Sep 22, 1992 - COCKS, D. A. 1981. Latitudinal relationships of esterase-6 and ... -John Wiley and Sons,. New York. THROCKMORTON, L. H. 1975.
Hereditas 119: 161- 1 70 (1993)
Geographical clinal variation at seven esterase-coding loci in Indian populations of Zaprionus indianus RAVI PARKASH AND J. P. YADAV Department of Biosciences, Maharshi Dayanand University, Rohtak- 124001, India
PARKASH, R. and YADAV,J. P. 1993. Geographical clinal variation at seven esterase-coding loci in Indian populations of Zaprionus indianus. - Hereditas 119: 161-170. Lund, Sweden. ISSN 0018-0661. Received September 22, 1992. Accepted May 3, 1993 Twelve Indian natural populations of Zaprionus indianus, collected along 22" latitudinal range, were analysed electrophoretically for allozymic variation of esterase gene-enzyme system. Interestingly, all the seven Est loci were found to be highly polymorphic in all the populations of Z . indianus. The genetic structure of Z . indianus populations was characterized by extensive inter-populational genotypic as well as allelic frequency heterogeneity and higher genic differentiation at all the esterase-coding loci. All the polymorphic loci in geographical populations of Z. indianus revealed latitudinal clines, and changes in allelic frequencies were found to correlate with latitude. The Occurrence of higher genetic variability in Z . indianus populations was in agreement with its habitat-generalist or broad niche-width characteristics, i.e., the species populations utilized diverse food resources and displayed adaptation to variable climatic conditions. Thus, the observed genic divergence patterns in colonizing populations of Z . indianus could be maintained by balancing natural selection varying spatially along the north-south axis of the Indian sub-continent. Ravi Parkash, 508-Rl20 (Near Park), D.L.F.Colony, Rohtak-124001, India
Evolutionary genetic studies of natural populations of diverse taxa attempt to understand how organisms are adapted to their respective environments (WILLS 1981). The nature and extent of genetic variability uncovered through gel electrophoretic techniques have revealed that: (a) most species populations are highly polymorphic; (b) individual gene loci may show different patterns of spatial allelic differentiation, ranging from constant genetic composition over space to very sharp clinal variation patterns; and (c) spatial genetic variations in certain cases have shown statistical correlation with patterns of environmental variation (SPIESS1989). Recently, the levels of genetic diversity have been compared in continental populations of colonizing sibling species pair of D . melanogaster and D. simulans and such studies revealed extensive clinal as well as geographical genetic divergence among D. melanogaster populations as compared to genetic uniformity among D . simulans populations (ANDERSON1981; DAVID 1982; TRIANTAPHYLLIDIS et al. 1982; SINGH et al. 1982; ANDERSONand OAKESHOTT1984; CHARLES-PALABOST et al. 1985; WATADAet al. 1986; SINGH and RHOMBERG1987). Thus, electrophoretic analysis of genetic structure of some colonizing species had helped in elucidating the genetic potential for colonizing as well as in under-
standing bio-geographical origin of such species (ENDLER1986). However, such studies have not been attempted on the colonizing drosophilids of the Indian sub-continent. Zaprionus indianus constitutes one of the most successful colonizing species of the Indian sub-continent. Twenty species of Zaprionus were found to be endemic to Africa (SCIANDRA et al. 1973; PASTEUR 1978; BENNET-CLARK et al. 1980; TSACASet al. 1981). It had been argued that the genus Zaprionus evolved from close to the immigrans species group radiation and that various Zaprionus species might have originated in the Afrotropical continent and later on colonized other tropical continents such as India (THROCKMORTON 1975). There is little information on the occurrence of various Zaprionus species in the Indian sub-continent, i.e., so far only four species have been described and only Z. indianus was found to be abundantly available species. The population genetic studies on Afrotropical and Indian colonizing populations of Zaprionus species are totally lacking. Since gel electrophoresis has helped in elucidating the genetic structure of geographical populations of diverse taxa, the present studies were made to analyze the extent of genic divergence at esterase loci in colonizing populations of Z . indianus from the Indian sub-continent.
162
R. PARKASH AND J.
P. YADAV
Hereditas I I9 (1993)
Fig. 1. Map of the Indian sub-continent showing the collection sites of Zuprionus indiunus populations. Populations include: 1 . Ernakulam, 2. Bangalore, 3. Tirumala, 4. Hyderabad, 5. Nagpur, 6. Bhopal, 7. Jaipur, 8. Rohtak, 9. Roorkee, 10. Dehradun, 11. Chandigarh, 12. Jammu.
