Reaction norms of size characters in relation to growth temperature in Drosophila melanogaster: an isofemale lines analysis

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Reaction norms of size characters in relation to growth

temperature in Drosophila melanogaster: an isofemale

lines analysis

Jr David, B Moreteau, Jp Gauthier, G Pétavy, A Stockel, Ag Imasheva

To cite this version:

Original

article

Reaction

norms

of size characters

in

relation

to

_growth

_temperature

in

_{Drosophila melanogaster:}

an

isofemale

lines

analysis

JR David

B

Moreteau

JP Gauthier

G

_Pétavy

₁

A Stockel

2

AG

Imasheva

3

1

CNRS,

Laboratoire de

_Biologie

et

_Génétique

Évolutives,

91198

_{Gif sur-Yvette Cede!;}

2

INRA,

Station de

_{Zoologie Agricole, 33140 Pont-de-la-Maye,}

!’a7ice;

3

Vavilov Institute

_of

General

_Genetics,

3 Gubkin

_Street,

117809

Moscow,

Russia

(Received

7 June 1993 ;

accepted

21 December

₁₉₉₃₎

Summary - Ten isofemale lines of

_{Drosophila melanogaster, recently}

collected in a French

vineyard,

were submitted to 7 different

_{developmental}

_{temperatures,} from 12 to

_31°C,

encompassing

the whole

_{physiological}

range of the species. For each line and _temperature, 10 flies of each sex were collected

_randomly

and 2 size-related traits were measured:

_wing

and thorax

_length.

Both traits exhibited similar response curves: a maximum size at a low temperature and a decrease on both sides. ANOVA showed

_significant

variations between lines and also

_{significant line-temperature interactions, demonstrating}

different

norms of reaction among the various lines. The

shapes

of the curves were further

_analysed

by considering slope variations,

ie

_{by calculating empirical}

derivative curves. The most

interesting

observation is that the temperature of maximum size

_(TMS)

is not the same

for the

_wing

_(average

15.73 !

_0.29°C)

and the thorax

_(average

19.57 !

_0.47°C).

Genetic differences seem to exist between

lines,

and TMS for both traits are correlated. Sexual

dimorphism

was

_{analysed by considering}

the

_female/male

ratio for

_wing

and thorax. Both traits

_provided

the same information: sexual

dimorphism increased,

from 1.10 to _1.16, with

increasing

temperature, and

significant

differences were found between lines.

Finally

the

wing/thorax

ratio

_appeared

as an

_original

and most

interesting

trait. This ratio, which is less variable than

_wing

or

_thorax,

exhibited a

_{monotonously decreasing sigmoid shape,}

from 2.80 to 2.40, with

increasing

temperature. It is

_suggested

that this

ratio,

which may be related to

_{flight capacity}

at various _{temperatures,} could be the direct _target of natural selection.

reaction norm

_/

_{wing length}

_/

thorax length

/

developmental temperature

/

sex

Résumé - Normes de réaction de caractères de taille chez _{Drosophila melanogaster} en

fonction de la _température de développement : une _analyse de _lignées isofemelles.

Dix

_{lignées isofemelles}

de

_{Drosophila melanogaster,}

récemment récoltées dans un

_vignoble

français

du sud-ouest de la

_France,

ont été soumises à 7

_{températures différentes}

_(de

12 à

_!1°C)

compatibles

avec le

_{développement}

de

_l’espèce.

Pour

_{chaque Lignée}

et

_chaque

température,

10 mouches de

_chaque

sexe ont été choisies au hasard. Sur

_{chaque individu,}

2 caractères

_relatifs

à la taille ont été mesurés : la

_longueur

de l’aile et la

_longueur

du thorax. Les courbes de

_réponse

des 2 caractères ont la même

_forme

et mettent en évidence une taille maximum en dessous de 20°C et une décroissance de _part et d’autre de ce maximum. Des variations

_{significatives}

entre les

_lignées

de même que des interactions

significatives lignée-température

sont mises en évidence _par

ANOVA,

ce _{qui montre que} les normes de réaction des

différentes lignées

ont des

_{formes différentes. L’analyse}

de la

forme

des courbes a été réalisée en considérant les variations des pentes pour

chaque

intervalle

de

température,

c’est-à-dire en calculant _{empiriquement} une dérivée. L’observation

la plus

remarquable

concerne la

_température

_pour

_laquelle

la taille est maximale:

