Genetic differentiation in natural populations of Drosophila ananassae

B. N. Singh Genetics Laboratory?, Department of Zoology, Banaras ffind~ University, ~arana~i-221~05, India

Abstract

Inversion polymorphism has been studied in three natural populations of Droso~~iIa anana~sae. 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.

Introduction

In Drosophila, chromosomal polymorphism due to inversions constitutes an adaptive character (Dobzhansky, 1951; Da Cunha, 1960; Sperlich, 1973). The amount of chromosomal polymorphism in a population is frequently correlated with the diversity of environments which the population ex- ploits (Dobzhansky et al., 1950; Da Cunha et al., 1950). According to Carson (1959) selection fa- vours heterozygotes (heteroselection) due to hete- rotic buffering in large, central and outcrossing populations whereas homoselection predominates in small and inbred populations. Thus highly poly- morphic populations have reached a high adapted- ness whereas less polymorphic populations have a high adaptability based on free genetic recombina- tion (Da Cunha et al., 1959).

D. ananassae is a cosmopolitan and domestic species. It shows a high degree of chromosomal polymorphism (for references see Singh, 1982). ‘Most inversions have a restricted distribution and are found in a very low frequency while the three paracentric inversions (subterminal, terminal and basal), are cosmopolitan and are of frequent occur- rence (Shirai & Moriwaki, 1952; Futch, 1966; Singh, 1970). The frequencies of these cosmopoli-

Genetiea 63.49-52 (1984). 0 Dr W. Junk Publishers, The Hague. Printed in the Netherlands.

tan inversions vary in Indian natural populations (Singh, 1974; Reddy & Krishnamurthy, 1974). The present paper reports further data on the frequen- cies of various gene sequences in three natural pop- ulations of D. ananassae.

Material and methods

Flies were collected from Lucknow and Kanpur in the last week of August, 1982 and from Varanasi in the third week of October, 1982. The present analysis is based on identification of the karyotype of one F, larva from each wild female. Varanasi, Lucknow and Kanpur are three different cities of Uttar Pradesh, India. The distance between Kan- pur and Lucknow is less than 100 km whereas both these cities are separated from Varanasi by a dis- tance of more than 300 km.

Results

All three cosmopolitan inversions, the subtermi- nal (alpha or 2LA), terminal (delta or 3LA) and basal (eta or 3RA), were detected in the samples of D. ananassae collected from Varanasi. Lucknow

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Table 1. Observed and expected numbers of different karyotypes in natural populations of D. ananassae.

Population Karyotypes 2L 3L 3R

ST/ST ST/AL AL/AL ST/ST ST/DE DE/DE ST/ST ST/ET ET/ET

Total no. of larvae analysed

Varanasi obs. 58 34 8 88 8 4 89 11 0 I00 exp. 56.25 37.50 6.25 84.64 14.72 0.64 89.30 10.40 0.30

Lucknow obs. 2 6 4 8 4 0 11 1 0 12 exp. 2.08 5.83 4.08 8.33 3.33 0.33 11.02 0.96 0.02

Kanpur obs. 4 21 14 37 2 0 23 16 0 39 exp. 5.39 18.22 15.39 37.03 1.95 0.03 24.64 12.72 1.64

and Kanpur . Table 1 presents the data on observed and expected numbers of different genotypes (ka-

ryotypes) in na tu ra l popula t ions of D . a n a n a s s a e .

The expected frequencies of different karyotypes were calculated fol lowing the Hardy-Weinberg rule. In the Varanasi popula t ion the S T / S T homo- zygotes in all the chromosomes are found in high frequencies with other gene-arrangement homozy-

gotes and heterozygotes being found in low fre- quencies. The na tura l popula t ions of K a n p u r and Lucknow are different f rom the Varanas i popula- tion: in both, the A L / A L homozygotes occur with frequencies higher than that of the S T / S T homozy- gotes. On the whole, no significant deviat ion from

Hardy-Weinberg equi l ibr ium is visible. The frequencies of different gene ar rangements

and the mean n u m b e r of heterozygous inversions per indiv idual are shown in Table 2. The chromo- somes with ST gene sequence occur always with

frequencies higher than those with inverted gene order in the popu la t ion from Varanasi . In the na tu- ral popula t ions of Lucknow and Kanpur , on the other hand, the AL chromosomes are more fre- quent than ST. However, the ST sequence in the third chromosome is more frequent than the inver-

sion. The value of the mean number of heterozy-

gous inversions per individual for the Varanasi popu la t ion is 0.53 and for the Lucknow and Kan-

pur popula t ions it varies from 0.92 to 1.00.

