Starvation and desiccation tolerance in Drosophila melanogaster: differences between European, North African and Afrotropical populations

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Starvation and desiccation tolerance in Drosophila

melanogaster: differences between European, North

African and Afrotropical populations

Jl da Lage, P Capy, Jr David

To cite this version:

Original

article

Starvation and desiccation tolerance

in

_{Drosophila melanogaster:}

differences

between

_European,

North African and

_Afrotropical

_populations

JL

Da

_Lage

P

_Capy

JR David

CNRS,

Laboratoire de _Biologie et

_Génétique

_Evolutives,

’

91198 _{Cif sur-Yvette Cedex,} !1-ance

(Received

5 January 1990; accepted 13 July

1990)

Summary - Starvation tolerance

_(mean

survival time with water

_only)

and desiccation tolerance

_(mean

survival with no food and zero %

humidity)

were measured at 17°C in adult flies from 3 different _{geographic populations living} in different climates. A

fairly

large uncontrolled

_variability

was observed and two successive

_generations

of the various isofemale lines were

_investigated

for each _population. For desiccation _tolerance, a Tunisian population from an oasis was found to be more tolerant than French or

_Congolian

populations. For starvation _tolerance, the survival of the

_Congolian

population was about

twice the values found for French or Tunisian flies. It is _suggested that the Afrotropical

flies which live in a _hot, humid environment, are _{poorly protected against} desiccation but need a

_high

starvation tolerance because of their

_high

metabolic rate due to the

_high

ambient temperature.

Drosophila melanogaster / geographic race _{/ ecological genetics /} environmental

stress

Résumé — Tolérance à l’inanition et à la dessiccation chez _{Drosophila melanogaster :}

différences entre _{populations d’Europe, d’Afrique} du Nord et _d’Afrique tropicale. La tolérance à l’inanition

_(durée

de survie en _présence seulement

d’eau)

et la tolérance à la dessiccation

_(durée

de survie sans nourriture en _atmosphét!e

_sèche)

ont été étudiées à 170 C sur des mouches adultes _provenant de

_{9 régions}

_{géographiques.} Une assez

forte

variabilité non contrôlée a été observée et 2 _{générations} successives ont été étudiées pour les diverses

lignées isofemelles de _{chaque population.} Pour la tolérance à la dessiccation, la _population

tunisienne _provenant d’une oasis a été trouvée plus tolérante _que les populations de France ou du

Congo.

Pour la résistance à l’inanition, la _population du

_Congo

est environ _{2 fois}

plus tolérante que les populations de France ou de Tunisie. Il est _proposé que les populations

d’Afrique tropicale, qui vivent dans un environnement chaud et

humide,

_{sont peu protégées} contre la dessiccation mais _qu’elles ont besoin d’une

_forte

résistance à _{l’inanition,} compte

tenu du

_fait

_que la chaleur ambiante leur _impose un métabolisme élevé.

Drosophile / race _{géographique / génétique écologique /} stress dû à l’environnement

*

INTRODUCTION

During

the last

decade,

attention has been drawn to the

_possible

_significance

of abiotic environmental stress for the

_{evolutionary biology}

of

_Drosophila

_species

(David

et

_al,

_{1983; Parsons, 1983,}

_1987).

Climatic environmental stress differs

considerably

according

to

_geographic

_parameters and

_significant

variations between

populations

are more

_likely

to be found in

_species

with a broad

geographic

_range. In this _respect, D

_{melanogaster,}

which

_proliferates

both in _temperate and

_tropical

countries

_(David

and

Tsacas, 1981;

David and

_Capy,

₁₉₈₈₎

has become an excellent

model for

_checking

local

_adaptations.

Drosophila

adults are

_{poorly protected against}

desiccation

(David

et

_al,

₁₉₈₃₎

and the water balance is maintained

_by

water

_ingestion

_(Fairbanks

and

_Burch,

_1970;

Arlian and

_Eckstrand,

_1975).

In addition the

_availability

of resources is variable among localities and seasons, and the

demography

principally

depends

on two

parameters, ie resources and favorable temperature

(David

et

_{al, 1983;}

David et

al, 1984).

Variations in desiccation tolerance have been

_{mainly investigated}

in Australian natural

_populations

_(Parsons,

_1980;

_Stanley

and

Parsons, 1981; Davidson, 1988,

1989).

