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Phenotypic and genetic variability of morphometrical
traits in natural populations of Drosophila melanogaster
and D simulans. I. Geographic variations
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.
I.
Geographic
variations
P Capy*
E
Pla,
JR
David
Centre National de la Recherche
Scientifique,
Laboratoire de
Biologie
etGenetique
g
volutives,
91198Gif sur-Yvette Cedex,
France(Received
30 March 1993;accepted
10August 1993)
Summary -
Geographical variability
between naturalpopulations
of the 2 relatedcos-mopolitan
speciesDrosophila melanogaster
and D simulans wasinvestigated
on alarge
number of
populations
(ie
55 and 25,respectively)
for 6morphometrical
traitsconcern-ing weight,
size,reproductive capacity
and bristle numbers. For 21populations, sympatric
samples
of the 2 species were available. For most traits, the mean values of Dmelanogaster
arehigher
than those of D simulans, with the exception of thesternopleural
bristle num-ber, for which the species are similar. In Dmelanogaster,
similar latitudinal variations existalong
anAfrican-European
axis, in bothhemispheres,
and on the American continent. In Dsimulans,
a latitudinal cline that isparallel
to those observed in Dmelanogaster
wasobserved
suggesting
thatvariability
betweenpopulations
ispartially adaptive.
In additionto these
parallel
variations, in which the mean values of all traits increase withlatitude,
inter-continental variations were also detected in D
melanogaster
whenpopulations
sam-pled
at similar latitudes werecompared
(eg, West
Indian and Far Easternpopulations).
Different
demographic strategies
(r
orK)
couldexplain
such variations.Analysis
ofmor-phological
distances(Mahalanobis
generalized
distanceD
2
)
betweenpopulations
of the2 species, showed that D
melanogaster
is much more diversified than D simulans. All the traits except thesternopleural
bristle number are involved in these differences.Drosophila melanogaster
/
Drosophila simulans/
morphometrical trait/
geographicvariability
/
isofemale lineRésumé - Variabilité phénotypique et génétique de caractères morphologiques dans les populations naturelles de Drosophila melanogaster et de Drosophila simulans. I. Variabilité géographique. La variabilité
géographique
entrepopulations
naturelles des 2espèces cosmopolites affines Drosophila melanogaster
et D simulans a étéanalysée
sur un*
grand
nombre depopulations
(55
et 25respectivement),
pour 6 caractèresmorphologiques
liés au
poids,
à lataille,
à lacapacité
dereproduction
et aux nombres de soies. Pour21
populations,
un échantillon des2 espèces
étaitdisponible.
Sur l’ensemble descaractères,
D simulans
présente
des moyennesplus faibles
que Dmelanogaster,
àl’e!ception
dunom-bre de soies
sternopleurales
pourlequel
les 2espèces
sontidentiques.
Chez Dmelanogaster,
des variations latitudinales similaires existent lelong
d’un axeAfrique-Europe,
de part etd’autre de
l’équateur,
et sur le continent américain. Pour Dsimulans,
un clinelatitudi-nal
parallèle
à ceux détectés chez Dmelanogaster
a été observésuggérant qu’une
partiedes variations
interpopulations
est de natureadaptative.
Enplus
de ces variationspar-allèles où les moyennes de l’ensemble des caractères augmentent avec la
latitude,
des variations inter-continentales ont été décelées chez Dmelanogaster
si l’on compare despopulations
échantillonnées surdifférents
continents à des latitudescomparables
(popu-lations des Antilles et
d’Extréme-Orient).
Desdifférences
destratégies
démographiques
(r
ouK)
pourmient expliquer
ce type de variations.L’analyse
des distancesmorphologiques
(D
2
de Mahalanobis)
entre lespopulations
au sein de chacune des 2espèces
montre queD
melanogaster
estglobalement
bienplus diversifiée
que D simulans pour l’ensemble descaractères à
l’exception
du nombre de soiesstemopleurales.
DrosopLila melanogaster / Drosophila simulans / caractères morphométriques / variabilité géographique
/ lignées
isofemellesINTRODUCTION
The
sibling
species
Drosophila
melanogaster
and D simulanspresent strong
mor-phological
similarities.They
were often confused until Sturtevant(1919)
describedD simulans as a close relative of D
melanoga.ster.
