Epistatic interaction between unlinked inversions in Indian natural populations of Drosophila melanogaster

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Epistatic interaction between unlinked inversions in

Indian natural populations of Drosophila melanogaster

Bn Singh, A Das

To cite this version:

Original

article

Epistatic

interaction

between unlinked inversions

in Indian natural

_populations

of

_{Drosophila melanogaster}

BN

_Singh

A Das

Centre

of Advanced Study

in

_Zoology,

Banaras Hindu

_University,

Genetics

_Laboratory,

Varanasi-221 005, India

(Received

29 October

1990; accepted

14 June

₁₉₉₁₎

Summary - Fourteen Indian natural

_populations

₍₆

from the north and 8 from the

_south)

of

_{Drosophila rn,elanogaster}

were screened for chromosome inversions and 23 paracentric

inversions

_including

4 common

_cosmopolitan

_{(In(2L)t, In(2R)NS, In(3L)P}

and

_In(3R)P),

2 rare

_cosmopolitan

_(In(3R)Mo

and

_In(3R)C)

and a recurrent endemic

_(In(3L)IB)

found

to be common in distribution were detected.

_Comparison

of the observed and

_expected

numbers

_(via

the

_{Hardy-Weinberg}

_equilibrium)

of different

_{karyotypes produced by}

all these inversions

_(each

treated

_{independently)}

showed no

_significant

deviation from

expectation in any of the

_{populations analysed. During}

the _present

_{investigation}

data

on intra- and interchromosomal associations have been obtained to test chromosome interactions in Indian natural

_populations

of D

_{melanogaster.}

The results show that different associations between linked inversions of the second and third chromosomes

occur

_{randomly, providing}

no evidence for

_epistatic

interaction between linked inversions.

Furthermore,

the

majority

of

pairs

of unlinked inversions of

_major

autosomes also occur

in random combinations.

_{However, highly significant}

non-random associations were found

between

_In(2R)NS

and

_In(3R)C

in all the

_populations

from south India and between

In(2L)t

and

_In(3R)P

in 11 _populations out of 14

_analysed.

There is a

_significant

excess

of individuals which are either

_{doubly homozygous}

for ST

_(standard)

at both unlinked inversion loci or

_{doubly heterozygous, indicating}

_epistatic interactions between unlinked inversions in these

_populations.

Drosophila

melanosgaster

/ inversion polymorphism

/ epistatic interaction

/ Indian

populations

Résumé — Interaction _épistatique entre des inversions non liées dans des popula-tions naturelles de _{Drosophila melanogaster} de l’Inde.

_{Quatorze populations}

naturelles

*

de _Drosolhila

_melanogaster

de l’Inde

₍₆

du Nord el 8 du

_Sud)

ont été examinées _pour des inversions

_{chromosomiques. Vingt-trois}

inversions

_{paracentriques}

ont été

_détectées,

do7il, 4 communes et cosmopolites

(In(2L)t, ln(2R)NS,

In(3L)P

et

_In(3R)P),

2 rares et

cosrrtopolites

(Irt(3/Z)Mo

et

_In(3R)C),

et une inversiort

_endémique

récurrente

_(In(3I)IB)

communément dislribuée. La _comparaison des nombres attendus et observés

_(sur

la base de

l’équilibre

de

_{Ilardy-Weinbery)}

des

différents

caryotypes résultant de toutes ces inversions

(chacune

trailée

_{indépendamment)}

ne montre aucun écart

_significatif

dans aucune des

pop-ulalions

_analysées.

Dans cette

_élude,

des données sur des as.sociations entre chromosomes

et inlra-cltrorrtosome ont été obtenues pour tester les interactions

chromosomiques

dans les

ponulalions

naturelles de D

_melanogaster

de l’Inde. Les résultats montrent que

différentes

combinaisons entre des inversions liées des deuxième et troisième chromosomes appa-raissent d’une manière

_aléatoire,

ce

qui n’apporte

aucune _preuve d’interaction

épistatique

entre des inversions liées. De

_plus,

la

majorité

des

_couples

d’inversions non liées

impli-quant les autosomes importants sont aussi des combinaisons aléatoires.

