Incipient reproductive isolation between Drosophila nasuta and Drosophila albomicans

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Incipient reproductive isolation between Drosophila

nasuta and Drosophila albomicans

Y Inoue, O Kitagawa

To cite this version:

Original

article

Incipient reproductive

isolation

between

_Drosophila

nasuta

and

_Drosophila

albomicans

Y Inoue*

O

_Kitagawa*

Department

of Biology,

Tokyo Metropolitan University, Setagaya, Tokyo 158, Japan

(Received

28 _{September 1988; accepted} 24 October

₁₉₈₉₎

Summary - Genetic

_divergence

was _investigated between 2 _closely related _allopatric

species, Drosophila nasuta and D albomicans, which have not evolved sexual

_(pre-mating)

isolation. Several _post-zygotic components of fitness were _analysed in intra- and

inter-specific hybrids. The results show that these 2 _species are _{reproductively} isolated because

they are different _co-adapted

systems.

Among

_{geographic populations} of D albomicans,

genetic differentiation has also occurred. The evidence for _{primary subspeciation} in

D albomicans is discussed.

Drosophila nasuta _{subgroup /} fitness component / speciation / subspeciation

Résumé - Début d’isolement reproducteur entre _Drosophila nasuta et Drosophila

albomicans - On a

_analysé

la _{divergence génétique} entre 2 _espèces

_affines

allopa-tiques, Drosophila nasuta et D _{albomicans, qui} n’ont pas développé d’isolement sexuel

précopulatoire. Plusieurs _{composantes post-zygotiques} de la

_fitness

ont été

_analysées

chez les _hybrides

_{intraspécifique}

et _{interspéc%fiques.} Les résultats _{montrent que} les 2 _espèces sont

isolées au _point de vue

reproduction

parce-qu’elles ont des

_systèmes

_coadaptés

_différents.

Parmi les _populations

_{géographiques}

de D _albomicans, une

différenciation génétique

s’est

aussi _produite. La _possibilité d’une subspéciation primaires chez D albomicans est discutée.

sous-groupe Drosophila nasuta / composantes de la fltness / spéciation / subspéciation INTRODUCTION

The

Drosophila

nasuta

_subgroup

of the

_{immigrans species}

group consists of more

than 10

_species

and

_{subspecies, therefore,}

this

_subgroup

is well suited for the

study

of the

_genetics

of

_speciation.

Members of the D nasuta

_subgroup

are

widely

distributed from the Pacific Ocean to

_Africa,

_through

South-east Asia and the Indian Oceans areas

(Kitagawa

et

_al,

_1982).

This

_subgroup

is

comparable

to the

widlistoni

species

group as

_subjects

for the

study

of

speciation

mechanisms.

However,

a

_conspicuous

difference exists between these 2 groups: the former are island

*

Present address: Biological Laboratory, Osaka University of _Foreign Studies, Aomadani, Mino,

Osaka 562, Japan **

populations,

whereas the latter are continental. This distinction may

produce

a

fundamental difference in their mode of

_speciation.

For the

_study

of the

_speciation

mechanisms,

analyses

of

_genetic

differentiation

at the first step of

_speciation

_processes among

closely

related taxa should be instructive. D nasuta and D albomicans are _very

_closely

related

_{species. Sajjan}

and

_{Krishnamurthy}

₍₁₉₇₂₎

and

_{Rajasekarasetty}

et al

_{(1979) regard}

D albomicans

as a

subspecies

of D nasuta.

However,

there is a

_striking

difference in

karyotypes

between the two. The basic

_karyotype

of this _{group is} 1V + 2R + 1D

_(ie,

2n =

8),

yet from _{among all} members of this group,

only

D albomicans has 2V + 1D

_(2n

=

6),

a result of fusions of the third and the sex chromosomes

(Wakahama

and

Kitagawa,

1972;

Wakahama et

_al,

_1983).

