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Genetica 97: 321-329, 1996. (~) 1996 Kluwer Academic Publishers. Printed in the Netherlands.

Population and behaviour genetics of Drosophila ananassae B.N. S i n g h Genetics Laboratory, Department o f Zoology, Banaras Hindu University, Varanasi 221005, India Received 16 August 1994 Accepted 17 September 1995

Key words: Drosophila ananassae, population and behaviour genetics

Abstract Drosophila ananassae is a cosmopolitan and domestic species. It occupies a unique 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 populations 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 breakdown 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 sternopleural 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. Introduction

In studies of population and behaviour genetics, Drosophila has proved to be uniquely useful and a large body of information on this subject has been accumulated as a result of the work done on various species. The population genetics studies have mainly involved concealed genetic variability caused by deleterious genes, chromosomal variability and allozyme polymorphisms. In various species of Drosophila, it has been demonstrated that sexual and non-sexual

behaviour of adults and behaviour of larvae are influenced by genetic factors. Drosophila ananassae, a cosmopolitan and domestic species, belongs to the ananasae species complex of the ananassae subgroup of the melanogaster group (Bock & Wheeler, 1972). Kikkawa (1938) selected D. ananassae as material for genetic studies because of its excellent viability, high mutability and certain peculiarities in its cytological and genetic behaviour. It has become clear that it is unique among the various Drosophila species thus far investigated. D. ananassae

322 has been used for genetic studies by Japanese, Indian, North American and French workers (for references see Moriwaki & Tobari, 1975; Singh, 1985a, 1988a; Tobari, 1993). D. a n a n a s s a e occupies a unique status among the D r o s o p h i l a species due to certain peculiarities in its genetic behaviour. One example is an appreciable level of spontaneous meiotic male recombination (Kale, 1969; Hinton, 1970; Moriwaki, Tobari & Oguma, 1970; Singh & Singh, 1988a). Other unusual features are varied chromosomal polymorphism, high mutability, Y-4 linkage of nucleolus organizer, segregation distortion, parthenogenesis, extrachromosomal inheritance and lack of coadaptation (for references see the review by Singh, 1985a). A spontaneous bilateral genetic mosaic, which was characterised by three mutant characters (cu, e, se) on the left side and all normal characters on the right side, was detected while scoring the progeny of a test cross between heterozygous males and mutant females. Its probable origin is attributed to mitotic recombination in the zygote which was genotypicaly heterozygous (Singh & Mohanty, 1992). A number of investigations carried out on chromosomal polymorphism in D. a n a n a s s a e have revealed that it presents a high degree of chromosomal variability in its populations (for references see Singh, 1988a; Tobari, 1993). A total of 69 paracentric inversions, 17 pericentric inversions and 13 translocations have been detected in natural populations of D. a n a n a s s a e (Tobari, 1993). The occurrence of pericentric inversions and translocations is rare in other species of D r o s o p h i l a and reflects unusual mutational properties of D. a n a n a s s a e . There is evidence for intra- and interchromosomal effects of heterozygous inversions on crossing-over in males and females of D. a n a n a s s a e (Singh & Singh, 1987, 1988a; Singh & Mohanty, 1991). Crossing-over between linked inversions has also been studied cytologically and the results have indicated that there is strong suppression of crossingover between inversions in D. a n a n a s s a e (Singh, 1973; Singh & Singh, 1988; Singh & Mohanty, 1990). It has been suggested that this genetic characteristic of the species may confer advantages to it due to low levels of inversion heterozygosity in natural populations. Isozyme polymorphism has also been studied in certain populations of D. a n a n a s s a e , indicating the presence of genetic variability among populations (Johnson, 1971). Multiple amylase genes in D. a n a n a s s a e have also been reported by Da Lage et al. (1992). On the basis of positive response to selection, evidence for polygenic control and additive genetic vari-

A

2L r

, 2R

~1 AL

3L

J 3R

~

DE

ET

Fig. 1. Location of AL (2L), DE (3L) and ET (3R) inversions in different chromosomes of Drosophila ananassae.