Temperate

populations

were found to be more resistant to desiccation

stress than

populations

from

_{subtropical regions,}

in _agreement with what could be

_expected

from consideration of local climates. Recent

_{investigations}

_(Hoffman

and

_Parsons,

_1989a,b)

have

_suggested

that tolerance to different stress could be mediated

_by

the same basic

_{physiological}

_process,

_namely

a lower

_resting

metabolic

rate.

_According

to this

_hypothesis,

we _{may expect} that starvation

tolerance,

which

depends

on the amount of available reserves, and

especially

of

lipids

(David

et

al,

1975)

could also be related to a lower metabolic rate and to other environmental

stress

_(Hoffmann

and

_Parsons,

_1989a).

However,

starvation tolerance has been

mainly investigated

for its

_{physiological significance (David}

et

_{al, 1975;}

Da

_Lage

et

_al,

₁₉₈₉₎

and for

_{comparing artifically}

selected lines

_(Service

et

_al,

_1985;

Service,

1987;

Hoffmann and

_Parsons,

_1989b)

while natural

_populations

are

_poorly

documented.

In a

_previous

_paper

(David

and

_Capy,

1988),

we

_suggested

_that,

with _respect

to their

_history,

natural

_populations

of D

_medanogaster

could be divided into three _{groups :}

₁₎

ancestral

_populations

found in the

_{Afrotropical region}

south of the

_Sahara;

₂₎

&dquo;old&dquo; or &dquo;ancient&dquo;

populations,

established

_{independently}

of the

activity

of modern _man, and found in the Eurasian

_continent;

₃₎

&dquo;new&dquo; or &dquo;recent&dquo;

populations,

introduced

_by

man a few _{centuries ago} and found in America and Australia. Desiccation tolerance studies have focused on such recent

_populations,

while almost

_nothing

is known of more ancient

_populations.

In the _present

_study,

we.have

_compared

three _types of

_populations

from different latitudes and

_living

under _very different climatic conditions.

_Using

the isofemale

MATERIALS AND METHODS

Three natural

_populations

were

_compared.

An

_equatorial

African

_population

from

Loua near Brazzaville

_(Congo)

_living

all year round in a

_humid,

warm and favorable

environment. A North African

_population

from a Tunisian oasis

(Nasrallah

near

Kairouan)

exposed

each year to _strong heat-desiccation stress

_during

the Summer

months,

as is

_typical

of all Mediterranean climates. A

_population

from southern

France, represented

by

two

_samples,

Moulis and

Lorp,

two localities a few kilometers

apart from St-Girons near Toulouse. This

_population

lived under a cool temperate

climate without any strong desiccation stress but faced the difficult

_problem

of

overwintering during

the coldest months of the year.

Samples

were collected

_using

either banana

_fermenting

baits or

by sweeping

over

natural

_breeding

_sites,

ie

_Opu!tia

fruits in Tunisia or manihot

_peelings

in

_Congo.

In each _case, wild collected females were used to initiate isofemale lines. These lines

were

_kept

in the

_laboratory

for a number of

_{generations ranging}

between 5 and 12 before the

_experiments

were undertaken.

Population

size in each line was

_always

more than 20 flies for each

_generation.

Starvation and desiccation tolerance was studied

_{by measuring}

the survival

duration of adult flies

_kept

without food. With the isofemale line

_technique,

male and female data are correlated

(David, 1979)

since both sexes of each line exhibit a

genetic

similarity and,

moreover, are submitted to a common

_environment;

therefore

only

males were

_compared

for the.3

_{3 geographic}

_populations.

The

experimental

procedures

have been described in a

_previous

_paper

_(Da

_Lage

et

_al,

₁₉₈₉₎

and

are summarized here. For each

_line,

the larvae were _grown on a killed _yeast,

_high

nutrient medium

_(David

and

_Clavel,

_1965).

On emergence, adults were

etherized

and distributed _{into groups} of 10 flies. _{Each group} of 10 was fed on killed _yeast

medium for 2 or 3

_days

and then transferred to the

_experimental

vials. For starvation

tolerance,

water was

_provided

in each vial. For desiccation

_tolerance,

a relative

humidity

of 0% was maintained with silica

gel.

Experiments

were made at 17°C

since,

at this _temperature, the survival time is

_longer

so that the mean value is calculated with better

_precision.

For each

isofemale

line and _treatment, two

independent vials,

ie 20

_males,

were studied. The

_{repeatability}

of the measurements

was

_{assessed, by studying}

two successive

_generations

for each

_population.

_Early

in the trials it was _apparent that

_{repeatability}

was not

_excellent,

as is often the

case with

physiological

traits

(Carton

et

_al,

1989;

Da

_Lage

et

_al,

_1989),

so that

considering

the results at the individual level would be almost

_meaningless.