15, 73 ±

0, 29°C

pour l’aile et

19, 57

f

0, 47°C

pour le thorax. Des

différences génétiques

entre les

lignées

sont mises en évidence _{pour cette}

_température

de taille _maximum, et les valeurs obtenues pour les 2 caractères sont corrélées. Le rapport

femelle-mâle

pour l’aile ou le thorax _permet

d’étudier le

dimorphisme

sexuel. Le _{rapport augmente} de

1,10

à

1,16

quand

la

température

passe de 12 à 31° C. Il existe aussi des

différences significatives

entre les

Lignées.

Il est

montré que le rapport aile-thorax est un critère

_original

et d’un

_grand

intérêt. Ce rapport

est relativement moins variable _que l’aile ou le thorax. Il décroît selon une

_sigmoïde

à

mesure _que la

_température

_augmente et varie de

_2,80

à

_2,40.

Vraisemblablement en relation

avec la

_capacité

de vol en

_fonction

de la

_{température,}

le _rapport aile-thorax _pourrait être

la cible directe de la sélection naturelle.

normes de réaction

/

_longueur de l’aile et du thorax

_/

_température de développe-ment

_/

_dimorphisme

_{sexuel / rapport}

aile-thorax

_/

capacité de vol

INTRODUCTION

For ectothermic

_organisms,

like

_Drosophila,

_temperature

is the most

_important

abiotic factor for

_explaining

the

geographic

distribution and abundance of

_species

(David

et

_al,

_{1983; Parsons, 1983;}

Hoffmann and

Parsons,

1991).

Among

more

than 20

_species

that now exhibit a

_cosmopolitan

_status,

_only

2

_(D

_melanogaster

and D

_simulans)

were able to

_adapt

to different climates and

_proliferate

both in

temperate

and

_{tropical regions}

_(David

and

_Tsacas,

_1981).

Various

_species,

_including

D

_subobscura,

D

_robusta,

D

_melanogaster

and D simulans

_(see

David et

al, 1983;

Capy

et

_al,

_1993),

exhibit

_genetic

latitudinal clines for their

_size,

and flies are

larger

at

_higher

latitudes. Also

_laboratory

_experiments

made on D

_{pseudoobscura}

(Anderson, 1966),

D willistoni

_{(Powell, 1974)}

and more

_recently

on D

_melanogaster

(Cavicchi

et

_al,

₁₉₈₅₎

have described a

genetically

determined increase in size

by

The

_problem

becomes still more

_complicated

if we consider that size also exhibits a broad

_{phenotypic plasticity}

_which,

in natural

_populations,

is

_expressed

_by

a

_high

value of the standard deviation or the coefficient of variation of size characters

(Atkinson,

1979;

David et

_{al, 1980;}

_Coyne

and

_Beecham,

_1987).

Two kinds of environmental factors control adult size

_{during development:}

larval nutrition and

_temperature.

_Among

individuals collected at the same

_time,

size differences are

mainly

due to nutritional

effects,

although

some

_temperature

variations _may also occur. Thermal

_effects,

on the other

_hand,

are more

_important

when different seasons are

_compared

_{(Atkinson, 1979).}

Natural size variations _may be heritable

_(Coyne

and

_Beecham,

_1987).

On the

other

_hand,

a

_positive

correlation seems to exist between size and fitness in wild

living

males

_(Partridge

et

_al,

₁₉₈₇₎

or females

_{(Boul6treau, 1978).}

How a natural

population keeps

a stable size

presumably

implies

trade-offs between fitness

_traits,

but the

_precise

mechanisms remain unknown.

From an

_{ecophysiological}

_point

of

_view,

the _response curves of size characters

(weight,

lengths

of various

_body

_parts)

are

_broadly

known

(see

David et

_al,

1983)

and,

when

_{plotted against}

_temperature

on the X

_axis,

exhibit the

_shape

of an inverted U.

_Many

points

however remain

insufficiently analysed

and deserve

further

_study.