Cependant,

des a.ssociations non aléatoires ltautemertt

_{significatives}

ont été trouvées entre

_In(2R)NS

et

I

TI

(

3

11 )C

dans toutes les

_populations

du Sud de l’Inde et entre

_In(2L)t

et

_In(3R)P

dans 11 des _1!,

_{populations artalysées.}

Il y a un excès

significatif

d’irtdividus doubles

homozygotes

pour ST

(slandard)

aux 2 locus d’inversion non liés ou doubles

_{hélérozygoles}

_pour les 2

in 2

rn.rsion.s, ce _qui

_indique

des interactions

_{épistatiques}

entre des inversions non liées dans ces

populations.

Drosophila melanogaster

/

polymorphisme d’inversion

_/

interaction épistatique

/

population de l’Inde

INTRODUCTION

Genes do not act

_{independently.}

Rather

they

tend to

_organize

themselves in functional _gene

_complexes

which confer an

_{adaptive advantage}

to the

_recipient

genotype

(Darlington

and

_llather,

_1949).

In

_general,

relative selective values can

properly

be

_assigned

to the

_genetic

_system

as a whole and thus evolution

_depends

upon the

fitting together

of a harmonious

_system

of _gene effects

(Wright, 1964).

Epistatic

selection and balanced

_polymorphism

constitute a

_major

feature of

evolution. The 1 locus-2 alleles

_system

has been

_extensively

used in

_population

genetic

work which established the modern

_{understanding}

of evolution. But it has been realised that

_assumption

of

_independent

genes is unrealistic since most

significant adaptation

involves interaction of many

polymorphic

loci.

Chromosomal

_{polymorphism mainly}

due to

_paracentric

_{inversions is very} com-mon in different

_species

of

_Drosophila

and constitutes an

_adaptive

trait

_(da

_Cunha,

1960;

Dobzhansky,

1970;

Parsons,

1973;

Sperlich

and

Pfriem,

1986).

It offers very

good

material to test

_epistatic

_{gene interaction.}

_Epistatic

interaction between linked

inversions is well documented in various

_species

of

_{Drosophila. However,}

less atten-tion has been

_paid

to the

_study

of interaction between unlinked inversions. Prakash

(1967)

demonstrated the existence of interchromosomal interactions on the basis

of non-random association between unlinked inversions in D robusta. In contrast to

_this,

no evidence for interchromosomal interaction has been found in D

Singh

and

_Singh,

₁₉₈₉₎

as various interchromosomal associations occur

_randomly

in these

_species.

Drosophila melanogaster,

a

_cosmopolitan

and domestic

_species,

_presents a

_high

degree

of inversion

_polymorphism

in its natural

populations

and

_populations

show

geographic

differentiation of inversion

polymorphism

(for

references see Lemeunier et

_al,

_1986).

Data on intra- and interchromosomal associations in natural

popula-tions have been

_{reported by}

numerous

_{investigators}

from several _parts of the world.

In certain

_populations

interactions between linked inversions as well as between

unlinked inversions is evident

_(Alahiotis

et

_al,

_1976;

_{Stalker, 1976; Choi,}

_1977;

Langley

et

_al,

_1977;

Inoue and

_Watanabe,

_1979;

_Yamaguchi

et

_{al, 1980;}

Knibb et

al,

1981;

Yamazaki et

_al,

_1984;

Aulard and

_Lemeunier,

_1985;

Afonso et

_al,

_1985).

However,

previous

study by

the _present authors of 6 Indian natural

_populations

indicates no evidence for intra- and interchromosomal interactions between

com-monly

occurring

chromosome inversions in D

_melanogaster

_(Das

and

_Singh,

_1990).

