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.).     

Developmental stability in hybrids between the sibling species pair,Drosophila melanogaster and Drosophila simulans

Drosophila melanogaster and its sibling species D. simulans were hybridized in the laboratory to test the hypothesis that developmental homeostasis in hybrids between two species having no prior gene flow would be significantly reduced. Developmental stability was assessed by measuring fluctuating asymmetry for three bilateral traits: sternopleural chaetae, wing length, and fronto-orbital plus frontal chaetae. Male F₁ hybrids showed no decrease in developmental stability compared to males of parental species. Female hybrids showed significant fluctuating asymmetry compared to other flies. The results are discussed with respect to ideas about coadaptation and gene flow based upon previous studies of hybrid developmental stability.     

Genetics and the environment in interspecific competition: a study using the sibling species Drosophila melanogaster and Drosophila simulans

The outcome of interspecific competition of two closely related species may depend upon genetic variation in the two species and the environment in which the experiment is carried out. Interspecific competition in the two sibling species, Drosophila melanogaster and D. simulans, is usually investigated using longterm laboratory stocks that often have mutant markers that distinguish them. To examine competition in flies that genetically more closely resemble flies in nature, we utilized freshly caught wildtype isofemale lines of the two species collected at the same site in San Carlos, Mexico. Under ordinary laboratory conditions, D. melanogaster always won in competition. However, in hotter and drier conditions, D. simulans competed much more effectively. In these environmental conditions, there were genetic differences in competitive ability among lines with the outcome of competition primarily dependent upon the line of D. melanogaster used but in some cases also influenced by the line of D. simulans used. Differences in the measures of productivity and developmental time did not explain the differences in competitive ability among lines. This suggests that the outcome of competition was not due to differences in major fitness components among the isofemale lines but to some other attribute(s) that influenced competitive ability. When lines of flies were combined, the outcome of competition was generally consistent with competitive outcomes between pairs of lines. In several cases, the combination of lines performed better than the best of the constituent lines, suggesting that competitive ability was combined heterotically and that the total amount of genetic variation was important in the outcome of interspecific competition.     

Analysis of differences in the structure of ribosomal DNA from two sibling species: Drosophila melanogaster and Drosophila simulans

Southern-blot hybridization studies have revealed structural differences within the ribosomal DNA clusters of two sibling species, Drosophila melanogaster and Drosophila simulans. The approach used was shown to be suitable for taxonomic identification of the species examined.     

Differences in the quinacrine staining of the chromosomes of a pair of sibling species: Drosophila melanogaster and Drosophila simulans

The patterns of intense fluorescence after staining with quinacrine dihydrochloride were studied in both the polytene chromosomes and mitotic chromosomes of a pair of sibling species, Drosophila melanogaster and D. simulans. Consistent differences between the two species were found in the pattern of fluorescence of both polytene and mitotic chromosomes. In addition, it was discovered that our stock of D. melanogaster (Oregon-R) is polymorphic at one autosomal position for the property of intense fluorescence after quinacrine staining. On the basis of these findings, the usefulness of quinacrine staining in the study of the cytogenetic structure of evolutionarily interesting populations is discussed.     

Clonal analysis in hybrids between Drosophila melanogaster and Drosophila simulans

We have analysed the viability of cellular clones induced by mitotic recombination in Drosophila melanogaster/D. simulans hybrid females during larval growth. These clones contain a portion of either melanogaster or simulans genomes in homozygosity. Analysis has been carried out for the X and the second chromosomes, as well as for the 3L chromosome arm. Clones were not found in certain structures, and in others they appeared in a very low frequency. Only in abdominal tergites was a significant number of clones observed, although their frequency was lower than in melanogaster abdomens. The bigger the portion of the genome that is homozygous, the less viable is the recombinant melano-gaster/simulans hybrid clone. The few clones that appeared may represent cases in which mitotic recombination took place in distal chromosome intervals, so that the clones contained a small portion of either melanogaster or simulans chromosomes in homozygosity. Moreover, Lhr, a gene of D. simulans that suppresses the lethality of male and female melanogaster/simulans hybrids, does not suppress the lethality of the recombinant melanogaster/simulans clones. Thus, it appears that there is not just a single gene, but at least one per tested chromosome arm (and maybe more) that cause hybrid lethality. Therefore, the two species, D. melanogaster and D. simulans, have diverged to such a degree that the absence of part of the genome of one species cannot be substituted by the corresponding part of the genome of the other, probably due to the formation of co-adapted gene complexes in both species following their divergent evolution after speciation. The disruption of those coadapted gene complexes would cause the lethality of the recombinant hybrid clones.     