_First,

is there a

_genetic

_variability

not for size

itself,

but for the

shape

of the curve, ie for what is now called the norm of reaction?

Second,

are there different norms between various

_{morphological}

traits which are all related

to size?

_Third,

how can we

_interpret

the norms of reaction in an

evolutionary

perspective ?

More

_precisely,

which traits are

_specifically

related to natural selection

and

adaptation,

and which can be considered as

_contingent,

ie related to internal

genetic

constraints ?

In the

_present

_paper, variations of 2 size characters

_(wing

and

_thorax)

have been considered in relation to

_growth

_temperature.

Genetic variations of the norms of reaction were

analysed

_by

_comparing

10 isofemale lines. The norms of reactions of

_wing

and

_{thorax, although similar,}

are not

_identical,

and

_especially

the

_temperatures

of maximum size are different.

Moreover,

these

parameters

exhibit

_genetic

variations which are correlated for

_wing

and thorax. The

_adaptive

significance

of the

_shape

of the response curves is not

_obvious,

_although

the

wing/thorax

ratio could be more

_interesting

in this

_respect.

The norm of reaction of this trait is more

_simple

since we found a

_{regularly decreasing}

curve with

_increasing

temperature.

We

_suggest

that this

_ratio,

or some other related

_parameter,

could be the immediate

_target

of natural

_selection,

in relation to the

_flight

capacity

at

different

_{temperatures.}

MATERIALS AND METHODS

Flies from a wild

_{living vineyard}

_population

were collected with banana

_traps

in the

Grande Ferrade

estate,

in

_{Pont-de-la-Maye,}

near Bordeaux. About 20 females were

isolated in culture vials

_(cornmeal

medium with live

_yeast)

and

_produced

a first

laboratory

generation, Gl,

grown at 25°C. Ten lines were then

_randomly

chosen

to

_produce

the

_experimental

flies. For

_this,

10 females and 10 males from each G1 1

transferred at 1 of the 7

experimental

constant

_{temperatures,}

ie

_{12, 14, 17, 21, 25,}

28 and 31°C. With this

_procedure

larval

_density

was not

_{strictly controlled,}

and the number of adults

_emerging

from a vial

generally ranged

between 100 and 200. This is a

_{fairly high density.}

On the other

_hand,

the use of a _very rich medium for the

development prevented

significant crowding

effects which often result in a decrease

in

_fly

size.

For each

_temperature

and

line,

we used

only

a

single

culture vial. A

long

experience

with the

_technique

has shown that variations due to vial differences

(ie

common environment

_effects)

are

_negligible.

On the other

_hand,

the occurrence

of such effects would increase the error variation and make

_genetic

differences

(eg,

between

_lines)

more difficult to demonstrate.

From each line at each

_temperature,

10 females and 10 males were

_randomly

chosen and studied. On each

_fly

2 traits were measured with an ocular micrometer in a binocular

_{microscope: wing}

_length

with a 25 x

_{magnification}

and thorax

_length

with a 50 x

_{magnification.}

In the Results section

_lengths

are

expressed

in hundreths

of _mm, ie micrometer units were

_multiplied

_by

2 for the thorax and

_by

4 for the

wing.

Thorax

_length

was measured on a left side

_view,

from the anterior

_margin

at the

neck level to the

_tip

of the scutellum. For

_wing

_length

a

_difficulty

exists in

_defining

the anterior basis of the

_wing.

We used the middle

part

of the thoracic

coast,

in front of the

_tegula,

since we found it easier to

_identify

this

_point

with _accuracy on a lateral view. For the

posterior

part

we used the

tip

of the

_wing

at the end of the third

_longitudinal

vein.

Statistical

_analyses,

and

_{especially analysis}

of variance

_(ANOVA),

were done

with SAS

_(SAS

Institute

_Inc,

_1985).

_Temperature,

lines and sex were considered as

fixed effects.

RESULTS

We will first consider

_wing

and thorax

_length,

and in a second

_section,

the

wing/thorax

ratio,

which

_appeared

to be an

_original

and

interesting

trait. The illustrations deal either with

_lengths

or with the ratio. In the

tables, however,

we often include simultaneous

_{analyses concerning}

_wing,

thorax and

_ratio,

in order to

save _space. Data included in the tables but

_concerning

the ratio is discussed in the second section.