ation for phototactic behaviour in D. a n a n a s s a e has been presented (Markow & Smith, 1979). Transposable elements have also been reported in D. a n a n a s s a e . The t o m element is involved in mutations at the O m (optic morphology) locus (Hinton, 1984; Shrimpton, Montgomery & Langley, 1986; Matsubayashi e t al., 1991). RFLP studies (Stephan, 1989) at the X-linked O m (1 D) locus of D. a n a n a s s a e populations from Burma, India and Brazil showed variation in the average heterozygosity per nucleotide and restriction sites. In the present review, the work done in India on population and behaviour genetics of D. a n a n a s s a e is summarised.

Population genetics Studies on chromosomal polymorphism in Indian populations of D. a n a n a s s a e were initiated by RayChaudhuri and Jha (1966, 1967) who detected several chromosomal aberrations and found geographic differentiation of inversion polymorphism. Since then a number of investigations on chromosomal polymorphism in Indian populations ofD. a n a n a s s a e have been carried out, reporting several chromosomal aberrations including paracentric and pericentric inversions and translocations (Singh, 1970, 1983a; Singh & Singh, 1991; Singh, Mishra & Jha, 1971; Singh, Jha & Rahman, 1972; Nirmala Sajjan & Krishnamurthy, 1970, 1972; Reddy & Krishnamurthy, 1972a,b). The three cosmopolitan inversions (Fig. 1) have become coextensive with the species considering the monophyletic origin of these inversions. Extensive studies on the frequencies of these inversions in Indian populations have been reported. Reddy and Krishnamurthy (1974) observed significant changes in the frequency of inversion heterozygotes in natural populations from Nilgiri range in South India. They found significant differences in the chromosomal constitutions of D. a n a n a s s a e populations inhabiting different altitudes in the western range of Nilgiri hills. In a population from Orrisa, temperature related changes in the frequency of 2LA (AL) inversion were observed (Dasmoha-

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patra, Tripathi & Das, 1982). Singh (1974a, 1984a,b, 1989a,b, 1991a) studied inversion polymorphism in natural populations ofD. a n a n a s s a e from 29 geographical locations, including Andaman and Nicobar Islands (Fig. 2). The results show that the frequencies of different gene arrangements vary significantly among the populations analysed (Table 1). Furthermore, the level of heterozygosity (measured in terms of mean number of heterozygous inversions per individual) also varies

among the populations. Populations from Southern India, particularly Tamil Nadu, Kerala and Andaman and Nicobar Island, situated near the equator, maintain inversions in higher frequency than those inhabiting different localities in Uttar Pradesh and other northern states. With some exception in the north, results in general indicate the existence of a north-south cline in inversion frequency. The degree of genetic divergence among different populations has been quantified by cal-

324 Table 1. Frequencies (in percent) of diferent gene arrangements in twenty nine Indian natural populations of Drosophila ananassae. Population

