Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D simulans. II. Within-population variability

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Phenotypic and genetic variability of morphometrical

traits in natural populations of Drosophila melanogaster

and D simulans. II. Within-population variability

P Capy, E Pla, Jr David

To cite this version:

Original

article

Phenotypic

and

_{genetic variability}

of

_{morphometrical}

traits

in natural

_populations

of

Drosophila melanogaster

and

D

simulans.

II.

_{Within-population variability}

P

_Capy,

_{E Pla,}

JR David

Centre National de la Recherche

_{Scientifique,}

Laboratoire de

_Biologie

et

Genetique Evolutives,

91198

_{Gif-sur-Yvette Cedex,}

France

(Received

30 March 1993;

accepted

10

_August

₁₉₉₃₎

Summary -

Within-population variability

was

investigated

in the 2

_sibling

_species

Drosophila mela!nogaster

and D simulans at both

_phenotypic

and

genetic

levels. Six

quantitative

traits were studied in 55 different

populations

of D

_melanogaster

and 25

populations

of D simulans encompassing most of the

_cosmopolitan

range of the 2

_species.

The

_phenotypic

variabilities of all the traits were

compared

_using the coefficients

of variation

_(CV).

Differences _among CV’s were broader than

_expected

from their

theoretical

_sampling

distribution.

_{Temperate populations}

were

_generally

less variable than

tropical

ones.

Moreover,

in both

_species,

the CVof the 3 size-related traits

(fresh

_weight,

wing

length

and thorax

_length)

were correlated.

Comparison

of the 2

_species

showed that

the average variabilities

(mean

values of

Ct!

were almost identical with the exception

of ovariole number which is much less variable in D simulans

_(6%

_against

_8%).

At the

genetic level,

distributions of intraclass correlations did not show any

departure

from

the

expected sampling distributions, suggesting

that all

populations

harbored a similar

amount of

_{genetic variability.}

For most traits, no

_significant

difference was found between the 2 species, except

again

for the ovariole number which is

_genetically

less variable in

D simulans. An overall

_analysis

of the total

_variability

showed that 78% of the total

variance was

_{explained by}

the

_{within-population}

_components in D simulans

_against

50%

in D

_{melanogaster.}

Drosophila melanogaster

/

Drosophila simulans _{/ morphological} traits

_/

within-population variability

/

isofemale lines

Résumé - Variabilité phénotypique et génétique de caractères morphologiques dans les populations naturelles de Drosophila melanogaster et _Drosophila simulans. II. Vari-abilité _{intrapopulation.} La variabilité

intrapopulation

a été

analysée

dans les

populations

naturelles de 2

_{espèces jumelles, Drosophila melanogaster}

et D simulans. Six caractères

morphologiques

ont été mesurés dans 55

_populations

de D

_melanogaster

et 25

phénotypique,

on a observé chez les

_{2 espèces}

et pour tous les caractères _que la variabilité de la distribution des

_coefficients

de variation

_(CV)

était

_supérieure

à la variabilité

atten-due dans le cas d’un

_{échantillonnage}

au hasard. Cela met en évidence _que des

populations

sont

beaucoup plus

variables _que d’autres.

Ainsi,

les

_{populations tempérées}

sont moins

variables que les

populations tropicales.

Par

ailleurs,

les CV de 3 caractères

_(le

_poids

frais,

les

_longueurs

de l’aile et du

_thorax)

sont

_positivement

corrélés. La

_comparaison

des 2

espèces

sur la base des _moyennes des distributions des CV ne _{permet pas} de mettre en

évidence de

_{différences significatives,}

à

l’exception

du nombre

_{d’ovarioLes,}

_qui est moins

variable chez D simulans. Au niveau

_génétique,

les distributions observées de la corrélation intraclasse sont

_conformes

aux distributions

_théoriques

attendues.

À

_{l’exception}

du nombre

d’ovarioles qui s’avère une nouvelle

_fois

moins variable chez D

_simulans,

il n’existe _pas,

pour les autres

_caractères,

de

_{différences significatives}

entre les moyennes des distributions de ce

_paramètre

chez les 2

_{espèces. Ainsi,}

_pour la majeure partie des caractères

_analysés

au cours de ce

travail,

les

_{2 espèces présentent}

des niveaux de variabilité

_comparables.

