The influence of species frequency,temperature regime and previous development condition on relative competitive ability between Drosophila melanogaster and Drosophila simulans

Some fitness components of Drosophila melanogaster and D. simulans were measured in control and inter-specific competition tests. The effects derived from different relative frequencies of the competitors were examined under a factorial scheme with two temperatures, 21 °C or room temperature, and with adults developed in mixed- or pure-species cultures. D. melanogaster appeared as a strong competitor and outnumbered D. simulans in all the culture conditions. This was because intraspecific competition was stronger than inter-specific competition for D. melanogaster whereas the reverse occurred for D. simulans. In competition, the productivity of both species generally appeared as frequency-dependent, although density-dependent productivity seems to be a more accurate explanation. D. simulans was very sensitive to variations of laboratory conditions. Room temperature and previous development with D. melanogaster were more favorable for D. simulans than 21 °C and previous development in pure cultures. These factors did not substantially affect D. melanogaster, which showed a greater ability of adaptation to laboratory conditions than its sibling D. simulans.     

THE REPRODUCTIVE RELATIONSHIPS OF DROSOPHILA SECHELLIA WITH D. MAURITIANA,D. SIMULANS,AND D. MELANOGASTER FROM THE AFROTROPICAL REGION

Hybridization tests among the four sibling species of the Drosophila melanogaster complex were made to determine the reproductive status of the recently discovered D. sechellia (which is endemic to a few islands and islets of the Seychelles archipelago) with regard to its three close relatives, D. mauritiana (endemic to Mauritius) and Afrotropical strains of the two cosmopolitan species D. melanogaster and D. simulans. Interstrain variation in the ability to hybridize with other species was also analyzed for D. melanogaster and D. simulans. D. mauritiana and D. simulans appear to be more weakly isolated from each other than either species is from D. sechellia. A striking unilateral mating success is observed in the cross of D. sechellia with D. simulans. The most extreme isolation is between D. melanogaster and its three siblings. Variation in the ability of strains to hybridize is observed in heterospecific crosses between D. simulans and either D. melanogaster or D. mauritiana.     

Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D. simulans

Reaction norms to growth temperature of two size-related traits, wing and thorax length, were compared in tropical (West Indies) and temperate (France) populations of the two sibling species, Drosophila melanogaster and D. simulans. A major body size difference was found in D. melanogaster, with much smaller Caribbean flies, while D. simulans exhibited little size variation between geographical populations. The concave norms of reaction were adjusted to second- or third-degree polynomials, and characteristic points calculated i.e. maximum value (MV) and temperature of maximum value (TMV). TMVs were confirmed to be higher for thorax than for wing length, higher in D. melanogaster than in D. simulans, and higher in females than in males. For both traits Caribbean populations exhibited higher TMVs in the two species, strongly suggesting an adaptive shift of the reaction norms toward higher temperature in warm-adapted populations. The wing/thorax ratio was also analysed, and found to be significantly lower in tropical populations of both species. This ratio, which is related to wing loading and flight capacity, might evolve independently of body weight itself.     

THE GENETIC BASIS OF SEXUAL ISOLATION BETWEEN DROSOPHILA MELANOGASTER AND D. SIMULANS

The genetic analysis of sexual isolation between the closely-related species Drosophila melanogaster and Drosophila simulans involved two experiments with no-choice tests. The efficiency of sexual isolation was measured by the frequency of courtship initiation and interspecific mating. We first surveyed the variation in sexual isolation between D. melanogaster strains and D. simulans strains of different geographic origin. Then, to investigate variation in sexual isolation within strains, we made F₁ diallel sets of reciprocal crosses within strains of D. melanogaster and D. simulans. The F₁ diallel progeny of one sex were paired with the opposite sex of the other species. The first experiment showed significant differences in the frequency of interspecific mating between geographic strains. There were more matings between D. simulans females and D. melanogaster males than between D. melanogaster females and D. simulans males. The second experiment uncovered that the male genotypes in the D. melanogaster diallel significantly differed in interspecific mating frequency, but not in courtship initiation frequency. The female genotypes in the D. simulans diallel were not significantly different in courtship initiation and interspecific mating frequency. Genetic analysis reveals that in D. melanogaster males sexual isolation was not affected by either maternal cytoplasmic effects, sex-linked effects, or epistatic interaction. The main genetic components were directional dominance and overdominance. The F₁ males achieved more matings with D. simulans females than the inbred males. The genetic architecture of sexual isolation in D. melanogaster males argues for a history of weak or no selection for lower interspecific mating propensity. The behavioral causes of variation in sexual isolation between the two species are discussed.     