In most of the

_following

_analyses,

the mean of each line is considered as the basic

observation,

and the

_variability

between lines will

_mainly

be used for

_calculating

the standard error of the mean of each

_population.

RESULTS

Survival time in

_dry

and humid conditions

The mean survival durations of the various

_populations

are

_given

in Table I. As

expected

(Da

Lage

et

_al,

_1989),

life duration is

_always

much less under

_desiccating

(starvation

tolerance of the Tunisian

_population),

the differences between the two

successive

_generations

were not

_significant.

In the case of the Tunisian

_population,

a third

_generation

was studied and the

following

_{average values}

(in hours)

were

obtained : m = 31.22f1.01

(n

=

30)

for desiccation

tolerance,

and m = 75.41t2.91

(n

=

25)

for _starvation tolerance.

_Compared

_to table I

_values,

we find that

desiccation tolerance is

_{significantly}

lower than in the first two

_generations,

while for starvation

_tolerance,

the mean is intermediate and not

_{significantly}

different from the other two. These fluctuations illustrate the

_possible

low

_{repeatability}

of

some

_results,

due to uncontrolled variations in the

_experimental

conditions. For the

Tunisian

_population,

the mean life duration in

_dry

conditions of the 3

_generations

is 36.8

_h;

the true value could be a little

_higher

_{(38-39 h)}

if we admit that the third

generation

was submitted to some

_{uncontrolled,}

unfavorable effects. For starvation

tolerance,

on the other

hand,

the mean value of the 3

_generations,

ie 76

h,

_may be

For each

_generation

and

_population,

a one-way ANOVA

(data

not

_shown)

indicated that the between line variance was

_{always significantly higher}

than the

within line variance. Such a result is often considered to be an indication of the occurrence of

_genetic

variations between lines

_(Hoffmann

and

_Parsons,

_1988;

Carton et

_{al, 1989; Capy}

et

_al,

_1990).

A _way to

_appreciate

the amount of variation between lines is to calculate the coefficient of intraclass

correlation,

t. The values

_given

in table _{I range between 0.09} and

_0.53,

with mean values of 0.21 f 0.03 and 0.28 ! 0.05

_(n

=

8)

for

dry

and humid conditions

_{respectively;}

these values _are

significantly

different from zero

(P

<

_0.01).

Another _{way to} demonstrate

_genetic

variations between lines is to show that their mean values are

_repeatable

in different

generations

(Carton

et

_al,

_1989;

_Davidson,

_1989).

The correlation coeflicients between

_generations

_{(table 1)}

are

_generally

low and

_only

one

(starvation

tolerance,

Tunisia)

is

_significant.

The overall mean of these coefficients

(m

= 0.29 ±

0.15,

n =

8)

is _not

significantly

different from _zero,

_{again suggesting}

that variations between lines _may arise from

_{uncontrolled,}

common-environment effects more than

from

_genetic

differences.

Comparison

between

_geographic

_populations

For the two French

_{samples, Lorp}

and

_Moulis,

the mean values are not

_{statistically}

different,

with one

_exception,

starvation tolerance in

_generation

2. Of course, no

difference was

expected,

since the two

_samples

were collected a few kilometers

apart, under similar

_ecological

conditions. The overall

_similarity

of these results allows the

_pooling

of the observations into a

_unique

French

_sample,

as shown in

table I.

Under

_desiccating

_conditions,

the

populations

from France and

_Congo

are not

different,

with a mean survival times of about 26 h. On the other

hand,

the survival

time is

_{significantly longer}

_{(38-39 h)}

in the Tunisian

_population.

In the presence of water, the

_ranking

of the

_populations

differs. A small

difference,

not

_always

_significant,

may exist between Tunisia and

France,

with survival times of 77 and 63 h

_{respectively.}

The

_{Congolian population}

_is,

_by

contrast, very

different,

with an _{average survival time of 133}

_hours,

ie twice the value found for French flies.

However,

in

_spite

of such a

_large

_average

difference,

some

_overlap

exists between the

Afrotropical

and the Tunisian

_population

when the distributions of the isofemale lines are

considered,

as shown in

figure

1.

Relationship

between survival in

_dry

and humid conditions

As discussed

_by

Da

_Lage

et al

_(1989),

such a

_comparison

_may

_help

to measure the

specific

effects of the desiccation stress. For each

line,

two traits will be considered here: the difference between survival in humid or

_dry

_conditions,

and the ratio of

these two values. The results are

_given

in table III.