Material and methods Zaprionus indianus represents a genus related to Drosophila and occurs widely in the Afrotropical regions as well as Indian sub-continent. Z . indianus was described from India and could be collected almost throughout the Indian sub-continent (GUPTA1970). The population samples of Z. indianus were bait-trapped from twelve latitudinally varying sites (Table 1, Fig. 1). Wild-caught males as well as F, individuals from isofemale lines were analysed electrophoretically (SMITH1976). The homogenates of single individuals were analysed electrophoretically in 12 % starch gels at 250 V, 30 mA at 4°C for four hours using tris citrate/Sod. borate continuous buffer system, pH 8.65. The gel slices were stained for esterase gene-enzyme using phosphate buffer pH 6.5 (HARRIS and HOPKINSON 1976). Esterases were analysed on the basis of
substrates (a and 8-naphthyl acetate and acetylthiocholine iodide), inhibitors (acetazolamide, eserine sulphate, di-isopropyl fluorophosphate and neostigmine bromide). Thermoresistant (Tr) and Table 1. Data on the collection of Zaprionus indianur populations from latitudinally varying sites of the Indian subcontinent
Sites
Latitude
Longitude
Collection month and year
Ernakulam Bangalore Tirumala Hyderabad Nagpur Bhopal Jaipur Rohtak Roorkee Lkhradun Chandigarh Jammu
1 O"N 12.58"N 13.40"N 17.20"N 21.09"N 23.16"N 26.55"N 28.94"N 29.52"N 30.19"N 30.43-N 32.74"N
76.1 5"E 77.38"E 79.20"E 78.30"E 79.09"E 77.36"E 75.52"E 76.38'E 77.53"E 76.38"E 76.54"E 75"E
Feb., 1990 May, 1989 Feb., 1990 Jan., 1990 Jan., 1990 Jan., 1990 Oct., 1989 Jan., 1989 Dec., 1989 Nov., 1989 a t . , 1989 Jan., 1989
LATITUDINAL VARIATION AT ESTERASE LOCI
Hereditas 119 (1993)
thermosensitive (ts) variants were examined by heat treating the enzyme in situ in starch gel slice at 55°C for 15 f 1 min while the other gel slice served as control. The genetic basis of banding patterns was interpreted from the segregation ratios of electrophoretic phenotypes of the parents as well as F, and F, progeny of several genetic crosses. The calculation of genetic indices such as allelic frequencies, observed and expected heterozygosities, contingency x 2 analysis, Wright’s fixation index (F,,), simple correlation coefficient (r), and regression coefficient (b) were followed from standard sources (WORKMAN and NISWANDER 1970; FERGUSON 1980; ZAR 1984). The log-likelihood x 2 (G-test) was used to assess whether the observed genotypes were in agreement with Hardy-Weinberg expectations.
lil lil 1 1 1 lilil I I fill1 l i l
lilll l i l lil L
rn
Results
II)
T‘
l
m m
t
I II 1 II I l II I II
I I I
I I II I
I I IIII I I II II I I I I Ill II I I I I I I I I I I I Ill I I I I II
rn
m
m m m
v)
v,
v,y,v,
u
163
‘ U ’
4
The analysis of esterase on the basis of thermostability, substrate, and inhibitors revealed that seven esterase zones included /3-esterases (EST- 1 and EST-2) and a-esterases (EST-3 to EST-7); thermoresistant (EST-1 to EST-4) and thermosensitive (EST-5 to EST-7); carboxyl esterases (EST-1 to EST-4) and cholinesterases (EST-5 to EST-7). Lack of inhibition of any esterase zone with acetazolamide confirmed that the banding patterns did not include carbonic anhydrase contamination (BERGMEYER 1974). The electrophoretic phenotypes of different esterase loci have been depicted in Fig. 2. Gel slices stained for esterases have revealed seven polymorphic zones of activity. The two cathodal zones (EST-I and EST-2) are represented by segregating single-band variants and triple-band patterns while the other five esterase zones have revealed occurrence of segregating single-band variants (fast or slow) and two-banded patterns (Fig. 2). The segregating patterns of esterase bands at different zones are independent of each other. Genetic crosses between individuals having triple-banded and single-band patterns at EST-2 produced about equal proportions of offspring ( 1:l) with electrophoretic phenotypes like the parents. The genetic crosses between individuals having triple-banded patterns at Est-2 resulted in 1:2:1 proportions of offspring with alternating single-band variants and tripleband patterns (Table 2). Likewise, genetic crosses between individuals having two-banded and/or sin-
Fig. 2. Schematic representation of electrophoretic phenotypes of esterases (EST, EC 3.1.1.1) in homogenates of single individuals of Z . indianus. Each polymorphic zone is controlled by a distinct autosomal locus. EST-I and -2 are dimeric and segregating single-band variants (fast, medium and slow) and various triple-banded patterns
represent homozygous and heterozygous genotypes. The occurrence of interzone hybrid bands between EST-1 and EST-2 has been shown by dotted bands. Arrow indicates the direction of current flow.