D nasuta had been collected in the

_{Seychelles, Madagascar,}

Maurituis, Reunion,

India and the east coast of

_{Africa, mainly by}

one of the authors

_(Kitagawa).

David and Tsacas

₍₁₉₈₁₎

_reported

D nasuta on the west coast of

_Africa,

and

_they

assumed

that the

expansion

in the distribution of this

_species

occurred

_by

a form of

man-made

_{transportation.}

D albomicans is distributed from south-western _parts of

_Japan

and Taiwan to the south-east of the Asian

continent, Burma,

Cambodia, China,

India,

Malaysia

and Thailand. The &dquo;dot&dquo; chromosome of D albomicans

_{(No. 4}

for the

_subgroup)

differs

depending

on

_locality.

The

Japanese

and Taiwanese

populations

have the

longer

type of &dquo;dot&dquo;

chromosomes,

which consists of

_large

heterochromatic

_regions.

The

other

_populations

have shorter &dquo;dot&dquo; chromosomes

_(Wilson

et

al, 1969;

Wakahama et

_al,

_{1983; Hatsumi,}

_1987).

D nasuta and D albomicans cannot be

_{distinguished}

_{by morphology.}

No sexual

reproductive

isolation has been detected between these 2

_species,

and both male and female

F

l

inter-specific hybrids

are fertile

(Kitagawa

et

_al,

_1982),

but in some crosses the

_F

₁

hybrids

males are almost sterile

(Hatsumi

and

Kitagawa, unpublished

data).

The most common alleles at the Est-a and

_Est-

₍

₃

_isozyme

loci are the

same for both

_species,

but

frequencies

of alleles

differ,

thus

indicating

that

genetic

differentiation has occurred between the 2

species

(Kitagawa

et

_al,

_1982).

The

karyotypes

of fertile

_hybrids

of D nasuta and D albomicans

_(as

D n nasuta and D n

albomicans,

respectively)

have been studied over _many

generations by

Ramachandra

and

_Ranganath

_(1986).

_They

have demonstrated

that,

in certain cases, stable

&dquo;Cytoraces&dquo;

evolve,

wherein individuals possess chromosomes

originating

from both

species.

We have shown

_(Inoue

and

_Kitagawa,

1974;

1975)

that the fitness of

_hybrids

varies

_{greatly depending}

on the

_origin

of the

founding

strains;

the

frequency

of

sterility

in

F

1

hybrid

males _{ranges from 3.2} to 4.8%.

The _present

_study

further clarifies the

_genetic

differentiation between D

na-suta and D

_albomicans;

we

investigated

certain _components of fitness relevant to

post-mating reproductive

isolation and show that

_hybrid

breakdown occurs in

sub-sequent

generations following interspecific hybridization. Futhermore,

we discuss

the _apparent

_primary

_{subspeciation}

among local

populations

of D albomicans.

MATERIALS AND METHODS

Six

_geographical

strains were used:

Okinawa, Japan

(designated

as

OKA),

Wulai,

Lanka

_(KDY),

_Mahe,

_{Seychelles (SEZ),}

and

_{Mombasa, Kenya}

_(MBA)

for D nasuta

(Fig 1).

Each

_geographic

strain was established

_{by pooling}

iso-female

_lines,

which

descended

from

_{single wild-caught}

mated females. Ten iso-female lines were used

for

OKA and

_FOR,

5 lines for

_CNX,

4 lines for

_KDY,

10 lines for SEZ and 6 lines for MBA. After 2

_generations

_{following pooling}

of the

_cultures,

the

_experiments

were started.

All

_possibles

diallel crosses were

_{simultaneously}

undertaken with the 6 strains.

For each cross, 15 females and 20 males were put into a vial

immediately

after

eclosion,

and were

kept

_together

for 7

_days

to ensure

_mating.

Their _progeny

(F

l

)

were obtained from the

_vial,

and

_thereafter,

the

_F

₂

and

_F

₃

flies were reared

_by

successive

_sib-matings.