The

_present

_{paper reports} data on interchromosomal associations in Indian natu-ral

_populations

of D

_melanogaster

which

_provide

evidence for

_epistatic

interaction

between unlinked inversions.

MATERIALS AND METHODS

To

_study

inversion

_polymorphism

in Indian

_populations

of D

_{melanogaster,}

flies

were collected from 14 localities. The

_geographic

location of the collection

_sites,

state in which situated and the month of collection have been shown in

_figure

1. In all the

_places

flies were collected

by exposing

fermented banana

_traps

in

vegetable

and fruit stalls and also near human habitations. Each

naturally

inseminated female

was

kept individually

in a fresh food vial. The

F,

larvae were

_squashed

to detect chromosome inversions

_by

the lacto-acetic orcein method. The

_quantitative

data

are based on the identification of the

_karyotype

of

_only

one

_F

_l

larva from each

wild female. In total 23

_paracentric

inversions

_including

4 common

_cosmopolitan

(In(2L)t, In(2R)NS, In(3L)P

and

_In(3R)P),

2 rare

_cosmopolitan

_(In(3R)Mo

and

In(3R)C)

and a recurrent endemic

_(In(3L)IB)

found to be common in distribution

were detected. The

description

of inversions and their

frequencies

have been

reported

elsewhere

_(Das

and

_Singh,

_1991).

The

_frequency

of 4 inversions

_showing

non-random association is shown in table I.

_During

the _present

_study,

these data

have been

_analysed

to obtain the

_frequency

of various intra- and interchromosomal

associations in India natural

_populations

of D

_{melanogaster.}

To test whether there

is

_positive

correlation between different

_karyotypes

produced by

unlinked inversions in natural

_populations,

the correlation coefficient

_(r)

was calculated.

RESULTS

occur in all the

populations analysed

except

In(3L)P

in Patna and the

populations

in the south maintain these inversions at

_higher

_frequencies

than those in the north.

The

_In(3R)Mo

is

_present

in all the

_populations

but at low

_{frequency. Interestingly,}

In(3R)C

could be detected

_only

in

_populations

from the south. The recurrent endemic inversion

_In(3L)IB

occurs in all

_populations

_except

_Shillong

at substantial

frequency.

Comparison

of the observed and

expected

numbers

_(ie,

the

Hardy-Weinberg

equilibrium)

of different

_{karyotypes produced by}

all these 7

_inversions,

treating

each inversion as an

_{independent locus,}

showed no

_significant

deviation

from

_{Hardy-Weinberg equilibrium}

_{in any} of the

_{populations analysed}

_(data

not

shown).

To determine chromosome

_{interactions,}

all these inversions have been used. At each inversion

locus,

3

_{lcaryotypes -}

_{ST/ST, ST/In}

and

_In/In

are

_expected.

If all

the 3

_karyotypes

are ascertained at each

_locus,

9

_types

of

_karyotypic

combinations will be

_expected

between 2 inversion loci.

_However,

in some

_populations

_only

6

types

could be found due to the absence of inversion

_homozygote

_(In/In)

for

certain inversions. The

_expected

numbers of various association

_types

have been calculated from

_marginal

totals of R x C

_contingency

tables.

_{Any significant}

deviation from

_expectation

would indicate non-random association

_resulting

from interaction

_causing

differential

_viability

of different associations between inversions. Intrachromosomal associations

The observed and

_expected

numbers of various intrachromosomal associations

con-sidering

different

_pairs

of linked inversions

_{(In(2L)t-In(2R)NS, In(3L)P-In(3R)P,}

In(3L)P-In(3R)Mo, In(3L)P-In(3R)C, In(3L)IB-In(3L)P, In(3L)IB-In(3R)P,

In(3L)IB-In(3R)Mo, In(3L)IB-In(3R)C, In(3R)P-In(3R)C, In(3R)P-In(3R)Mo

There is a

_good

_agreement

between observation and

_expectation

in all the

popula-tions for different

_pairs

of linked inversions which indicates that there is no evidence

for

_{linkage disequilibrium}

between these inversions.