Discussion

The results of the present study reveal the pres- ence of three cosmopol i tan inversions in na tura l popula t ions of D . a n a n a s s a e from Varanasi , Kan- pur and Lucknow. It is evident f rom the present

results that the Varanasi popu la t ion is clearly dif- ferent f rom the other two popula t ions with respect to the gene-ar rangement frequencies and the level of inversion heterozygosity. K a n p u r and Lucknow are bigger cities than Varanas i and are separated by a smaller distance. The genetic differentiat ion be- tween these popula t ions may have some correlat ion with the variations in ecological niches and geograph-

ic distance between these populat ions. Data on the frequencies of cosmopol i tan inversions in D. a n a n a s s a e have been reported earlier by other in- vestigators. Dobzhansky and Dreyfus (1943) found that in all Brazilian localities, about one-half of the

Table2 . Frequencies (in percent) of different gene arrangements and mean number of heterozygous inversions in natural populations of O. ananassae.

Population Gene arrangements Total no. Mean no. 2L 3L 3R of chromo- of hetero- ST AL ST DE ST ET somes zygous in-

examined versions per individual

Varanasi 75.00+ 3.06 25.00_+ 3.06 92.00+ 1.92 8.00± 1.92 94.50_+ 1.61 5.50_+ 1.61 200 0.53 Lucknow 41.67_+10.06 58.33+10.06 83.33+7.61 16.67+7.61 95.83+4.08 4.17+4.08 24 0.92 Kanpur 37.18_+ 5.47 62.82+ 5.47 97.44+1.79 2.56+1.79 79.49+4.57 20.51±4.57 78 1.00

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individuals are heterozygotes for subterminal in- version, nearly 40 per cent of flies are heterozygotes for terminal inversion and nearly 30 per cent of individuals are heterozygotes for basal inversion. Freire-Maia (1952) found no difference in the mean frequency of heterozygous inversions per individual in several Brazilian localities. Singh( 1974) reported that the frequencies of inversions show considerable changes in Indian natural populations and the mean number of heterozygous inversions per individual ranges from 0.43 to 1.40. Reddy and Krishnamurthy (1974) observed significant alterations in the fre- quencies of inversion heterozygotes in natural pop- ulations from the Nilgiri range in South India. From the results presented here and reported earli- er, it is apparent that there are quantitative varia- tions in the amount of chromosomal polymor- phism in Indian natural populations of D. ana- nassae.

Central populations of a species are better adapt- ed to their heterogeneous environments by means of a high degree of heterozygosity for inversions and heterozygosity decreases in marginal popula- tions. This has been found in D. ~~ll~stoni (Dobz- hansky et al., 1950; Da Cunha et al., 1950), D. robusta (Carson, 1955) and D. subobscura (Prevos- ti, 1966; Sperlich et al., 1980; Sperlich & Pinsker, 1980). Carson (1955) suggested that cosmopolitan species have originated from marginal populations and have retained the open system of recombina- tion. Carson (1965) has distinguished four groups of geographically widespread species of Drosophila based on the geographical characteristics of their chromosomal polymorphisms. The first group in- cludes D. ananassae, D. busckii, D. h~)dei, D. im- migrans and D. melanogaster. He states that all members of this group show chromosomal poly- morphism but inverted gene orders are rarely ob- served to rise above fifty per cent. The data on the frequencies of inversions presented here and pub- lished earlier (Singh, 1974) provide evidence that inverted gene orders may rise above fifty percent in many natural populations of D. ananassae and the amount of chromosomal polymorphism also varies in different populations. Furthermore the naturally occurring inversion heterozygotes exhibit heterosis (Moriwaki & Tobari, 1975; Singh & Ray-Chaud- huri, 1972; Singh, 1972, 1981, 1982, 1983). There- fore, it may be suggested that the pattern of chrom- osomal polymorphism in D. ananassae does not

closely resemble that of other cosmopolitan species with which it has been grouped by Carson (1965). Thus, D. ananassae stands out as distinct from other cosmopolitan species.