Divergent strategies in low temperature environment for the sibling species Drosophila melanogaster and D. simulans: overwintering in extension border areas of France and comparison with African populations

The two sibling species D. /melanogaster and D. simulans adopt different overwintering strategies in northern border areas situated in France. If the winter is mild, both species reappear in early spring to refound the population. If the winter is cold, with several weeks of temperatures below 0 °C, D. melanogaster leave their shelters in April whereas D. simulans, which do not use shelters, reappear in late June, probably after returning from further south. Here, we tried to identify life-history characteristics responsible for this difference. For this, we studied developmental duration, viability, fecundity, fertility and longevity, and compared the abilities of French and African populations to survive when food supplies were inadequate, at different temperatures (14, 11, 7 °C). These temperatures are lower than those commonly used in the laboratory but closer to real conditions encountered in the wild. When the temperature was mild (14 or 11 °C) and the food supply was adequate, D. simulans performed better than D. melanogaster: it had a higher fecundity, a longer life expectancy and the males remained fertile, allowing outdoor reproduction late in winter. However, D. simulans was less resistant in more extreme conditions. At 7 °C D. simulans survived shorter on normal medium and its ability to survive when food supplies were inadequate was insufficient to allow outdoor overwintering. In contrast, D. melanogaster could not reproduce during winter: its fecundity was low and males were sterile at 11 °C. Nevertheless, if only protein-deficient resources were available, temperate D. melanogaster could survive for longer than D. simulans at all the temperatures tested. This greater resistance to underfeeding allows the species to survive until spring, in shelters for several months. A comparison of French and African population performances showed differences in the evolution of the two species during the colonization of more northern areas. African D. simulans, which are efficient at mild temperatures, underwent few modifications. In contrast, the viability of D. melanogaster improved at low developmental temperatures. This species also displayed higher fecundity, longer survival and higher underfeeding resistance at low temperatures. The relationship between the long retention genotype and underfeeding resistance or survival ability observed in French D. melanogaster populations may not exist in African populations.     

Divergence of water balance mechanisms in two sibling species (Drosophila simulans and D. melanogaster): effects of growth temperatures

Drosophila simulans is more abundant under colder and drier montane habitats in the western Himalayas as compared to its sibling D. melanogaster but the mechanistic bases of such climatic adaptations are largely unknown. Previous studies have described D. simulans as a desiccation sensitive species which is inconsistent with its occurrence in temperate regions. We tested the hypothesis whether developmental plasticity of cuticular traits confers adaptive changes in water balance-related traits in the sibling species D. simulans and D. melanogaster. Our results are interesting in several respects. First, D. simulans grown at 15 °C possesses a high level of desiccation resistance in larvae (~39 h) and in adults (~86 h) whereas the corresponding values are quite low at 25 °C (larvae ~7 h; adults ~13 h). Interestingly, cuticular lipid mass was threefold higher in D. simulans grown at 15 °C as compared with 25 °C while there was no change in cuticular lipid mass in D. melanogaster. Second, developmental plasticity of body melanisation was evident in both species. Drosophila simulans showed higher melanisation at 15 °C as compared with D. melanogaster while the reverse trend was observed at 25 °C. Third, changes in water balance-related traits (bulk water, hemolymph and dehydration tolerance) showed superiority of D. simulans at 15 °C but of D. melanogaster at 25 °C growth temperature. Rate of carbohydrate utilization under desiccation stress did not differ at 15 °C in both the species. Fourth, effects of developmental plasticity on cuticular traits correspond with changes in the cuticular water loss i.e. water loss rates were higher at 25 °C as compared with 15 °C. Thus, D. simulans grown under cooler temperature was more desiccation tolerant than D. melanogaster. Finally, desiccation acclimation capacity of larvae and adults is higher for D. simulans reared at 15 °C but quite low at 25 °C. Thus, D. simulans and D. melanogaster have evolved different strategies of water conservation consistent with their adaptations to dry and wet habitats in the western Himalayas. Our results suggest that D. simulans from lowland localities seems vulnerable due to limited acclimation potential in the context of global climatic change in the western Himalayas. Finally, this is the first report on higher desiccation resistance of D. simulans due to developmental plasticity of both the cuticular traits (body melanisation and epicuticular lipid mass) when grown at 15 °C, which is consistent with its abundance in temperate regions.     