These 2cosmopolitan species
arewidely
distributed in bothtemperate
andtropical regions.
However,
whilethey
aresympatric
in manyplaces,
their relativeproportions
are notalways
the same. Forinstance,
inAfrica,
the relativeproportion
of the 2species
exhibits ageographic
gra-dient from the
Ivory
Coast,
where D simulans is almost absent and Dmelanoga.ster
is the main
species,
to islands in the Indian Ocean close to the African coast where D simulan.s is more abundant than Dmelanogaster
(Lachaise
etal,
1988).
Moreover,
D simulans is not found in several countries in the Far
East,
or has beenrecently
introduced there.
At first it was
expected
that because of their commonancestry,
the 2species
would exhibit similar
patterns
in thegenetic
variability
of their naturalpopulations.
During
the last 2decades,
they
have beencompared
for numerous kinds oftraits,
including:
chromosomal inversions(Ashburner
andLemeunier,
1976;
Lemeunier etal,
1986);
mitochondrial DNA(Solignac
andMonnerot, 1986;
Hale andSingh,
1985);
enzymatic
polymorphism
(Hyytia
etal,
1985;
Singh
etal, 1987;
Singh,
1989;
Choudhary
andSingh,
1987) ;
dispersed
repetitive
DNA(Dowsett
andYoung,
1982);
protein
polymorphism analysed by
2-dimensionalelectrophoresis
(Ohnishi
et
al,
1982,
Choudhary
etal,
1992);
physiological
traits(Parsons
1983;
David etal,
1983);
behavioural traits(Cobb
etal,
1985, 1986,
1987);
cuticularhydrocarbons
In most of these
analyses,
it was found that Dmelanogaster
hasgreater
variability
between
populations
than D simulans.Only
2exceptions
can be mentioned.First,
D simulans was found to be 3 times more variable than D
melanogaster
for theinter-pulse
interval(IPI)
ofcourtship
song,(Kawanishi
andWatanabe,
1981).
Second,
at the DNAlevel,
the restriction-sitepolymorphism
wasgreater
in D simulans in therosy
region
(Aquadro
etal,
1988)
and inregions
on the X chromosomeincluding
the y,
Pgm
and per genes(Begun
andAquadro,
1991).
Although
the 2species
werecompared
for manytraits,
fewmorphological
data are available. In the works cited above that deal with thesequantitative
traits,
the
geographical
variability
between naturalpopulations
of Dmelanogaster
and D .simulans wasinvestigated
in a restricted area and from a small number ofpopulations.
Moreover,
according
to their differentauthors, investigations
werecarried out under different
laboratory
conditionsmaking comparisons
difficult orimpossible.
Therefore, only
tendencies wereevidenced,
from thesedata,
and it wasdifficult to draw
general
conclusions.The aim of this work is to compare the
geographical
variability
of Dmelanogaster
and D simulans from naturalpopulations
collected in various parts of the world. Two relatedquestions
will beconsidered;
i)
how muchgeographical variability
isfound in the 2
species
andii)
whether thepatterns
found formorphometrical
traitsmatch those observed for other
genetic
traits.To answer these
questions,
thevariability
betweenpopulations
(this paper)
andthe
within-population variability
(Part
II,
Capy
etal,
1994)
wereinvestigated
for6
morphological
traits. These traits can be clustered as follows: traits related tosize
(weight,
wing
and thoraxlengths);
a trait related to thereproductive
capacity
(ovariole number);
and 2 bristle numbers. The first 2types
of traits arelikely
under selective pressures in natural
conditions,
while bristle numbers aregenerally
considered as more neutral.
Such a
diversity
of characters allows variouscomparisons
of the 2species.
Fromselected
traits,
it ispossible
to determine whethergeneral
rules ofgeographical
variations exist and thus whichgeographical
or climatic related factors are involved.On the other
hand,
thegenetic
variability
observed betweenpopulations
for neutraltraits could be
partly
due togenetic
drift. It is alsointeresting
to compare the2
species
forcomplex
traitsinvolving
alarge
number of genes, such as freshweight,
and for traits determined
by
a fewmajor
genes, such as bristle number(Shrimpton
and
Robertson,
1988a,
1988b).
MATERIALS AND METHODS Natural
populations
Fifty-five
naturalpopulations
of Dmelanogaster
and 25 of D simulans wereanal-ysed;
21populations
of eachspecies
weresympatric
(table I).