Interchromosomal associations

To

study

interchromosomal

_{interactions,}

the observed and

expected

numbers of different

_genotypes

were calculated. In the

_majority

of _cases, for

exam-ple,

(In(2L)t-In(3L)P, In(2L)t-In(3L)IB, In(2L)t-In(3R)C, In(2L)t-In(3R)Mo,

In(2R)NS-In(3L)P, In(2R)NS-In(3L)IB, In(2R)NS-In(3R)P

and

In(2R)NS-In(3R)Mo),

the differences between observed and

_expected

numbers of various

inter-chromosomal combinations are

non-significant (data

not

_shown).

_However,

in the 2

comparisons,

ie

_In(2L)t

and

_{In(3R)P; In(2R)NS}

and

_{In(3R)C, (all}

the 4 inversions

showing significant

associations are located in autosomes

_{(figure 2),}

the differences

are

significant.

The observed and

expected

numbers of various interchromosomal

associations

_{involving In(2L)t}

and

_In(3R)P

are

_given

in table II. Due the absence of

_homozygotes

for

_In(2L)t,

_only

6

_karyotypic

combinations could be ascertained in

north Indian

_populations.

The differences between observed and

_expected

numbers

are

_significant

in most of the

_populations.

The

_karyotypes

in 2L and 3R are

asso-ciated

_{randomly only}

in 3

_populations

_(Shillong,

_Tirupati

and Fort

_Cochin).

The

values obtained

_by

the correlation coefficient

_analysis

also show a similar

_pattern

of statistical

_significance

for different

_karyotypic

associations

_{(table IV).}

The observed and

_expected

numbers of different interchromosomal associations

involving

In(2R)NS

and

_In(3R)C

are

_given

in table III. As

In(3R)C

occurs

only

in south Indian

_populations,

the

_study

is limited to

_only

8

_populations.

The

homozygotes

for

_In(3R)C

could not not be found in certain

_populations

and

as a result of this

_only

6

_karyoptypic

combinations could be ascertained in all the

_populations.

The deviation from randomness is

_highly

_significant

in all the

populations.

The individuals which are either

_{doubly homozygous}

for ST

_(standard)

or

_{doubly heterozygous}

are in

_significant

excess. On the other

hand,

there is a

deficiency

of those individuals which are

_homozygous

in one arm and

heterozygous

for inversion in the other arm. An identical

_pattern

has been found in all the

populations

and deviation from randomness is

_{highly significant.}

_{Statistically}

DISCUSSION

The results of the present

study

indicate that Indian

_populations

of D

_melanogaster

are

highly

polymorphic

for chromosome inversions and several inversions have

widespread geographical

distribution. When it was

_possible

to

_analyze

chromosome

interactions,

no evidence for non-random associations between linked inversions was

found in any of the

_populations

studied. Based on

this,

it is

suggested

that evidence

for

_epistatic

interaction between linked inversions is

_lacking

in Indian

populations

of D

_{melanogaster.}

Similar results were

_reported

earlier

_by

the

_present

authors

(Das

and

_Singh,

₁₉₉₀₎

who studied this

_phenomenon

in 6 natural

_populations

of D

melanogaster

from north India. Non-random associations

_{(linkage disequilibrium)}

between linked inversions

_resulting

from interaction have been found in certain

populations

from

_{Japan, Greece, Australasia, America, Korea,}

Tunisia and

_Congo

(Alahiotis

et

_{al, 1976; Choi,}

_1977;

_Langley

et

_{al, 1977;}

Inoue and

Watanabe,

1979;

Yamaguchi

et

_al,

_1980;

Knibb et

_{al, 1981;}

Aulard and

_Lemeunier,

₁₉₈₅₎

but not in

others

_(Mukai

et

_{al, 1974; Stalker,}

_1976;

Mukai and

_{Voelker, 1977;}

Voelker et

_al,

1977;

Paik and

_{Yang, 1983;}

Yamazaki et

_{al, 1984;}

Aulard and

Lemeunier,

1985).

