Evolutionary genetics of Drosophila ananassae: evidence for trade-offs among several fitness traits

Correlated responses to bi‐directional selection on thorax length, examined on several life‐history traits and chromosome inversion polymorphisms, have revealed apparent novel trade‐offs in Drosophila ananassae. We provide evidence of trade‐offs between hatching time and pupal period, pupal period and egg‐pupa development time, and pupal period and larval development time (LDT). Body size shows positive correlations with ovariole number, LDT and DT (egg–fly). We provide evidence of sexual dimorphism for trade‐offs between longevity and body size and starvation and longevity in females only. Trade‐offs between wing/thorax (W/T) ratio and longevity, W/T ratio and starvation, and DT (egg‐ fly) and longevity are evident in males only. Sexual dimorphism is also evident for inversion polymorphism with body size and longevity. A longevity assay suggests that low line females outlived high line females whereas high line males outlived low line males. The mean longevity in males is negatively correlated with the 2L‐ST and 3R‐ST arrangement frequencies whereas the 3L‐ST arrangement frequency is positively correlated with the mean longevity in males but opposite arrangements are found in females. Absolute starvation resistance is negatively correlated with 2L‐ST and 3R‐ST chromosome arrangements and results in a trade‐off between longevity and absolute starvation resistance in females. Analyses of fecundity, hatchability, and viabilities based on age intervals in both G₁₀ and G₁₃ suggest that the early reproduction is favoured in D. ananassae. The productivity percentage is highest in the high line and there is no effect of late reproduction on it. Overall, we provide some unravelled trade‐offs and striking sex differences, which may help in understanding the life‐history evolution of the species. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 669–685.     

Population genetics of Drosophila ananassae: inversion polymorphism and body size in Indian geographical populations

Twelve Indian natural populations of Drosophila ananassae, a cosmopolitan and domestic species, were sampled and laboratory populations (mass cultures) were established from naturally impregnated females. These populations were maintained in the laboratory for some generations and were analysed chromosomally to know the frequency of different inversions. The chromosomal analysis revealed the presence of three cosmopolitan inversions. The data on the whole show that there are significant differences in the frequencies of different chromosome arrangements in these populations. Body size (wing length and thorax length) was measured in both sexes (50 females and 50 males), in all the 12 geographical populations of D. ananassae. There are statistically significant differences in wing length as well as in thorax length of both sexes among different geographical populations. Five geographical strains were crossed reciprocally and body size (wing length and thorax length) was measured in F₁ and F₂ progeny. The comparison of body size (both traits) between mid‐parent, F₁ and F₂ shows that there is an increase in body size in F₁ and F₂ progeny as compared with parents. Thus, there is no break down of heterosis in F₂, which suggests absence of coadaptation in geographical populations of D. ananassae. Scaling test statistical analysis showed additive, dominance and epistatic effects in certain crosses involving geographical strains of D. ananassae. Correlation between chromosome arrangement frequency and body size has also been tested and significant negative correlation has been found between 2L – ST chromosome arrangement and male thorax.     

Interracial hybridization in Drosophila ananassae

Crosses were made between strains of Drosophila ananassae, homozygous for the ST or AL gene sequences in the second chromosome, and originating from geographically distant localities in India. All interracial crosses were maintained separately in culture bottles for ten generations. After ten generations it was observed that the inversion heterozygotes were heterotic. Thus it was found that interracial hybridization does not lead to breakdown of heterosis. Therefore, it has been suggested that localised coadaptation is absent in the natural populations of Indian D. ananassae. Thus D. ananassae does not show the pattern of some other species.     

On the degree of genetic divergence in Drosophila ananassae populations transferred to laboratory conditions

Twelve natural populations of Drosophila ananassae were sampled and laboratory populations were derived. All the populations were maintained in food bottles in the laboratory for ten generations by transferring fifty flies (females and males in equal number) in each generation. After ten generations they were analysed chromosomally to determine the frequency of different chromosome arrangements. The results show that there is significant variation in the frequencies of chromosome arrangements and in the level of inversion heterozygosity. Although some of the populations became mo-nomorphic for certain inversions, in general all populations remained polymorphic even after ten generations. The degree of genetic differentiation in the populations after they were transferred to laboratory conditions has been estimated by calculating genetic identity and distance between the initial and final populations based on the differences in chromosome arrangement frequencies. The estimates of I and D suggest that there is considerable variation in the degree of genetic divergence in D. ananassae populations. Some populations have remained unchanged while others have diverged to a considerable extent.     