In all

_experiments,

_except the

_productivity

_experiment,

4

replications

were _{set up} for each cross in the successive 3

_generations.

Insemination rate

Following

the

_{7-day mating period,}

females were dissected to examine

_spermathecae

and seminal

_receptacles

for the presence of sperm. The

proportion

of the fraction

(inseminated females/total females)

is

_regarded

as the insemination rate.

Pre-adult

_viability

On the next

_day

of the

_{mating period,}

50 _eggs were

sampled

from each cross and

_placed

in a new vial

_containing

the standard cornmeal-molasses medium. The

the eggs had been

_sampled.

The

_proportion

of the number of adult flies to _{eggs is}

regarded

as the

_{pre-adult viability.}

Hatchability

After the

_{7-days mating period,}

flies were transferred to a new vial

_containing

_partly

modified Delcour’s

₍₁₉₆₉₎

medium for 10 h. Two

_{days later,}

the number of hatched and unhatched eggs were counted. The

_proportion

_{hatched/total}

_{eggs is}

_regarded

as

_{hatchability.}

Productivity

After the

_{mating period,}

flies were transferred

_everyday

to a new vial

_containing

20% boiled _yeast

_medium,

for 8

_days.

The number of progeny from the

lst,

3rd,

5th

and 7th

_cultures,

and the number of eggs laid on the

_2nd,

_4th,

6th and 8th

_days

were counted to determine

_{productivity.}

Sex ratio

The number of male and female _progeny

_{(õ’ /( õ’ + 9 ),}

_produced

on standard

medium,

were recorded from

_samples

of all crosses over the 3

_generations.

All

experiments

were carried out at 25 ± 1°C.

RESULTS

Insemination rate

A total of 6 480 females were dissected to examine _{sexual organs} for the presence of sperm. The results are shown in Table 1. All the

_{intra-population}

crosses showed

high

insemination rates, except for

_CNX,

which showed

_only

a 50% insemination.

In the

_{intra-specific}

crosses of D _nasuta, most values did not differ

_{significantly}

from the

parental

values,

except that the

_F

₂

_generation

of

_{MBA 9}

x SEZ d’showed a

significantly higher

rate, and the F1 of

_{MBA 9}

showed a lower rate than the

mid-parent

value, comparing

confidence limits about means. In 17 combinations out of 54

_{inter-specific generation combinations, significantly}

lower insemination rates

were

observed, especially

in the

_F

₁

and

F

3

generations.

Hatchability

The

results

are shown in Table II. In

_total,

135 949 _eggs were counted to estimate

the

_{hatchability,}

from which _{112 969 eggs hatched. The average}

_hatchability

in the

_parental

strains was 91.8%. In the intra-albomicans _crosses, 3 cases of

hybrid

breakdown were detected _among 18 crosses. In the intra-nasuta crosses, all 6

2nd-generation

crosses had

_higher

values than the

_parental

_strains,

3 of which were

significant.

No

_hybrid

breakdown

_appeared

in _any

_generation.

In the crosses of albomicans

₉

x nasuta

_d,

no

_hybrid

_vigour

was observed and

the crosses of

_{nasuta 9}

x albornicans

_d’,

2 out of 9 crosses in the _F1

_generation

showed

_{hybrid breakdown,}

3 out of 9 in the

F

2

generation,

and all 9 in the

F

3

generation

showed

_{significant hybrid}

breakdown.

Thus,

the results for

_hatchability

were

approximately

the same in the

_reciprocal

crosses.

Pre-adult

_viability

In

total,

21600 eggs were

_sampled

from which 11618 flies

_emerged

(Table

III and

Fig

2).

In contrast to the

_{hatchability,}

the

_original

strains

_apparently

carried different mutations

_affecting

larval

_mortality.

The average

viability

was

only

68.6%

in the

_original

strains. The value of the CNX strain was

_considerably

lower

(34.7%).

