Body size reaction norms in Drosophila melanogaster: temporal stability and genetic architecture in a natural population

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Body size reaction norms in Drosophila melanogaster:

temporal stability and genetic architecture in a natural

population

Dev Karan, Jean-Philippe Morin, Emmanuelle Gravot, Brigitte Moreteau,

Jean R. David

To cite this version:

Original

article

Body

size reaction

norms

in

_{Drosophila melanogaster:}

temporal

stability

and

_genetic

architecture in

a

natural

population

Dev

_{Karan, Jean-Philippe Morin,}

Emmanuelle

_Gravot,

Brigitte

Moreteau Jean R. David*

Laboratoire

populations, génétique

et

_évolution,

Centre national de la recherche

_{scientifique,}

91198 Gif-sur-Yvette

_cedex,

France

(Received

2 March

_{1999; accepted}

16

_August

₁₉₉₉₎

Abstract - A natural

population

of

Drosophila melanogaster

was

sampled

twice over

a

_5-year

interval from the same French

_locality

in the same season. Reaction norms of

wing

and thorax

_length

and

_wing/thorax

_{ratio, according}

to

growth

temperature

(12-31

°C)

were

_analysed

in ten isofemale lines for each

_sample.

Reaction norms were

very similar between years,

showing

not

only

a remarkable

_stability

of the _average

size but also of the

_reactivity

to _temperature.

_Wing

and thorax

_length

reaction norms

were characterized

_by

the co-ordinates of their maxima

_(MV

= _maximum value of

character;

TMV = _temperature of maximum

value).

The

wing/thorax

_ratio,

which

exhibited a

decreasing sigmoid

_norm, was characterized

by

the co-ordinates of the

inflexion

_point.

_Again,

these characteristic values were found to be very similar for

samples

between years. The results were further

_{analysed by pooling}

the 20 lines into

a

single

data set.

_Heritability

was

significantly

variable

according

to _temperature,

but in a

_{fairly irregular}

_way with lowest values at extreme _{temperatures.} Genetic

variance of the three traits exhibited more

_regular

variation with a minimum at

intermediate _temperatures and maxima at extreme

_high

or low _{temperatures.} Such

was also the case of

_{evolvability,}

i.e. the

_genetic

coefficient of variation.

_Heritability

and

_evolvability

were found to be

_slightly

but

_{negatively correlated, showing}

that

they provide independent biological

information. The

_{temporal stability}

of a natural

population

over the _{years suggests} some

_stabilizing

selection for both mean

_body

size

and

plasticity.

For

laboratory

evolution

experiments,

the natural

origin population

might

be useful as a

_genetic

control over time.

_©

_{Inra/Elsevier,}

Paris

phenotypic

plasticity

/ growth temperature

/ wing

and thorax length

/

wing/thorax

ratio

_/

_evolvability

*

Correspondence

and reprints

Résumé - Normes de réaction de la taille corporelle chez Drosophila melanogaster :

stabilité _temporelle et architecture génétique dans une _population naturelle. Une

population

naturelle de

_{Drosophila melanogaster}

a été échantillonnée deux fois à

cinq

ans _{d’intervalle,} dans la même localité et à la même saison. Les normes de réaction de la

_longueur

de l’aile et du

thorax,

ainsi _que du rapport

aile/thorax,

ont été

_analysées

en fonction de la

température

de

développement

chez dix

lignées

isofemelles pour

chaque

échantillon. Les normes de réaction se sont avérées très semblables dans les deux

échantillons,

montrant ainsi une

_remarquable

stabilité de la taille _moyenne

et aussi de la réactivité à la

_{température.}

Les normes de réaction de l’aile et du

thorax ont été caractérisées par les coordonnées de leur maximum

(MV

= valeur

maximale du

caractère ;

TMV =

_température

de la valeur

maximale).