Differences between

_generations

are not

_significant,

_except for the Tunisian

population.

In addition the correlations between

_generations

are

_generally

low

and non

_significant,

_except for the Tunisian

_population.

If we consider the means

(difference

in survival duration or

ratio),

we find that French and Tunisian flies are

survival times is _{about 35 h while the average ratio is about} 2.1. The

_Congolian

population, by

contrast, is

_completely

_different,

with a mean ration of 5.5 and a mean difference of 107 h. These observations are summarized in

_figure

2 which shows

that,

in

_spite

of the

_large

_average difference between

_Afrotropical

and temperate

flies,

a small

_overlap

exists when

_single

isofemale lines are considered.

Finally

the

correlations between starvation and desiccation tolerance are close _{to zero, except}

in the French

_population.

DISCUSSION AND CONCLUSION

With the

_possible

_exception

of French

_flies,

our data confirm a

_previous

result

(Da

Lage

et

_al,

₁₉₈₉₎

_concerning

the

_{physiological independence}

of starvation and desiccation tolerance. In the presence of water, and when the _temperature is not

extreme, death occurs when all reserves,

especially

the

_lipids,

have been exhausted

(David

et

al, 1975;

Da

_Lage

et

_al,

_1989).

On the other

_hand,

under

_desiccating

conditions,

the

_lipids

are not exhausted before death occurs

_(Da

_Lage

et

al,

1989)

and the tolerance of the adult

_fly

seems

_dependent

on its

capacity

to control the

opening

of its

_spiracles

_(Fairbanks

and

_{Burch, 1970;}

Arlian and

_Eckstrand,

_1975; Hoffman and

_Parsons,

_1989b).

In selection

_experiments

for increased desiccation

tolerance,

Hoffmann and Parsons

_(1989b)

found a correlated _response for increased

starvation tolerance. A similar

_positive

correlation was also found

by

Service et al

(1985)

and Service

₍₁₉₈₇₎

in lines selected for

postponed

senescence. As discussed

_by

Hoffmann and Parsons

_(1989a),

such a correlation could be

_explained

_by

a

_lowering

of the

_resting

metabolic

_activity.

_Obviously

the situation which

_prevails

in natural

A

_significant

_{heterogeneity}

between isofemale lines is often considered to be an

indication of

_genetic

differences

_{(Parsons, 1983).}

However,

the

_{heterogeneity}

may also occur from common environmental

effects,

ie from the fact that the lines are

grown in different vials. In the present

study,

the low correlation observed between the two successive

_generations

is an _argument for such common-environment effects.

A convenient estimate of the

_variability

between lines is the coefficient of intraclass correlation. If common-environment effects. can be

_neglected,

as is the

case for _many

_{morphological}

traits

_(Capy

et

al,

1990),

the intraclass correlation is related to

_genetic

variations

_(Falconer,

_1981;

_Slatkin,

_1981;

Hoffmann and

Parsons,

1988).

If dominance and

_epistatic

effects are

_neglected,

we _expect to find t =

0.5h

2

.

However,

there is not a

_priori

reason for

_neglecting

dominance or

_epistatic

effects

and a

_general

_expectation

is that the ratio

h

2

/t

will range between 1 and 2. In the _present

_study,

we found a

_fairly

low _average value for t of 0.25 t

_0.03,

which is accounted

_for,

in part,

by

non

_genetic

effects. Therefore the &dquo;true isofemale line

heritability&dquo;

should be

_{lower, suggesting}

also a low narrow sense

heritability

h

2

.

However,

in their selection for starvation

_tolerance,

Hoffmann and Parsons

_(1989b)

found a

_high

value

_(0.64)

for the realized

_{heritability. Again,}

more extensive studies

The variations between

_{geographic populations}

need to be discussed from various

points

of view. With

_only

a few

_exceptions,

the mean values obtained for the two

generations

of a

_given

_population

are similar and not

_{statistically}

different. On the other

_hand,

_{the averages} of a

_single

line _may be

_quite

different in the two

generations,

due to uncontrolled fluctuations in the

_experimental

_conditions,

and

especially

in larval

_density.

The fact that the overal mean remained stable _suggests

that the uncontrolled fluctuations were the same in each

_generation

and

_randomly

distributed _among lines. This overall

_stability

of the mean for a

_given

_population

allows us to conclude that the _greater

_differences,

which were sometimes observed between

_{geographic populations,}

have a

_genetic

basis.

For the three

_populations

_investigated

_here,

it was not

_possible

to

_study

the isofemale lines in their first

_generation

of

_laboratory.