gle-banded esterase at various EST zones patterns have revealed agreement with monogenic Mendelian segregation ratios of 1:2:1 or 1:l. The singleband variants and two-banded (triple-banded) patterns represent homozygotes and heterozygotes respectively. The occurrence of two-banded heterozygotes (at EST-3 to EST-7) and triple-banded heterozygotes (at EST-1 and EST-2) has revealed that the former are monomeric esterases while the latter are dimeric. Between the two cathodal zones of esterase activity (EST-1 and EST-2), one or more low density esterase bands occur exactly midway between the mobility values of bands of EST-1 and EST-2 zones. These intermediate bands represent interlocus hybrid isozymes and might have resulted due to multimerisation of the sub-units of dimeric esterases (EST-1 and EST-2). However, this suggestion needs to be verified by empirical
164 R. PARKASH AND J. P.
Hereditas I19 (1993)
YADAV
Table 2. Testing the Mendelian segregation of esterase enzyme electrophoretic phenotypes in several genetic crosses of Zaprionus indianus ~
~
Zones
Parental phenotypes
Esterase phenotypes of progeny
FF EST-2
FFxFF
ss x ss FF x ss
FF x FS FS x FS FM x F F FM x SS MS x FF MS x MS FM x FM
EST-1 EST-3 EST-4 EST-5
EST4 EST-1
xzp
25 30 40
-
-
-
-
42
1:1
0.09
1:1:2 1:l 1:l
0.48
MM
SS
FM
MS
FS
-
-
-
-
30
-
-
-
20 25 42
-
-
-
-
40 22 57
112 80
38 44 56 72
25
-
30
-
-
-
38
-
-
20
18
-
-
-
21
-
23
-
13
15
28
-
-
-
-
19
FSxFF FSxFF F S X FS FX x SS FS x SS FF x FS FFxFS FS x FS FFxFS
* Non-significant at 5 %
Test ratio
Total
14
37
-
FF
ss
FS
18
-
22 23 27 20 26 28
27 11 -
24 20 26 32
14 -
22 -
30 -
18
60 30
40 50 52 20
48 52 38 116 62
-
1:1
l:l:2 1:1:2
I:1 I:I
l:1:2
0.20 0.10 0.09 0.14 0.31
0.40 0.32 0.42
-
-
1:l 1:l 1:l 1:1:2 1:l
0.33 0.31 0.10 0.41
0.06
level
data involving dissociation-reassociation analysis of EST-1 and EST-2 isozymes. The data on the distribution of genotypes and allelic frequencies of esterase polymorphic loci in twelve natural populations of Z. indiunus is given in Tables 3-4. All seven polymorphic Est loci revealed significant variation in allelic frequency among geographical populations. The clinal variation was observed at all the polymorphic loci in Indian geographic populations of Z. indiunus. The population genetic structure of Z. indiunus was analysed in terms of distribution of genotypes as well as allelic frequencies at seven polymorphic loci. Contingency chi-square analysis is given in Tables 3-4. The populations revealed significant allelic heterogeneity at six loci (Est-1, Est-2, Est-3, Est-5, Est-6, Est-7). Data on observed and expected heterozygosity at polymorphic loci in twelve natural populations of Z. indiunus are given in Table 5. The heterozygosity levels revealed significant differences at most of the Est loci among different geographical populations (Table 5). Thus, the genetic structures of geographical populations at Est loci of 2. indiunus were found to be consistently heterogeneous. Est-2 locus revealed significant interpopulation genotypic heterogeneity as well as significant deviation from Hardy-Weinberg equilibrium in most of the populations (Table 5).