Le _rapport

aile/thorax,

qui présente

une norme décroissante

_sigmoïde,

a été caractérisé _par les

coordonnées du

point

d’inflexion. Ces valeurs

_{caractéristiques}

ont aussi été trouvées très semblables dans les deux échantillons. Les résultats ont été ensuite

_analysés

en

réunissant les 20

_lignées

dans un seul échantillon. L’héritabilité s’est avérée variable

en fonction de la

_{température,}

mais de

façon

assez

_{irrégulière}

avec les valeurs les

plus

basses aux extrêmes. La variance

génétique

des trois caractères a

_présenté

une variation

_{plus régulière,}

avec un minimum aux

_{températures}

_moyennes et des

maximums aux

températures

extrêmes. L’évolvabilité estimée par le coefficient de

variation

_génétique,

a montré des variations similaires. L’héritabilité et l’évolvabilité

se sont avérées

légèrement

mais

_{négativement corrélées,}

montrant

qu’elles

fournissent des informations

_biologiques

différentes. La stabilité

temporelle

d’une

population

naturelle au cours des années

suggère

une sélection stabilisante à la fois pour la

taille moyenne et la

plasticité.

Dans des

expériences

d’évolution en

_laboratoire,

la

population

naturelle

_{d’origine pourrait}

être utilisée en _{tant que} contrôle

_génétique

au cours du _temps.

@

Inra/Elsevier,

Paris

plasticité phénotypique

/

température de développement

/

longueur de l’aile et

du thorax

_/

rapport

aile/thorax /

évolvabilité

1. INTRODUCTION

In

_{microevolutionary studies,}

an

_interesting

approach

is to consider the

tem-poral

stability

of a

_{given population.}

A

persistant stability

is often

interpreted

as a _consequence of

_balancing

selection while

regular

variations

according

to

environmental

changes

(e.g.

season)

may also reveal

strong

selection forces

_[25,

42,

44].

Long-term irregular

or

_regular

trends in the same

_locality

_may be

due to drift or to some

_progressive

modification of the environment. Since the

pioneering

works of

Dobzhansky

on chromosome inversions in

_Drosophila

pseu-doobscura,

all these different

patterns

of variation have been observed in various

Drosophila species,

but

_mostly

refer to chromosome

_{rearrangements}

or

_allozyme

frequencies,

with in most cases an

_{adaptive interpretation}

[27].

For

_{quantitative traits, investigations}

on natural

_populations

have

_mainly

demonstrated

spatial genetic

variations such as latitudinal clines in various

species

[2,

4, 14,

23,

25],

and

temporal

variations are less well documented.

This seems to be due to several

_practical

difficulties and to the fact that such

_variations,

if _any, are

_likely

to be smaller than those observed across

long

distances. One

_difficulty

is a lack of consensus on how to measure a

_quantitative

trait. For

example, wing

size is

_generally

estimated as

_wing

length

but there are numerous dimensional

_parts

which have been

equated

to the

length.

Another

difficulty

is the

_sensitivity

of

_quantitative

traits to

_experimental

conditions,

frequent

lack of

_{repeatability}

and an

_apparent

instability

when the same

measurement is undertaken several times on the same

population

[9, 17!.

A final

problem

is the likelihood of

_genetic

drift or

conversely

of

laboratory adaptation

when a

population

is

kept

for a

_long

time under

_laboratory

conditions.

Facing

such

_{difficulties,}

it has sometimes been

_argued

that natural

_populations

of

Drosophila

are too unstable for a convenient

analysis

of natural selection

upon fitness related traits.

According

to Rose et al.

[36],

the

analysis

of

evolutionary

mechanisms should be

simplified

in an

_{&dquo;experimental}

wonderland&dquo;

by controlling

in the

_laboratory

one or a few

conveniently

chosen environmental

factors. This

_approach

was

already

used in

population

cages of

Drosophila

for

analysing,

for

example, adaptation

to different

_growth

_temperatures

_[1,

_6,

_33!.

The

_difficulty

is that

_{simple laboratory}

conditions may have

nothing

to do

with the

_reality

of natural conditions. An

_example

is

_provided

_by

desiccation and starvation tolerance in

_Drosophila.

Several

laboratory investigations

have

repeatedly

found a

_positive

correlation between these two traits

_[19,

_38,

_39].

Studies of natural

_populations

have

shown,

in

_contrast,

a

_{systematic negative}

correlation in several

_species,

each

_apparently

_{reacting adaptively}

to some

environmental

_gradient

related to latitude

_{[7, 24!.}

If we _argue that natural

populations

might

be

preferred

to

laboratory

ones

for

_{evolutionary studies,}

a

_{major problem}

to be raised is their

_stability.