It is believed that

_{linkage disequilibrium}

is most

_{easily produced}

under a 2-allele

system

and its occurrence becomes more difficult as the number of alleles

_present

in the

_populations

increases

_(Yamazaki

et

_al,

_1984).

_Also,

it is

_possible

that most

polymorphic

loci are of

_multiple

allele

_systems

(Singh

et

al,

1975).

Therefore,

it is

highly

likely

that the non-occurrence of

linkage

disequilibrium

between inversions

highly

developed

chromosome inversion

_system.

_However,

non-random associations of linked inversions occur in other

_species

of

_Drosophila

_(Levitan,

1958;

Levitan and

Salzano, 1959; Brncic,

1961;

Mather,

1963;

Stalker, 1964; Prakash,

1967;

Sperlich

and

_{Feuerbach-Mravlag,}

_1974;

_Singh,

_1983,

_1984;

_Shyamala

et

_al,

_1989).

In most cases it is maintained in the

populations by

natural selection

involving

epistatic

interaction _{between linked gene}

_{arrangements.}

_However,

in the absence of

_selection,

recombination over _years will lead to a random association

_causing

linkage equilibrium

between the 2

_physically

linked

_inversions,

if

_present

for a

long

time in a

population.

Linkage

disequilibrium

_may also occur due to

_suppression

of

crossing-over

(Sperlich

and

_{Feuerbach-Mravlag,}

₁₉₇₄₎

and

_genetic

drift

_(Singh

and

Singh,

1990a,

b).

In

_{Drosophila melanogaster}

all the 4

_major

autosomal arms are

highly

poly-morphic

for inversions and 4 common

_cosmopolitan

inversions are located in each

of them. Besides the 4 common

_cosmopolitan

_inversions,

2 rare

_cosmopolitan

in-versions in 3R and 1 recurrent endemic inversion in 3L are

_widespread

in Indian

natural

populations. Thus,

it offers a

_good

_opportunity

to test

_epistatic

interac-tion between unlinked inversions. In our earlier

study

(Das

and

Singh,

1990),

no

evidence for interaction between unlinked inversions in 6 natural

populations

of D

_melanogaster

was found as various interchromosomal associations occurred

ran-domly. During

the

_present

_study

it has been found that

_karyotypes

of different chromosomes in several

_comparisons

are associated

randomly

in 14 Indian natural

populations

of D

_{melanogaster. However, epistatic}

interaction between unlinked in-versions could be detected between

_IN(2R)NS

and

_IN(3R)C

in 8

_populations

from south Indian and between

_In(2L)t

and

_In(3R)P

in 11

_{populations coming}

from both north and south.

Thus,

our results from Indian

_{populations clearly}

show that

certain inversions on different chromosomes _may show

epistatic

interaction

(inter-chromosomal

_{interaction).}

_Furthermore,

the same inversions may show interaction

in some

_populations

but not in others.

Choi

₍₁₉₇₇₎

tested interchromosomal interaction in a Korean

_population

of

D

_melanogaster

but could not find

_significant

deviation from

_expectation

_{in any} of the combinations tested.

_However,

he detected an excess of double

_{heterozygotes}

in

all cases.

_Inoue

and Watanabe

₍₁₉₇₉₎

also found no evidence for interchromosomal

interaction in

_Japanese

_populations

of D

_melanogaster

as various

_lcaryotypes

on

different chromosomes were associated

randomly.