Effect of directional selection for body size on fluctuating asymmetry in certain morphological traits in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

Variation in the subtle differences between the right and left sides of bilateral characters or fluctuating asymmetry (FA) has been considered as an indicator of an organism’s ability to cope with genetic and environmental stresses during development. However, due to inconsistency in the results of empirical studies, the relationship between FA and stress has been the subject of intense debate. In this study, we investigated whether stress caused by artificial bidirectional selection for body size has any effect on the levels of FA of different morphological traits in Drosophila ananassae. The realised heritability (h²) was higher in low-line females and high-line males, which suggests an asymmetrical response to selection for body size. Further, the levels of FA were compared across 10 generations of selection in different selection lines in both sexes for sternopleural bristle number, wing length, wing-to-thorax ratio, sex comb-tooth number and ovariole number. The levels of FA differed significantly among generations and selection lines but did not change markedly with directional selection. However, the levels of FA were higher in the G10 generation (at the end of selection) than G0 (at the start of selection) but lower than the G5 generation in different selection lines, suggesting that the levels of FA are not affected by the inbreeding generated during the course of selection. Also, the levels of FA in the hybrids of high and low lines were significantly lower than the parental selection lines, suggesting that FA is influenced by hybridisation. These results are discussed in the framework of the literature available on FA and its relationship with stress.     

The lack of evidence for coadaptation in geographic populations of Drosophila ananassae

Crosses were made between geographic races of Drosophila ananassas from different localities in India. All these strains employed in the present experiments were polymorphic for the gene arrangements in the second chromosome due to the occurrence of alpha (subterminal) inversion. After ten generations it was observed that the heterozygotes were the most superior genotype and their frequencies remained above fifty percent in all these strains which served as controls and in the hybrid populations of mixed geographic origin. Thus it was found that interracial hybridization does not lead to breakdown of heterosis. The chief conclusion from these experiments is that evidence for coadaptation is lacking in D. ananassae. This finding apparently conflicts with what has been claimed for other species.     

Effect of chromosome arrangements on mate recognition system leading to behavioral isolation in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

The mechanisms of speciation that appear in the early stages of reproductive isolation has been of recent interest to evolutionary biologists. Experiments were conducted to study behavioral isolation between karyotypically different homozygous strains derived from natural populations of Drosophila ananassae. Three mass cultures stocks established from flies collected from natural populations were employed and homozygous stocks (ST/ST and AL/AL) were made through selection for homozygosity. By employing male-choice technique, mating success was scored by direct observation in the Elens–Wattiaux mating chamber. There is preference for homogamic matings in all the three populations and the differences between homogamic and heterogamic matings are statistically significant in two populations (Lucknow and Varanasi). These findings provide evidence that there is incipient sexual isolation between karyotypically different strains of D. ananassae derived from natural populations which shows that chromosome arrangements may affect the mate recognition system in D. ananassae.     

INVERSION POLYMORPHISM,LONGEVITY, AND BODY SIZE IN A NATURAL POPULATION OF DROSOPHILA BUZZATII

In this study we present the results of an analysis of differential longevity associated with Drosophila buzzatii second chromosome inversion karyotypes based on the assessment of more than 1000 individuals collected in a natural population. Comparisons of inversion frequencies between emerged and bait-collected flies showed not only that inversion arrangements were associated with differential longevity, but also that selection was sex specific. Because each individual fly was scored for thorax length and karyotype, we were able to show that longevity selection favoring larger flies coupled with the average effect of inversions on thorax length can account for the change of inversion frequencies due to longevity in females. The observed genotypic-by-sex interaction could be an important mechanism involved in the maintenance of the polymorphism. Arrangement 2Jz³, which was shown to impaired fecundity in two independent previous studies, exhibited a positive effect on longevity. This pattern of negative pleiotropy may be another plausible mechanism accounting for the maintenance of the polymorphism.     

STUDIES OF LINKAGE IN POPULATIONS. XIV. HISTORICAL CHANGES IN FREQUENCIES OF GENE ARRANGEMENTS AND ARRANGEMENT COMBINATIONS IN NATURAL POPULATIONS OF DROSOPHILA ROBUSTA

Abstract Data are reported showing large directional changes in the frequencies of some gene arrangements and arrangement combinations in certain natural populations of Drosophila robusta in the eastern United States. The changes involve the same X‐chromosomal inversion differences in two of the three localities studied and similar autosomal inversions in all three. These genetic changes provide a rare opportunity to observe evolutionary forces at work in nature. They are interpreted as being due to natural selection.     