L’analyse globale

de la variabilité des

_{2 espèces}

montre _que 78% de la variance totale de D simulans est observée au niveau

_{intrapopulation,}

contre 50% chez D

_{melanogaster.}

Drosophila melanogaster

/

Drosophila simulans

_/

caractères _{morphologiques /} varia-bilité intrapopulation

/

lignées isofemelles

INTRODUCTION

Although

it is

_generally

assumed that

_phenotypic

traits are

_{the_}

_primary

_target

of natural selection

_{(Lewontin, 1974),}

_analysis

of such characters has been somewhat

neglected

in favor of molecular variations and most

_analyses

have been devoted to

laboratory

rather than to natural

populations.

In this

_respect,

_Drosophila

_melanogaster

has been used as a model

_organism

for

quantitative genetics

and a

_huge

amount of data has been accumulated. Numerous

investigations

have dealt with selection

_experiments

_(see

Roff and

_{Mousseau, 1987,}

for a

review)

and tried to locate _genes with

_major

effects

_(Thoday,

_1961;

_Thompson,

1975;

Shrimpton

and

Robertson,

1988).

By comparison,

the

_analysis

of the

_{morphological variability}

of natural popu-lations has remained less

_developed.

Such variations were

_investigated

in several

species

such as D

robusta,

D

subobscura,

D

_persimilis

and D

pseudoobscura,

D

_melanogaster

and D simulans

_(see

David et

_al,

_1983,

for a

review).

But in all

cases, the main interest was focused more on the

_geographic

_variability

of the

mean values of various traits

_{(between-population variability)}

than on the

within-population variability.

One

_possible

reason for which the

_genetic

architecture of natural

_populations

has remained less

_investigated

is that

_quantitative

_genetic

techniques

need a

_large

amount of data if the

_heritability

is to be estimated with

precision.

So,

with a few

_exceptions

_(Suh

and

_{Mukai, 1991,}

and references

_therein)

the

_possibility

that

_genetic

_variability

could _vary

_according

to some

_geographic

trend has not been considered.

for which 55 different

_populations

were

_available,

and its

_sibling

_species

D

simulans,

which also exhibits a

_cosmopolitan

distribution and for which 25

_populations

have

been studied. These 2 sets of

_populations

were used to _compare the

_phenotypic

and

genetic

variabilities within natural

_populations

of the 2

_sibling

_species.

The interest of such a

_comparative

approach

arises from the fact that these 2

cosmopolitan

species

are

_sympatric

in most

_parts

of the

_world,

show similar seasonal

_demographic

profiles

(David

et

_al,

₁₉₈₃₎

and are

probably exposed

to similar environmental

pressures. From

analyses

of other traits

(see

discussion of

Capy

et

al,

1993),

it

seems that

ecological

success and colonization

ability

of these 2

species

are based on different

_genetic

_strategies

(Singh

et

_al,

_1987).

_Therefore,

in such a

_context,

it is

important

to

_analyze

their

_phenotypic

and

_{genetic variability}

for various kinds of

traits,

in order to determine whether

_they

share similar

_genetic

architectures. In this

_work,

we have found that the 2

_species

exhibit similar levels of

phenotypic

and

_genetic

_variability

for most of the traits considered here. The main

_exception

concerns the ovariole number for which D

melanogaster

is much more variable

than D simulans both

_{phenotypically}

and

_genetically.

Our results will be discussed

according

to what is known for these 2

_species

for other traits.

_Finally,

the

apportionment

of the total

_variability

in these 2

_species,

from the

_{within-population}

component

to the

_variability

between

_geographical

_regions,

will also be discussed.

MATERIALS AND METHODS

Natural

populations

and

_{morphological}

traits

The natural

_{populations morphological}

traits here studied and the

techniques

used

(isofemale lines)

have

_already

been described in the

_previous

paper

(Capy

et

_al,

1993).

Estimation of

_variability

The

_variability

of each natural

_population

was estimated

_{by using}

the coefficient

of variation for the

_{phenotypic variability}

_{( C!}

and the intraclass correlation

_(t),

calculated from an

analysis

of variance. This latter

_parameter

is related to the

genetic

variability

(Falconer, 1981)

and can be assimilated to an isofemale line

heritability

(Parsons, 1983).

Comparison

of

_{phenotypic variability}

of the different

populations

was

performed

using

Levene’s test for

_.homogeneity

of variances

_{(Levene, 1960).}

Variates of each

population

were transformed

_according

to the

_following

formula:

where

_%

is the value of individual

k,

for the

_{variate j in}

the

_population

i and where

_{Ln V}

_ij

_.

is the mean of the

_logarithm

of the

_population

i. To test whether the average absolute deviations were identical for the different

populations,

a

single

one-way

analysis

of variance was

performed.

