss, longer copulation duration and greater fecundity as compared with lighter flies. Phenotypic variations in body melanisation can be interpreted in relation with seasonal changes in temperature as well as humidity (Tcv and RHcv) of the sites of origin of populations. Thus, elevational changes in body melanisation may represent genetic response to selection pressures imposed by colder and drier climatic conditions in the Western Himalayas.     

Spatiotemporal dynamics and genome‐wide association analysis of desiccation tolerance in Drosophila melanogaster

Water availability is a major environmental challenge to a variety of terrestrial organisms. In insects, desiccation tolerance varies predictably over spatial and temporal scales and is an important physiological determinant of fitness in natural populations. Here, we examine the dynamics of desiccation tolerance in North American populations of Drosophila melanogaster using: (a) natural populations sampled across latitudes and seasons; (b) experimental evolution in field mesocosms over seasonal time; (c) genome‐wide associations to identify SNPs/genes associated with variation for desiccation tolerance; and (d) subsequent analysis of patterns of clinal/seasonal enrichment in existing pooled sequencing data of populations sampled in both North America and Australia. A cline in desiccation tolerance was observed, for which tolerance exhibited a positive association with latitude; tolerance also varied predictably with culture temperature, demonstrating a significant degree of thermal plasticity. Desiccation tolerance evolved rapidly in field mesocosms, although only males showed differences in desiccation tolerance between spring and autumn collections from natural populations. Water loss rates did not vary significantly among latitudinal or seasonal populations; however, changes in metabolic rates during prolonged exposure to dry conditions are consistent with increased tolerance in higher latitude populations. Genome‐wide associations in a panel of inbred lines identified twenty‐five SNPs in twenty‐one loci associated with sex‐averaged desiccation tolerance, but there is no robust signal of spatially varying selection on genes associated with desiccation tolerance. Together, our results suggest that desiccation tolerance is a complex and important fitness component that evolves rapidly and predictably in natural populations.     

Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the bush-dwelling land snail Trochoidea simulata

Resistance to desiccation was examined in six populations of the Israeli bush-dwelling snail Trochoidea simulata , a desert species distributed mainly between the 100–200 mm isohyets.
The present study revealed significant intraspecific differences in resistance to desiccation which are correlated with habitat and climatic gradients within the distribution range of the species. Populations from more arid sites were more resistant to desiccation and heat exposure than those from more mesic areas. However, the population from the Rift Valley (an extremely arid region) was surprisingly poorly resistant. Rates of population water loss under the controlled experimental conditions in the laboratory generally matched the calculated water losses during natural summer aestivation.