Total no. of chromosomes

Gene arrangements 2L

3L AL

ST

Mean no. of heterozygous inversions

3R

examined

ST

DE

ST

ET

Jammu

262

46.60

53.40

Agra Shiliguri Guwahati

104 56 90

34.62 10.71 17.78

65.38 89.29 82.22

57.20

42.80

1.18

50.96 35.71 28.89

88.20 96.15 80.36 67.78 95.83

11.80

49.04 64.29 71.11

3.85 19.64 32.22 4.17

0.83 1.04

Lucknow Kanpur Shillong

24 78 70

41.67 37.18 15.71

58.33 62.82 84.29

83.33 97.44 70.00

16.67 2.56 30.00

79.49 67.14

20.51 32.86

Ghazipur Bhagalpur Varanasi Jamsoti

I00 130 200 60

77.00 20.00 75.00 100.00

23.00 80.00 25.00 0.00

88.00 69.23 92.00 78.30

12.00 30.77 8.00 21.70

97.00

3.00 20.77 5.50

Lowari

42

100.00

0.00

78.60

21.40

Ukhara

30

43.30

56.70

60.00

40.00

73.30

26.70

Calcutta

240

10.83

89.17

85.00

15.00

Birlapur Bhubaneswar Purl

200 104 100

25.00 16.35 11.00

75.00 83.65 89.00

83.00 64.42 64.00

17.00 35.58 36.00

78.33 85.00

21.67 15.00

62.50 64.00

Bombay Hyderabad

208 140

3.37 22.86

96.63 77.14

83.17 55.00

16.83 45.00

37.50 36.00 28.37

Goa

140

12.86

87.14

35.71

64.29

85.00 83.57

Madras Port Blair Trichur

100 122 204

27.00 30.30 46.57

73.00 69.70 53.43

14.00 43.40 20.10

86.00 56.60 79.90

65.00 68.80 96.57

35.00

1.12

31.20 3.43

1.40

Ernakulam

210

14.76

85.24

47.14

52.86

80.48

Madurai Quilon

158 108

46.84 23.15

53.16 76.85

6.33 14.81

93.67 85.19

67.09

19.52 32.91

Tfivandrum Kamorta

140 26

15.71 34.60

84.29 65.40

1 7 . 1 4 82.86 42.30 57.70

Kanniya Kumari

100

11.00

89.00

26.00

74.00

79.23 94.50 100.00 95.20

71.63

85.19 85.71 61.50 98.00

0.00 4.80

15.00

16.43

per individual

1.22 0.92 1.00 1.14

0.64 1.22 0.53 0.43 0.52 1.26 0.80 0.94 1.33 1.14 0.78 1.06 1.04

0.80 1.00 0.94

14.81 14.29

1.02 0.89

38.50 2.00

1.38 0.62

On the basis of data reported by Singh (1974a, 1984a,b, 1989a,b, 1991a)

culating genetic distance (D) and genetic identity (I) on the basis of differences in the chromosome arrangement frequencies (Singh, 1984c, 1986, 1989b; Singh & Anand, unpublished). In general, the populations from the south show more differentiation than those from the north. The relationship between the populations has been shown by constructing a dendrogram (Fig. 3) based on UPGMA clustering of genetic identity values. There is no strong positive relation between the genetic difference and geographic distance, although many pairwise comparisons show that populations separated by small geographic distances show low levels

of genetic difference (higher genetic identity). There is strong evidence from studies on inversion polymorphism by the present author that Indian populations of D. a n a n a s s a e have undergone a considerable degree of genetic divergence. The south experiences a tropical and humid climate. Localities near the sea coast differ from those away from it. Rural populations of Jamsoti and Lowari, situated in the vicinity of Chakia forest, have very high frequencies of standard gene orders in all the chromosomes, the level of inversion heterozygosity remaining very low (Singh, 1974a). All domestic species are characterised by a high degree of

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Trlvandrum (Z?) Quilon (26) ½anniya Kumart ( 291 Trlcbur (23)

Fig. 3.

Dendrogramof naturalpopulationsofD. ananassae basedon UPGMAclusteringof geneticidentityvalues.

interpopulation migration because of their close association with man. Although the effect of migration in D. a n a n a s s a e has not been studied, it has been suggested by Futch (1966) that the populations of D. a n a n a s s a e separated by oceans and mountains may still experience gene exchange because the flies are transported by human travel. Dobzhansky and Dreyfus (1943) have also pointed out that this species has depended on man for its present widespread distribution; the coextensive distribution of three cosmopolitan inversions is suggested as evidence for this. In addition, D. a n a n a s s a e continues to show geographic differentiation of inversion polymorphism. Based on the results obtained in D. a n a n a s s a e , it has been suggested that chromosomal polymorphism may be adaptively important even in a widespread domestic species, and populations may undergo divergence as a consequence of their adaptation to varying environments. Singh and Ray-Chaudhuri (1972) conducted population cage experiments by using ST and AL gene arrangements of the second chromosome derived from Indian populations. They found that all the experimen-