The distributions of the intraclass correlations were also

_analyzed.

To test the

theoretical distributions were

compared

by

a

Kolmogorov-Smirnov

test

_assuming

that the ratio:

follows an F distribution with

N — 1,

N(n - 1)

degrees

of freedom

_{(Bulmer, 1985).}

In this

expression, M

1

and

M

2

are the observed mean _squares between and within isofemale lines. Theoretical

_density

functions and

_{probabilities}

were calculated

_using

the

_{approximation}

of

_Jaspen

_(1965).

Comparisons

between D

_melanogaster

and D simulans were

_performed

_assuming

that the variables are

_normally

distributed.

_Therefore,

classical tests such as

Student’s test for

_comparisons

of means and Fisher-Snedecor test for

_comparisons

of

_variances,

were used. The

_comparisons

were also made

by

_{using non-parametric}

methods like the

_Mann-Whitney

U test or

_Spearman

rank correlation. Whatever

the method

used,

the conclusions of the test were identical.

RESULTS

Phenotypic

variability

Basic

_data,

ie mean values and standard errors of each

_trait,

were

_given

in table I of

_Capy

et al

_(1993).

As

_previously

indicated,

significant

variations exist between

means of the different

_populations

_according

to their

_geographic

_origin.

When several distributions have different means, a

_positive

correlation between mean

and variance is

_generally

_expected,

due to a

_scaling

effect. From the

_present

_data,

only

one correlation between means and variances

(ie

for the

sternopleural

bristle

number in D

_{melanogaster)}

was

significantly

_positive,

and 5 correlations _{among 12} were

_negative

(not shown).

_Thus,

in both

_species,

there is no clear evidence that

higher

means

_imply

_higher

variance.

_{However, variability}

has also to be

_compared

between

_species.

For most

_traits,

mean values of D simulans are smaller than those

of D

_melanogaster

_(Capy

et

_al,

_1993).

For this reason a relative measurement of

variability,

ie the coefficient of

variation,

CV,

has been used

_throughout

this _paper.

Moreover,

the CV allows the

_comparison

of variabilities of different traits

_expressed

with different

metrics,

such as

_wing

length

and ovariole number.

Because of _space

_shortage,

a table with the CVs of the various traits in each

population

is not

_given.

_But,

for all

traits,

the lowest

_{CV is,}

in

_general,

2- to 4-fold less that the

_highest

CV.

Moreover,

it is often observed that a

_given

population

may be

highly

variable for some traits while not for others. For

_example,

in

D

_{melanogaster,}

the Ottawa

_population

_(Canada),

which was the most variable for fresh

_weight,

was _among the least variable for thoracic

length.

The same

phenomenon

could be observed for D simulans

_(Seville

_population,

_Spain).

For this

species,

it may also be stressed that the Bizerte

_population

_(Tunisia)

was _among

the least variable for 3 of the 6 traits:

_FW,

TL and WL.

Means and variances of the distributions of the CVs are

_given

in table I for the 6

_{morphological}

traits. In each

_species,

there is no

_significant

difference

or the 21

_sympatric

_populations

are considered.

_Therefore,

for each

_species,

these

21

_populations

are a convenient

sample

of the overall

populations.

The

_comparison

of the 2

_species

shows a clear difference for the ovariole number

which is less variable in D simulans than in D

_melanogaster

_(average

CVs are 6.2

and

_7.6).

The same conclusion arises when all

_populations

of the 2

_species

are

considered. For the other

_traits,

the mean CVs of the 2

species

are not different. If

we then _compare the variances of the

CVdistributions,

we find that

they

are

_always

greater

in D

_{melanogaster,}

but

_{significantly}

so in

_only

2

cases

’

(ON

and

TL).

Finally,

correlations between CVs of the 2

_species

are

_generally

not

_significant,

_except

for fresh

_{weight, suggesting}

that there are no

_parallel

variations of the

_phenotypic

variability

between D

_melanogaster

and D simulans for the other traits.

Levene’s tests for

_homogeneity

of variances

_{(not given)}

show

that,

for all

_traits,

a

_{significant population}

effect exists or, in other

words,

that

within-population

variances are

heterogeneous.