For

example,

several French

populations

of D.

_melanogaster

were

investigated

with

the isofemale line

technique

for size and other

_quantitative

traits and

_slight

but

significant

variations were shown between them

(4!.

Since the measurements

were made for different _years on lines sometimes

_kept

in the

laboratory

for

many

generations,

the

origin

of these variations has remained unknown. More

recently,

a

_significant

difference in reaction norms of

body pigmentation

was

demonstrated in two

_{sibling species}

from two French

_localities,

_presumably

reflecting,

in that case, an

adaptation

to local thermal conditions

_(16!.

In the

_present

work we

sampled

_twice,

over a

_{5-year interval,}

the same

population

at the same time of the year and

analysed

two size-related

_traits,

wing

and thorax

_length.

We also calculated the

_wing/thorax

ratio,

which is related to

_{wing loading}

and

_flight

_capacity

and

_might

be a direct

_target

of natural selection

_{[34, 41].}

Measurements were not restricted to a

_single

laboratory condition,

as was the case in former

investigations.

We

analysed

phenotypic plasticity

related to

_growth

_temperature

over the whole thermal

range of the

species.

We found a remarkable

_stability

not

only

of size but also of the reaction norms and of their

_genetic

characteristics. Also a

_curvilinear,

apparently quadratic

variation of the

_genetic

variance is shown

according

to

growth

temperature.

2. MATERIALS AND METHODS

Wild D.

_melanogaster

adults were collected with banana

_traps

in Grande

Fer-rade near Bordeaux

(southern

France)

over 2 different _years. A first collection

was made in autumn

_1992,

and a second in 1997 from the same

_vineyard

and

same season. Isofemale lines were established and ten of them were

randomly

chosen for further

study.

For the 1992

_sample,

lines were

kept

for 5 months

1993. For the 1997

_sample,

measurements were made on the second

_laboratory

generation

in December 1997.

For

investigating

growth

temperature

effects,

ten

_pairs

of adults were

ran-domly

taken from each line and used as

_parents.

_They

were allowed to

_oviposit

at room

_temperature

_{(20 iL}

_{1 °C)}

for a few hours in culture vials

_containing

a

high

nutrient medium based on killed

_yeast

[8].

Such a medium

_prevents

crowding

effects which could affect

_fly

size.

_{Density ranged}

between 100 and 200 _{eggs per} vial. These vials with eggs were

immediately

transferred to one of

seven

experimental

_temperatures

(12,

_{14, 17,}

_{21, 25,}

28 and 31

°C).

From each

line at each

_temperature,

ten females and ten males were

_randomly

taken and

measured for two

_quantitative

traits

_(wing

and thorax

_length)

with a

binoc-ular

microscope equipped

with a micrometer. The results were

_expressed

in mm x 100.

_{Wing length}

was measured from the thoracic articulation to the distal

tip

of the

_wing,

and the thorax was measured on a left side view from

the neck basis to the

_tip

of the scutellum

_{[10, 28!.}

The

_wing/thorax

ratio was

also calculated.

A small

_experiment

was

performed

from a mass culture to measure the

effect of larval

_crowding

on adult size. Larval

_density

was controlled

_by

transferring 10,

20,

40,

80,

160 and _{320 eggs} to culture vials. A still

_higher

density

(650

emerging

adults)

was obtained as a _consequence of a

large

number

of

_parents

_{(50 females)}

_{directly laying}

in a

_single

vial for a few hours.

Data were

_analysed

with the Statistica software

_[43].

As in

_{previous studies,}

the response curves were

adjusted

to

_polynomials

_!28!.

For

_wing

_length,

thorax

length

and

_wing/thorax

_ratio,

a cubic

_polynomial

was chosen for

_describing

the norms. For

_genetic

variance

(V

9

)

and coefficients of

_genetic

variation

(CV

9

),

a

_{quadratic polynomial}

was chosen. With cubic

_polynomials,

numerous

characteristic values can be calculated

_!11!.

In the

_present

_case, we used the

polynomial

parameters

to calculate the co-ordinates of a

_maximum,

minimum

or inflexion

_point,

for

_wing

and thorax

_length,

_Vg

and

_CTl9

or

wing/thorax

ratio,

respectively.