Sexual Isolation Between Drosophila Melanogaster, D. Simulans and D. Mauritiana: Sex and Species Specific Discrimination

The sexual isolation among the related species Drosophila melanogaster, D. simulans and D. mauritiana is asymmetrical. While D. mauritiana males mate well with both D. melanogaster and D. simulans females, females of D. mauritiana discriminate strongly against males of these two species. Similarly, D. simulans males mate with D. melanogaster females but the reciprocal cross is difficult. Interspecific crosses between several populations of the three species were performed to determine if (i) males and females of the same species share a common sexual isolation genetic system, and (ii) males (or females) use the same genetic system to discriminate against females (or males) of the other two species. Results indicate that although differences in male and female isolation depend on the populations tested, the isolation behaviour between a pair of species is highly correlated despite the variations. However, the rank order of the isolation level along the populations was not correlated in both sexes, which suggests that different genes act in male and female sexual isolation. Neither for males nor for females, the isolation behaviour of one species was paralleled in the other two species, which indicates that the genetic systems involved in this trait are species-pair specific. The implications of these results are discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

Alcohol tolerance: An ecological parameter in the relative success of Drosophila melanogaster and Drosophila simulans

Summary Laboratory experiments have shown D. melanogaster adults to be more tolerant to alcohol in the environment than D. simulans, with the females being more tolerant than the males of their species. Larval development on alcohol supplemented media also demonstrated an increased tolerance by D. melanogaster although the effect was not as clear cut as for the adult survival. Oviposition choice experiments demonstrated a marked rejection of alcohol impregnated laying sites by D. simulans when compared to standard medium sites. D. melanogaster showed a slight preference for alcohol supplemented sites.Collections in the maturation cellar of a vineyard produced, with the exception of a single D. simulans fly, entirely D. melanogaster adults while larvae and pupae from the cellar were also all D. melanogaster. Away from the alcohol resource, outside the cellar, both species were collected with D. simulans being the more common. However, the outside distribution of the two species was affected by alcohol fumes during vintage, as was the distribution of the sexes of D. melanogaster, with the more tolerant species or sex being closer to the source. The field results were thus in agreement with the laboratory predictions that D. melanogaster is better able to utilize an alcohol resource than D. simulans.     

The effects of acclimation and rearing conditions on the response of tropical and temperate populations ofDrosophila melanogaster andD. simulans to a temperature gradient (Diptera: Drosophilidae)

The effects of rearing and acclimation on the response of adultDrosophila to temperature were investigated in a gradient.D. melanogaster flies preferred a higher mean temperature and were distributed over a wider range of temperatures thanD. simulans flies. Acclimating adults at different temperatures for a week did not influence the response of either species. Adults reared at 28°C as immatures had a lower mean preference than those reared at cooler temperatures, suggesting that flies compensated for the effects of rearing conditions. Adults from tropical and temperate populations ofD. melanogaster andD. simulans did not differ in the mean temperature they preferred in a gradient, suggesting little genetic divergence for this trait within species. The species differences and environmental responses may be related to changes in optimal physiological conditions for the flies.     