Another method

proposed by

Brotherstone and Hill

(1986),

based on the

_comparison

between the observed and the theoretical

distribu-tions of the standard deviadistribu-tions or of the coefficients of

_variation,

_provided

similar

results.

The

_{intra-specific}

correlations between the CVs of the different traits are

_given

in table II.

_Although

most of these correlations are not

_significant,

there is an

average

tendency

toward

_positive

values

_(21/30).

Three of

_them,

_concerning

the 3 traits related to

_size,

are

_{significantly}

_positive

in both

_species.

This result is

not

_unexpected

since the mean values of these traits are themselves

positively

correlated. On the other

_hand,

the

_positive

correlation found in D

_melanogaster

between fresh

_weight

_variability

_(measured

in

_males)

and female ovariole number

Phenotypic variability

was also

analyzed according

to the

_geographic

_origin

of the

populations

(table III).

In D

_{melanogaster,}

for which more

_populations

are

available,

3 traits

_(FW,

AB and

_TL)

exhibit a

_significant

_negative

correlation with latitude of

_origin.

_{Populations living}

at

_higher

latitudes are less variable than

tropical

ones.

When

_geographic

groups are

considered,

3 traits

_(SB,

TL and

_ON)

show a

_significant

between-group

heterogeneity.

Interestingly,

for 2 of them no

_significant

correlation

was found with latitude.

Level of

_{significance:}

*

<

_5%;

** <

_1%;

r = coefficient of correlation; F = result of an

ANOVA

_testing

the

_region

effect. This

_analysis

was

performed

on the natural

_populations

clustered

_according

to their

_{geographical origin.}

For D

_melanogaster

10 groups were

considered and 6 for D simulans.

Geographical

groups for D

melanogaster.

France,

USSR,

North

Africa, Tropical Africa,

Islands of Indian Ocean close to the African continent, South

Africa,

North

_America,

West Indies and Mexico, Far East and Australia

_Geographical

groups for D simulans: France, North

Africa, Tropical Africa,

South

Africa,

French West

Indies,

Mexico and

USA,

Islands of Indian Ocean close to the African continent.

On the

whole,

we find that D

melanogaster

exhibits a

significant

geographic

differentiation not

_only

for the mean values of the traits but also for their

vari-ability.

In D simulans none of these

analyses

showed _any

significant geographical

Genetic

_variability

The total variance of each

_population

may be

partitioned

into 2

components:

variance within and variance between

isofemale

lines. A _one-way

_analysis

of variance

gives

the mean _squares within and between

families,

and from the

_expectations

of

these mean _{squares, it is}

_possible

to estimate the intraclass correlation t.

_Assuming

that

_epistatic

_{interactions,}

common environmental

effects,

and the dominance

variance are small

compared

with the additive

_genetic

variance,

t estimates half the

narrow sense

heritability

(Falconer,

_1981;

Capy,

1987)

or estimates the isofemale

heritability according

to Parsons

₍₁₉₈₃₎

and Hoffmann and Parsons

_(1988).

Means and standard deviations of intraclass correlations are

_given

in table IV. In

both

_species,

the observed and theoretical distributions are identical

(not shown)

and none of the

_{comparisons using}

a

Kolmogorov-Smirnov

test are

significant,

leading

to the conclusion that there is no

_genetic

_{heterogeneity}

between

_populations.

Significant

differences exist between intraclass correlations

_{( ie}

isofemale

_{heritability)}

of the various traits. In both

_species,

the

_highest

heritabilities are observed for traits

related

to

_size,

ie fresh

_weight

and

_wing

_length

with values

_ranging

between 0.40 and 0.53. We then find the bristle numbers

_(range

0.21 and

_0.32).

_Although

thorax

length

is related to

_size,

it is less variable

_(0.18

and 0.23 in the 2

_species).

Ovariole number also exhibits a

_fairly

low

_genetic

_variability

_(0.25

and

_0.14).

When the 2

_species

are

_compared,

2

significant

differences are

found,

for

sternopleural

bristles and ovariole numbers. For both

_traits,

D simulans is less variable. On the other

_hand,

when the t values of the

_sympatric

_populations

of the

2

_species

are

considered,

none of the coefficients of correlation is

significant.

Thus,

living

in the same area does not lead to similar

_{intrapopulation genetic}

variations.