3. RESULTS

3.1. Larval

_density

and size variation

Figure

1 shows the

_relationship

between larval

_density

and

_wing

or thorax

length

or

wing/thorax

ratio. A _one-way ANOVA

(not shown)

on these data

demonstrated

_significant

differences for

_wing

and thorax

_length

but not for

wing/thorax

ratio. For

_wing

and thorax

_length,

_however,

the results became

homogeneous

(no

effect of

_density)

when the extreme values

_(densities

of 10 and

₆₅₀₎

were excluded from the

_analysis.

We _may conclude that a

_density

range of 100 to 200 flies per vial will have no effect on the measured characters.

3.2. Mean reaction norms of

_wing

and thorax

_length

and

wing/

thorax ratio

The _{average response} curves of size traits

_according

to

_growth

_temperature

are shown in

_figure

2. Female and male curves are

_{separated showing}

the

for each

_trait,

the reaction norms of _years 1992 and 1997 are almost identical.

For each

character,

a maximum was observed at low

_temperature,

i.e. around 15 °C for

_wing

length

and 19 °C for thorax

_length,

in

_agreement

with

_previous

studies

_[10,

_28].

Reaction norms of

wing/thorax

ratio are

_given

in

figure

3.

In both sexes a

_{decreasing sigmoid}

was observed with

_only

a

_slight

difference

The data were submitted to

_ANOVA,

in which lines were considered as a

random factor and nested within _years: no

significant

differences were found

evidenced due to

_line,

_sex,

_temperature

and their interactions. The interactions

involving

year were

always

non-significant.

These

analyses

confirm the

high

similarity

of the

_{2-year samples.}

3.3. Characteristic values of reaction norms

As indicated

_previously,

the response curves were

adjusted

to

_polynomials

and the

parameters

were used to calculate characteristic values

_!11!.

For the two

concave norms

(wing

and thorax

length),

we considered

only

the co-ordinates of the

_maximum,

i.e. MV

_(maximum

_value)

and TMV

_(temperature

of maximum

value) (table 77).

Maximum values were _very similar between _years. Coefficients of variation

among lines were small and similar for both traits: 1.99 ! 0.13 for

_wing

and

1.42 ! 0.19 for thorax

_length.

Temperatures

of maximum value were also

similar for the two

_samples

_{(table 11).}

The data confirmed

previous

observations

according

to which TMVs were lower in males than in females and lower for

wing

length

than for thorax

_length.

Coefficients of variation were

_higher

than

for MV: 6.06 and 4.54 for

_wing

and

_{thorax, respectively.}

We

_finally

_compared

the

_sigmoid

norms of the

W/T

ratio

_{by calculating}

the co-ordinates of the

inflexion

_points

_{(table IQ,}

that

_is,

the

phenotype

at the inflexion

_point

_(PIP)

and the

temperature

of the inflexion

_point

_(TIP).

For this

_character,

non-plausible

values were found for some

_lines,

for

_example,

a PIP

_superior

to 10

that PIP were similar in males and females and also between

_samples

(average

2.64).

The

_temperatures

of the inflexion

_point

were not different between _years

(average

18.53 !

_0.48)

but

_variability

_among lines was

higher

(average

CV:

13.65).

3.4. Isofemale line heritabilities

Since we could not demonstrate _any

_significant

_year

_effect,

we

_pooled

the

data into a

single sample

of 20 lines in order to further

_analyse

the

_genetic

architecture of this Bordeaux

_population.

Genetic

_variability

was

_analysed

by calculating,

for each

temperature

and

trait,

the coefficient of intraclass correlation

_{(table III)}

which estimates a broad sense

heritability

and is often

considered as a

_specific

_parameter,

i.e. isofemale line

_heritability

_[5,

15, 17,

18,

40!.

ANOVA on these data

(table I!

demonstrated a

slight

effect of sex

(higher

major

difference was found between

_traits,

and

_especially

a

higher

heritability

of

_wing

_length,

as

_already

found

_{by Capy}

et al.

_[5]

with the same method.

3.5. Genetic variance and

_evolvability

across

_temperatures

We calculated the

_genetic

variance

_(see

_!17!)

for each

_temperature,

sex and

trait. The results are illustrated in

_figure

_!!.