The data on the amount of genetic differentiation at seven polymorphic loci in twelve populations of Z. indiunus were calculated in terms of Wright's fixation index (F,,), and the heterozygosity at the polymorphic esterase loci was partitioned into within-population as well as between-population components (Table 6). Est-5 locus revealed significantly higher genetic differentiation while Est-I and Est- 7 revealed moderate genic differentiation; all other Est loci revealed lower amount of genetic differentiation. In order to find relationship between changes in gene frequencies with latitude and longitude, correlation coefficient (r) and regression coefficient (6) were calculated and are given in Table 6. The frequencies of E s t - l F , Est2', E ~ t - 3E~ ~, t - 4Est-SS, ~, Est-ds, Est- 7s showed positive correlation with the latitude (Table 6, Fig. 3). Thus, significant clinal variation patterns on the basis of latitudinal correlations were observed at all the Est loci except Est-2 locus.
Discussion Evolution of a species population is intimately related to the nature and amount of genetic variability occurring in it (WILLS 1981; PARKASH 1987). Electrophoretic analysis of esterases in Z .
57
FF
51
FS
386
-
FF
ss
FS
ss
25 8 24
-
FF
FS
ss
FS
-
21 8 22
FF
ss
FS
ss
28 0 16
FF
451
56 0 4
29 6 29
10
54 0
30 6 30
34 3 19
6
-
-
-
-
-
0 21
6 32
27
421
-
-
60
21 8 25
36 0 6
30 6 24
41 2 29
-
6
-
-
-
30 4 3
17
41 5
Tirumala
-
30 0 12
32 2 21
Bangalore
-
-
9
* Significant at 5 YO level
Total
ESI-7
Est-6
Esr-5
Est-4
Est-3
SS'
MS MS'
FS'
FF FM FM FS
ss
FS
-
21
FF MM
Est-2
30 6 21
FF
Est-l
ss
Emdkulam
Genotypes
Locus
492
64 0 6
26 12 31
54 3 12
32 9 35
30 4 26
-
-
0
-
2 32
-
-
34 2 6
41 3 28
Hyderabad
523
10
55 0
20 14 31
40 5 20
32 9 31
46 4 20
-
0
-
9 30
-
414
41 0 10
16 13 28
33 5 19
21 6 24
32 5 20
-
-
-
-
21
-
6
-
-
13
24
0
44 4 24
Bhopal
436
12
1
41
15 15 30
26 8 26
26 5 19
25 5 20
-
0
-
3 31
-
25 0 13
60 4 20
JaiPur
493
17
1
50
16 19 33
40
20 8
29 4 21
10
616
65 3 20
20 27 41
42
11
29
51 7 30
38
20 4 30
21 2 19 5 2 6 26 4 3 0 0
12
1
75
Roorkee
40
26 0 20 2 2 4 53 0 2 4 0
55 1 12
Rohtak
602
62 5 19
18 28 40
32 15 39
53 5 28
41 10 35
-
4
-
21 0 19 0 6 4 26
I5 0 12
Dehradun
560
68 4 I8
16 29 35
26 11 31
41 6 21
31 13 36
20 0 15 0 5 9 21 0 5 0 5
13
0
61
Chandigarh
581
56 5 22
14 31 38
25 19 39
50 5 28
31 14 38
5 30 0 9 6 0
-
15 6 12
75 0 8
Jammu
5981
611 19 138
242 210 385
432 97 290
434 16 319
405 14 321
5
10
15 48 356 4 35
7
311 14 141
648 34 222
Total
9.06
10.38
2.84
10.46
3.43
9.95
223.14*
x2
10
12
II
12
12
59
12
df
x 2 analysis of phenotypic (or genotypic) frequencies in twelve Indian natural populations of Z. indiunus at esterase
38
54 8 34
NagPur
Tublr 3. Data on distribution of genotypes/phenotypes and contingency loci b
....