Wing

and thorax

_length

Average

response curves

The _{average response} curves are shown in

_figure

1. Female and male curves are

separated, showing

the well-known fact that males are smaller than females. The norms of reaction of the 2 traits have

_quite

similar

_shapes,

_confirming

_previous

results

_(David

et

_al,

_1983).

A maximum size is observed at a

_fairly

low

_temperature,

around 15°C for the

_wing

and 19°C for the thorax. A

_significant

decrease is observed

Sources of variation

The data shown in

_figure

1 were submitted to

_ANOVA,

in order to

_identify

the

significant

sources of

_variation,

and the results are

_given

in table I. The main

variations are due to sex and

_temperature.

A

highly significant

line effect due to

genetic

differences is also observed. All the double interactions are

highly significant,

while the

_triple

interaction is not. The line x

_temperature

interaction means that the norms of reaction of the various lines are not

parallel

and exhibit different

shapes.

The sex x line interaction means that there is some sexual

_dimorphism

in the norms of reaction.

Within-line

_variability

This

_variability

deserves further attention. We _may ask 2 related

_questions:

does

variability change

with

_temperature,

and are some lines more variable than others? In this

_analysis,

we have considered 2

_parameters,

the standard deviation and the

CV

_(coefficient

of

_variation),

and the results are shown in

_figure

2.

Standard deviations are much

_higher

for the

_wing

than for the thorax. For the

wing,

a decrease in the standard deviation is observed with

_increasing

_temperature,

as well as a lower value in males. Some of these differences may be due to the

fact that the

_wing

is about 2.5 times

_longer

than the

_thorax,

and that males are smaller than females. To avoid this

_scaling

effect,

we used a relative

measurement,

the CV. Of course, each CV was calculated on a _group of 10 flies

(same

line and

temperature)

so that the total number of observations is 140 for 1400 individuals.

and is also similar for both traits. These data were submited to ANOVA

_{(table II)}

and the conclusion was

significant

effects for

_temperature

in both

_traits,

while line

differences

_(p

=

0.011)

and _sex

(p

=

0.016)

were

_{significant only}

for the thorax. None of the interactions were

significant. Concerning

the

_temperature

effect

(see

figure

11

_below)

we note a relative

_stability

of the CV at intermediate

_temperatures

and an increase at extreme

_{temperatures,}

_especially

at 12 and 31°C.

Between-line variability

and intraclass correlations

Variation between lines is illustrated in

_figure

3. The

_significant

line x

_temperature

interaction is visualized on the

_{graph by}

the intercrosses of the lines.

For each

temperature,

the between-line variance was

calculated,

and also the coefficient of intraclass correlation which estimates an ’isofemale line

_{heritability’}

(Hoffmann

and

_Parsons,

_1988).

Results are shown

graphically

in

figure

4 and

analysed

with ANOVA in table III.

For

_wing

_length,

no effects are

significant,

and the mean values are 0.58 ! 0.03 and 0.51 ih 0.03 for females and

_males,

_{respectively.}

The

_picture

is different for the thorax: males have

_{significantly}

lower values than females

_{(0.30 !}

0.04

_against

0.37 t

_0.04)

and variations occur

_according

to

_temperature

_(see

_figure

_4).

More

precisely,

intraclass correlation is

_higher

at

_high

_temperatures

_(25-31°C)

than at

low

_temperatures

_(12-21°C).

A last conclusion is that the overall

_{genetic variability}

Between-sex correlation and sex

dimorphism

Previous

_analyses

have

_already

evidenced numerous sex differences and sex inter-actions with other factors. In this section we consider correlations between sexes at

the same

_temperature,

and also the

female/male

ratio.

Male-female correlations can

_only

be

_{analysed by considering}

the mean values of each line. The results are shown in table IV. The average correlation is

_higher

for the

_wing

_(0.91)

than for the thorax

_(0.76).

This is

_significant

if we consider the

average difference over

_temperatures

(d

= 0.144 t

0.054,

_{t =}

2.66,

_n =

7).