Knibb et al

(1981)

studied 50

individual

_comparisons

of associations between

_pairs

of unlinked inversions in 19 Australasia

_samples

and detected

_only

2

_significant

assocations

_{(In(2L)t—In(3L)P}

and

_{In(2L)t-In(3R)P)}

in the 2

_{populations. Interestingly,}

_they

found that the northern

_populations

were characterized

by

a consistent

deficiency

of

_gametes

with

inversions in both autosomes whereas the

_populations

from the south had an excess

of

_gametes

_having

inversions in both autosomes.

_Thus,

our results are in

_agreement

with those of Knibb et

_al,

₍₁₉₈₁₎

that certain unlinked inversions may show

epistatic

interactions in certain

_populations

which may be considered

adaptive.

Yamazaki et al

₍₁₉₈₄₎

also obtained data on interchromosomal associations in

2

_{Japanese populations}

of D

_melanogaster

which do not indicate the existence of interchromosomal interaction. Aulard and Lemeunier

₍₁₉₈₅₎

analysed

3

_populations

of D

_melanogaster

from

_France,

Tunisia and

_Congo

and found

_significant

of different inversions

_combined)

in the French and

_Congolese

_populations

but not in the Tunisian

_{populations. However,}

when inversions where tested

_{independently,}

no

significant

deviation was detected in any of the

_populations

studied.

It is evident from the results obtained in D

_melanogaster

_populations

from different

_regions

of the world

_(including

Indian

_populations)

that various intra- and interchromosomal associations occur

_randomly

in the

_majority

of cases.

_However,

there are cases in which certain intra- and interchromosomal associations occur

non-randomly,

resulting

from selection

_involving

_epistatic

interaction.

_Thus,

certain

chromosomal associations may be

adaptive

in a

_given

set of environments. The

variation in the result in different

_populations

_may be due to the fact that

_genetic

factors _{may vary in} different

_populations

of the same

_species.

The intra- and interchromosomal interactions have been tested in various

_species

of

_Drosoplaila

and different situations exist when results from different

_species

are

compared.

In D

_robusta,

evidence for both intra- and interchromosomal

interac-tions have been

_presented

_(Levitan,

_{1958, 1961, 1973; Prakash,}

_1967).

In D sub-obscura intrachromosomal interaction is found but evidence for interchromosomal

interaction is

_lacking

_(Sperlich

and

_{Feuerbach-Mravlag, 1974).}

D ananassae is also

characterised

_by

_linkage

_{disequilibrium}

between

independent

inversions

_resulting

from

_epistatic

interaction as well as

_suppression

of

_{crossing-over}

but

interchromo-somal interaction could not be found

_(Singh,

_{1982, 1983, 1984;}

_Singh

and

_Singh,

1989,

1990a,b).

On the other

_hand,

in most of the _cases, evidence for intra- and interchromosomal interactions is

_lacking

in natural

populations

of D

_{melanogaster.}

However,

in certain

_{populations adaptive}

interactions could be detected between certain

_pairs

of linked as well as unlinked inversions.

Thus,

the

_genetic

structure of different

_species

_may be different and different

_species

may achieve success

_by

different modes of

_adjustment

within their _gene

_pools.

ACKNOWLEDGMENTS

The financial support from the Centre of Advanced

_Study

in

_Zoology,

Banaras Hindu

University

in the form of a Senior Research

_Fellowship

to A Das is

_thankfully

acknow-ledged.

We thank the anonymous reviewers for their comments on the

_original

draft of the

manuscript.

REFERENCES

Afonso

_JM,

Hernandez

_M,

Padron

_G,

Gonzalez AM

₍₁₉₈₅₎

Gametic non-random

as-sociations in North-West African

_populations

of

_{Drosophila melanogaster.}

Genetica

67,

3-11

Alahiotis

_S,

Pelecanos

M, Zacharopoulou

A

₍₁₉₇₆₎

A contribution to the

_study

of

linkage

disequilibrium

in

_{Drosophila melanogaster.}

Can J Genet

_Cytol

_18,

739-745

Aulard

S,

Lemeunier F

₍₁₉₈₅₎

Distribution et association des inversions

chromo-somiques

dans trois

_populations

naturelles de

_Drosophila

_melanogaster

de

_France,

Tunisie et

_Congo.