0.82 0.18
0.67 0.33
1.0
-
0.65 0.35
F F M S S'
F S
F S
F S
F S
F S
Est-2
Esf-3
Est-4
Est -5
Est-6
Est - 7
-
1.0
0.97 0.03
-
-
1.0
0.66 0.34
0.93 0.07
0.70 0.30
0.79 0.21
-
0.96 0.04
0.60 0.40
0.87 0.13
0.65 0.35
0.72 0.28
0.92 0.08
0.55 0.45
0.77 0.23
0.66 0.34
0.80 0.20
-
0.64 0.05 0.31
-
0.74 0.26
NagPur
0.91 0.09
0.53 0.47
0.75 0.25
0.68 0.32
0.74 0.26
~
0.34
-
0.66
-
0.78 0.22
Bhopal
0.88 0.12
0.50 0.50
0.65 0.35
0.71 0.29
0.70 0.30
-
0.58 0.02 0.40
-
0.83 0.17
Jaipur
0.86 0.14
0.48 0.52
0.59 0.41
0.73 0.27
0.65 0.35
0.02 0.48 0.06 0.42 0.02
0.10
0.90
Rohtak
0.85 0.15
0.46 0.54
0.57 0.43
0.75 0.25
0.67 0.33
0.04 0.47 0.09 0.38 0.02
0.92 0.08
Roorkee
0.56 0.44 0.42 0.58
0.60 0.40
0.44 0.56
~
0.84 0.16
0.76 0.24
0.78 0.22
0.83 0.17
0.61 0.39
0.92 0.08 0.03 0.44 0.12 0.38 0.03
Chandigarh
0.68 0.32
-
0.03 0.49 0.05 0.43
0.93 0.07
Dehradun
*Weighted by population sample size ** Significant at 5 % level df (degrees of freedom) = (k l)(r - l), where k is the number of alleles and r is the number of populations
-
0.68 0.32
0.92 0.08
0.68 0.32
0.78 0.22
-
-
0.39
-
0.67 0.04 0.29
-
-
0.63 0.1 1 0.26
0.76 0.24
Hyderabad
0.79 0.21
Tirumala
0.77 0.23
~
Bangalore
0.57 0.07 0.36
0.61
~
0.71 0.29
F S
Est - I
Ernakulam
Alleles
Locus
0.716 0.284
0.77 0.23
0.81 0.19
0.40 0.60
0.895 0.105
0.520 0.480
0.711 0.289
0.706 0.294
0.60 0.40
0.54 0.46
0.011 0.543 0.071 0.364 0.010
0.843 0.157
Mean* (P)
0.39 0.19 0.38 0.04
-
0.95 0.05
Jammu
191.61**
0.02108 0.02426
0.00396 0.00409
72.35**
50.28**
19.21
0.00254 0.00177
0.00626 0.00864
39.84**
177.02"
90.33**
x2
0.00503 0.00602
0.00027 0.0 0823 0.00281 0.00116 0.00021
0.00679 0.00684
Variance* (O*P)
11
11
11
11
44
11
df
Table 4. Data on the distribution of gene frequencies and contingency chi square analysis of gene frequencies among twelve Indian natural populations of Z. indiunus at polymorphic esterase loci ?
LATITUDINAL VARIATION AT ESTERASE LOCI
Hereditas 119 (1993)
167
Table 5. Data on the distribution of observed and expected heterozygosities and G-values for log-likelihood x z test for fit to Hardy-Weinberg expectations at seven polymorphic esterase loci in twelve Indian natural populations of 2.indianus
Locus Genetic indices
Erna- Banga- Timkularn lore mala
Hydera- Nagpur Bhopal Jaipur Rohtak bad
Roorkee
Dehradun
Chandi- Jarnrnu garh
0.14 0.15 0.37
0.14 0.13 0.90
0.16 0.15 1.15
0.10
0.52 0.47 0.62 0.57 21.87* 41.87'
0.56 0.65 36.89.
0.60 0.67 30.02*
0.45 0.48 0.22
0.46 0.48 0.17
Het. (obs.) 0.37 Het. (exp.) 0.41 G-values 0.63
0.38 0.35 0.45
0.27 0.33 2.28
0.39 0.36 0.47
0.35 0.38 0.61
0.33 0.34 0.11
0.24 0.28 1.53
0.18 0.14
Est-2 Het. fobs.) 0.47
0.51 0.54 2.07
0.42 0.52 26.96*
0.45 0.47 12.55'
0.43 0.49 10.48*
0.47 0.45 0.16
0.47 0.50 3.60
0.59 0.59 37.26.