tal populations remained polymorphic for several generations and both the chromosomes were maintained at a definite frequency. Thus chromosomal polymorphism is balanced due to adaptive superiority of inversion heterozygotes. The differential mortality during the larval period in a highly crowded population cage favours the survival of inversion heterozygotes, which was shown while comparing egg and adult samples (Singh & Ray-Chaudhuri, 1972). Chromosomal polymorphism due to three cosmopolitan inversions often persists in laboratory stocks established from females collected from nature (Singh, 1982a, 1983a,b,c, 1987, 1988b). This demonstrates that heterotic buffering is associated with cosmopolitan inversions. However, the degree of heterosis may vary depending upon the allelic contents of the chromosomal variants (Singh, 1983b,c). Inversion frequency may also change due to random genetic drift in small populations (Singh, 1987, 1988b). Singh (1972, 1974b, 1981, 1985b)conducted interracial hybridization experiments by employing homozygous as well as chromosomally polymorphic

326 strains of D. a n a n a s s a e originating from different localities. It has been found that inversion heterozygotes formed by chromosomes of different geographic origins exhibit heterosis which persists in interracial crosses involving polymorphic strains. The chief conclusion from these results is that there is lack of evidence for coadaptation in geographic populations of D. a n a n a s s a e . This situation apparently conflicts with what has been found in other species by Dobzhansky and others (for references see Singh, 1991b). Singh (1985b) suggested that heterosis associated with cosmopolitan inversions in D. a n a n a s s a e appears to be simple luxuriance rather than population heterosis (coadaptation) and thus luxuriance can function in the adjustment of organisms to their environments. There are several studies on intra- and interchromosomal associations in natural populations and laboratory stocks of D. ananassae. Various combinations of unlinked inversions occurring in random association indicate no interchromosomal interactions in D. a n a n a s s a e (Singh, 1982b, 1983d; Singh & Singh, 1989). Two linked inversions of the third chromosome which strongly suppress recombination between them when heterozygous often show non-random associations in laboratory stocks (Singh, 1973, 1974c, 1983d, 1984d; Singh & Singh, 1988, 1988b, 1990, 1991). This is likely to be due to epistatic interaction and suppression of crossing-over. It has also been suggested that linkage disequilibrium between inversions in certain isofemale strains may occur due to random genetic drift (Singh & Singh, 1990). The tight linkage between the two inversions enhances the chance of drift in isofemale strains. There are a few reports on genetic heterogeneity for a matrical character (Singh & Mathew, 1994) and allozyme polymorphism in Indian populations of D. a n a n a s s a e (Jha, Mishra & Pandey, 1978; Parkash & Jyoutsna, 1988; Sharma, Sharma & Parkash, 1993). Electrophoretic studies on the alcohol dehydrogenase isozymes in two geographic strains of D. a n a n a s s a e show that biochemical genetic differentiation exists between them (Jha, Mishra & Pandey, 1978). Sharma, Sharma and Parkash (1993) analysed A d h genic variation in six geographic populations of D. a n a n a s s a e collected along a 20 ° latitudinal range and found clinal variation. They found latitudinal variation in the frequency of A d h F and in ethanol tolerance, lending support to the hypothesis that clinal variations are adaptively maintained by natural selection.