References

Carson, H. L.. 1955. The genetic characteristics of marginal populations of Drosophila. Cold Spring Harb. Symp. quant. Biol. 20: 276-287.

Carson, H. L., 1959. Genetic conditions which promote or re- tard the formation of species. Cold Spring Harb. Symp. quant. Biol. 24: 87-105.

Carson, H. L., 1965. Chromosomal morphism in geographicaIly widespread species of Drosophila. In: The genetics of colon- izing species, eds. H. G. Baker & G. L. Stebbins, Academic Press, New York, pp. 503-531.

Da Cunha, A. B., 1960. Chromosomal variations and adapta- tion in insects. Ann. Rev. Ent. 5: 85-I 10.

Da Cunha, A. B., Burla, H. & Dobzhansky, Th., 1950. Adaptive chromosomat polymorphism in Drosophila willistoni. Evo- lution 4: 212-235.

Da Cunha, A. B., Dobzhansky, Th., Pavlovsky, 0. & Spassky, B., 1959. Genetics of natural populations. XXVIII. Supple- mentary data on the chromosomal polymorphism in Droso- phila willistoni in its relation to environment. Evolution 13: 389-404.

Dobzhansky, Th., 195 I. Genetics and the origin of species. Third Edition. Columbia Univ. Press, N.Y.

Dobzhansky, Th. & Dreyfus, A., 1943. Chromosomal aberra- tions in Brazilian Drosophila ananassae. Proc. natn. Acad. Sci. U.S.A. 44: 622-629.

Dobzhansky, Th., Burta, H. & Da Cunha, A. B., 1950. A com- parative study of chromosomai polymorphism in sibling species of the willisoni group of Drosophila. Am. Nat. 84: 229-246.

Freire-Maia, N., 1952. Chromosomal variation in Brazilian do- mestic species of Drosophila. Drosoph. Inf. Serv. 26: 100.

Futch, D. G., 1966. A study of speciation in South Pacific populations of Drosophila ananassae. Univ. Texas. Publ. 6615: 79-120.

Moriwaki, D. & Tobari, Y. N., 1975. Drosophila ananassae. In: Handbook of genetics, ed. R. C. King, Plenum, N.Y., pp. 513.-535.

Prevosti, A., 1964. Chromosomal polymorphism in Drosophila subobscura populations from Barcelona (Spain). Genet. Res. 5: 27-38.

Reddy, G. S. & Krishnamurthy, N. B., 1974. Aititudinal gra- dients in the frequencies of three common inversions in Drosophila ananassae. Drosoph. Inf. Serv. 51: 136-137.

Shirai, M. & Moriwaki, D., 1952. Variations of gene sequences in various strains of Drosophila ananassae. Drosoph. Inf. Serv. 26: 120-121.

Singh, B. N., 1970. Distribution of most common inversions of Drosophila ananassae in different parts of India including Andaman and Nicobar Islands. Indian Biol. 2(2): 78-81.

Singh, B. N., 1972. The lack of evidence for coadaptation in geographic populations of Drosophila ananassae. Genetica 43: 582.-588.

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Singh, B. N., 1974. Quantitative variation of chromosomal po- lymorphism in natural populations of Drosophila ananas- sae. Cytologia 39: 309-3 14.

Singh, B. N., 1981. Interracial hybridization in Drosophila ana- nassae. Genetica 57: 139-142.

Singh, B. N., 1982. Persistence ofchromosomal polymorphism in various strains of Drosophila ananassae. Genetica 59: 151-156.

Singh, B. N., 1983. An inversion within the subterminal inversion in Drosophila ananassae. Experientia 39.999100.

Singh, B. N. & Ray-Chaudhuri, S. P., 1972. Balanced chromo- somal polymorphism m experimental populations of Dro-

sophila ananassae. Indian J. exp. Biol. IO: 301-303. Sperlich, D., 1973. Populationsgenetik. G. Fischer Verlag, Stutt-

gart. Sperlich, D. & Pinsker, W., 1980. Distribution pattern of

chromosomal polymorphism in natural populations of Dro- sophila. Atti Ass. Genet. Ital. 25: 47-60.

Sperlich, D., Pinsker, W. & Pfriem, P., 1980. Inversion, allo- zyme and lethal frequencies in natural populations of Dro- sophila subobscura. Genetika (Yugosl.) 12: 91-101.

Received 26.11.1982 Accepted 21.4.1983.