0.34 0.34 0.03
0.37 0.33 1.13
0.43 0.40 0.30
0.29 0.32 0.75
0.35 0.38 0.53
0.40 0.42 0.11
0.55 0.46 2.69
0.07
0.41 0.44 0.36
0.45 0.44 0.15
0.40 0.42 0.13
0.46 0.46 0.02
0.43 0.45 0.14
0.42 0.44 0.05
0.38 0.41 0.29
0.39 0.40 0.01
0.34 0.37 0.70
0.33 0.34 0.25
0.34 0.36 0.56
0.34 0.35 0.61
0.16 0.15 0.85
0.14 0.13 0.47
0.17 0.23 2.95
0.31 0.35 1.09
0.33 0.37 0.84
0.43 0.45 0.13
0.59 0.48 3.18
0.48 0.49 0.07
0.45 0.48 0.27
0.46 0.49 0.33
0.47 0.50 0.28
0.45 0.44 0.13
0.42 0.45 0.33
0.45 0.48 0.27
0.48 0.49 0.10
0.49 0.50 0.02
0.50 0.50 0
0.48 0.50 0.05
0.47 0.50 0.34
0.47 0.49 0.28
0.44 0.49 0.82
0.46 0.48 0.17
0.07 0.06 0.19
-
0.08 0.08 0.29
0.15
0.15 0.86
0.18 0.16 0.97
0.20 0.21 0.08
0.25 0.24 0.13
0.23 0.25 0.76
0.22 0.28 3.33
0.23 0.27 2.09
0.27 0.31 1.68
Est-I
Het. (exp.) 0.48 G-values 0.02
Est-3 Het. (obs.) 0.36 Het. (exp.) 0.30 G-values 3.59
Est-4 Het. (obs.) 0.39 Het. (exp.) 0.44 G-values 0.97
Esf-5 Het. (obs.)
-
Het. (exp.) G-values -
Est-6 Het. (obs.) 0.42 Het. (exp.) 0.45 G-values 0.33
Esf-7 Het. (obs.) Het. (exp.) G-values
-
0.18
0.43
0.44
0.10 0.42
* Significant at 5 % level Table 6. Data on the extent of genetic differentiation at Esr loci on the basis of Wright's fixation index (FST) and the degree of correlation ( r ) and regression (b) of Est allelic frequencies with latitude as well as longitude in twelve Indian geographical populations of Z . indianus
Locus
Est-l Esf-2 ESI-3 Esr-4 Esf-5 Est-6 Esr-7
F-statistics values
Allele
Total heterozygosity (HT)
Subpopulation heterozygosity (H,)
0.278 0.559 0.409 0.410 0.395 0.487 0.176
0.264 0.545 0.399 0.407 0.344 0.481 0.168
* Significant at 5 %
Fixation index
Correlation ( r ) values
Regression (b) values
Latitude
Longitude
Latitude
+0.89* +0.55 +0.89*
-0.53 -0.78. -0.58. -0.58. -0.45 -0.53 -0.59.
0.009. 0.003 0.008* 0.005* 0.021' 0.012* 0.008*
FST)
0.050 0.025 0.024 0.007 0.129 0.012
0.045
Est-IF E~t-2~ Est-3' E~t-4~ E~t-9 Est-@ Esf-7s
+0.81*
+0.99* +0.98* +0.98*
level
indianus has revealed that natural populations are heterogeneous mixtures of largely heterozygous individuals at Est loci. Since esterases are known to regulate a variety of tissue functions (such as reproduction, juvenile hormone metabolism and insecticide degradation etc.), the observed esterase heterogeneity may increase the species flexibility and adaptability to possible changes in the environment (ZERAet al. 1985). The observed higher level of esterase polymorphism in 2. indianus parallels significant levels of esterase variation at Est-5
locus in D. pseudoobscura and Est-6 locus in D. melanogaster and D. simulans (DE ALBUQUERQUE and NAPP 1981; KEITH 1983; ANDERSONand OAKESHOTT 1984). The twelve populations of Z. indianus, sampled along the 22" latitudinal range along the northsouth axis of the Indian sub-continent, differ in their ecogeographical conditions such as extent of precipitation, day length, temperature, and humidity etc. Various geographical populations do experience gene flow and are adapted to local
168
R. PARKASH AND I. P. YADAV
Hereditas 119 (1993)
Fig. 3. Patterns of changes in allelic frequencies at seven polymorphic esterase loci in twelve Indian natural populations of Zuprionus indiunus from latitudinally varying localities along the North-South transect of the Indian sub-continent.