Correlations between t values of different traits are

_given

in table V. As

previously

observed for the coefficient of

_variation,

_only

correlations

_involving

FW,

TL and WL

are

_significant

in D

_{melanogaster.}

_Although

these correlations do not

_correspond

to

_{genetic correlations,}

such a result

_suggests

that these

_traits,

which are related to

_size,

either share a common

_genetic

basis or are submitted to similar internal

constraints or are under similar external selective _pressures. In D

simulans,

only

the correlation between FW and WL is

_significant

while the thorax

_length

seems to be

_independent

of these 2 traits.

_Therefore,

it is

_possible

that this difference between the 2

_species

reflects some differences in the

_genetic

structure of these

traits. For

_example,

some

pleiotropic

effects could exist in D

rnelanogaster

but not

in D simulans.

The

_analysis

of the

_geographical

distribution of intraclass correlations does

not show _any latitudinal variations and

_{region effects,}

with an

_exception

for the

abdominal bristle number in D simulans.

_Therefore,

all

_regions

exhibit a similar

level of

_genetic

_variability

for most of the traits considered

here,

in

_spite

of the

geographical

variability

of the mean values of the

_traits,

and also of the total

DISCUSSION AND CONCLUSIONS

Our

_analysis

of the

_{within-population variability}

of the 2

_sibling

_species

shows that for most of the traits considered

here,

the 2

_species

exhibit similar levels of

variabil-ity.

The main

_exception

concerns the ovariole number for which D

_melanogaster

is

phenotypically

and

_genetically

more variable than D simulans. The

_large

amount

of biometrical data

_presented

in this _paper will be discussed in several _ways.

Phenotypic

variance and coefficients of variation

It is well known

_(David

et

al,

1980)

that wild

_living

Drosophila

adults are submitted to variable environments

_during

their

_development,

_resulting

in a broad

_phenotypic

variance in natural

_populations.

For

_genetic

_purposes, we need to control

_growth

conditions and reduce the environmental

_component

_{(David, 1979).}

The coefficients of variation measured in the

_laboratory

are often 2 or 3 times less than in nature.

Our results show that

_significant

differences in CV values exist between different

traits in the 2

_species.

Size-related traits are the least variable

(from

2.5 to

_5.5%)

while bristle numbers are most variable

_(from

8.9 to

_11.0%).

A classical

interpre-tation

_{(Lerner, 1954)}

is that traits related to fitness are submitted to a permanent selection and

_{developmental}

canalization,

thus

_resulting

in a low

variability.

Our

results are in

_agreement

with this

general

_expectation:

size is

certainly

related

to

_fitness,

while for bristle

numbers,

the

_relationship

is dubious. Ovariole

num-ber is known to be related to _egg

_production,

at least under

_laboratory

conditions

(Bouletreau-Merle

et

_al,

₁₉₈₂₎

and is thus a clear

_component

of fitness. However

this trait exhibits a

_large

_variability

between

individuals,

since in D

_melanogaster

the _average CV is

8%.

A

_possibility

could be that the ovariole number in nature

is less related to

_fecundity

than in the

_laboratory.

In D

simulans,

the

_variability

is much less

_(6.2%).

_Maybe

in this

_species,

a

_stronger

_relationship

exists between ovarian size and egg

production.

An

_interesting

result is the

_{heterogeneity}

of the CVs between

_populations.

Such

a result was

previously

found

by

_comparing

laboratory

mass cultures

_(David

et

al,

1978)

but in that case, no

_{interpretation}

was

provided,

since the reduction of

hypothesis

can be excluded: different natural

_{populations really}

exhibit different

levels of

_phenotypic

variance. The conclusion is enforced

_by

the fact that most

_CV

_S

_,

at least in D

_{melanogaster,}

exhibit

_{significant geographic}

_patterns

and

_especially

a

negative

correlation with latitude. In this case, a

_biological

_{interpretation}

can be

proposed.

This could be related to the average

population

size which is

likely

to be

higher

in the

_tropics

than in

_temperate

countries with a winter bottleneck.

Intraclass correlation and

_heritability

With the isofemale-line

technique,

the

genetic

variability

within a natural

popu-lation is

_approached

_by

_calculating

the coefficient of intraclass correlation t. In

most works

_using

this

_technique

_(see

_{Parsons, 1983,}

for

_references),

_{investigators}

are satisfied with

demonstrating

a

_genetic

_component

of the trait under

study.

This

work

_presents

a

_large

amount of

_{comparative data,}

which makes a

deeper

_analysis

possible.