Nucleotide Polymorphism at the rp49 region of Drosophila subobscura: Lack of geographic subdivision within chromosomal arrangements in Europe

Restriction-site polymorphism at the rp49 gene region has been studied in 234 lines of Drosophila subobscura representing different gene arrangements for the O chromosome. The population surveyed (El Pedroso, Spain) was sampled four times in each of two consecutive years. The data indicate that the two chromosomal classes studied, O_[ST] and O_{[3 + 4]}, are genetically differentiated in El Pedroso. Comparison of the present results with those previously obtained for two other populations further supports that, for a given chromosomal class, European populations are not genetically differentiated. This lack of differentiation at the rp49 region within O_[ST] and within O_{[3 + 4]} stands in contrast to the clear latitudinal clines found in Europe for these arrangements.     

REACTION NORMS OF MORPHOLOGICAL TRAITS IN DROSOPHILA: ADAPTIVE SHAPE CHANGES IN A STENOTHERM CIRCUMTROPICAL SPECIES?

Reaction norms of wing length, thorax length, and ovariole number were studied according to growth temperature in the circumtropical Drosophila ananassae, and compared to similar data from the cosmopolitan D. melanogaster. In the two species convex reaction norms were observed, but they were not parallel and sometimes exhibited intersections either at high (wing) or at low (thorax) temperature. On average, D. ananassae may be considered as a species with a bigger thorax but shorter wings than D. melanogaster. The shapes of reaction norms were analyzed and compared after quadratic polynomial adjustments. Significant differences were observed, in several cases between polynomial parameters, and in all cases between characteristic points that is, Maximum Value (MV) and Temperature of Maximum Value (TMV). The wing/thorax ratio may also be considered as a specific trait related to wing loading. Major differences were observed between the two species for the mean value and the shape of the response curves of this trait. The main observation of this work was however a shift of TMVs for wing and thorax length and ovariole number in D. ananassae toward higher temperatures. These variations in the reaction norms corresponded to a shift in the species thermal range, suggesting that temperature adaptation was accompanied by a modification of the shape of the response curves.     

Geographic pattern of allozyme and inversion polymorphism on chromosome O of Drosophila subobscura and its evolutionary origin

The chromosome O of Drosophila subobscura was studied with respect to genetic variability at three enzyme loci (Odh, Me, and Lap-4) and with respect to inversion polymorphism. Population samples were taken from seven localities along a north-south gradient from Sweden and Scotland to Tunisia.The chromosomal analysis revealed clinal frequency changes for gene arrangements from north to south. With the enzyme loci Odh and Me allele frequencies are similar throughout the distribution range. Both loci are located outside the common inversion complex O₃₊₄. On the other hand, frequency changes parallel to those of the gene arrangements were observed for the alleles of the Lap-locus. Nonrandom associations between Lap-alleles and the superimposed gene arrangements O_ST, O₃₊₄, O₃₊₄₊₈, and O₃₊₄₊₂₃ were found. These gene arrangements differ from each other with respect to allele frequencies at the Lap-locus but for a given gene arrangement the relative frequencies of Lap-alleles remain relatively constant along the north-south gradient. Thus allele frequencies at the Lap-locus can be predicted from inversion frequencies.These observations can be interpreted in such a way that the pattern of allozyme variation within gene arrangements is due to founder effects caused by the unique origin of inversions. The gene blocks in the different inversions seem to represent more or less separated gene pools. In polymorphic populations the coexistence of genetically differentiated inversions presumably gives rise to heterotic interaction.     

THE EVOLUTIONARY HISTORY OF DROSOPHILA BUZZATII. VIII. EVIDENCE FOR ENDOCYCLIC SELECTION ACTING ON THE INVERSION POLYMORPHISM IN A NATURAL POPULATION

The pattern of selection acting in nature on the chromosomal polymorphism of the cactophilic species Drosophila buzzatii was investigated by comparing inversion and karyotypic frequencies through four different life-cycle stages: adult males, eggs, third-instar larvae, and immature adults. All population samples were obtained in June 1981 at an old Opuntia ficus-indica plantation near Carboneras, Spain. The analysis rests on several assumptions which are explicitly set forth and discussed. The results, if these assumptions prove true, indicate strong directional selection for larval viability acting on the second-chromosome karyotypes and also suggest selective differences in fecundity and longevity. Heterotic selection, however, cannot be ruled out for other fitness components such as male mating success. This kind of selection could be operating on the fourth-chromosome polymorphism as well. Some gene arrangements showed significant and opposite changes in frequency at different parts of the life cycle, thus demonstrating endocyclic selection.     