From the intra-albomicans and intra-nasuta crosses,

significant

vigour appeared

the

_{inter-specific}

crosses,

significant

breakdown

appeared

in the 2nd- and

3rd-generations

of

_{albomicans 9}

x nasuta

_d’(8

and 6 crosses out of

_9,

_{respectively).}

In crosses of

_{nasuta 9}

x albomicans

_d,

_hybrid

breakdown was observed

_mainly

in the _Fl and

_F

₃

_generations.

_Only

in the

F

2

_generation

of

_{KDY 9}

x FOR _d’ was

hybrid vigour

detected.

Productivity

The patterns of

_daily

_productivity

of _{eggs and progeny} were similar to the

_parental

strains. When males and females mated

_just

after _emergence, fertile _eggs were not

laid for a few

_days

and the

_{peak egg-laying}

_capacity

was between 7 and 10

_days

after emergence. In

total,

167 437 _eggs and 80 126 progeny were

_counted;

the results are shown in Tables IV and V. On _average, a female of the

_original

strain laid 20.4 eggs per

day,

from which 12.6 flies

emerged.

out of the 6

_{second-generation}

crosses showed

hybrid vigour, averaging

29.4

eggs/female/day.

In the crosses of

_{albomicans 9}

x nasuta

_d,

_hybrid

_{vigour appeared}

more

frequently

than breakdown in the 1st and 2nd

_generation,

but

_hybrid

break-down was

frequently

shown in the 3rd

_generation.

In the crosses of

_{nasuta 9}

x

albomicans

_{(T ,}

_hybrid

breakdown

_appeared

in 5 crosses out of the 9

_{third-generation}

crosses. In

_{productivity, hybrid}

breakdown was clear in the

_{inter-specific}

3rd

gen-eration of both sets of

_reciprocal

crosses.

The number of _progeny

_produced

in the intra-albnmicans crosses indicate

_vigour

in 3 cases of the Ist- and

_{3rd-generation}

crosses

_each,

and

_hybrid

breakdown occurred in 3

_{second-generation}

crosses and in 1 of the

third-generation

crosses. In

the _{intra-nasuta crosses, all 6} crosses showed

_{hybrid vigour}

in the 2nd

_generation.

In the crosses of

_{albomicans 9}

x nasuta

_d

_,

_{hybrid vigour appeared}

in the 1st

generation

(6

cases out of

_9),

and

_hybrid

breakdown was seen in the 2nd

(8

out of

all 9 cases showed

_{significant hybrid}

breakdown in the 3rd

_generation.

In

_general,

the results of _progeny

_productivity

were similar to _{those of egg}

_fecundity.

Sex ratio

The sex ratio

_(numbers

of

_males/total

_flies)

of the

_original

strains and their

_hybrids

in the 3 successive

_generations

are shown in

_Fig

3.

Altogether,

69 981 females

counted. No differences were found _{among the 6}

_original

_{strains, ie,}

48.9 ±0.9% on

average.

In the intra-albomicans _crosses, 3 cases out of 18 showed

_significant

_distortion;

the 2nd

_generation

of

_{OKA 9}

x FOR d’showed a marked excess of males

_(p

<

_0.01),

although

the

_reciprocal

cross was normal.

_{Significantly}

fewer males

_(p

<

_0.05)

were observed in the

_F

₃

_generation

of

_{FOR 9}

x OKA d’ and the F2

generation

of FOR

Q x

CNX _{c3’ .} In the intra-nasuta crosses, all cases were normal.

An abnormal sex ratio was

_frequently

detected in the

_{inter-specific}

crosses. In 27

cases of

_{albomicans 9}

x nasuta _{c3’ crosses,} 9 showed reductions in the numbers of males

_{(OKA 9}

x rcasuta

c? ,

and

_{FOR 9}

x nasuta

_{d’ ),}

whereas a

_significant

excess

of males was observed

only

in the

_F

₂

_generation

of CNX

_Q

x KDY c?. In the cross of

_{FOR 9}

x KDY

_{d’ ,}

_significant

male

_{under-representation}

was observed in _every

generation.