Sexual

_differences,

for each line and each

_temperature,

were examined

_by

calculating

the

_female/male

ratio. Results of ANOVA are

_given

in table V. For both

traits,

temperature

and line effects are

significant.

Heritable variations occurred between lines. The

_temperature

effects are shown in

_figure

5. Both traits show the same

_pattern:

the

_female/male

ratio decreases

_regularly

from

_high

temperatures

(1.16)

to low

temperatures

(1.10).

The 2 sexes are more similar when _{grown at} low

temperature.

Finally,

the

relationship

between the sexual

dimorphism

of

_wing

and thorax was

investigated by calculating

the correlation at each

_temperature.

The mean value

for the 7

_temperatures

_(r

= 0.67 !

0.07)

is

clearly

_positive

and

significant:

sexual

Shape

of the norms of reaction: variation of the

_slope

and derivative curves

For each isofemale

_line,

the size variation for a

_given

_temperature

interval allows the calculation of a

slope

(ie

size variation for one

_degree

_change)

if we

_accept

a linear

_{intrapolation.}

When this

_operation

is

_repeated

over successive

_temperature

intervals,

we

_get

an

empirical

derivative of the norm of reaction.

_Examples

of such curves are

_given,

for females

_only,

in

_figure

6. For both

_traits,

the

_slope

is

monotonously

decreasing

from

_positive

to

_negative

values. The

_point

where the curve crosses the zero line indicates the

_temperature

of maximum size

_(TMS).

As seen in

_figure

_6,

some variations exist for the same trait between

_lines,

but there is no

Statistical

_analyses

are

presented

in table VI.

Significant

effects are due to

temperature

and sex, but not to lines. On the other

hand,

a

significant

line x

temperature

interaction is

_observed,

which means that the derivative curves of the various lines have different

_shapes.

Figure

6 shows that variation in

_slope

is much

_greater

for

_wing

than thorax

(notice

that the ordinate scales are not the same on the 2

graphs).

However,

as with the standard

_deviation,

this _may be due to a

_scaling

effect related to the

comparable,

and the main difference seems to be a translation of the thorax curves

to the

_right,

ie toward

_higher

temperatures.

A difference also exists between _sexes,

the female curves are also to the

_right

of the male curves.

Temperature

of maximum size

_(TMS)

As indicated in

_figure

_6,

the

_temperature

at which the derivative is zero

_corresponds

to the maximum size of the trait. For each

line,

the TMS was calculated

by

_assuming

a linear variation of the derivative between the lowest

_temperature

and the 17-21°C interval for the

wing,

the 21-25°C interval for the thorax. More

_precisely,

if we consider the average curves of

_figure

7,

3

_points

were used to calculate the TMS of

Variations of the TMS are shown in

_figure

_8,

and mean values are

_given

in table VII.

_{ANOVA, applied}

to these

_data,

demonstrated

_significant

effects of

_traits,

sex and lines.

The left-hand

_graph

of

_figure

8 illustrates the

_large

difference between the 2

_traits,

with no

_overlap

between the distributions.

_Moreover,

the

_positive

correlation between sexes of the same line

_suggests

a

_genetic

basis. A better characterization

of each line is obtained

_{by averaging}

the TMS of both _sexes, as done in

_figure

8

some lines exhibit a maximum size at a low

_temperature

(around

14°C for the

_wing

and 17°C for

_thorax);

others a maximum size at

_higher

_temperatures

_(17°C

for the

wing

and 21°C for the

_thorax).

Covariation of

_wing

and

_thorax;

the

_wing/thorax

ratio

In the

_{previous section,}

the

_relationship

between

_wing

and thorax

_variability

was

already

considered in some cases, for

example,

for sexual

_dimorphism

and TMS. In this

section,

we extend this

investigation

by considering

the

_wing/thorax

correlation and the

_wing/thorax

ratio.

The

_wing/thorax

correlation

The

_wing/thorax

correlation _may be

_investigated

at the individual level

_(the

10 flies measured in each line and each

_temperature)

or the line level

(the

10 lines at each

are

_quite

stable over

_temperature.