In each case,

higher

values were

observed at extreme

_high

or low

_temperatures

and lower values in the middle of the thermal _range. As in Noach et al.

_!30!,

we

_adjusted

these convex curves to a

quadratic polynomial

and

_calculated,

in each case, a

_temperature

of minimum

value

_(T

_minv

₎

_(table

_T!.

_{Fairly high}

_temperatures

were found for

_wing

_length

(average

27.9

_°C)

while

_T

_minv

_s

were in the middle of the thermal _range for thorax

_length

and

_wing/thorax

ratio

_(average

22.4

_°C).

For

_wing

and thorax

length, higher

variances were observed in

_{females, presumably}

in relation to

We also standardized the

_genetic

_variability

to the mean value of each trait

by calculating

the

_genetic

coefficients of variation

_(CV

₉

_).

The

_CVg

characterizes the

_capacity

of a trait to

_respond

to natural selection and was called

_evolvability

!21, 22!.

All these coefficients also exhibited convex _response curves

according

to

growth

temperatures

(figure 5).

A

significant

difference between sexes

_persisted

only

for

_wing

_length.

_T

_min

_VS

were all in the middle of the thermal

_range

(table

V)

with an _average of 21.6 °C.

We

_compared

_CV

₉

_s

with isofemale line

_heritability

_{by analysing}

their

cor-relations. In all six cases

(traits

and

_sexes)

negative

values were found

ranging

from - 0.15 to - 0.87

_(average

r = -0.44 !

0.012).

These

_negative

correlations

are illustrated in

_figure

6.

_They

show that

_heritability

and

_evolvability

do not

provide

the same

_biological

information

_!21!.

4. DISCUSSION AND CONCLUSIONS

We found a remarkable

stability

of the reaction norms of

body

size traits

in two

_samples

collected in the same

_place

over a

_5-year

interval. This result

was obtained

using

a

_high

nutrient

_food,

and a

specific experiment

showed that

the results were not influenced

_by

larval

_density.

We may also

suggest

that

experimental technique

and food

_ingredients

did not

_change

over the _years.

Using

such

_conditions,

_any

_significant

difference between two

_samples

could therefore be considered as

_reflecting

a

_{genetic divergence.}

In

_spite

of the

_striking

similarity

of the _{average curves,} each

sample

harboured a noticeable

genetic

variability

between isofemale lines. The overall

_stability

_suggests,

but does not

demonstrate,

that in a local

_population,

size traits

_might

be submitted to some

stabilizing

selection,

not

_only

for their mean value in a

_given

environment

but also for their

_reactivity

to

_growth

_temperature.

The fact that reaction

norm

_shape

_{may vary}

_{adaptively according}

to environmental conditions is demonstrated

_by

_major

differences found between

temperate

and

tropical

populations

(29].

Over the _years

_{polynomial adjustments}

of the reaction norms also established

a remarkable

_stability

of their characteristic

values,

either

MV, TMV,

PIP

70

_individuals,

is

_mainly

a

_{genetic property}

of the line. Sex differences also

have a

_genetic

basis.

_{Using family}

_means, we calculated the correlations between

males and females at each

_temperature.

No difference was found either between

years or

_{temperatures,}

with _average values of 0.82 ! 0.05 for

_wing

_length

and 0.70 t 0.08 for thorax

_length.

Heritabilities

_{(intraclass correlations)}

were

significantly

different _among

traits with

_higher

values for

_wing

_length,

in

_agreement

with

_previous

obser-vations

_{[5, 10].}

_Significant

variations were also observed

_according

to

temper-ature but in a

_quite

_irregular

_way.

_Especially,

there was no

_regular

increase in

heritability

under extreme conditions as was

_{suggested by}

other

_{investigations}

[3, 20].

Genetic variances

_(Vg)

varied

according

to

_growth

_temperature

with

_higher

values at low and

_high

_temperatures

and a minimum around the middle

of

_{developmental}

range. Such a convex

_pattern

was

previously

observed

_by

Noach et al.

_[30]

in a Tanzanian

_{population and, interestingly,}

the

_temperature

of minimum value was also less for thorax than for

_{wing length.}

Noach

et al.

_[30]

_failed,

however,

to find such a

_pattern

in a French

_population.