Behaviour genetics Certain aspects of behaviour genetics of D. a n a n a s sae have also been studied by Singh and coworkers. Females showed a preference for oviposition into the surface of peripheral areas of food medium (Srivastava & Singh, 1993a). Furthermore, significant variation for oviposition site preference was found among different strains, which was attributable to genetic heterogeneity among the strains tested (Srivastava & Singh, 1993b). The existence of sexual isolation within D. a n a n a s s a e has been reported (Singh & Chatterjee, 1985a,b). The degree of isolation is stronger in isofemale lines than in natural populations. Thus reproductive isolation may originate as a side effect of genetic divergence which affects the mate recognition system, ultimately resulting in the strains showing incipient isolation. Mating propensity was tested by using certain mutant and wild strains ofD. a n a n a s s a e and the results extend evidence for its genetic basis (Singh et al., 1985; Chatterjee & Singh, 1987, 1988; Singh & Chatterjee, 1987). Two sex-linked genes, w h i t e and Beadex, were found to diminish the sexual activity of males. Significant variation among different wild strains was found with respect to mating propensity and fertility (Singh & Chatterjee, 1987). The strains showing greater sexual activity produced more progeny-- males contribute more to variation than females, and thus are inherently more subject to intrasexual selection. Singh and Chatterjee (1986, 1988a) studied the mating ability of homo- and hetero-karyotypes due to subterminal (2L) inversion derived from natural populations of D. ananassae in which the frequencies of different chromosome arrangements were known. Their main conclusions are: a) the chromosome occurring in high frequency is associated with higher mating activity in all the populations analysed; b) heterokaryotypic males are superior in mating propensity to the corresponding homokaryotypes, indicating the existence of heterosis associated with the AL inversion with respect to male mating activity; and c) males show greater variation than females, which indicates striking sex differences in D. ananassae. Thus inversion polymorphism in D. ananassae may have a partial behavioural basis, as has been demonsrated in other species of Drosophila. Polygenic control of mating activity has been demonstrated on the basis of positive response to selection for high and low mating propensity (Singh & Chatterjee, 1988b). It has also been found that males are much more affected by selection than females. The significant difference in mating activity of hybrids produced

327 by the fast and slow males indicates the possibility of a Y-linked influence of mating activity in D. a n a n a s s a e . When red eye males were tested separately with s e p i a and c a r d i n a l mutants at nine different ratios, it was found that both types of males were equally successful in mating when present in the same ratio. However, they were more successful in mating when in a minority. This advantage disappeared when the males became common (Singh & Chatterjee, 1989). This provides evidence for rare male mating advantage in D. ananassae.

Pupation site preference has been studied by measuring pupation height in D. a n a n a s s a e (Singh & Pandey, 1991, 1993a,b; Pandey & Singh, 1993). Although pupation height is influenced by various biotic and abiotic factors, evidence for genetic control of larval pupation behaviour has been presented. Positive response to selection for high and low pupation height, and intermediate pupation height of F1 hybrids produced by making reciprocal crosses between high and low lines, show that pupation height in D. a n a n a s s a e is under polygenic control (Singh & Pandey, 1993a). The results of various crosses between two stocks with significant differences in pupation height have demonstrated that inheritance of pupation height fits a classical additive polygenic model, and there is a substantial amount of additive genetic variation in natural populations of D. a n a n a s s a e (Singh & Pandey, 1993b). Furthermore, the analysis of reciprocal backcrosses has shown a significant maternal effect. Since the maternal effect was found only in backcrosses but not in the F1, it is suggested that the maternal effect on pupation height follows the pattern of inheritance of a transient maternal effect (Singh & Pandey, 1993b).

Conclusions is one of the most common species in tropical regions of the world, particularly in and around places of human habitation. Its common occurrence in India, coupled with many unusual genetic features, attracted the attention of Indian workers. It is evident from the work done on population and behaviour genetics of D. a n a n a s s a e from India that the natural populations have undergone a considerable degree of genetic divergence, in spite of the fact that D. a n a n a s s a e is characterised by a high degree of interpopulation migration because of its close association with man. Indian populations of D. a n a n a s s a e are genetically differentiated with respect to chromoDrosophila ananassae

somal variability, allozyme polymorphism and quantitative characters. Genetic heterogeneity with respect to certain behavioural traits in Indian populations of D. a n a n a s s a e has also been observed. These findings provide important and interesting information concerning certain aspects of evolutionary genetics such as selection, genetic drift, heterosis and genetic coadaptation, balanced polymorphism, crossing-over, epistasis and linkage disequilibrium, reproductive isolation and sexual selection. It is hoped that future studies employing molecular genetic techniques will be undertaken and our knowledge of population and behaviour genetics of D. a n a n a s s a e will be immensely enriched.

Acknowledgements The work of the present author cited in this review has been supported by DST, CSIR, UGC, New Delhi and CAS in Zoology, Banaras Hindu University. The author is thankful to the anonymous reviewer for helpful comments on the manuscript.