At the

_individual,

within-line

level,

the values do

not vary

significantly according

to

_temperature:

_{the average}

_phenotypic

correlations are 0.71 for the females and 0.76 for males. In an extensive

study,

Scheiner et al

₍₁₉₉₁₎

found values at 19 and 25°C somehow

_higher

_{(average 0.82).}

Genetic

correlations found

_by

Scheiner et al

₍₁₉₉₁₎

were a little lower

(0.73

for

females)

in

close

agreement

with the between-line correlations we found in the

_present

_study

(table VIII).

The

_wing/thorax

ratio: mean values

During

the

_development

of our

_{investigations,}

it turned out that the covariation

of the

_wing

and thorax could be

_investigated

in an

_interesting

_way:

by calculating

the

_wing/thorax

ratio. This

_trait,

as well as the

length,

varies

according

to sex,

Variations are shown

graphically

either at the line

_level,

or

_{by considering}

the

average values of each sex

(fig 9).

The ratio exhibits a monotonic decrease from low

_temperatures

_(about

_2.8)

to

high

temperatures

(about 2.4).

Interestingly,

male and female values are _very

_close,

The

_wing/thorax

ratio:

_slopes

and derivative curves

For each line and

_temperature

interval the

slope

was calculated. As an

_example,

the female values are shown for the 10 lines in

_figure

10.

_Large

variations exist

between lines. With one

_exception,

all values are

_{negative, indicating}

that the ratio decreases with

_increasing

_temperature.

In

_spite

of the broad

dispersal

it is

_possible

to conclude that the

_slope

varies

_according

to

_temperature

_(ANOVA,

table

_VI).

This is also illustrated

_by

_considering

the confidence intervals of the mean values in

figure

10. For

_example,

_{the average}

_slope

between 17 and 21°C

_{(—0.03)}

is much less than between 28 and 31°C

_(-0.01).

Such variations of the derivatives demonstrate that the decrease of the

_wing/thorax

ratio,

illustrated in

_figure

_9,

is not a linear function of

_temperature,

but a

_{decreasing sigmoid.}

Within-line

_variability

of the

_wing/thorax

ratio

As for the

_lengths,

the

_variability

of the ratio was

_investigated

_by

_considering

a relative

measurement,

the coefficient of variation. Results of ANOVA

_(table

_II)

demonstrated _very

_significant

effects of

_temperature

and lines but no difference between sexes.

Interestingly,

_genetic

differences between lines are much more

pronounced

for the ratio than for the traits themselves. The

_temperature

effect is illustrated in

_figure

11,

and

_compared

to the CV of

_wing

and thorax. The overall

shapes

are similar and

_correspond

to

_U-shaped

curves.

_Variability

is minimum at

averages about

1.2%,

while it is around

1.8%

for the

wing

or thorax

length.

Such a reduction of the relative

variability

of the ratio is a _consequence of the

_positive

correlation

_existing

between

_wing

and thorax

_{(table VII).}

Between-line

_variability:

intraclass correlation

The values of the coefficients of intraclass correlation for the

_wing/thorax

ratio are

given

in table IX. Thera are no

_significant

variations between sexes or

_{temperatures.}

The overall mean, calculated on 14

observations,

is 0.52 ! 0.02. The isofemale line

DISCUSSION

As

_pointed

out in the

Introduction,

numerous observations and

_{arguments suggest}

that size variations are

_strongly

related to fitness and that size is a

_regular

_target

of natural selection. On the other

_hand,

the overall size is a difficult

_entity

to

define since measurements deal

_only

with size-related traits.

_Wing

and thorax

_length

and adult

_weight

are the most

_generally

used traits

_(Capy

et

_al,

₁₉₉₃₎

but other dimensions have also been considered in the

_literature,

such as head width or the

lengths

of various

_parts

of the

_legs.

As far as we know

(David

et

al,

1983),

all

these traits exhibit similar convex _response curves to

_growth

_temperature,

with a maximum below 20°C and a decline on both sides. A maximum size is often

referred to as an

’optimum’

(Gabriel

and

Lynch,

1992)

but this must be considered

cautiously

(see

David et

_al,

_1983).

In the

_present

_work,

we demonstrated that

temperatures

of maximum

_length

for

_wing

and thorax are

clearly

separated,

thus

making

the

_argument

of an

_optimum

size still more difficult.