Allpopulations
orig-inated from low altitudes and were collected with attractive
fermenting
fruittraps.
In all cases, isofemale lines were
used,
ie wild inseminated females were isolated in culture vials toproduce
progeny. Because wild females may be inseminatedby
more than 1 male
(Milkman
andZietler,
1974),
thefollowing
procedure
was used.One male and 1 female from 2 different initial lines were mated to initiate a new
line. These
parents
were transferred to ahighly
nutritive food(killed
yeast
medium,
David and
Clavel,
1965).
To avoidcrowding
effects,
a maximum of 50 eggs werereared in the same tube and the emergences
(full-sib individuals)
were used for themorphological analyses.
Thus,
from n initiallines,
n/2
new lines wereproduced
and 10 individuals per line were measured. In some cases, the new lines were
gen-erated and studied after the initial lines had been
kept
in thelaboratory
for a fewMorphological
traitsSix
morphometrical
traits were considered: freshweight
(FW)
measured a fewhours after emergence
(expressed
in mg x100);
the sum of the abdominal bristleson the fourth and fith
tergites
(AB) ;
the sum of thesternopleural
bristles on theright
and left sides(SB);
the thoraciclength
(TL)
in lateral view(expressed
inmm x
100);
wing length
( WL)
measured between the humeral cross-vein and thetip
of the thirdlongitudinal
vein(expressed
in mm x100);
and the total ovariole number(Ol!
of both ovaries(David, 1979).
Since ahigh
correlation exists betweenmales and females of the same line
(David
etal,
1977;
Capy
1987)
measurementsGeographic diversity
Morphological
distances between naturalpopulations
were estimatedby
theMa-halanobis
generalized
distance(D
2
)
over the 6 traits considered here. This is a Euclidian distance based on thegeneralized Pythagoras
theorem and related to theHoteling
T!
used
in discriminantanalysis.
The Mahalanobis distance was calculatedusing
the mean values of each isofemale line as basic data. To visualize the differenceof
morphological variability
between the 2species,
some trees based on the matricesof the distance are
proposed.
These trees were builtusing
PHYLIP(version
2.9).
To this
end,
populations
were clustered into several groupsaccording
to theirgeo-graphic
proximity.
For Dmelanogaster,
13 groups were considered:France,
CIS(ex
USSR);
EastMediterranean;
WestMediterranean;
Tropical
Africa;
theSeychelles
and the MascareneIslands;
SouthernAfrica;
North America(northern
USA andCanada);
WestIndies;
southern USA andMexico;
theSociety
Islands andHawaii;
the Far
East;
and Australia. For Dsimulans,
only
8 groups were considered:France;
East
Mediterranean;
WestMediterranean;
Tropical
Africa,
SouthAfrica;
FrenchWest
Indies;
Southern USA andMexico;
and theSeychelles
and the Mascarene Islands.Latitudinal variations of the 6
morphometrical
traits weremainly analysed along
a transect betweentropical
Africa andEurope.
For Dmelanogaster
bothhemi-spheres
and a transect between Mexico and North America were also considered.For this
species,
intercontinental variations betweenAmerica,
North Africa and Far East were alsoanalysed.
RESULTS
Table I
gives
the mean values of the 6quantitative
traits for all thepopulations
sampled.
This table will beanalysed according
to 3 mainpoints:
general
trends of the betweenpopulation variability
in bothspecies,
andgeographical
variationsaccording
to either latitude or different continents.General trends
Table I shows that D
melanogaster
values aregenerally higher
than those ofD simulans.
However,
due the broad range of variation found in eachspecies,
some
overlaps
can be found. Forexample,
male freshweight
in French D simulans(eg,
84.44 inPerpignan)
may be muchhigher
than the same trait in AfricanD
melanogaster
(eg,
76.14 inCotonou).
A bettercomparison
isprovided
whenonly
thesympatric
populations
arecompared
(table II).
As shown in table
II,
the overall mean values arestatistically
inferior in Dsim-ulans than in D
melanogaster,
with theexception
of the number ofsternopleural
bristles. A detailed
analysis
of table I shows that this is ageneral
phenomenon
when
sympatric populations
arecompared.
Mean values of Dmelanoga.ster
arealways higher
forFW, TL,
WL andON;
all these traits are related to size orre-production.