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328 Kale, P.G., 1969. The meiotic origin of spontaneous crossovers in Drosophila ananassae males. Genetics 62: 123-133. Kikkawa, H., 1938. Studies on the genetics and cytology of Drosophila ananassae. Genetica 20:458-516. Markow, T.A. & L.D. Smith, 1979. Genetics of phototactic behaviour in Drosophila ananassae, a member of the Drosophila melanogaster species group. Behav. Genet. 9: 61-68. Matsubayashi, H., Y.N. Tobari & S.H. Hori, 1991. Genetic analysis of the Om (2D) locus in Drosophila ananassae. Jpn. J. Genet. 66: 387-397. Moriwaki, D. & Y.N. Tobari, 1975. Drosophila ananassae, pp. 513535 in Handbok of Genetics, edited by R.C. King, Plenum Press, New York. Moriwaki, D., Y.N. Tobafi & Y. Oguma, 1970. Spontaneous crossing over in the male of Drosophila ananassae. Jpn. J. Genet. 45: 41-420. Nirmala Sajjan, S. & N.B. Krishnamurthy, 1970. Report on two new translocations in a natural population of Drosophila ananassae from Hiriyur (Mysore State, India). Dros. Inform. Serv. 45: 166. Nirmala Sajjan, S. & N.B. Krishnamurthy, 1972. New gene arrangements in Drosophila ananassae. Dros. Inform. Serv. 48: 103104. Pandey, M.B. & B.N. Singh, 1993. Effect of biotic and abiotic factors on pupation height in four species of Drosophila. Ind. J. Exp. Biol. 31: 912-917. Parkash, R. & Jyoutsna, 1988. Allozyme variation in three Drosophila species of ananasae species subgroup. Curr. Sci. 57: 10711074. Ray-Chaudhuri, S.P. & A.P. Jha, 1966. Studies on the salivary gland chromosomes of Indian Drosophila ananassae. Proc. Int. Cell. Biol. Meet. Bombay, pp. 352-383. Ray-Chaudhuri, S.P. & A.P. Jha, 1967. Genetics of natural populations of Indian Drosophila ananassae. Nucleus 10: 81-89. Reddy, G.S. & N.B. Krishnamurthy, 1972a. Aberrant gene sequences in Drosophila ananassae from South India. Dros. Inform. Serv. 48: 139. Reddy, G.S. & N.B. Krishnamurthy, 1972b. Two new gene arrangements in Drosophila ananassae from South India. Dros. Inform. Serv. 48: 140-142. Reddy, G.S. & N.B. Krishnamurthy, 1974. Altitudinal gradients in the frequencies of three common inversions of Drosophila ananassae. Dros. Inform. Serv. 51: 136-137. Sharma, M., S. Sharma & R. Parkash, 1993. ADH polymorphism and ethanol tolerance in three species ofananassae species subgroup. Evol. Biol. 7: 51-62. Shrimpton, A.E., E.A. Montgomery & C.H. Langley, 1986. Om mutations in Drosophila ananassae are linked to insertions of a transposable element. Genetics 114: 125-136. Singh, A.K. & B.N. Singh, 1988a. Heterozygous inversions and spontaneous male crossing over in Drosophila ananassae. Genome 30: 445-450. Singh, A.K. & B.N. Singh, 1988b. An extreme linkage between inversions in Drosophila ananassae. Curt. Sci. 57: 400--402. Singh, A.K. & B.N. Singh, 1989. Further data on interchromosomal associations in Drosophila ananassae. Naturalia 14: 19-30. Singh, A.K. & B.N. Singh, 1991. A new inversion in Indian Drosophila ananassae. Dros. Inform. Serv. 70: 201-202. Singh, B.N., 1970. Distribution of most common inversions of Drosophila ananassae in different parts of India including Andaman and Nicobar Islands. Ind. Biol. 2: 78-81. Singh, B.N., 1972. The lack of evidence for coadaptation in geographic populations of Drosophila ananassae. Genetica 43: 582-588.