Life history adaptations and stress tolerance of four domestic species of Drosophila

Life history traits and stress tolerance were studied in four domestic species of Drosophila–D. melanogaster, D. simulans, D. auraria and D. immigrans– to understand how they adapt to their environments. In all species, larval weight approximately doubled in 1 day. The relative egg weight (egg weight : pupal weight) was smaller and the larval period was longer in D. immigrans than in the other three species. The pupal period was the longest in D. auraria. However, the adaptive significance of these differences in larval and pupal periods was not clear. The pupal case was generally thicker in the larger species, probably to support the larger pupal body. The start of oviposition was earliest and reproductive effort was greatest in female D. simulans, followed by female D. melanogaster. In contrast, starvation tolerance and the increase in bodyweight after eclosion was greater in D. immigrans and D. auraria than in the other two species. Pupal desiccation tolerance was greatest in D. melanogaster and lowest in D. auraria, and the less tolerant species seemed to select more humid sites for pupation. Adult tolerance to desiccation was greatest in D. melanogaster and lowest in D. simulans. In contrast, adult cold tolerance was greater in D. auraria and adult heat tolerance was lower in D. immigrans than in the other species. These differences in life history traits and stress tolerance represent the Drosophila species differential adaptations, and are assumed to allow coexistence of the species.     

EVOLUTIONARY GENETICS OF TWO SIBLING SPECIES,DROSOPHILA SIMULANS AND D. SECHELLIA

Drosophila simulans and D. sechellia are sibling species, the former cosmopolitan and the latter restricted to the Seychelles Islands. We used classical genetic analysis to measure the numbers and effects of genes responsible for reproductive isolation and morphological differences in male genitalia between these species. At least five loci are responsible for male sterility in hybrids, with the strongest effects produced by at least two genes on the X chromosome. At least three (and probably four) loci are responsible for the interspecific difference in the size of the posterior process of the male genital arch. These genetic results, as well as the pattern of morphological divergence between the species, show several parallels with the divergence between D. simulans and its other island relative, D. mauritiana. We also present the DNA sequence of a 4.5 kilobase region containing the alcohol dehydrogenase (Adh) locus of D. sechellia, and combine this with previous data to reconstruct the phylogenies of the three species and their more distant relative D. melanogaster. Both D. mauritiana and D. sechellia are very closely related to D. simulans. Although most phylogenies show the two island species to be independent offshoots of the D. simulans lineage (with D. sechellia the more recent), the branch points are too close to make this conclusion unambiguous. The genetic and evolutionary parallels between the simulans/mauritiana and the simulans/sechellia divergences may therefore represent either a striking evolutionary convergence or a close common ancestry of the island species. A comparison of Adh alleles within species shows that the divergence among them may be almost as large as among alleles from different species. We conclude that many of the nucleotide differences among these species actually represent polymorphisms within common ancestors. It may be difficult to build accurate phylogenies using only a single DNA sequence from each species.     

Structural and genetic studies of the proliferation disrupter genes of Drosophila simulans and D. melanogaster

To examine whether structural and functional differences exist in the proliferation disrupter (prod) genes between Drosophila simulans and D. melanogaster, we analyzed and compared both genes. The exon–intron structure of the genes was found to be the same – three exons were interrupted by two introns, although a previous report suggested that only one intron existed in D. melanogaster. The prod genes of D. simulans and D. melanogaster both turn out to encode 346 amino acids, not 301 as previously reported for D. melanogaster. The numbers of nucleotide substitutions in the prod genes was 0.0747 ±  per synonymous site and 0.0116 ± 0.0039 per replacement site, both comparable to those previously known for homologous genes between D. simulans and D. melanogaster. Genetic analysis demonstrated that D. simulans PROD can compensate for a deficiency of D. melanogaster PROD in hybrids. The PRODs of D. simulans and D. melanogaster presumably share the same function and a conserved working mechanism. The prod gene showed no significant interaction with the lethality of the male hybrid between these species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Contrasting patterns of geographic variation in the cosmopolitan sibling species Drosophila melanogaster and Drosophila simulans