D simulans is then smaller with a lowerreproductive capacity
thanThe 2
species
arequite
similar for the thoraxlength
(92.45
for Dmelanogaster
versus 90.27 for Dsimulans)
whilewing
length,
freshweight
and ovariole number aresubstantially
different(190.22
versus170.26;
89.81 versus77.87;
and 42.10 versus36.89).
The conformation and theshape
of individuals are therefore different in the2
species
and theirrespective wing
loads are notexactly
the same.Variances between
populations
(table
II)
aremainly
due tolong-range geographic
variations. In all cases,
they
arehigher
in Dmelanogaster
than in D simulans butonly
2 arestatistically significant
forwing
length
and ovariole number. This is afirst indication that different traits do not
exactly
follow the same rules of variationin the 2
species.
Forexample, wing
length
is far more variable in Dmelanogaster
than in D simulans and thorax
length
exhibits a similarpattern.
For each
morphological
trait,
correlations between mean values ofsympatric
populations
arepositive,
and 4 out of 6 aresignificant
(table II).
Such a resultevidences
parallel
variations in the 2species
andsuggests
anadaptive
significance.
Geographic
variability
Nlorphological
distances between naturalpopulations
of eachspecies
were estimatedby
the MahalanobisD
2
,
taking
into accountsimultaneously
the 6 traits. The distributions of this distance aregiven
for the 2species
infigure
1. The differences between Dmelanoga.ster
and D .simulan.s are clear both when all(white histograms)
or
only sympatric
(black histograms)
populations
are considered. Arepresentation
is
given
infigure
2,
in whichpopulations
have been clusteredaccording
to theirgeographical origin
(Materials
andmethod.s).
The trees show that the distances betweenpopulations
within eachspecies
areclearly
different(compare
the 2 trees on the samescale),
but the classification ofpopulations
areroughly
the same.All the
morphological
traits studied here are involved in the differentiation of the2
species
with theexception
of thesternopleural
bristle number.For D
melanoga.ster,
3 main groups ofpopulations
can bedistinguished:
popula-tions of
temperate
regions including
northernUSA, Canada,
France andex-USSR;
populations
oftropical regions
including
the WestIndies,
theSociety
Islands andHawaii ;
andpopulations
intropical
Africa,
theSeychelles
and the Mascareneis-lands. Between these 3 main groups, we find
populations
living
inregions
within-termediate climates such as South
Africa,
Mediterraneancountries,
southern USAand
Mexico,
the Far East and Australia.For D
.simulans,
3types
ofregion
arefound,
ietropical regions,
Mediterranean countries and Australia.However,
it must be stressed that for thisspecies,
tem-perate
countries wererepresented
only
by
Frenchpopulations;
thesepopulations
mainly
originated
in southern France thusexplaining
why
they
are close toMediter-ranean
populations.
Latitudinal clines
Most of the
populations
studied herebelong
to
anAfrican-European
transect fromSouth Africa to France. For D
melanogaster,
similar latitudinal clines are observedwhen the 2
hemispheres
are consideredindependently.
In both cases, the meanOn the north American
continent,
although only
11populations
wereavailable,
a latitudinal clineshowing
the same tendencies for all traits was also observed. All the correlations between mean values and latitude aresignificantly
positive.
axis are
parallel.
As anexample,
therelationship
between latitude and ovariolenumber is
given
infigure
3 for the whole set of 55populations.
For D
simulans, only
theAfrican-European
axis wasconsidered,
with 19pop-ulations. All the correlations with latitude are
positive
butonly
3 aresignificant.
However,
when all thepopulations sampled
are considered all the correlations withlatitude become
significant.
Latitudinal variations may also be
analysed simultaneously by combining
the 6morphometrical
traits in aprincipal
componentanalysis.
The results obtained for Dmelanogaster along
theEuropean-African
transect are shown infigure
4. Axis 1 ismostly
related to latitude and we see that South Africanpopulations
are close tothose in the Mediterranean.
Significant
differences are alsoexpressed
on the secondaxis,
especially
for thepopulations
of Mauritius and theSeychelles.
Thepopulation
Africa. Historical evidence
suggests
that Dmelanogaster
wasrecently
introducedinto the
Seychelles archipelago
(David
andCapy,
1982)
but thegeographical
ori-gin
ofcolonising
populations
remains unknown. From theanalysis
ofallozymes
frequencies
and ethanoltolerance,
thispopulation
is almost identical toEuropean
populations.