Comparative population genomics of latitudinal variation in Drosophila simulans and Drosophila melanogaster

Examples of clinal variation in phenotypes and genotypes across latitudinal transects have served as important models for understanding how spatially varying selection and demographic forces shape variation within species. Here, we examine the selective and demographic contributions to latitudinal variation through the largest comparative genomic study to date of Drosophila simulans and Drosophila melanogaster, with genomic sequence data from 382 individual fruit flies, collected across a spatial transect of 19 degrees latitude and at multiple time points over 2 years. Consistent with phenotypic studies, we find less clinal variation in D. simulans than D. melanogaster, particularly for the autosomes. Moreover, we find that clinally varying loci in D. simulans are less stable over multiple years than comparable clines in D. melanogaster. D. simulans shows a significantly weaker pattern of isolation by distance than D. melanogaster and we find evidence for a stronger contribution of migration to D. simulans population genetic structure. While population bottlenecks and migration can plausibly explain the differences in stability of clinal variation between the two species, we also observe a significant enrichment of shared clinal genes, suggesting that the selective forces associated with climate are acting on the same genes and phenotypes in D. simulans and D. melanogaster.     

High level of divergence of male-reproductive-tract proteins, between Drosophila melanogaster and its sibling species, D. simulans

We compared male-reproductive-tract polypeptides of Drosophila melanogaster and D. simulans by using two-dimensional gel electrophoresis. Approximately 64% of male-reproductive-tract polypeptides were identical between two randomly chosen isofemale lines from these two species, compared with 83% identity for third-instar imaginal wing-disc polypeptides. Qualitatively similar differences were found between reproductive tracts and imaginal discs when D. sechellia was compared with D. melanogaster and with D. simulans. When genic polymorphism was taken into account, approximately 10% of male- reproductive-tract polypeptides were apparently fixed for different alleles between D. melanogaster and D. simulans; this proportion is the same as that found for soluble enzymes by one-dimensional gel electrophoresis. Strikingly, approximately 20% of male-reproductive- tract polypeptides of either D. melanogaster or D. simulans had no detectable homologue in the other species. We propose that proteins of the Drosophila male reproductive tract may have diverged more extensively between species than have other types of proteins and that much of this divergence may involve large changes in levels of polypeptide expression.      

MDG1het and aurora--non-mobile retrotransposons of Drosophila melanogaster]

Non-mobile retrotransposons mdg1het and aurora localized in Drosophila melanogaster heterochromatin were studied. A novel retrotransposon aurora comprising 324 bp LTRs was revealed as a 5 kb insertion causing 5 bp duplication of integration site in the heterochromatic Stellate gene. All the aurora copies are immobilized in D. melanogaster heterochromatin and adjoining chromosome regions 40, 41C and 80BC. Mobile aurora copies were revealed in D. simulans euchromatin by in situ hybridization technique. A comparison of 2.5 kb sequence of immobile mdg1het (including a half of ORF2 and 3'-LTR) with the correspondent sequence of transposable mdg1 copy [9] allowed to conclude that evolution of mdg1 subfamilies occurred under the selective pressure for the ability to transpose. The time period passed since the aurora and mdg1 copies integrated in heterochromatin was roughly estimated via divergence extent between the left and right LTR; for aurora copy it is 0-0.15 Myr, and for mdg1het copies it is 0-0.7 Myr.     

Conservation of locus-specific microsatellite variability across species: a comparison of two Drosophila sibling species, D. melanogaster and D. simulans

Fifteen microsatellite loci were studied in Drosophila melanogaster and Drosophila simulans, two closely related sibling species which split 2- 3.5 MYA. Within-species variances in repeat number were found to differ up to 1,000-fold among individual microsatellite loci. A significant correlation of log variances between both species indicated a locus- specific mutation rate of microsatellites. Hence, locus-specific effects are apparently among the major forces influencing microsatellite variation and deserve more consideration in microsatellite analysis.      

Comparative Life Histories and Ecophysiology of Drosophila melanogaster and D. simulans

Numerous laboratory investigations have compared Drosophila melanogaster and D. simulans for various life history traits and fitness related ecophysiological parameters. From presently available information, it is however difficult to get a general comparative pattern describing the divergence of their ecological niches and understanding their demographic success. Two environmental factors seem however to have played a major role: temperature and alcoholic resources. From an ecophysiological approach, D. simulans may be described as generally more sensitive to stresses; other results point to this species as more cold adapted than its sibling; in some cases, however, D. simulans may appear as better adapted to a warm environment. When investigated, ecophysiological traits show a lesser geographic variability in D. simulans than in D. melanogaster. Presently available information does not explain the ecological prevalence of D. simulans in many places with a mild temperate or subtropical climate. This is presumably due to the fact that most comparisons have been done at a single, standard temperature of 25 degrees C. Comparative studies should be undertaken, spanning the thermal ranges of the two species, and the phenotypic plasticity of ecophysiological traits should now be considered.     