An electrophoretic study was carried out to compare the geographic pattern of genetic variation in Drosophila simulans with that of its sibling species, Drosophila melanogaster. An identical set of 32 gene-protein loci was studied in four geographically distant populations of D. simulans and two populations of D. melanogaster, all originating from Europe and Africa. The comparison yielded the following results: (1) tropical populations of D. simulans were, in terms of the number of unique alleles, average heterozygosity per locus, and percentage of loci polymorphic, more variable than conspecific-temperate populations; (2) some loci in both species showed interpopulation differences in allele frequencies that suggest latitudinal clines; and (3) temperate-tropical genetic differentiation between populations was much less in D. simulans than in D. melanogaster. Similar differences between these two species have previously been shown for chromosomal, quantitative, physiological, and middle-repetitive DNA variation. Estimates of N _m (number of migrants per generation) from the spatial distribution of rare alleles suggest that both species have similar levels of interpopulation gene flow. These observations lead us to propose two competing hypotheses: the low level of geographic differentiation in D. simulans is due to its evolutionarily recent worldwide colonization and, alternatively, D. simulans has a narrower niche than D. melanogaster. Geographic variation data on different genetic elements (e.g., mitochondrial DNA, two-dimensional proteins, etc.) are required before these hypotheses can be adequately tested.We thank the Natural Science and Engineering Research Council of Canada for financial support (Grant A0235 to R.S.S.).     

Direct and correlated responses to selection for desiccation resistance: a comparison of Drosophila melanogaster and D. simulans

Replicate lines of Drosophila melanogaster and D. simulans originating from the same location in Australia were selected at two selection intensities (50%, 85% mortality) for increased resistance to desiccation, and scored for correlated responses to see if similar physiological changes were associated with the selection responses. Realized heritabilities were much higher in D. melanogaster. Selected lines of both species were more resistant than control lines to starvation and a toxic ethanol concentration. Both species also showed similar correlated responses for traits underlying the selection response: selected lines lost water at a slower rate and had reduced activity levels in a dry environment, but they did not differ in wet or dry body weight or in water content. For D. melanogaster, realized heritabilities for lines selected at 85% mortality were higher than for lines selected at 50% mortality, but there was no effect of selection intensity for D. simulans. Comparative studies of this nature may be useful in predicting the extent to which species can adapt to stress in the wild.     

Hybrid lethal systems in theDrosophila melanogaster species complex

Lethal phases of the hybrids betweenDrosophila melanogaster and its sibling species,D. simulans are classified into three types: (1) embryonic lethality in hybrids carryingD. simulans cytoplasm andD. melanogaster X chromosome, (2) larval lethality in hybrids not carryingD. simulans X, and (3) temperature-sensitive pupal lethality in hybrids carryingD. simulans X. The same lethal phases are also observed when either of the two other sibling species,D. mauritiana orD. sechellia, is employed for hybridization withD. melanogaster. Here, we describe genetic analyses of each hybrid lethality, and demonstrate that these three types of lethality are independent phenomena. We then propose two models to interpret the mechanisms of each hybrid lethality. The first model is a modification of the conventional X/autosome imbalance hypothesis assuming a lethal gene and a suppressor gene are involved in the larval lethality, while the second model is for embryonic lethality assuming an interaction between a maternal-effect lethal gene and a suppressor gene.     