On the otherhand,
from biometricaltraits,
thispopulation
remainsintermediate between
temperate
andtropical populations,
eventhough
thefrom either Mediterranean or South African
populations.
Its intermediateposition
could also reflect a
partial
adaptation
to a newtropical
environment.Variability
between continentsIn D
melanogaster, although parallel
latitudinal clines are evidenced on 2continents,
populations
from the same latitude but different continents do not show similarmorphological
characteristics. Forinstance,
whentropical
populations
are orderedalong
alongitudinal
gradient,
from the West Indies totropical
Africa and the FarEast,
significant
differences are observed for freshweight,
thorax andwing
lengths
and ovariole number. For the first 3
traits,
the mean values increase from West Indian to Far Easternpopulations
(fig 5)
while the mean values of ovariole numberdecrease. In other
words,
individuals in the West Indies arelighter
and smaller thanthose in the Far
East,
butthey
also have ahigher reproductive
capacity;
Africanpopulations
are intermediate for all these traits.Correlations with climatic factors
Previous observations often
suggest
thatgeographical variability
reflectsadaptive
responses to local environment. To check whether a
simple
climatic factor washottest and coldest
months,
the difference between these 2 values and the averagetemperature
of theyear).
The 4remaining
parameters
were related to rainfall(average
total rainfall of the wettest anddryest months,
the difference between these 2 values and average total rainfall of theyear).
These data were taken fromthe World
Meteorological
Organisation
(1982)
andcorrespond
to average valuesover a
period
of at least 10 years. Because most climaticparameters
werehighly
correlated with latitude
(in
general
p <0.001),
partial
correlations(to
subtract the latitudinaleffect)
between climatic data andmorphometrical
traits were calculated.Few
partial
correlations remainsignificant
but none of the correlations observed forD
melanogaster
exist in D simulans. DISCUSSION AND CONCLUSION Isgeographic
variability adaptive ?
Our results from a
large
number of naturalpopulations
show that Dmelanogaster
isgeographically
much more diversified than D simulans. In Dmelanogaster,
similar variations are observed in differenthemispheres
or continents and these variationsare
parallel
to those observed in Dsinzulan.s,
with theexception
of thesternopleural
bristle number.In D
melanogaster,
parallel
latitudinalclines,
observed on the Americanconti-nent and between
tropical
Africa andEurope, strongly
suggest
anadaptive
signifi-cance of the
geographical variability.
Anotherpossibility
could be that colonisationprior
to invasion. In otherwords,
thevariability
observed on this continent couldbe a
transposition
of apre-existing
variability.
Forexample, populations
of Canadaand northern USA could
originate
fromEurope.
Those from the WestIndies,
Mex-ico and southern USA could
originate
fromtropical
Africa. Such a scenario isquite
possible
since colonisation of the North American continent occurredduring
thelast centuries from different
European
and Africanpopulations
(David
andCapy,
1988).
However,
the similar clines in bothhemispheres
and in the 2sibling
species
favour the
adaptive hypothesis
of thegeographical variability.
Nevertheless,
it isalso
possible
that the colonisation of the American continent from differentparts
of the world reduced the
adaptation
time of thecolonising
populations
to their newenvironment. On the other
hand,
it must be stressed thatadaptation
to newenvi-ronmental conditions can be
rapid.
In thisrespect,
we should indicatethat,
afterits introduction from
Europe
to South America(in Chile),
D subo6scv,ra has been able to establish new latitudinal clines for chromosomalarrangements
in less than adecade
(Prevosti
etal,
1985).
Similarphenomena
were also observed foralloenzyme
frequencies
in D sirnulan.s a few years after the colonisation of theJapanese
islands(Watada
etal,
1986).
Existence of a latitude-related
morphological variability
suggests
that selective factors liketemperature
or rainfall could be involved. Astrong
negative
correlationis observed between latitude and mean annual
temperature,
thetemperature
ofthe coldest month and total annual rainfall.
Morphometrical
latitudinal clinesare thus
strongly
correlated to these averageparameters.