ecogeographical factors. The southern populations 1975; NEWKIRK and DOYLE1979; SINGHand have revealed significant allelic frequency differ- RHOMBERG 1987). Since various Indian populaences at all the seven Est loci as compared to the tions of 2. indianus can potentially intermix and northern populations. The observed genic diver- were sampled from continuously connected regence at seven Est loci might be due to the geo- gions, Z . indiunus populations might also be exgraphical environmental gradient along the pected to reveal transient dinal variation. On the north-south axis of this country. The patterns of basis of present observations, it would be fair to changes in allelic frequencies, heterozygosity, argue that the clines may be transient and could be Wright’s fixation index (FsT values), and the steep- the result of historical events (founder effect, drift, ness of latitudinal clines were found to differ for all selection in the past, etc.). At least some of the the seven polymorphic Est loci. Since gene flow is esterase system could as well be influenced by expected to influence allelic frequency changes in selection at other loci and the clines could, therean identical manner at all the esterase polymorphic fore, be also explained by hitch-hiking. loci, the observed patterns of geographical differenThe occurrence of equilibrium clines results from tiation in Z . indianus may not be explained solely the action of natural selection that causes clinal on the basis of gene flow. Furthermore, the gene variation in gene frequencies along a continuously flow between formerly disjunct populations could varying environmental gradient (ENDLER1986). result in transient clinal variation (NAGYLAKIThe steepness of such clinal variation depends
LATITUDINAL VARIATION AT ESTERASE LOCI
Hereditas 119 (1993)
upon the range of environmental gradient. The observed latitudinal clines and gene frequency changes at all the Est loci except Est-2 in Indian populations of Z. indianus revealed statistically significant correlations with latitude. Thus, it may be argued that observed geographical variation at Est allozymic loci could represent equilibrium or adaptive gene clines under the dictates of spatially varying natural selective pressures. The extent of genic polymorphism as well as clinal variation at polymorphic loci in Z . indianus populations were found to be comparable to the genic variation patterns occurring in geographical populations of D. melanogaster. The patterns of genic variability in Z. indianus parallels latitudinal clines at polymorphic loci in allopatric populations of D . melanogaster, i.e., diverse continental populations (SINGHet al. 1982; SINGHand RHOMBERG 1987), et al. 198I), Australian populations (OAKESHOTT Afrotropical populations (DAVID1982), Japanese populations (WATADAet al. 1986), and Chinese populations (JIANGet al. 1989). Since various colonizing drosophilids differ significantly in their evolutionary history, the existence of parallel clinal allelic frequency changes at many polymorphic loci could be due to the action of latitudinally related environmental gradient. The observed data could be explained on the basis of a niche-width variation hypothesis. According to this hypothesis, the amount of variation in a species is proportional to the niche-width of the species (ENDLER1986). It had been argued that a species inhabiting a wide range of food resource or environmental gradient should possess a significantly higher amount of genic variation as compared to a narrow-niche species (SPIESS 1989). Thus, in a broad niche cosmopolitan species such as D. melanogaster, the reported levels of significant geographical differentiation among global populations of D. melanogaster might have resulted due to their varying capacity for macroclimatic adaptations (SINGHand RHOMBERG 1987). The observed genetic divergence among geographical populations of Z. indianus is in agreement with the habitat generalist characteristic of this species. The extent of genic polymorphism as well as clinal variation at polymorphic esterase loci in Z. indianus populations were found to be comparable to the genic divergence variation patterns occurring in global populations of D. melanogaster (OAKESHOTT et al. 1981). Both these colonizing species are characterized by adaptive flexibility to spatial range of climatic conditions throughout the Indian sub-
169
continent. Thus, the allozymic divergence in Z. indianus populations might constitute a genetic strategy of this colonizing species in terms of its broader niche-width. Acknowledgements. - Financial assistance from CSIR, New Delhi is gratefully acknowledged. We are grateful to the reviewers for their helpful comments on the manuscript.