From crosses of OKA

₉

and FOR _õ’to all D nasuta

_males,

drastic

male breakdown was detected in the

F

2

generation,

with

_only

8.6% males

_produced

by

_{OKA 9}

x SEZ

_{d’ ;}

_yet, these males were fertile. In 27 cases of nasuta

₉

x

crosses. Six cases of male excess and

_only

6 cases of male reduction were seen. In

contrast, the 2nd

generation

of the

_{inter-specific}

crosses was characterized

by

a

large

excess

of

females from

_{albomicans 9}

x nasuta

_d

_{’ ,}

and

_by

a male excess from

the

_reciprocal

_{nasuta 9}

x albomicans C3’ .

DISCUSSION

The

_genetic

constitutions of natural

_populations

of

_{diploid organisms}

are

_integrated,

co-adapted

gene

complexes being produced by evolutionary

processes

(Dobzhan-sky,

1970).

Hybrids

between local

_populations

which have evolved different

_genetic

in D

_{pseudoobscura}

_(Vetukhiv,

_{1954, 1956; Brncic, 1954, 1961;}

_Orr,

₁₉₈₇₎

_and in D

_melanogaster

_{(Wallace, 1955).}

The results of the _present

_study

demonstrate that

_significant

_genetic

_divergence

has occured between 2

_closely

related members of the

_Drosophila

nasuta

_subgroup

(D

nasuta and D

_albomicans),

as indicated

_{by hybrid}

breakdown.

_Furthermore,

inter-population

crosses within

_species

show that _greater

_genetic

_divergence

exist

Intra-population

crosses

These served as control

_experiments

for both intra- and

inter-specific

crosses. All

strains except the

_Chiangmai

_(CNX)

showed

_high

fitness in the various character-istics examined. For the

_CNX,

the insemination rate was about

half,

and

pre-adult

viability

and the number of progeny were less than

half, compared

to the other

5 strains.

However,

the number of eggs laid and _egg

_hatchability

were normal.

The low fitness of the CNX

_population

_{might partly}

be attributed to the existence

of _{supernumerary chromosomes in this}

_population

_(Hatsumi

and

_Kitagawa,

_1980;

Hatsumi,

1987).

Inter-strains within

_species

crosses

This is one of the useful scales to determine differentiation within

_species.

In

D

albomicans,

the

_F

₂

breakdown was

commonly

seen in combinations of crosses

measuring

the number of progeny and

pre-adult viability.

Remarkable F2 break-downs were observed from crosses between CNX females to OKA and FOR males. In addition to the existence of _{the supernumerary} chromosomes mentioned

above,

CNX have shorter &dquo;dot&dquo; chromosomes

_compared

to those of OKA and FOR pop-ulations. The results of

_{pre-adult viability}

indicated that the CNX

_population

has

genetically

differentiated from the island

_populations,

OKA and FOR.

Subspecia-tion among

geographic populations

of D albomicans is discussed below.

For D _nasuta, the number of progeny from crosses of

_{KDY 9}

x SEZ

c?

MBA

d’ was lower in the

F

1

and

F

3

generations

and

higher

in the

F

2

generation.

The

F

l

hybrids

of

_{MBA 9}

x KDY d’ showed

_extremely

low

_{pre-adult viability}

_(38%).

Yet,

in many cases,

hybrids

between local

populations

showed

hybrid vigour.

This seems

to _suggest that

_geographic

_populations

of D nasuta have

_sufficiently

differentiated to exhibit heterosis

_{(hybrid vigour).}

However,

compared

to D

albomicans,

the

genetic

differentiation among local

populations

of D nasuta is less advanced. This

is consistent with David and Tsacas’s

₍₁₉₈₁₎

_suggestion

that D natusa has

_only

recently expanded

its distribution to the Indian Ocean area and to Africa.

