B i o / o @ a l J o u d ojthe Linnean Society (1981). 16: 227-241. with 3 figures
Evolutionary relationships to parasitism
by seven species of the
D rosophila melanogaster subgroup
Y.CARTON AND H.KITANO*
Laboratoire de Biologie et Ginitique Evolutives,
CNRS 91 190, Gf-sur-Yvette, France
Acceptedfor publicationJune 1981
Parasitic wasps are an important component of the niche of DTOSOphih species. The susceptibility to
the Cynipid Leptopilina boulardi was estimated in the seven sibling species of Drosophila belonging to
the m l a n o p t e r subgroup. Three categories of Hies can be distinguished, according to the level of
cellular immune reaction and success of parasitism. Drosophila mclanogastcr and D. mauritiana belong to
the category 1, specified by no encapsulative reaction and a high rate of successful parasitism.
Category 2, characterized by a moderate encapsulation rate and a high mortality include D. simuhn.5,
D . erecta and D . orena. Category 3, with D. y a h b a and D . tcissien', is specified by a very low rate or
absence of successful parasitism due to a highly efficient immune cellular reaction. This classification
parallels the phylogenic relationship based upon polytene chromosome banding sequences. Such
specific ditferences in susceptibility to parasites may plan an important role in the competition
between these species in Africa.
KEY WORDS:- Drosophila - parasitic wasps - immune reaction - evolutionary relationship
specificity.
- host
CONTENTS
Introduction . . . . . . . . . . . . . . . . . .
Materials and methods
. . . . . . . . . . . . ..
Hosts
. . . . . . . . . . . . . . . . ..
Parasites
. . . . . . . . . . . . . . . . .
Experimental procedures . . . . . . . . . . .
Method for calculating the three weighted parameters .
.
Results
. . . . . . . . . . . . . . . . . ..
.
Responses to the parasite during the host selection process
Degree of the immune cellular responses against the parasite .
Discussion
. . . . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . .
References
. . . . . . . . . . . . . . . . . .
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227
228
228
229
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230
251
231
231
235
240
240
INTRODUCTION
Some principles of the general theory of predation apply to a certain extent to
parasitoid-host systems (Pianka, 1978; Hassel, 1978; Price, 1980). This theory
*Present address: Department of Biology, Tokyo Gakugei University, Koganei Tokyo 184, Japan.
0024-4066/8 1/070227 + 15S02.00/0
221
0 1981 The Linnean Society of London
228
Y. CARTON AND H. KITANO
predicts a coevolutionary process between the two interacting species: whereas
the host is permanently selected for increasing its tolerance, the parasite tends to
improve its success (Pimentel, 1961; Levin, 1972; Clarke, 1976). It is frequently
observed that a parasite has more success on the host with which it has long been
associated; authors frequently thus define a ‘natural’ host. Of course, such a
host-parasite association lives in habitats where competition between species of
the same trophic level are also likely to occur, so that the analysis of genetic
coevolution and parasite specificity cannot be separated from the study of natural
populations and communities (MacArthur, 1965; Futuyma, 1979).
Entomophagous parasites now appear to be an important component of the
niche of various Drosophilu species (Parsons, 1977). For example, Brncic (1966)
observed in Chile that about 50% of D.,@uopilosu pupae are parasitized by parasitic wasps. Among pupae of D . mehgaster and D . simulum collected from
Opuntia in Tunisia, levels of parasitism by Leptopilinu, a cynipid parasite, have
ranged between 47 and 64% (Rouault, 1979). In the Ivory Coast, among the 145
D . yukubu emerged from a h i t of Deturium, 37% of the individuals had a
melanotic capsule in their abdomen due to a successful reaction against a cynipid
parasite (Lachaise & Couturier, pers. comm.). The selective pressure exerted by
these parasites upon natural populations of Drosophilu is consequently very
important. The Drosophilu model provides an excellent opportunity to analyse the
various aspects of coevolution. In this paper, we focus our interest on the problem of host specificity, as studied in laboratory experiments and its relationship
to host phylogeny
Extensive collections of Drosophilu in Africa during the years 1970-1975 have
greatly increased our knowledge on the species closely related to D . melunogaster.
The melunogaster subgroup now includes seven members and, except for D .
melunogaster and D . simuluns, appears to be restricted to Afi.ica (Tsacas& Bocquet,
1976; Tsacas, 1979). These seven species can be considered as veryrlosely related
(Parsons, 1975; David et d.,1974; Tsacas & David, 1978). The females are difficult
to identify with certainty, but the males are easily characterized by their genitalia.
The evolutionary relationship between these species has been studied through the
banding pattern analysis of their polytene chromosomes (Lemeunier &
Ashburner, 1976). The degree of susceptibility of these seven species to a specific
wasp Leptopilinu boulurdi (Barbotin et ul., 1979; Nordlander, 1980) is evaluated in
this study. Drosophilu larvae are able to roduce a cellular immune reaction
(Carton et ul., 1980)which is more or less e ective in inhibiting the parasite egg or
larval development. We find differential susceptibilities and defense capacities
among these seven possible hosts which broadly correspond to their phylogenic
relationships.