A first

_interesting

conclusion is the

apparent

homogeneity

of the intraclass correlations in natural

_populations.

The variations observed are

mainly

due to

sampling

errors and

_especially

to the fact

_that,

in most cases,

only

10 isofemale lines were considered in each

population.

Such a result contrasts with the

_geographic

differences observed at the level of

_phenotypic

variances. In

_practice,

the within-and between-line variances are correlated in each

_population,

thus

explaining

the

lower

_variability

of t as

compared

to CV.

A second observation concerns the differences between the _average values of t

for various traits. In this

_respect

the most

_genetically

variable trait is the fresh

weight

(about 0.50)

followed

_{by wing}

_length

_{(about 0.40).}

Bristle numbers are less

variable

_{(range 0.21-0.32).}

Thorax

_length

also exhibits a low

_variability

_(0.18-0.23),

significantly

much less than

_wing

_length.

Finally,

the ovariole number also has a

low

_heritability

_{(isofemale heritability),}

_especially

in D simulans which is

_genetically

less variable than its

_sibling.

A final

_interesting

_point

is the

_{possible relationship}

between isofemale

_heritability

and usual

heritability

(narrow

sense

heritability).

In the case of D

_{melanogaster,}

numerous

experimental

data are available and were

compiled by

Roff and Mousseau

(1987).

The results are

_compared

in table

_VI,

and also include a

_wing

_{length analysis}

in D simulans.

True

_heritability

estimates are much

_higher

for bristle numbers that for

_wing

or thorax

_length.

This makes _sense,

_according

to Fisher

_(1930),

if we assume that

bristle numbers are more or less

neutral,

while thorax and

_wing

length

are more

directly

related to fitness. We

_{already pointed}

out

_that,

under some

_simplifying

assumptions

(Falconer, 1981),

2t should be

_equal

to

h

2

.

The ratios indicated in

table VI never reach such a value. We see however that for bristle

numbers,

a value

close to 1.5 is found. Also for the thorax

_length,

t is

_clearly

less than

h’.

These observations

_suggest

that for these

_traits,

_genetic

variations in natural

_populations

are

mainly

due to additive effects.

Wing

length

in both

_species

shows a

_completely

Apportionment

of total

_variability

in the 2

_species

It seemed

_interesting

to consider the results of this _paper

_together

with those of

Capy

et al

₍₁₉₉₃₎

in order to

_get

an overall view of the

_{apportionment}

of the

variability

in each

_species.

Table VII

_gives

the

_proportion

of the total

_variability

If we consider the _average values for the 6

_traits,

we see that the

_proportion

of the within-isofemale line

_variability

is much

_larger

in D simulans than in D

melanogaster

(55

versus

34%)

while the reverse situation is found for the

long-range variation between

regions

(34%

in D

_melanogaster

_against

8%

in D

_simnlans).

This

_again

illustrates the fact that D

_melanogaster

is much more diversified into

geographic

races

(see

Capy

et

al,

1993).

If we consider variations between

isofemale

lines from the same

_population

or between

_populations

of the same

_region,

the

2

_species

are

_quite

similar. Besides the

general

trend outlined

above,

differences exist

between traits. For

_example,

if we consider the 3 size-related

_traits,

the variations

between

_regions

_explain

51%

of the total variance in D

_{melanogaster,}

but

_only

8%

in D simulans.

_Thus,

the contrast between the 2

_species

is more

_pronounced

for

these traits. For bristle

numbers,

most of the variation is harbored within local

populations,

ie

90%

in D simulans and

76%

in D

_melanogaster

at the 2 first levels.

Finally,

for the ovarioles

_number,

variations are more

_evenly

distributed.

Is D

_melanogaster

more variable than D simulans ?

The

_analysis

of the

_{between-population variability}

of _{many traits} has shown that the

_geographical

_divergence

of D

_melanogaster

is

_higher

than that of D simulans

However,

the within- and the

_{between-components}

of the total variance must be considered

_together.

Indeed,

while the 2

_species

have similar amount of

_variability

at the

_{within-population level,}

_{they greatly}

differ at the

_{between-population}

level. This observation is in

_agreement

with several

analyses dealing

with other traits

(Hyytia

et

_al,

_1985;

Inoue and

_Yamamoto,

_1987;

_Singh

et

al, 1987;

Capy

et

al,

1993).

