On intra- and interchromosomal associations in Drosophila ananassae

In Drosophila ananassae, three cosmopolitan inversions are very common in natural populations. Chromosomal polymorphism due to these inversions often persists when strains are maintained in the laboratory. A chromosomal analysis of a number of strains was made. Data on the frequencies of different gene sequences will be described separately. During the present investigation the same data have been analyzed in order to test the intra- and interchromosomal interactions in D. ananassae. The results reveal that interchromosomal interactions do not occur with respect to viability as unlinked inversions are associated randomly. However, the linked inversions of the third chromosome show non-random associations maintained by epistatic gene interaction and suppression of crossing over.     

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.     

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.     

Linkage disequilibrium in laboratory populations of Drosophila nasuta

Summary Natural populations of Drosophila nasuta are polymorphic for many gene arrangements. Two non-overlapping inversions of the third chromosome, III-2 and III-35, are most common and display extreme linkage disequilibrium. Six randomly mating laboratory stocks, each founded by one gravid female heterozygous in coupling for both III-2 and III-35, were observed after 32 generations. Significant linkage disequilibrium was observed in all stocks. Recombinants were found in only two stocks. The absence of effective recombination in some stocks and its presence in others might be due to different genotypic backgrounds. We suggest that natural selection, influencing recombination rates in several ways, and intrachromosomal epistasis between the two inversions were the main factors for the maintenance of linkage disequilibrium in D. nasuta.     

Analysis of male recombination in third chromosomes of Drosophila melanogaster

Data on male recombination in twenty third-chromosomal lines of Drosophila melanogaster are presented. Frequencies of female and male recombination have been calculated in seven intervals along the third chromosome. The influence on male recombination (M.R.) exercised by different factors such as population origin (cellar, vineyard), the presence of heterozygous inversions and recessive lethal chromosomes, is analyzed. The results obtained lead to the main conclusion that M.R. is not affected by the presence of heterozygous inversions which reduce female recombination in the same lines. In the light of this effect, the possible mechanism operating on male recombination is discussed. Lethal chromosomes reduce significantly the number of male recombination events as compared with wild chromosomes. We have not obtained significant differences in male recombination frequencies between the cellar and the vineyard lines.     

The influence of heterochromatin, inversion-heterozygosity and somatic pairing on x-ray induced mitotic recombination in Drosophila melanogaster

Summary Mitotic recombination has been induced with X-rays in Drosophila melanogaster larvae and assayed later as twin mosaic spots in the adult eyes. When the X-chromosomes are marked with zeste and white and the third chromosomes with roughoid and sepia, the frequency of twin spots was about 20 times higher for the X-chromosome than for the third chromosome. The greater amount of heterochromatin in the X-chromosome was considered responsible for the difference.Experiments with different inversion heterozygotes support this interpretation. Euchromatic inversions of different lengths have, when heterozygous, little or no influence on the twin spot frequency. The shorter the heterochromatic segment between the kinetochore and the proxomal break point of the inversion the stronger is the reduction of the twin spot frequency.The heterozygotes for the long sc ⁸ and sc ^S1 inversions gave exceptionally low twin spot frequencies. It seems possible that potential twin spot daughter cells die after recombination because of genetic imbalance and/or lack of proper cell separation resulting from the persistence of the dikinetic chromosome elements.To test whether inaccurate somatic pairing in inversion heterozygotes could help explain the low twin spot frequencies in those of sc ⁸ and sc ^S1, neuroblast chromosomes were investigated. They show that chromosomal arrangement during metaphase is determined exclusively by the location of the kinetochore, which always points, irrespective of earlier somatic pairing, toward the center of the metaphase plate. It is possible that there is a lack of proper chromosome alignment at the X-ray sensitive stage for mitotic recombination.     

Lack of correlation between crossing-over and chromosome distance between inversions in Drosophila ananassae

Two linked inversions, AL and ZE, located in the opposite limbs of the second chromosome of Drosophila ananassae are separated from each other by nearly 32% of the total length of the second chromosome. Crossing-over between these inversions when heterozygous was studied in females and males by the salivary-gland smear technique using karyotypically homozygous stocks. The results of recombination experiments show that there is a strong suppression of recombination between inversions when heterozygous, in spite of a large euchromatic distance available for crossing-over between them. Thus there is no correlation between chromosome distance and crossing-over between heterozygous inversions in the second chromosome of D. ananassae when studied cytologically.     