This contradiction _may be

_{explained by}

the fact that we used a broader

thermal _range

_(12-31

°C instead of 17.5-27.5

_°C).

_According

to de

_Jong

_[12,

13]

and Scheiner

_[37],

a minimum

_genetic

variance should be

_expected

at

the

_predominant

value of the environmental variable where the

_stabilizing

selection pressure on the trait is the

_strongest.

Our data on thorax

_length

and

wing/thorax

ratio fit this

_expectation,

since the minimum

_genetic

variances

are observed at

_temperatures

around 22 °C which

_correspond

to the summer

temperature

in the Bordeaux area. The

_identity

of the average reaction norms over a

_5-year

interval also

_suggests

that

_stabilizing

selection

_might

occur not

only

in the middle of the thermal _range but also at other

_{temperatures.}

This is

likely

to occur in

_Bordeaux,

since low

_temperatures

are

_{experienced by spring}

and autumn

_generations.

It has been

_proposed

that a

_{higher genetic}

variance under extreme stressful conditions should

_permit

a faster

_adaptive

_response to an environmental

change

[3,

12,

19].

However,

as

_{argued by}

Houle

_{[21, 22],}

_knowing

the

_genetic

variance and

_{calculating heritability}

do not

_permit

the

_speed

of an

_adaptive

change

to be

_predicted.

For this kind of

_prediction,

it is better to standardize the

_genetic

variance to the mean and estimate the

_evolvability

of a trait

_by

using

the

_genetic

coefficient of variation. We found that

_evolvability

_changed

over

_temperature

(figure 5)

with minimum values at middle

_{temperatures.}

In other

_words,

_evolvability

was

_clearly

_higher

under extreme environments so

that

_{adaptive changes}

should be faster under such conditions when needed. Both

_heritability

_{(intraclass correlation)}

and

_evolvability

are ratios with the

genetic

variance as the numerator. It

_might

be

_argued

that both

_parameters

estimate the same

_thing

and should thus be

_positively

correlated. We calculated these correlations

_separately

for the three traits and two sexes. All the six

coefficients were

_negative

with a mean value of r = -0.44 !

0.12,

significantly

less than zero. Such a

_negative

correlation is difficult to

_explain.

It rules

_out,

however,

the above-mentioned

_possible

bias of

_measuring

the same

_thing

twice.

In the

_{future, evolvability}

of a trait should receive

_increasing

attention.

As discussed in the

_{Introduction,}

_laboratory

evolution

_experiments,

in-terpret

in terms of selection

_{although they might}

not be relevant to natural selection in nature. On the other

_hand,

natural

_{populations integrate}

so _many

environmental variables that their effects may be

impossible

to

_disentangle.

As also discussed in detail

_by

Rose et al.

_!36!,

_laboratory

_experiments

are

_plagued

by

a need for convenient controls. Flies collected in nature and

_brought

to

the

_laboratory

are

likely

to

_undergo

some

rapid adaptation

to

_general

labora-tory

conditions such as a stable

_{temperature, permanent}

food

_{availability, early}

reproduction

and absence of

_flight

and

_dispersal.

For that reason, numerous

ex-periments

were started from

_{populations already kept}

as

_laboratory

cultures

[6,

31, 32,

35!.

Laboratory

evolution

implies

the establishment of

aliquot

strains under new conditions

(e.g.

different

temperatures)

while

_maintaining

the initial

ones. As stated

_by

Rose et al.

_[36]

&dquo;the best control _may be

_{perfectly preserved}

specimens

from the

_{founding population&dquo;.}

Such a

_goal

was attained on bacteria

by keeping

aliquot samples

of the

_{starting population}

frozen

_!26!.

Our

_result,

if

it was

_generalized

_by

further

_{investigations, might provide}

a similar stable

refer-ence for

Drosophila.

In this

_respect,

evolutionary

_experiments

might

_encompass

two kinds of controls: classical ones,

kept

under usual

_{laboratory conditions,}

and wild

_living

flies

_{repeatedly sampled}

from the same

_locality.

ACKNOWLEDGEMENTS

This work was

_supported

_by

the Indo-French Centre for the Promotion of Advanced Research

_{(IFCPAR -}

_Project

No.

_1103-1)

and

_by

the Centre

Interprofessionnel

des Vins de Bordeaux

_(CIVB).

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