Singh, B.N., 1973. Recombination between heterozygous inversions in Drosophila ananassae. Genetica 44: 602-607. Singh, B.N., 1974a. Quantitative variation of chromosomal polymorphism in natural populations on Drosophila ananassae. Cytologia 39:309-314. Singh, B.N., 1974b. Persistence of heterosis in crosses between geographic races of Drosophila ananassae. Ind. J. Exp. Biol. 12: 376-377. Singh, B.N., 1974c. On the combinations of different gene arrangements in the third chromosome of Drosophila ananassae. Caryologia 27: 285-292. Singh, B.N., 1981. Interracial hybridisation in Drosophila ananassae. Genetica 57: 139-142. Singh, B.N., 1982a. Persistence of chromosomal polymorphism in various strains of Drosophila ananassae. Genetica 59:151-156. Singh, B.N., 1982b. The lack of evidence for interchromosomal interactions in Drosophila ananassae. Naturalia 7: 29-34. Singh, B.N., 1983a. An inversion within the subterminal inversion in Drosophila ananassae. Experientia 39: 99-100. Singh, B.N., 1983b. Cosmopolitan inversions in Drosophila ananas. sac. Caryologia 36: 333-344. Singh, B.N., 1983c. Variations in the gene arrangement frequencies and the degree of heterosis in laboratory strains of Drosophila ananassae. Braz. J. Genet. 6: 407-414. Singh, B.N., 1983d. On intra and interchromosomal associations in Drosophila ananassae. Genetica 60: 231-235. Singh, B.N., 1984a. Genetic differentiation in natural populations of Drosophila ananassae. Genetica 63: 49-52. Singh, B.N., 1984b. High frequency of cosmopolitan inversions in natural populations of Drosophila ananassae from Kerala, South India. J. Hered. 75: 504-505. Singh, B.N., 1984c. Genetic distance in inversion polymorphism among natural populations of Drosophila ananassae. Genetica 64:211-224. Singh, B.N., 1984d. Epistatic interaction between linked gene arrangements in Drosophila ananassae. Braz. J. Genet. 7: 175181. Singh, B.N., 1985a. Drosophila ananassae - - A genetically unique species. Nucleus 28: 169-176. Singh, B.N., 1985b. Heterosis without selectional coadaptation in rosophila ananassae. Theoret. Appl. Genet. 69: 437-441. Singh, B.N., 1986. Genetic similarity between natural populations of Drosophila ananassae from Kerala and Andaman and Nicobar Islands. Genetica 69: 143-147. Singh, B.N., 1987. On the degree of genetic divergence in Drosophila ananassae populations transferred to laboratory conditions. Zeit. Zool. Syst. Evoh 25: 180-187. Singh, B.N., 1988a. Chromosomal polymorphism of Drosophila ananassae. Ind. Rev. Life Sci. 8: 147-168. Singh, B.N., 1988b. Evidence for random genetic drift in laboratory populations of Drosophila ananassae. Ind. J. Exp. Biol. 26: 85-87. Singh, B.N., 1989a. Chromosomal variability in natural population of Drosophila ananassae from Jammu. Ind. J. Genet. Plant Breed. 49: 241-244. Singh, B.N., 1989b. Inversion polymorphism in Indian populations of Drosophila ananassae. Hereditas 110:133-138. Singh, B.N., 1991a. Chromosomal polymorphism in Drosophila ananassae: Similarity between widely distant populations from India. Kor. J. Genet. 13: 27-33. Singh, B.N., 1991b. Genetic coadaptation in Drosophila. Ind. Rev. Life Sci. 11: 205-231.