In the

_{Drosophila literature,}

_{many papers} have dealt with the

_genetic

architec-ture and

_heritability

of

_wing

or thorax

length

(reviewed

in Roff and

_Mousseau,

1987).

The isofemale line

_technique

also

_provides

an

_opportunity

to estimate the

intrapopulation variability

with the coefficient of intraclass correlation

_(Hoffmann

and

_Parsons,

_1988).

We have found that this ’isofemale line

_{heritability’}

is

_higher

for

_wing

than

_thorax,

thus

_confirming

extensive data on numerous

_geographic

pop-ulations

_(Capy

et

al,

1994).

More

_interesting

is the fact

_that,

for the thorax

_only,

this

_heritability

seems to _vary

_according

to the

_environment,

_{being higher}

at

_high

temperatures.

As

_pointed

out several times

_(De

_Jong,

_1990;

Falconer, 1990;

Scheiner and

Lyman, 1989, 1991; Scheiner,

1993),

phenotypic plasticity

may be considered as a

specific trait,

independent

of the mean. Most

_empirical

and theoretical

_analyses

have considered

_only

linear variations evaluated

_{by considering}

2 environments. For

example,

Scheiner and

_Lyman

_{(1989, 1991)}

studied thorax

_length

at 19 and 25°C

and found that the

_heritability

of

_plasticity

was much less than that of thorax

length.

In a recent _paper, Gavrilets and Scheiner

₍₁₉₉₃₎

have

_suggested

a model for

_{investigating}

nonlinear _norms, and indicated the need for

_empirical,

extensive

data.

Wing

and thorax

_changes

are

_obviously

nonlinear when studied over a broad

range of

temperatures.

Such was also the case for

pigmentation

(David

et

_al,

_1989).

Presumably,

most

_{morphometrical}

traits exhibit nonlinear norms, thus

complicating

mathematical

_analyses

and theoretical

_{interpretations.}

In the

_present

_work,

we

as has been done

previously

for

_pigmentation

(David

et

al,

1989).

This

technique

is most convenient for

_comparing

different traits. In this

_study,

it enabled a

_precise

calculation,

for each

_trait,

of the TMS. The facts that for each

_trait,

the male and female TMS are correlated and also

_that,

_among

_lines,

the thorax and

_wing

TMS are also

_correlated,

are

_{strong arguments}

for

_assuming

a

_genetic

basis to these variations. Some lines have a maximum size at lower

temperature,

others at

_higher

temperature:

TMS itself is a trait which could be selected with the isofemale line

technique

as

_already

used

by

Scheiner and

Lyman

(1991).

In

_Drosophila,

as in most insect

_species,

females are known to be

_bigger

than

males,

although

their

_development

is faster

_(David

et

_al,

_1983).

We estimated the sexual

_{dimorphism by}

_calculating,

for each

_trait,

the

_female/male

ratio. Our

_data,

based on the mean values of isofemale

_lines,

led to several

_interesting

conclusions.

First, wing

and thorax

_lengths

_provide

about the same information on

_dimorphism.

Second,

sexual

_dimorphism

increases with

_growth

temperature,

from a low 1.10 at

12°C to a

_high

1.16 at 28-31°C.

_{Third, genetic}

variations exist between lines so

that sexual

_dimorphism

could also be selected.

Another

_ratio,

which turned out to be _very

_interesting,

is the

_wing/thorax

_ratio,

calculated either at the individual or line levels. The

significance

of this ratio for biometrical studies was

_{already pointed}

out in recent _papers on D buzzatii

(Robertson,

1987; Thomas,

1993).

Since,

at the individual

_{level, wing}

and thorax are correlated

_(r

is about

_0.70),

the ratio is less variable than the traits themselves.

Comparing

the

_variability

of various traits

_having

different means needs a relative

measurement,

ie the coefficient of variation

_(CV).

Relative variabilities of

_wing

and

thorax are low and similar with an _average value of

1.8%

at medium

_{temperatures.}

An increase which is found at extreme

_(low

or

high)

_temperatures

_may be considered as an increase of the

_{developmental}

noise under stressful conditions.