Moreover,

in few cases, D simulans appears to be more variable than D

_melanogaster

(Kawanishi

and

_Watanabe,

_1981;

_Aquadro

et

_al,

_1988;

_Begun

and

_Aquadro,

_1991).

How can we

_explain

these differences of

_variability

at the between- and

within-population

levels? Two of the

_hypotheses

_(summarized

in

_Capy

et

al,

1993)

proposed

to

_interpret

the

_geographical

differences between D

_melanogaster

and

D

_simulans,

based on

_migration

rates

_(m)

and on effective

_population

sizes

_(N

_e

_),

could

_explain

such a

_phenomenon.

Under the

_{migration-rate}

_{hypothesis, proposed}

from the

_analysis

of

_enzymatic

polymorphism

(Choudhary

and

_Singh,

_1987),

it is assumed that this rate should be 2-4-fold times lower in D

_{melanogaster.}

On the other

_hand,

under the effective

population

size

_hypothesis,

based on a lower level of nucleotidic variation in

D

_{melanogaster,}

it is

_suggested

that

_N

_e

of D simulans should be 6-fold

_higher

than that of D

_melanogaster

thus

_leading

to an increased

_purifying

selection

_(Aquadro

et

_al,

_1988).

These 2

_hypotheses

assume that the mutation rate is similar in the 2

_species.

However,

several

reports,

including

those of Dowsett and

_Young

₍₁₉₈₂₎

and Leme-unier and Aulard

_(1993),

_suggest

that this rate could be lower in D simulans.

In

_conclusion,

it seems that the different

_hypotheses

are

plausible

and not

mutually

exclusive. But due to a lack of

ecological

and

_{genetic information,}

it is

not

_possible

to choose between them

_and/or

to determine their relative

_impact

on

the

_variability

of the 2

_species.

Moreover a

_general

_comparison

of these 2

_species,

including

data from molecule to

_ecology

and to

_{biogeography,}

will be _necessary to

try

to understand how these 2

_species,

which share a recent common _ancestor, have

ACKNOWLEDGMENTS

We thank the numerous

_people

who

_helped

us

_{by providing samples}

of natural

_populations.

This work has benefited from a PIREN

_{(French CNRS)}

grant.

REFERENCES

Aquadro

CF,

Lado

_KM,

Noon WA

₍₁₉₈₈₎

The _rosy

_region

of

_Drosophila

melano-gaster

and

Drosophila

simulans. 1.

_Contrasting

levels of

_naturally

_occurring

DNA restriction _{map variation} and

_divergence.

Genetics

_119,

875-888

Begun DJ,

Aquadro

CF

₍₁₉₉₁₎

Molecular

_{population genetics}

of the distal

_portion

of the X chromosome in

_Drosophila:

evidence for

_genetic

_hitchhiking

of the

yellow-achaete

_region.

Genetics

_129,

1147-1158

Bouletreau-Merle

_J,

Allemand

_R,

Cohet

_Y,

David JR

₍₁₉₈₂₎

_Reproductive

_strategy

in

_Drosophila

_{melanogaster. significance}

of a

_genetic

divergence

between

_temperate

and

_tropical

_{populations. Oecologia}

_(Berl)

_53,

323-329

Brotherstone

_S,

Hill WG

₍₁₉₈₆₎

_{Heterogeneity}

of variance

_amongst

herds for milk

production.

Anim Prod

_42,

297-303

Bulmer MG

₍₁₉₈₅₎

The Mathematical

_{Theory of}

_Quantitative

Genetics. Clarendon

Press,

Oxford

Capy

P

₍₁₉₈₇₎

Variabilit6

_g6n6tique

des

_populations

naturelles de

_Drosophila

melanogaster

et

_Drosophila

simulans. These Universite de Paris

XI,

Orsay.

Capy

P,

Pla

_E,

David JR

₍₁₉₉₃₎

_Phenotypic

and

_genetic

_variability

of

morpho-metrical traits in natural

_populations

of

_{Drosophila melanogaster}

and D simulans.

1.

_Geographic

variations. Genet Sel Evol

25,

517-536

Choudhary

M,

Singh

RS

₍₁₉₈₇₎

A

comprehensive

study

of

_genic

variation in natural

populations

of

_Drosophila

_{melanogaster.}

III Variations in

_genetic

structure and their

causes between

_Drosophila

_melanogaster

and

_Drosophila

simulans. Genetics

_117,

697-710

David JR

₍₁₉₇₉₎

Utilization of

_{morphological}

traits for the

_analysis

of

_genetic

variability

in wild

_{populations. Aquilo}

Ser Zool

_20,

49-61

David

JR, Bocquet C,

de Scheemaeker-Louis

M,

Pla E

₍₁₉₇₈₎

Utilisation du coefficient de variation pour

l’analyse

de la variabilité de caract6res

_quantitatifs

chez

_{Drosophila melanogaster.}

_comparaison

de souches

_appartenant

a trois races

g6ographiques.