Inter-specific

crosses

The insemination rates of

_{inter-specific hybrids}

in the

_F

_l

and

_F

₂

_generations

were

significantly

lower than those of the _parents, with lower rates in 10 out of 18

combination-generation

crosses of D

nasuta !

and D adbomicans d’ The

reciprocal

crosses, is which KDY or MBA were used as

the

male _parents, showed insemination

rates in the

F

l

and

_F

₃

_generations.

As to _egg

_{hatchability,}

_4,

9 and 18 crosses out of 18 showed lower values than did their lower parent in the

_F

_l

_,

_FZ and

_F

₃

_{generations, respectively}

_{(Table II).}

In about half the numbers of combinations in the

_F

₁

and

_F

₂

_generations,

the numbers

of progeny

produced by

a female _per

_day

were

_{significantly higher}

than in the

parental

strains.

F

1

heterosis was seen in 10 out of 18 crosses, but

hybrid

breakdown

was

_frequently

demonstrated in the

subsequent

F

2

and

F

3

generations

(Table V).

In all crosses of D

_{natusa 9}

x D albimocans _d in the

_F

₃

_generation,

the numbers of progeny decreased significantly. These results

_support

the conclusion that D nasuta

in the

_F

₃

_generation

is

_partly

attributed to the

_major

_karyotype

difference between

the 2

_species

_(Sato

et

al,

1977).

Hybrid

breakdown in

_{pre-adult viability}

was detected in the

F

2

and

F

3

gener-ations of the crosses of D

albomicans 9

x D nasuta

_d

and also observed in the

F

l

and

_F

₃

_generations

in the

_reciprocal

crosses. In the former _case, the

_F

_l

flies

had 2n =

_7,

and abnormal

_segregation

of chromosomes in meiosis of the

F

1

males should be the main source of

_genetic

imbalance

(Sato

et

al,

1877).

The

_striking

sex-ratio distortion in the

_F

₂

_generation

of the cross between

D

_{albomicans 9}

x D nasu.ta d’ was of _great interest. In other _crosses, we did not

find any

significant

distortion in the

F

1

,

F

Z

and

F

3

generations,

except for the

_F

₂

generation

of

_{OKA 9}

x

FOR

d’ in D albomicans.

However,

in the

F

2

generation

of the crosses between D

albomicans

9

x D nasuta

_d

drastic decreases of males were

observed. The _{average recovery} of males in the

F

2

generation

was 11.2% in OKA

Q x

D nasuta

_{d’ ,}

and 32.2% in

_{FOR 9}

x D nasuta

d

Two fitness _components, egg

hatchability

and

pre-adult viability,

assess

develop-mental _processes of

_hybrids,

and

_thus,

the _components of fitness examined in this

study

demonstrate that the reduction in fitness observed _among

_hybrid

recombi-nants can be attributed to the differentiation of

_{co-adapted genetic}

_systems. It is

evident that

_significant

differences in

_genetic

constitution between D nasuta and D albomicans have evolved since

_hybrids

have reduced fitness at the

_post-zygotic

stage.

As a

_by-product

of

_genetic

_{differentiation,}

nasuta and albomicans

_produce

hybrids

with reduced fitness. Since the

_genetic

_divergence

has arisen in

_allopatry,

it

cannot be said to be caused

_{by hybridization; post-zygotic reproductive}

isolation of this _type conforms with the first

_phase

of

_{Dobzhansky’s}

₍₁₉₅₁₎

_{speciation model;}

hybridization

and reinforcement

_being

the second

_phase

_(see

also

_Ayala

et

al,

1974).

We believe that nasuta and albomicans are

_{incipient species}

at the first

_phase

of a

2-phase

speciation

process.