Genet Sel Evol

_17,

311-330

Brncic D

₍₁₉₆₁₎

Non-random association of inversions in

_Drosophila

_pavani.

Choi 1’

₍₁₉₇₇₎

Chromosomal

_polymorphism

in a Korean natural

_population

of

D-rosoplcila melanogaster.

Genetica

47,

155-160

Da Cunha AB

₍₁₉₆₀₎

Chromosomal variations and

_adaptation

in insects. Annu Rev Entomol

5,

85-110

Darlington CD,

Mather K

₍₁₉₄₉₎

The Elements

_of

Genetics. Allen and

Unwin,

London

Das

_{A, Singh}

BN

₍₁₉₉₀₎

The lack of evidence for intra- and interchromosomal interactions in Indian natural

populations

of

_{Drosophila melanogaster.}

Korean J

Genet

12,

95-103

Das

_A,

_Singh

BN

₍₁₉₉₁₎

Genetic differentiaton and inversion clines in Indian natural

populations

of

_Drosophila

melanogaster.

Genome

_34,

618-625

Dobrhanshy

T

₍₁₉₇₀₎

Genetics

of

the

_Evolutionary

Process. Columbia

_University

Press,

New York ,

Inoue

_Y,

Watanabe TK

₍₁₉₇₉₎

Inversion

_polymorphism

in

_Japanese

natural

popu-lations of

_{Drosoplaila melanogaster. Jpn}

J Genet

54,

69-82

Knibb

_vVR,

Oalceshott

JG,

Gibson JB

₍₁₉₈₁₎

Chromosome inversion

polymor-phisms

in

_{Drosophila melanogaster.}

I. Latitudinal clines and associations between

inversions in Australasian

_populations.

Genetics

98, 833-847

Langley

CH,

Ito

_K,

Voelker RA

₍₁₉₇₇₎

Linkage disequilibrium

in natural

popula-tions of

_{Drosoplcila melanogaster.}

Seasonal variation. Genetics

_86,

447-454

Lemeunier

_F,

David

_JR,

Tsacas

_L,

Ashburner M

₍₁₉₈₆₎

The

_{melanogaster species}

group. 7n: Tlae Genetics and

Biology

of

Drosophila

(Ashburner

M,

Carson

HL,

Thompson JN,

eds)

Academic

Press,

New

_York,

Vol 3e 147-256

Levitan M

₍₁₉₅₈₎

Non-random associations of inversions. Cold

_Spring

Harbor

_Symp

Quant Biol 23,

251-268

Levitan 1I

_(19G1)

Proof of an

adaptative

linkage

association. Science

134, 1617-1G18

Levitan 1-I

₍₁₉₇₃₎

Studies of

_linkage

in

_populations.

VI. Periodic selections for X chromosome gene

arrangement

combinations. Evolution

_27,

215-225

Levitan

_lI,

Salzano FM

₍₁₉₅₉₎

Studies of

_linkage

in

_populations.

III. An association of linked inversions in

_Drosoplaila

_guaramunv,.

Heredity

13,

243-248

!Iather WB

_(19G3)

Patterns of chromosomal

_polymorphism

in

_Drosophila

rubida. Am Nat

_97,

59-63

Mukai

T,

Voelker RA

₍₁₉₇₇₎

The

_genetic

structure of natural

_populations

of

Drosoplcila melanogaster.

XIII. Further studies on

_linkage

disequilibrium.

Genetics

86,

175-185

Mukai

_T,

Watanabe

TIi,

Yamaguchi

0

₍₁₉₇₄₎

The

_genetic

structure of natural

populations

of

Drosoplaila melanogaster.

XII.