Such isofemale lines are

submitted to

_genetic

drift but

_{drift, alone,}

should increase the between line variance without

_changing

their overall mean. On the other

hand, laboratory

cultures are

submitted to new conditions _very different from those

_prevailing

in nature: some

directional selection for a better

laboratory adaptation

is

expected.

However,

such

adaptation

should be the same for the various

_{populations and,}

in the

_long

term,

converge to a similar

phenotype. Thus,

the consistent differences observed here

between the

_geographic

populations

reflect

_{physiological}

properties

existing

in nature. These differences need to be discussed

_according

to the

_ecological

and climatic conditions

existing

in the countries of

_origin.

As stated

_previously,

_temperate

_populations

are submitted to different environ-mental selective pressures in their successive

generations

(David

et

_al,

_1984).

In the French

_locality

from which flies were

_collected,

the average annual temperature is about 15’C

_and,

because of seasonal

variations,

the

_development

of

_generations

is

possible only

in

_Spring,

Summer and Autumn. A

_major

_challenge

for the flies is

overwintering

while the desiccation stresses are limited. In

_Tunisia,

the _average

an-nual _temperature is

_higher

_(21°C)

and

_development

may occur

_during

the Winter months. The

_major

_problem

is the occurrence of stressful conditions in

Summer,

during

which

_high

_temperature is

_{accompanied by}

a low

humidity.

Such a

heat-desiccation stress occurs in all Mediterranean

_climates,

as is the _case, for

_example,

in southern Australia

_{(Davidson, 1989).}

_Finally,

in the

_equatorial

environment of the

_Congo,

the _{average temperature} is still

_higher

_(25°C)

but remains stable all year round. Seasonal variations are

_mainly

due to rainfall and

_they

affect much

more the

_availability

of resources than the relative

_humidity

_{(Vouidibio, 1985).}

For desiccation

_tolerance,

our observations confirm the

_ecological

_expectation:

the most tolerant flies are found in

Tunisia,

where a

hot, dry Summer,

_imposes

a

strong directional selection each year. We thus confirm the observations made in Australian

_populations

_(Stanley

and

Parsons, 1981; Davidson,

1989).

Interestingly,

Congolian

and French

_populations,

in

_spite

of their

_completely

different

environ-ments, exhibit very similar

properties.

For starvation

tolerance,

which is

_probably

related to the

_availability

of resources,

our results are

_quite

_unexpected,

since we find that

_tropical

flies are about twice

as tolerant as temperate ones. At

_first,

it

_might

be

_{expected that,}

in the

_tropics,

natural

_populations

encounter a

_scarcity

of resources

_during

Winter and

Spring

in

France and

_during

Summer in Tunisia.

Assuming

that differences between

_{geographic populations}

are the consequence of some local

_adaptations,

we need other

_{interpretations.}

One

might

be to consider the

_relationship

between starvation survival and _temperature

_{(Da Lage}

et

_al,

_1989).

All our

_experiments

were made at

_17°C,

a _temperature often encountered in France and Tunisia

_during

the

_breeding

season, but not in the

_{Congo. Obviously}

it is the absolute survival

_duration,

not a relative

_value,

which is selected for in nature.

From

_previous

_{physiological}

_experiments

_(Da

_Lage

et

_al,

₁₉₈₉₎

we know that

survival duration in the absence of food is

_{approximately}

divided

_by

two when the temperature

changes

from 17 to 25° C.

_Thus,

the survival of the

_Congolian

flies

at 25°C would be about 65

h,

ie very similar to that of French flies at 17°C. This

interpretation is, however,

not valid for the Tunisian

_population,

since

_ecological

observations _suggest that a

_scarcity

of resources occurs

_during

the hottest months of the year,

during

which temperatures exceed 25°C. In this case, we may argue

that, during

the Mediterranean

_Summer,

flies are more

likely

to die from desiccation than from

_starvation,

so that the

_capacity

to withstand starvation is an

_adaptive

phenotype only during

the colder months.

These observations show that more numerous

_{populations living}

under a

diver-sity

of climates should be

_investigated

if we are to correlate environmental and

physiological

variables. These

relationships

could be much more

complex

than

ex-pected

with

_simple

natural selection models in which each environmental factor is considered

_{independently}

of the other.

ACKNOWLEDGMENTS

We thank J

Vouidibio,

Y Carton and B

_Delay

for

_providing

the

_populations

from

Congo,

Tunisia and

_France,

and SF

_McEvey

for

_help

with the

_manuscript.

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