DifFerentiation _among D albomicans strains

Hybrid

breakdown was

commonly

observed in egg

hatchability

and in

pre-adult

viability

(egg

to

_adult).

The

_hybrids

between more

genetically

remote strains

are

_expected

to die at earlier

_{developmental}

_stages. The value &dquo;1 -

_(pre-adult

viability)&dquo;

can be

_regarded

as total

_mortality,

and &dquo;1 -

_(egg

_{hatchability)&dquo;}

as

embryonic mortality.

If the ratio of

_(embryonic

_{mortality)/(total}

_mortality)

is

_large,

it means a

_large

fraction of

_hybrids

die

_early

in their

_{development. Therefore,}

this

ratio can be used as a measure of

_genetic

differentiation between

geographic

strains.

The average ratio was calculated from the data in Tables II and III.

The

_degree

to which

_embryonic

death contributes to

_{pre-adult mortality}

of

_F

_l

_,

F

2

and

_F

₃

_generations

in all 36 combinations of crosses is shown in Table VI. The

_proportion

of

_{embryonic mortality}

to total

_mortality

in

_{inter-specific}

_hybrids

steadily

increased with

_generations.

The

_{intra-specific}

crosses of D albomicans show a similar _pattern of

_{increasing embryonic mortality}

with

_generations,

but to a

lesser

_degree

than the

_{inter-specific}

crosses. This _{pattern suggests} that

_geographic

populations

of D albomicans have achieved substantial

_{genetic divergence, perhaps}

to the level of

_semispecies.

The

_{inter-specific}

and intra-albomicans _pattern of

Moreover, significant hybrid

breakdown was observed in

_{pre-adult viability}

of

the

F

1

and

_F

₃

_generations

of

_{CNX 9}

x OKA

I

the

_F2 and

F

3

generations

of CNX

9

x FOR

_{d’ ,}

and in the

_F

₁

_generation

of FOR

_Q

x OKA

_{c3’ ;}

_whereas,

in the intra-nasuta crosses,

hybrid

breakdown was seen

_only

in the

F

1

generation

of

_{MBA 9}

x

KDY d’ . Sex-ratio distortion of

_hybrids

_(the

reduction of

_males)

was

_quite

different

among 3 strains of D albomicans

(OKA,

FOR and

CNX)

in the

F

2

generation

of

albomicans 9

x nasuta cr crosses. This is further evidence of differentiation at the

genic

level among albomicans strains. The

_population

located farthest from the

distribution border of D nasuta, the OKA

_population

of D

albomicans,

showed an

extreme sex-ratio distortion in the

_F

₂

_generation;

the next farthest

_population,

the

FOR,

was the next in the

_degree

of distortion. The CNX

_population,

located nearest

to D _nasuta, showed a normal sex ratio

(similar

to intra-nasuta

_crosses).

These observations _support the

_following

conclusion: the 3

_populations

of D albomicans

(OKA,

FOR and

_CNX)

are

_undergoing

_{primary subspeciation.}

_However,

further

studies are necessary to determine the

_{specific genetic}

differences between D nasuta and D

_albomicans,

and _among the

_{geographic populations}

of D albomicans.

ACKNOWLEDGMENTS

We wish _{to express} our _many thanks to Professor Emeritus S

_Ohba,

Drs YN

_Tobari,

Y

_Fuyama

and T

_{Aotsuka, Tokyo}

_Metropolitan

_University,

for invaluable criticism.

We also wish to _express our

_hearty

thanks to Professor B

_Grant,

_College

of William and

_Mary,

for

_reading

the

_manuscript

and for

_giving

invaluable criticism. We wish to thank Professor JR

_{David, CNRS,}

for

_writing

the French _summary. This work

(Field Research)

in 1971

_{(No. 7114),}

1979

_{(No. 404149),}

1980

_{(No. 504344),}

and

1981

_{(No. 5604149)}

of the

_Ministry

of

Education,

Science and Culture of

_Japan.

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