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.     

Intra-and interchromosomal effects of heterozygous inversions on recombination in the third chromosome of Drosophila ananassae

In order to study intra-and interchromosomal effects of heterozygous inversions on recombination in the third chromosome of D.ananassae, experiments were conducted using Stw-pr marker stock and five wild stocks with known karyotypes. The stocks used were homozygous for standard or inverted gene sequence in 2L, 3L, and 3R. Recombination was investigated in both sexes. There was complete absence of crossing-over in males in all the experiments which appeared to be the characteristic of marker stock as spontaneous male crossing-over was reported earlier with the same wild stocks when the second chromosome markers were used. Based on the data of karyotypically homozygous F1 females, the map distance between stw-pr was 36.55 map units. The heterozygosity due to a lengthy inversion in 2L increased the level of crossing-over between stw-pr genes of the third chromosome indicating interchromosomal effect. There was a considerable reduction in the rate of recombination between the same markers due to inversion heterozygosity in 3R indicating intrachromosomal effect. However, 3L inversion heterozygosity had no effect on crossover rate. These results provide evidence for intra-and interchromosomal effects of inversions on crossing-over in the third chromosome of D. ananassae.     

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.     

Heterosis without selectional coadaptation inDrosophila ananassae

Summary The relative viabilities of homozygous and heterozygous karyotypes were measured by making crosses between strains ofD. ananassae homozygous for ST or inverted gene orders in the second and third chromosomes. The strains utilized during the present study originated from widely separated localities in India, Kuala Lumpur and Kota Kinabaru, Malaysia and Chian Mai, Thailand. The presence of heterosis in many interpopulation crosses is evident from the results which show that the inversion heterozygotes formed by chromosomes coming from distant populations exhibit heterosis. On the other hand, heterosis is absent in two intrapopulation crosses. Thus the present results provide evidence that heterozygosis for many genes and gene complexes does produce high fitness without previous selectional coadaptation.     

Interchromosomal effects of inversions on crossover rate in maize

Summary The influence of heterozygous inversions on heterologous chromosome recombination has been studied in maize.Inv 2a causes an increase in crossing-over rate ofYg-Sh region of chromosome9: the reverse is true for the more proximal regionBz-Wx. The coincidence indexes for the traitYg-Sh-Bz is decreased, while the same index is increased for the regionSh-Bz-Wz. Inv 9a is accompanied by an high recombination rate in the distal region of chromsome2 Lg-Gl, while in the regionGl-V the effect is relatively less pronounced.The results seem to exclude mitotic recombination events, but are less suitable for supporting other specific interpretations. However, taking into considerationDrosophila experiments, our data are not conflicting with the physiological hypothesis proposed byRamel, which, at present, appears to explain most of the experimental results, although some difficulty arises in considering the cases of decreased recombination rate.The possibility of modifying, by genetical means, the recombination potential is of significance in some stage of plant breeding, at least in some species.With 2 Figures in the Text     

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.     

Cytogenetics of natural populations of Drosophila

D. bipectinata and D. malerkotliana differ from each other by three overlapping inversions in IIL, two included inversions in IIIL and two overlapping inversions in IIIR. These inversions were analysed on the basis of the salivary chromosome maps of D. malerkotliana. Bock's (1971) data revealed that the four members of the bipectinata species complex differ from each other with respect to overlapping inversions. The reason why the ancestral population which may have been heterozygous for common inversions split into at least four groups, each leading to the formation of a new species, and the possible mechanism of the origin of sexual isolation between the groups is discussed.     