329 Singh, B.N. & S. Chatterjee, 1985a. A study of sexual isolation among natural populations of Drosophila ananassae. Braz. J. Genet. 8: 457-464. Singh, B.N. & S. Chatterjee, 1985. Symmetrical and asymmetrical sexual isolation among laboratory strains of Drosophila ananassae. Can. J. Genet. Cytol. 27: 405-409. Singh, B.N. & S. Chatterjee, 1986. Mating ability of homo- and hetero-karyotypes of Drosophila ananassae from natural populations. Heredity 57: 75-78. Singh, B.N. & S. Chatterjee, 1987. Variation in mating propensity and fertility in isofemale strains of Drosophila ananassae. Genetica 73: 237-242. Singh, B.N. & S. Chatterjee, 1988a. Parallelism between male mating propensity and chromosome arrangement frequency in natural populations of Drosophila ananassae. Heredity 60: 269-272. Singh, B.N. & S. Chatterjee, 1988b. Selection for high and low mating propensity in Drosophila ananassae. Behav. Genet. 18: 357-370. Singh, B.N. & S. Chatterjee, 1989. Rare male mating advantage in Drosophila ananassae. Genet. Sel. Evol. 21: 447-456. Singh, B.N., S. Chatterjee & S. Roy, 1985. Behavioural analysis of mating between white eyed and wild type Drosophila ananassae. Ind. J. Exp. Biol. 23: 661~562. Singh, B.N. & S. Mathew, 1994. Genetic differentiation with respect to sternopleural bristle number in Indian populations of Drosophila ananassae. Genetika (subm.). Singh, B.N. & S. Mohanty, 1990. Lack of correlation between crossing over and chromosome distance between inversions in Drosophila ananassae. Genome 33: 592-595. Singh, B.N. & S. Mohanty, 1991. Effect of heterozygous autosomal inversions on recombination in X chromosome of Drosophila ananassae. Ind. J. Exp. Biol. 29: 422-425. Singh, B.N. & S. Mohanty, 1992. A spontaneous genetic mosaic in Drosophila ananassae. Curr. Sci. 62: 372-374. Singh, B.N. & M. Pandey, 1991. Intra- and interspecies variations in pupation height in Drosophila. Ind. J. Exp. Biol. 29: 926--929.

Singh, B.N. & M.B. Pandey, 1993a. Selection for high and low pupation height in Drosophila ananassae. Behav. Genet. 23: 239-243. Singh, B.N. & M.B. Pandey, 1993b. Evidence for additive polygenic control of pupation height in Drosophila ananassae. Hereditas 119: 111-116. Singh, B.N. & S.P. Ray-Chaudhuri, 1992. Balanced chromosomal polymorphism in experimental populations of Drosophila ananassae. Ind. J. Exp. Biol. 10: 301-303. Singh, B.N. & A.K. Singh, 1987. The effects of heterozygous inversions on crossing-over in Drosophila ananassae. Genome 29: 802-805. Singh, B.N. & A.K. Singh, 1988. Crossing over between linked inversions in Drosophila ananassae. Hereditas 109: 15-20. Siagh, B.N. & A.K. Singh, 1990. Linkage disequilibrium in laboratory strains of Drosophila ananassae is due to drift. Hereditas 112: 203-208. Singh, B.N. & A.K. Singh, 1991. Nonrandom associations between independent inversions in laboratory strains of Drosophila ananassae. Naturalia 16:11-18. Singh, V.K., M. Mishra & A.P. Jha, 1971. A new pericentric inversion in Drosophila ananassae. Dros. Inform. Serv. 47: 97. Singh, V.K., A.P. Jha & S.M.Z. Rahman, 1972. A new report of pericentric inversion in the fight arm of X chromosome of Drosophila ananassae. Bhagal Univ. J. 5: 8-9. Srivastava, T. & B.N. Singh, 1993a. Oviposition site preference in four species of Drosophila. Ind. J. Exp. Biol. 31: 460--462. Srivastava, T. & B.N. Singh, 1993b. lntraspecies variation with respect to oviposition site preference in certain Indian species of Drosophila. Evol. Biol. 7:193-205. Stephan, W., 1989. Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. 1I. The Om (1D) locus, Mol. Biol. Evol. 6: 624635. Tobari, Y.N. (ed.) 1993. Drosophila ananassae. Gentrical and Biological Aspects. Japan Scientific Societies Press, Tokyo.