Evolutionary genetics of Drosophila ananassae III. Effect of temperature on certain fitness traits in two natural populations

Ten isofemale lines of two natural populations of Drosophila ananassae were compared at four different temperatures for body size, W/T ratio, ovariole number and different life history traits. Three-factor nested ANOVA for thorax length and W/T ratio shows significant differences for temperature and sex, while for wing length it shows significant sex difference only. Two-factor nested ANOVA for ovariole number shows a significant difference between populations only, and not for different temperatures. Tests of correlations among different life history traits show novel trade-offs between LDT and pupal period and between pupal period and egg–pupa DT at different temperatures.     

Population and behaviour genetics of Drosophila ananassae

Drosophila ananassae is a cosmopolitan and domestic species. It occupies a nuique status among the Drosophila species due to certain peculiarities in its genetic behaviour. The most unusual feature of this species is spontaneous male recombination in appreciable frequency. The present review summarises the work done on population and behaviour genetics of D. ananassae from India. Population dynamics of three cosmopolitan inversions has been studied in Indian population of D. ananassae and it is evident from the results that there is a considerable degree of genetic divergence at the level of inversion polymorphism. In general, the populations from south India show more differentiation than those from the north. These three cosmopolitan inversions, which are coextensive with the species, exhibit heterosis. Interracial hybridization does not lead to beaakdown of heterosis, which suggests that evidence for coadaptation is lacking in geographic populations of D. ananassae. Heterosis appears to be simple luxuriance rather than populational heterosis (coadaptation). Unlinked inversions occur in random associations, indicating no interchromosomal interactions. However, two inversions of the third chromosome often show strong linkage disequilibrium in laboratory populations, which is due to epistatic gene interaction and suppression of crossing-over. Genetic variations for certain allozyme polymorphism and sternoleural bristle phenotypes in Indian populations of D. ananassae have also been observed.A number of investigations have also been carried out on certain aspects of behaviour genetics of Indian D. ananassae. There is evidence for sexual isolation within D. ananassae. Significant variations in mating propensity of several isofemale strains, inversion karyotypes, the diminishing effects of certain mutations on sexual activity of males and positive response to selection for high and low mating propensity provide evidence for genetic control of sexual behaviour in D. ananassae. Males contribute more to variation and thus are more subject to intra-sexual selection than females. Evidence for rare male mating advantage has also been presented. Geographic strains of D. ananassae show variation with respect to oviposition site preference. The results of studies on pupation site preference, which is an important component of larval behaviour, suggest that larval pupation behaviour in D. ananassae is under polygenic control with a substantial amount of additive genetic variation.     

Response to multi‐generational selection under elevated [CO2] in two temperature regimes suggests enhanced carbon assimilation and increased reproductive output in Brassica napus L.

Functional plant traits are likely to adapt under the sustained pressure imposed by environmental changes through natural selection. Employing Brassica napus as a model, a multi‐generational study was performed to investigate the potential trajectories of selection at elevated [CO₂] in two different temperature regimes. To reveal phenotypic divergence at the manipulated [CO₂] and temperature conditions, a full‐factorial natural selection regime was established in a phytotron environment over the range of four generations. It is demonstrated that a directional response to selection at elevated [CO₂] led to higher quantities of reproductive output over the range of investigated generations independent of the applied temperature regime. The increase in seed yield caused an increase in aboveground biomass. This suggests quantitative changes in the functions of carbon sequestration of plants subjected to increased levels of CO₂ over the generational range investigated. The results of this study suggest that phenotypic divergence of plants selected under elevated atmospheric CO₂ concentration may drive the future functions of plant productivity to be different from projections that do not incorporate selection responses of plants. This study accentuates the importance of phenotypic responses across multiple generations in relation to our understanding of biogeochemical dynamics of future ecosystems. Furthermore, the positive selection response of reproductive output under increased [CO₂] may ameliorate depressions in plant reproductive fitness caused by higher temperatures in situations where both factors co‐occur.     