Arch Zool

Exp

Gen

_118,

481-494

David

_JR,

Cohet

_Y,

Fouillet

_P,

Arens MF

₍₁₉₈₀₎

_Phenotypic

_variability

of wild collected

_Drosophila:

an

_approach

toward

_{understanding}

selective _{pressures in}

natural

_{populations. Egypt}

J Genet

_Cytol

9,

51-66

David

_JR,

Allemand

_R,

Van

_{Herrewege J,}

Cohet Y

₍₁₉₈₃₎

_{Ecophysiology:}

abiotic factors. In: The Genetics and

_{Biology of Drosophila}

_(M

Ashburner,

HL

_Carsons,

JN

Thompson Jr,

eds).

Acad

_Press,

London Vol

_3d,

105-170

Hoffmann

_AA,

Parson PA

₍₁₉₈₈₎

The

_analysis

of

_quantitative

variation in natural

populations

with isofemale strains. Genet Sel Evol

_20,

87-98

Hyytia P,

Capy

P,

David

_JR,

_Singh

RS

₍₁₉₈₅₎

_Enzymatic

and

_quantitative

variation

in

_European

and African

_populations

of

_Drosophila

simulans.

_Heredity

_54,

209-217 Inoue

_YH,

Yamamoto MT

₍₁₉₈₇₎

Insertional DNA and

_spontaneous

mutation at

the white locus in

_Drosophila

simulans. Mol Gen Genet

209,

94-100

Jaspen

N

₍₁₉₆₅₎

The calculation of

_{probabilities corresponding}

to values of z,

t,

F and

_chi-square.

Educ

_Psychol

Measur

_25,

877-880

Kawanishi

M,

Watanabe TK

₍₁₉₈₁₎

Genes

_{affecting courtship}

song and

mating

preference

in

_{Drosophila melanogaster, Drosophila}

simulans and their

_hybrids.

Evolution 35,

1128-1133

Lemeunier

_F,

Aulard S

₍₁₉₉₃₎

Inversion

_polymorphism

in

_{Drosophila melanogaster.}

In:

Drosophila

Inversion

_Polymorphism

_(CB

Krimbas,

JR Powell

_eds).

CRC

Press,

London,

339-405

Lerner IM

₍₁₉₅₄₎

Genetic Homeostasis. John

_Wiley,

New York

Levene H

₍₁₉₆₀₎

Robust tests for

_equality

of variances. In: Contributions to

Probability

and Statistics

_(I

Olkin,

ed)

Stanford Univ

_Press,

278-292

Lewontin RC

₍₁₉₇₄₎

The Genetic Basis

_{of Evolutionary Change.}

Columbia Univ Press

Parson PA

₍₁₉₈₃₎

The

_Evolutionary

_Biology

_{of Colonizing Species.}

Camb Univ Press Roff

DA,

Mousseau TA

₍₁₉₈₇₎

_Quantitative

_genetics

and fitness: lessons from

Drosophila. Heredity

58,

103-118

Shrimpton

A,

Robertson A

₍₁₉₈₈₎

The isolation of

_polygenic

factors

_controlling

bristle score in

_{Drosophila melanogaster.}

II. Distribution of the third chromosome

bristle effects within chromosome sections. Genetics

_118,

445-459

Singh

RS,

Choudhary

M,

David JR

₍₁₉₈₇₎

_Contrasting

_patterns

of

_geographic

vari-ation in the

_cosmopolitan

_sibling

_species

_Drosophila

_melanogaster

and D simulans. Biochem Genet

25,

27-40

Suh

DS,

Mukai T

₍₁₉₉₁₎

The

_genetic

structure of natural

_populations

of

_Drosophila

melanogaster.

XXIV. Effects of

_{hybrid dysgenesis}

on the

_components

of

_genetic

variance of

_viability.

Genetics

_127,

545-552

Thoday

JM

₍₁₉₆₁₎

The location

_{of polygene.}

Nature

_191,

368-370