References ANDERSON, P. R. 1981. Geographic cline and climatic associations of Adh & a-Gpdh gene frequencies in Drosophila melanogaster. - In: Genetic Studies of Drosophila Populations (eds J. B. GIBSONand J. G. OAKESHOTT),Australian National University, Canberra, p. 237-250 ANDERSON,P. R. and OAKESHOTT, J. G. 1984. Parallel geographical patterns of allozymic variation in two sibling Drosophila species. -Nature 308: 729-731 BENNET-CLARK, H. C., LEROY,Y.and TSACAS,L. 1980. Species and sex-specific songs and courtship behaviour in the genus Zaprionus (Diptera: Drosophilidae). - Anim. Behav. 28: 230235 BERGMEYER, H. V. 1974. Methods of Enzymic Analysis, Vol. 11. Academic Press, New York CHARLES-PALABOST, L., LEHMANN, M. and MEROOT,H. 1985. Allozyme variation in fourteen natural populations of Drosophila melanogaster collected from different regions of France. -Genet. Sel. Evol. 17: 201-210 DAVID, J. R. 1982. Latitudinal variability of Drosophila melanogaster: Allozyme frequencies divergence between European and Afrotropical populations. - Biochem. Genet. 20: 747-761 DEALBUQUERQUE, C. R. and NAPP,M. 1981. Genetic variability at the esterase-6 locus in natural populations of Drosophila simulans in relation to environmental heterogeneity. - Genetics 98 399-407 ENDLER,J. A. 1986. Natural Selection in the Wild. - Princeton Univ. Press, Princeton, N.J. FERGUSON, A. 1980. Biochemical Systematics and Evolution. Wiley, New York GUPTA,J. P. 1970. Description of a new species of Phorticella Zaprionus (Drosophilidae) from India. Ind. Natl. Sci. Acad. 3 6 62-70 HARRIS,H. and HOPKINSON, D. A. 1976. Handbook of Enzyme Electrophoresis in Human Genetics. - North-Holland, Amsterdam JIANG,C., GIBSON,J. B. and CHEN,H. 1989. Genetic differentiation in populations of Drosophila melanogaster from the People’s Republic of China: Comparison with patterns on other continents. - Heredity 62 193-198 KEITH,T. P. 1983. Frequency distribution of esterase-5 alleles in two populations of Drosophila pseudoobscura. - Genetics 105 135- 136 T. 1975. Conditions for the existence of clines. NAGYLAKI, Genetics 80 595-615 NEWKIRK, G. F. and DOYLE,R. W. 1979. CIinal variation at an esterase locus in Littorina saxatilis and L . obtusata. - Can. J . Genet. Cytol. 21: 505-513 OAKESHOTT,J. G., CHAMBERS, G. K., GIBSON,J. B. and WILLCOCKS, D. A. 1981. Latitudinal relationships of esterase-6 and phosphoglucomutase gene frequencies in Drosophila melanogaster. -Heredity 47: 385-396 PARKASH,R. 1987. Genetic polymorphism in natural populations. - Ind. Rev. Life Sci. 7: 141-164 PASTEUR,G. 1978. Affinities of Zaprionus and chromosomal evolution. - Drosophila Inf. S e n . 53 121 ~
~
170
R. PARKASH AND I. P. YADAV
SCIANDRA,R. J., ABDEL-HAMEED, F. and BENNETT,J. 1973. Chromosome complement of Zaprionus multisrriarus.- J. Hered. 64: 31-34 SINGH,R. S. and RHOMBERG,L. R. 1987. A comprehensive study of genic variation in natural populations of Drosophila melanogasrer. 11. Estimates of heterozygosity and patterns of geographic differentiation. - Genetics I1 7: 255-271
SINGH,R. S., HICKEY,D. A. and DAVID,J. 1982. Genetic differentiation between geographically distant populations of Drosophila melanogaster. - Genetics 101: 235-256 SMITH, 1. 1976. Chromatographic and Electrophoretic Techniques, Vol. 11. Zone Electrophoresis. - Heineman, London SPIESS, E. B. 1989. Genes in Populations. -John Wiley and Sons, New York THROCKMORTON, L. H. 1975. The phylogeny, ecology and geography of Drosophila. - In: Handbook of Generics (ed R. C. KING),Plenum Press, New York, p. 421 -469 TRIANTAPHYLLIDIS, C. D., SCOURAS, Z. G., PANOURGIAS, J. N. and IOANNIDIS, G. C. 1982. Allozyme variation in Greek wild
Hereditas 119 (1993)
populations of Drosophila melanogaster and D. simulans along a North-South gradient. - Generica 58: 129-136 TSACAS,L., LACHAISE, D. and DAVID,J. R. 1981. Composition and biogeography of the Afrotropical Drosophilid fauna. In: The Genetics & Biology of Drosophila (eds M . ASHBURNER, H. L. CARSONand J. N. THOMPSON JR.), Academic Press, New York, p . 1-97 WATADA,M., TOBARI,Y. N. and OHBA, S. 1986. Genetic differentiation in Japanese populations of D. simulans and D. melanogaster. 1. Allozyme polymorphisms. - Jpn. J . Genet. 61: 253-269
WILLS,C. 1981. Genetic Variability. - Clarendon Press, Oxford WORKMAN,P. L. and NISWANDER, J. D. 1970. Populations studies on South-Westem Indian Tribes. 11. Local genetic differentiation in the papago. -Am. J. Hum. Genet. 2 2 24-29 ZAR, J. H. 1984. Biostatistical Analysis (2nd ed.). - PrenticeHall, Englewood Cliys, N.J. ZERA,A. J., KOEHN,R. K. and HALL,J. G. 1985. Allozymes and biochemical adaptation. - Compr. Insect. Physiol. Biochem. Pharmacol. 1 0 633-674