_Indeed,

a low relative

_variability

may be considered as an indication of a

_{physiological optimum}

(see

David et

_{al, 1983,}

for

_discussion).

A

_{long-standing}

_argument

is that fitness-related traits should exhibit a low

_variability

due to

_genetic

homeostasis

_(Lerner,

1954)

and

_{developmental}

canalization

_{(Waddington, 1957).}

The fact that the ratio is still less variable

_(1.2%)

than the traits themselves is

_{mathematically}

due to

the

_significant

correlation

existing

between the 2 traits. On the other

hand,

the occurrence and

_persistence

of this correlation in

laboratory

grown flies may be

interpreted

as a _consequence of an internal constraint. This constraint could itself be an indication of a

relationship

between fitness and the

wing/thorax

ratio. Another

argument

is the overall

_shape

of the reaction norm, ie a

_decreasing

_sigmoid

curve. In this

respect,

there is a clear

_analogy

with the abdominal

pigmentation

of the last 3

_segments

_(David

et.

_al,

₁₉₈₉₎

for which an

_{adaptive significance,}

related to

the thermal

_budget,

is

_likely.

For the

_wing/thorax

_ratio,

a

possible

direct

adaptive

significance,

related to the

_flight

_capacity,

_may be

_proposed

_(P6tavy

et

_al,

_1992).

For a

_given

_fly,

the

_wing

beat

_frequency

increases with

_increasing

ambient

_temperature

(Reed

et

_al,

₁₉₄₂₎

_presumably

due to a better muscle

_efficiency.

On the other

_hand,

a

_{higher beating frequency}

should allow an increase of the

_wing

_loading,

ie the

weight

per surface unit of the

wing.

In

_preliminary

_experiments,

we measured the

wing

loading

of males _grown at 3

temperatures,

ie

_12,

21 and 30°C: _average

_wing

increase from 195 to 247 Hz was observed with

growth

_temperature,

_parallel

to the

morphological

increase of the

_wing

_loading.

Further more extensive studies are on the _way. These

_preliminary

data

suggest

that the

_{morphological}

variations related

to

_growth

temperature

are an

_adaptation

to

_flying

in a cold

_environment,

with a lesser muscular

_efficiency

and thus a decreased

_wing

_loading.

We also found that the

_wing/thorax

ratio is

_strongly

correlated to

_wing

_{loading. Interestingly,}

a similar decrease of the ratio with

_growth

_temperature

has also been described in D buzzatii

(Thomas,

1993).

This could be a

_general

feature in

_Drosophila.

A last

_problem,

which has been discussed several

_times,

is the

_relationship

be-tween

_plasticity

and natural selection

_(David

et

_{al, 1983;}

_Schlichting,

1986; Sultan,

1987;

De

_Jong,

_1989;

Gabriel and

_Lynch,

_1992;

Gavrilets and

_Scheiner,

_1993).

Under the

adaptive

hypothesis,

we should make 2

_{predictions. First,}

_phenotypic

plasticity

itself could be selected for in

_populations

and

_species

_living

in a variable

environment,

for

_example,

_{Drosophila populations}

in

_temperate

countries which

ex-perience

big

and

_predictable

seasonal thermal variations. On the other

_hand,

for

populations living

in the thermal

_stability

of

_tropical

_countries,

_plasticity

should be a

_contingent

_property

without a direct

relationship

to fitness. A second

prediction

is

_that,

if the

_change

in the mean

_phenotype

is

_adaptive

_(eg,

smaller flies in a warm

environment)

we should find a

_genetic

modification when the environment is stable

for many

generations.

We

_already

know that

_prolonged

culture at a

_higher

tem-perature

resulted in a decrease in size

_(Cavicchi

et

al,

1985)

and also that

_tropical

populations

of D

_melanogaster

have

a smaller size

(David

and

_Capy,

1988).

We now _argue that the

_wing/thorax

ratio

_(or

some related

_measurement)

could be the direct

target

of natural selection. If such is the case, a lower ratio should be found in

_tropical

_populations.

ACNOWLEDGMENTS

We thank S Scheiner and L

_Zhivotovsky

for

_helpful

comments on the _manuscript. This work benefited from a _grant from the Minist6re de I’Environnement

_(EGPN)

to JR David.

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