The interchromosomal effect of inversions in maize

Summary The interchromosomal effect of inversions in maize along the short arm of chromosome 9 yields results which are distinctly different from those which are reported with Drosophila melanogaster. Recombination was increased in the c ₁-sh₁ region of chromosome 9 while the sh ₁-wx region was unaffected. This increased frequency of recombination appears to be due to an increase in single exchange events as multiple events were unchanged. Increases in recombination were accompanied by either an increase in chromosome interference or normal interference levels. The magnitude of increase in recombination was much smaller than that seen in interchromosomal effects in Drosophila and is consistent with other observations made in maize. When two inversions were present in the same nucleus simultaneously, the effect on recombination was of the same magnitude as the effect of a single inversion. All inversions tested, regardless of size or position with respect to the centromere showed the same magnitude of increase.     

Comparative Cytogenetic Variation of the Salivary Gland Polytene Chromosomes in Chironomus riparius Mg., 1804 (Diptera, Chironomidae) from Two Polluted Biotopes of Bulgaria and Russia

The structural–functional variation ofChironomus riparius salivary gland polytene chromosomes was studied in two geographically isolated Palearctic regions, Bulgaria (village Pancharevo) and Russia (St. Petersburg). The two biotopes, where larvae were collected, were polluted with various heavy metals from anthropogenic sources. Hereditary paracentric heterozygous inversions were characteristic of the Russian population, whereas somatic paracentric or pericentric heterozygous inversions were more common in the Bulgarian one. All inversions occurred at low frequencies. Other aberrations found in the two populations included somatic deletions resulting in a pompon structure of chromosome IVG, heterozygous translocation between chromosomes IVG and IIIF, enlargement of individual disks, and the appearance of a heterozygous block close to the centromere of chromosome IVG. In addition, changes in functional activity of the nucleolus organizer and Balbiani rings (BRc/BRb) were observed. Several aberration breakpoints proved to coincide with satellites of the Alu and Hinf families.     

Cytogenetic analysis of recombination in males of Drosophila ananassae

Cytogenetic studies of recombination in males of Drosophila ananassae were carried out by examining F₁ males derived from the mating of marker females, b se; bri ru of the BS stock, with males of two wild strains, TNG and L8. The male recombination values in both sections b-se (chromosome 2) and bri-ru (chromosome 3) are high in TNG F₁ but extremely low in L8 F₁ We demonstrate the presence of chiasmata in TNG F₁ males at a frequency capable of accounting for the observed recombination values. A unique series of “iso-site aberrations” was also observed in TNG F₁ males. Because of a parallelism in the distribution pattern between the chiasmata and the isosite aberrations, we propose that recombination in males of D. ananassae is meiotic in origin and that the iso-site aberrations are related to chiasma formation.     

Abundance and chromosomal distribution of six Drosophila buzzatii transposons: BuT1, BuT2, BuT3, BuT4, BuT5, and BuT6

The abundance and chromosomal distribution of six class-II transposable elements (TEs) of Drosophila buzzatii have been analyzed by Southern blotting and in situ hybridization. These six transposons had been previously found at the breakpoints of inversions 2j and 2q ⁷ of D. buzzatii. These two polymorphic inversions were generated by an ectopic recombination event between two copies of Galileo, a Foldback element. The four breakpoints became hotspots for TE insertions after the generation of the inversion and the transposons analyzed in this work are considered to be secondary invaders of these regions. Insertions of the six transposons are present in the euchromatin but show an increased density in the pericentromeric euchromatin–heterochromatin transition region and the dot chromosome. They are also more abundant in the inverted segments of chromosome 2 rearrangements. We further observed that the accumulation of TE insertions varies between elements and is correlated between dot, proximal regions, and inverted segments. These observations fully agree with previous data in Drosophila melanogaster and support recombination rate as the chief force explaining the chromosomal distribution of TEs.Electronic Supplementary Material Supplementary material is available in the online version of this article at and is accessible for authorized users.Sequence data from this article have been deposited in the EMBL/GenBank Data Libraries under accession number DQ402469.     

Genetic differentiation in natural populations of Drosophila ananassae

Inversion polymorphism has been studied in three natural populations of Drosophila ananassae. The three cosmopolitan inversions have been detected in all the three populations analysed. Some quantitative variations in the inversion frequencies seem to exist and the level of inversion heterozygosity varies between the different populations.