The evolutionary history of Drosophila buzzatii XXVII

The correlation between body size and longevity was tested in an Argentinian natural population of Drosophila buzzatii. Mean thorax length of flies newly emerging from rotting cladodes of Opuntia vulgaris was significantly smaller than that of two samples of flies caught at baits. The present results which might be interpreted as directional selection for longevity favoring larger flies are in agreement with previous results achieved in a Spanish natural population of D. buzzatii. Flies emerging from different substrates showed significant differences in thorax length, suggesting that an important fraction of phenotypic variance can be attributed to environmental variability. However, laboratory and field work in different populations of D. buzzatii showed a significant genetic component for thorax length variation.     

Time-Series Analysis of Seasonal Changes of the O Inversion Polymorphism of Drosophila Subobscura

We have studied seasonal variation (spring, early summer, last summer and autumn) of inversion polymorphisms of the O chromosome of Drosophila subobscura in a natural population over 15 years. The length of the study allowed us to investigate the temporal behavior (short-term seasonal changes and long-term directional trends) of the O arrangements by the powerful statistical method of time series analysis. It is shown that the O inversion polymorphisms varied on two different time scales: short-term seasonal changes repeated over the years superimposed on long-term directional trends. All the common arrangements (O(3+4+7), O(ST), O(3+4) and O(3+4+8)) showed significant cyclic seasonal changes, and all but one of these arrangements (O(3+4+7)) showed significant long-term trends. Moreover, the degree of seasonality was different for different arrangements. Thus, O(3+4+7) and O(ST) showed the highest seasonality, which accounted for ~61 and 47% of their total variances, respectively. The seasonal changes in the frequencies of chromosome arrangements were significantly associated with the seasonal variation of the climate (temperature, rainfall, humidity and insolation). In particular, O(3+4+7) and O(ST), the arrangements with the greatest seasonal component, showed the strongest association with all climatic factors investigated, especially to the seasonal changes of extreme temperature and humidity.     

Chromosomal inversion polymorphism leads to extensive genetic structure: a multilocus survey in Drosophila subobscura

The adaptive character of inversion polymorphism in Drosophila subobscura is well established. The O(ST) and O(3+4) chromosomal arrangements of this species differ by two overlapping inversions that arose independently on O(3) chromosomes. Nucleotide variation in eight gene regions distributed along inversion O(3) was analyzed in 14 O(ST) and 14 O(3+4) lines. Levels of variation within arrangements were quite similar along the inversion. In addition, we detected (i) extensive genetic differentiation between arrangements in all regions, regardless of their distance to the inversion breakpoints; (ii) strong association between nucleotide variants and chromosomal arrangements; and (iii) high levels of linkage disequilibrium in intralocus and also in interlocus comparisons, extending over distances as great as approximately 4 Mb. These results are not consistent with the higher genetic exchange between chromosomal arrangements expected in the central part of an inversion from double-crossover events. Hence, double crossovers were not produced or, alternatively, recombinant chromosomes were eliminated by natural selection to maintain coadapted gene complexes. If the strong genetic differentiation detected along O(3) extends to other inversions, nucleotide variation would be highly structured not only in D. subobscura, but also in the genome of other species with a rich chromosomal polymorphism.     

Direct and correlated responses to chill‐coma recovery selection in Drosophila buzzatii

Chill‐coma recovery (CCR) is an important trait for thermal adaptation in insects. Multiple phenotypes could be affected by selection on CCR if the trait is genetically correlated with other adaptive traits. To test for heritable (co‐)variation in CCR, we examined direct and correlated responses to bi‐directional selection on CCR. Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae) was artificially selected for decreased and increased recovery time following exposure to 0 °C. After 18 selected generations, the selection response in CCR was significant but qualitatively asymmetric, with replicated lines for slow CCR showing the highest response. Knockdown resistance to high temperature was not affected by CCR selection. Starvation resistance in the adult fly showed no clear pattern of correlated responses to CCR selection. Selection on CCR had no impact on developmental time and body size. Chill‐coma recovery shows no apparent genetic trade‐offs with any of the multiple traits included in this study. These results are largely consistent with recent studies on clines in D. buzzatii, which showed that CCR is not across‐population correlated with other clinally varying traits of thermal adaptation. Cold adaptation may evolve toward increased cold resistance independent of upper thermal limits.