_{Linkage disequilibrium}

in a

_large

local

population.

Genetics

_77,

771-793

Paik

YIC, Yang

.JY

₍₁₉₈₃₎

A simultaneous

_study

of enzyme and chromosome

polymorphisms

in a Korean

population

of

Drosoplaila melanogaster.

Korean J Genet

5, 47-59

Parsons PA

₍₁₉₇₃₎

Behavioural

and

_Ecological

Genetics: A

_Study

in

_Drosophila.

Clarendon

Press,

Oxford

Prakash S

_(19G7)

Chromosome interactions in

Drosophila

robusta. Genetics

57,

385-400

Singh

AK,

Singh

BN

₍₁₉₈₉₎

Further data in interchromosomal association in

Drosophila

ananassae. Naturalia

_14,

19-29

Singh

BN

₍₁₉₈₂₎

The lack of evidence for interchromosomal interactions in

Drosophila

ananassae. Naturalia

_7,

29-34

Singh

BN

₍₁₉₈₃₎

On intra- and interchromosomal associations in

_Drosophila

ananassae. Genetica

_60,

231-235

Singh

BN

₍₁₉₈₄₎

_Epistatic

_{interaction between linked gene}

_arrangements

in

Drosophila

ananassae. Braz J Genet

_7,

175-181

Singh

BN,

Singh

AK

_(1990a)

_Linkage

_{disequilibrium}

in

_laboratory

strains of

Drosophila

ananassae is due to drift. Hereditas

_112,

203-208

Singh

BN,

Singh

AK

_(1990b)

Non-random associations between

independent

inver-sions in

_laboratory

strains of

_Drosophila

ananassae. Naturalia 16

(in press)

Singh

RS,

Hubby JL,

Thockmorton LH

₍₁₉₇₅₎

The

_study

of

_genic

variation

_by

electrophoretic

and heat denaturation

_techniques

at the octanol

_{dehydrogenase}

locus in members of the

_Drosophila

virilis _group. Genetics

_80,

637-650

Sperlich D,

Feuerbach-Mravlag

H

₍₁₉₇₄₎

_Epistatic

_gene

_{interaction, crossing-over}

and linked and unlinked inversions of

Drosophila

subobscura. Evolution

_28,

67-75

Sperlich D,

Pfriem P

₍₁₉₈₆₎

Chromosomal

_polymorphism

in natural and

experi-mental

_populations.

In: The Genetics and

_{Biology of Drosophila}

_(Ashburner

_M,

Carson

_{HL, Thompson}

JN

_Jr,

_eds)

Academic

_Press,

New

_York,

Vol 3e 257-309

Stalker HD

₍₁₉₆₄₎

Chromosomal

_polymorphism

in

_Drosophila

eurotonns. Genetics

49,

669-687

Stalker HD

₍₁₉₇₆₎

Chromosome studies in wild

_populations

of

_Drosophila

melanogas-ter. Genetics

_82,

323-347

Voelker

RA,

Mukai

T,

Johnson FM

₍₁₉₇₇₎

Genetic variation in

_populations

of

Drosoplaila melanogaster

from the western United States. Genetica

_47,

143-148

Wright

S

₍₁₉₆₄₎

_Biology

and the

_philosophy

of science. Monist

_48,

265-290

Yamaguchi

0,

Ichinose

M,

Matsuda

M,

Mukai T

₍₁₉₉₀₎

_Linkage

_{disequilibrium}

in

isolated

populations

of

Drosophila

melanogaster.

Genetics

_96,

507-522

Yamazaki

_T,

Matsuo

Y,

Inoue

Y,

Matsuo Y

₍₁₉₈₄₎

Genetic

analysis

of natural

populations

of

Drosophila

melanogaster

in

_Japan.

I. Protein

_{polymorphism,}

lethal

gene,

sterility

gene, inversion

polymorphism

and

linkage

disequilibrium. Jpn

J