We tried to reach moreprecise
conclusionsby
considering partial
correlations andtaking
out the latitudinalinfluence,
but thisanalysis
failed toproduce
significant
conclusions.Thus,
the mostsignificant
factorsregulating geographical
variations appear to betemperature
and rainfall. While the role of rainfall is difficult to understand andanalyse,
the effects oftemperature
treatments can beinvestigated
in thelaboratory.
In thisrespect,
several authorsincluding
Cavicchi et al(1985)
have shown thatbreeding
at differenttemperatures
may inducedivergence
ofwing
size andshape.
It islikely
that suchphenomena
could be observed for most of the traits related to size as was evidencedby
Anderson(1973)
in Dpsev,doo6sc!ra.
On the otherhand,
it is alsopossible
thatadaptation
is not the result of the effect of asingle
climaticparameter,
but couldbe due to a combination of these factors or to more
complex
environmentaleffects,
including
interspecific
competition.
Although
latitudinal trends of thegeographical variability
have beenclearly
evidenced,
somelongitudinal
variations were also observed. Forinstance,
at agiven
latitude, populations
may bequite
differentalthough they apparently
share similarenvironments. Such is the case of the West Indian and Far Eastern
populations
of D
melanogaster.
Our results on Far Eastenpopulations
are inagreement
with those of Teissier(1957)
and David et al(1976).
Thesepopulations
aregenerally
heavier than
Afrotropical
flies and even heavier thanEuropean
temperate
flies.They
contrast with West Indiesindividuals,
which are smaller thanAfrotropical
ones
(Capy
etal,
1986).
Becauseweight
and size may be related to life duration and because thereproductive
capacity
is also affected in anopposite
way, these resultssuggest
that intercontinental variations may reflect differentecological
strategies.
Indies could be r-selected. In other
words,
West Indianpopulations develop
morerapidly,
are smaller and invest less into eachoffspring
while Far Easternpopulations
develop
moreslowly,
arelarger
and invest more energy into each individual(Taylor
and
Condra,
1980 and referencestherein).
Such differences could be the result of different historiesand/or
local selective pressures.Indeed,
according
to David andCapy
(1988),
Far Easternpopulations
of Dmelanogaster
are ancient(possibly
morethan 10 000
years)
while West Indianpopulations
are recent(a
fewcenturies).
Such data are not available for D simulans since thisspecies
is absent in severalCaribbean islands
(David
andCapy,
1983),
does not exist in most Asian countries and hasonly recently
colonised someparts
of Far Eastern countries likeJapan
(Watanabe
andKawanishi,
1976).
D
melanogaster
versus D simulansTo
explain
the differences ingeographical
variability
between the 2species
severalhypotheses
have beenproposed, mainly by
Choudhary
andSingh
(1987)
andSingh
et al
(1987).
The first
hypothesis,
based on nichewidth, suggests
that Dmelanoga.ster
is morediversified than D sim!lan.s because of a
greater
physiological
and behaviouralflexibility.
Therefore,
thevariability
in bothspecies
should be anadaptive
trait.But,
what is the cause and what is the effect? In otherwords,
is the niche width ofD
melanogaster
larger
than that of D simulans because of greatergenetic
variability,
or is thevariability
of Dmelanoga.ster higher
because of itslarger
niche width?In
natural
conditions,
few data are available on the niche width of these 2species.
Itis
only
known that Dmelanogaster
is more related to human activities and can befound inside
buildings
while D simulan.s remains outside(Rouault
andDavid, 1982;
Capy
etal,
1987).
Intemperate
countries,
Dmelanogaster
is able to use resourceswith a
high
ethanol content while D simulans cannot(see
Parsons,
1983).
Moreover,
D
melanogaster
can be found athigher
latitudes than D simulan.s(Louis, 1983).
Finally,
inlaboratory
conditions,
manyexperiments
on tolerance totemperature,
showed that D
melanogaster
has alarger
spectrum of tolerance(Parsons,
1983;
David et
al,
1983)
suggesting
that thisspecies
could fit into alarger
number ofnatural situations than its
sibling.
Under this
hypothesis,
morphological
variability
between and withinpopulations
should behigher
in Dmelanogaster.
As shown in this paper, such a result is observedat the
between-population
level.However,
for more traits the 2species
have similar levels ofphenotypic
andgenetic
variability
within thepopulation
(see
PartII,
Capy
et
al,
1994).
A second
hypothesis
is that the 2species
have differentgenetic strategies
(Singh
et
al,
1987).