VARIATIONS IN CUTICULAR HYDROCARBONS AMONG THE EIGHT SPECIES OF THE DROSOPHILA MELANOGASTER SUBGROUP

In addition to protecting against desiccation, some of the hydrocarbons of the waxy cuticle have previously been shown to be mating pheromones in Drosophila melanogaster and D. simulans. Therefore, cuticular hydrocarbons were compared among the eight species in the D. melanogaster subgroup. For the two cosmopolitan species and several geographic strains that were studied, all males are quite similar with very abundant monoenes. The major compound in most cases is 7-tricosene. Only three exceptions were found: D. sechellia, and the Afrotropical strains of D. melanogaster and D. simulans. A significant sexual dimorphism exists in three species: D. melanogaster, D. erecta, and D. sechellia. Greater variation was observed in females than in males. D. erecta is singular in the production of long-chain molecules (31–33 carbons). Only three species (D. melanogaster, D. erecta, and D. sechellia) produce diene in significant amounts. Such products, especially 7,11-heptacosadiene, are known to act as aphrodisiacs for D. melanogaster males. In the five other species, females show only quantitative differences from males, generally with 7-tricosene as the most abundant compound. This compound is an aphrodisiac for D. simulans males. Some species such as D. yakuba, D. teissieri, D. orena, D. mauritiana, and the Seychelles strain of D. simulans are almost identical in the chemical composition of cuticular hydrocarbons. In contrast, important variations are observed between geographic populations of D. melanogaster and D. simulans.     

Inviability of hybrids between D. melanogaster and D. simulans results from the absence of simulans X not the presence of simulans Y chromosome

Interspecific crosses between D. melanogaster and D. simulans or its sibling species result in unisexual inviability of the hybrids. Mostly, crosses of D. melanogaster females X D. simulans males produce hybrid females. On the other hand, only hybrid males are viable in the reciprocal crosses. A classical question is the cause of the unisexual hybrid inviability on the chromosomal level. Is it due to the absence of a D. simulans X chromosome or is it due to the presence of a D. simulans Y chromosome? A lack of adequate chromosomal rearrangements available in D. simulans has made it difficult to answer this question. However, it has been assumed that the lethality results from the absence of the D. simulans X rather than the presence of the D. simulans Y. Recently I synthesized the first D. simulans compound-XY chromosome that consists of almost the entire X and Y chromosomes. Males carrying the compound-XY and no free Y chromosome are fertile. By utilizing the compound-XY chromosome, the viability of hybrids with various constitutions of cytoplasm and sex chromosomes has been examined. The results consistently demonstrate that the absence of a D. simulans X chromosome in hybrid genome, and not the presence of the Y chromosome, is a determinant of the hybrid inviability.     

Growth temperature and phenotypic plasticity in two Drosophila sibling species: probable adaptive changes in flight capacities

In the sibling species Drosophila melanogaster and D. simulans, growth and development at constant temperatures, from 12 to 30 °C, resulted in extensive variations of adult size and flight parameters with significant differences between species. Changes in body weight, thorax length and wing length were nonlinear, with maximum values of each trait at lower temperatures for D. simulans than for its sibling species. By contrast, the wing/thorax ratio and the wing loading varied monotonically with growth temperature. These traits were negatively correlated, the wing/thorax ratio decreasing with growth temperature while the wing loading increased. Wing/thorax ratio, which is easier to measure, thus appears as a convenient predictor of wing loading. During tethered flight at the same ambient temperature, the wingbeat frequency changed linearly as a function of the wing moment of inertia. More interestingly, the beat rate was strongly correlated with the increase of wing loading at growth temperature above 13 °C. The likely adaptive significance of these morphometrical changes for flight efficiency is discussed.     

DYNAMICS OF P-M HYBRID DYSGENESIS IN P-TRANSFORMED LINES OF DROSOPHILA SIMULANS

An autonomous P element from Drosophila melanogaster was introduced by microinjection into the germ line of its sibling species, Drosophila simulans. The invasion kinetics of P elements was studied in seven independent lines over 60 generations, using gel blotting, in situ hybridization, and dysgenic crosses. Some of the main phenotypic and molecular characteristics of P-M hybrid dysgenesis were observed, i.e., gonadal dysgenesis (GD sterility), chromosome rearrangements, and the occurrence of degenerate P elements. At least four lines reached a steady state with complete or nearly complete P-element regulation but with a moderate number of P elements (10–24 per haploid genome) and P activity (10–35% GD sterility). This failure to obtain strong P strains in D. simulans could be due to experimental conditions, a host-dependent component of P transposition, or more severe selection against the deleterious effects of this transposon.