Recombination and the frequency spectrum in Drosophila melanogaster and Drosophila simulans

Most "tests of neutrality" assess whether particular data sets depart from the predictions of a standard neutral model with no recombination. For Drosophila, where nuclear polymorphism data routinely show evidence of genetic exchange, the assumption of no recombination is often unrealistic. In addition, while conservative, this assumption is made at the cost of a great loss in power. Perhaps as a result, tests of the frequency spectrum based on zero recombination suggest an adequate fit of Drosophila polymorphism data to the predictions of the standard neutral model. Here, we analyze the frequency spectrum of a large number of loci in Drosophila melanogaster and D. simulans using two summary statistics. We use an estimate of the population recombination rate based on a laboratory estimate of the rate of crossing over per physical length and an estimate of the species' effective population size. In contrast to previous studies, we find that roughly half of the loci depart from the predictions of the standard neutral model. The extent of the departure depends on the exact recombination rate, but the global pattern that emerges is robust. Interestingly, these departures from neutral expectations are not unidirectional. The large variance in outcomes may be due to a complex demographic history and inconsistent sampling, or to the pervasive action of natural selection.     

A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia

A quantitative trait locus (QTL) genetic analysis of morphological and reproductive traits distinguishing the sibling species Drosophila simulans and D. sechellia was carried out in a backcross design, using 38 markers with an average spacing of 8.4 cM. The direction of QTL effects for the size of the posterior lobe was consistent across the identified QTL, indicating directional selection for this trait. Directional selection also appears to have acted on testis length, indicating that sexual selection may have influenced many reproductive traits, although other forms of directional selection cannot be ruled out. Sex comb tooth number exhibited high levels of variation both within and among isofemale lines and showed no evidence for directional selection and, therefore, may not have been involved in the early speciation process. A database search for genes associated with significant QTL revealed a set of candidate loci for posterior lobe shape and size, sex comb tooth number, testis length, tibia length, and hybrid male fertility. In particular, decapentaplegic (dpp), a gene known to influence the genital arch, was found to be associated with the largest LOD peak for posterior lobe shape and size.     

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.     

Multiple Allelism of the net Gene in Drosophila melanogaster and Drosophila simulans

Thenetgene mutations are known to cause abnormal pattern of veining in all wing regions except for the first posterior cells. In natural populations of Drosophila melanogaster, the net alleles were identified, which differ in phenotypic expression from standard mutations. The mutants net-extra-analis from a population Belokurikha-2000 have only a single additional vein in the third posterior cell. A line from Chernobyl-1986 population have another nontypical allele net ^Ch86 and shows a lower degree of abnormalities than that usually observed. About 10% of these flies have an additional vein fragment in the first posterior cell. In both males and females ofD. simulans population Tashkent -2001, which exhibit net ^ST91 mutation, a net of additional veins is formed as a specific additional fragment in the first posterior cell. The pattern of veining conferred by alleles net-extra-analis and net ^Ch86 is altered to a lesser extent; these alleles are dominant with respect to alleles net ^2-45 and net ^ST91, which cause more abnormalities. The heterozygotes for alleles net ^ST9 and net ^Ch86 and for Df(2) net ⁶² deletion have an additional fragment in the first posterior cell and show similarly strong deviations from normal wing vein pattern. The naturalnet alleles correspond, presumably, to different molecular gene defects involved into uncertain local interactions with numerous modifying factors and other genes that specify the wing vein pattern.     

Multiple allelism of the net gene in Drosophila melanogaster and Drosophila simulans

The net gene mutations are known to cause abnormal pattern of veining in all wing regions except for the first posterior cells. In natural populations of Drosophila melanogaster, the net alleles were identified, which differ in phenotypic expression from standard mutations. The mutants net-extra-analis from a population Belokurikha-2000 have only a single additional vein in the third posterior cell. A line from Chernobyl-1986 population have another nontypical allele netCh86 and shows a lower degree of abnormalities than that usually observed. About 10% of these flies have an additional vein fragment in the first posterior cell. In both males and females of D. simulans population Tashkent-2001, which exhibit netST91 mutation, a net of additional veins is formed as a specific additional fragment in the first posterior cell. The pattern of veining conferred by alleles net-extra-analis and netCh86 is altered to a lesser extent; these alleles are dominant with respect to alleles net2-45 and netST91, which cause more abnormalities. The heterozygotes for alleles netST9 and netCh86 and for Df(2) net62 deletion have an additional fragment in the first posterior cell and show similarly strong deviations from normal wing vein pattern. The natural net alleles correspond, presumably, to different molecular gene defects involved into uncertain local interactions with numerous modifying factors and other genes that specify the wing vein pattern.     

Morphometric discrimination of the sibling species Drosophila melanogaster (Meigen) and D. simulans (Sturtevant) (Diptera: Drosophilidae)

Abstract. The sibling species Drosophila melanogaster and D.simulans often co-occur. Males are easily distinguished using their genitalia while females of the two species are often deemed indistinguishable. A series of nine linear and two angular measurements were taken using the heads of both males and females of both species from the same locality. A simple comparison of cheek width and eye height accurately assigned all females to species. Multivariate techniques using linear head measures alone produced very good discrimination between both species and sexes. Drosophila simulans have significantly larger eyes and narrower eye margins than D.melanogaster. Unknown females collected from this locality could be easily and reliably assigned to species.