In thisrespect,
Dmelanoga.ster
would be finegrained
while D .simula!as would be coarsegrained
or with ageneral
purposegenotype
(Singh
andLong,
1992).
In otherwords,
facing
diverse environmentalsituations,
D simulans would have fewall-purpose
genotypes
while Dmelanoga.ster
would have manygenotypes
with limited
capacities.
Thishypothesis
assumes that thephenotypic
plasticity
ofD simulans should be
higher
than that of Dmelanogaster,
but is notsupported
by
thepreviously
mentionedexperiments
on tolerance to several stresses. At thetrident
(Capy
etal,
1988)
showing
that thephenotypic plasticity
of D simulans wasinferior to that of D
melanogaster.
It was alsoevidenced, however,
that thepotential
genetic
variation of D simulans washigh
since it waspossible
to selectrapidly
verydark flies with a
pigmentation
scorehigher
than that of Dmelanogaster
naturalpopulations.
The third
hypothesis, proposed by Singh
et al(1987),
refers to the recentworld
expansion
of D simulans from a few individuals native to an Africanancestral
population.
Thishypothesis
is based on the mtDNApolymorphism
whichis
drastically
reduced in D simulanscompared
to Dmelanogaster
(Baba-Aissa
andSolignac,
1984;
Hale andSingh,
1985;
Solignac
andMonnerot,
1986).
Formorphological
traits,
thishypothesis
raises thequestion
of the timerequired
for anewly
arrivedpopulation
to beadapted
to its new environmental conditions. In thisrespect,
theonly
naturalexperiment
is the recent introduction of D simulans into the main islands ofJapan
(Watanabe
andKawanishi,
1976).
Although
theorigin
of colonisers is not
known,
in less than 10 years some latitudinal cline werealready
observed for
morphological
traits(Watada
etal,
1986).
According
to theseauthors,
thegeographical
differentiation occursrapidly
for a trait like ovariolenumber,
and at variousspeeds
for other traitsdepending
on theiradaptive
value.Thus,
fortraits under
high
selective pressures, somegeographical divergence
mayrapidly
appear. In other
words,
even if theexpansion
of D .simulans wasrelatively
recentcompared
with that of Dmelanogaster
(Lachaise
etal,
1988),
there wasenough
time for the new
population
to beadapted
to the newenvironment,
at least forsome
morphological
traits.A fourth
hypothesis proposed
toexplain
the difference ofgeographical variability
between the 2sibling
species,
is that the mutation rate could behigher
inD
melanogaster.
The mainargument
in favour of thishypothesis
is that theproportion
of nomadic sequences issuperior
in Dmelanogaster
(Dowsett
andYoung,
1982),
such sequencesbeing
able togenerate
chromosomalrearrangements
and mutationsby
insertion orimprecise
excision.Singh
et al(1987)
argued
that thishypothesis
could notexplain
thegeographical
differentiation of the2
species.
On the otherhand,
it is also assumed that nomadic sequences liketransposable
elements may be involved in theadaptation
of naturalpopulations
to the environment
(McClintock,
1984;
McDonald etal,
1987).
Indeed,
mobility
of
transposable
elements may create a newvariability
which can be selected atthe
morphological
level(Mackay,
1984;
Pignatelli
andMackay,
1989).
Concerning
thediversity
oftransposable
elementsalready
described,
the 2species
are not sodifferent.
Although
Dmelanogaster
has been moreextensively studied,
most of the elements arepresent
in bothspecies,
with a fewexceptions
including
P andmariner
(Brookfield
etal,
1984;
Maruyama
andHartl,
1991).
It is notknown,
however,
whether the elements have different mobilities in the 2species.
Inoue and Yamamoto(1987)
showed that the mutation rateby
insertion of mobile elementsin the white gene of D
simulans,
was similar to that observed in Dmelanogaster,
suggesting
that the 2species
have similarpotential
variability.
In
conclusion,
and inspite
of severalhypotheses,
some of thembeing
notmutually
work
previously published,
thegeographical variability
wasmainly
considered whilethe
within-population
component
remainedpoorly investigated.
It is not known whether thepotential
forvariability
is the same in the 2species
and whether thesepotentialities
areexpressed
and used in similar ways. Thisproblem
is considered inPart II
(Capy
etal,
1994).
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