K
MATERIALS AND METHODS
Hosts
The list of Drosophilu species and strains which were used in the present stud
given below. The strain number refers to the Gif laboratory collection;
and collecting date are indJcated.
Drosophilu melanogarter Meigen ( 1830)
Strain 173-1 ; Petit Bourg, Guadeloupe; 7/75.
SUSCEPTIBILITY T O PARASITISM IN DROSOPHILA
229
Drosophila simulans Sturtevant ( 1929)
Strain 20-2; Brazzavillle, Congo; 7/70.
Drosophila muuritiana Tsacas and David ( 1974)
Strain 163-1 ; Tiviere Noire, Mauritius; 8/73.
Drosophila erecta Tsacas & Lachaise (1974)
Strain 154-1; Lamto, Ivory Coast; 6/71.
Drosophila orenu Tsacas 8c David ( 1978)
Strain 188-1; Bafut Ngemba, Cameroun; 10/75.
Drosophila yakuba Burla ( 1954)
Strain 185-3; Kounden, Cameroun; 10/75.
Drosophila teissieri Tsacas ( 197 1)
Strain 128-2; Mt Selinda, Rhodesia; 1/70.
All species grow well at 25OC on axenic medium without ethanol (David &
Clavel, 1965).
Paracites
The procedure for rearing of parasites has been given in a previous paper
(Carton, 1976). Leptopilinu boulurdi (strain G 301-1) lays its egg inside a Drosophilu
larva, especially in the second instar stage. The egg hatches within about 48 h; the
young wasp larva develops inside the Drosophila larva, which continues its development and finally pupates. The parasitic wasp larva completes its development
in the host puparium and emerges as an adult after 18 days at 25OC. Only one
parasite develops in each host.
Experimental procedures
Ten 5 day old experienced females of L. boulurdi were introduced for 24 h into a
plexiglass box (90 x 60 x 50mm) containing 40 host larvae deposited on a small
disc of medium (25mm diameter, 1.5 mm depth). Experienced females are those
which had oviposited before (van Lenteren, 1976). Host larvae were 24 h old at
the beginning of the experiments; consequently, parasitic females oviposited in
second instar larvae. Twenty-four hours later, larvae were picked up from the
medium, and divided into two equal batches. Those of the first were dissected 24
h later; those of the second were bred on medium up to eclosion of files (on day
9) and wasps (on day 21). This test was repeated at least eight times for each
Drosophila species. Controls with 40 unparasitized larvae were available for each
test to evaluate the mortality due only to experimental conditions of handling
and breeding. All experiments were conducted in a constant-temperature room
held at 25OC.
Larvae were dissected 24 h following the end of the parasite oviposition period,
i.e. 72 h subsequently to hatching, and four parameters were determined.
(1) The rate of mortality (%) of Drosophilu larvae in experiment (RLM) and
control (RLMc) during the host developmental period from 24 to 96 h. This
comparison permits evaluation of the susceptibility of the hosts to the injury
caused by parasite oviposition (piercing, probing by ovipositor, injection of
substances).
(2) The degree of infestation ( D I ): % of Drosophilu larvae containing one parasitic egg at least.
(3) The degree of superparasitism: % of Drosophilu larvae containing more than
one parasitic egg.
Y. CARTON AND H. KITANO
230
(4) The mean number of parasite eggs (MNE) per arasitized larva.
( 5 ) The encapsulation rate (ER), i.e. the intensity o cellular immunity against
the parasite: % of host larvae which encapsulated all the parasitic eggs present in
P
their general body cavity. Preliminary results showed no correlation between the
degree of superparasitism and the encapsulation rate.
Observations obtained on day 21 (emergence of adult flies and parasites) permit a determination of three parameters.
( 1 ) The rate of successful parasitism (RSP) of Drosophila: % of adult wasps
emerging.
(2) The rate of host emergence (RHE):% of adult flies emerged either from
unparasitized larvae or from parasitized larvae in which the development of the
parasitic egg was arrested by immune encapsulation.
(3) The rate of pupal mortality in experiments (RPM) and control (RPMc)
during the period from 72 h to day 21.
The sum of these three parameters equals 100%. They were calculated from the
number of surviving larvae at 72 h.
The efficiency of defense reactions of the seven Drosophila species can then be
compared exclusively if the influence ofvariow levels of infestation and ofmortality due
to breeding conditim is eliminated.
Preliminary experiments have been conducted and have shown that the entire
experimental mortality (RM),i.e. larval and pupal mortality was correlated to the
degree of infestation (RM=0.21 DI-2.34, r=0.78). We must point out that for
the evaluation of rate of mortality, we only take into account dead pupae from
which neither fly nor wasp emerge (Drosophila pupae giving a living parasite are
included in successful parasitism). In fact, preliminary dissections showed us that
these dead pupae never contain a dead parasite; death of parasitized pupae
occurs during its late development specially pupation. On the other hand, it
stands to reason that RSP is directly correlated to DI.Consequently, a weighting
factor F was conducted to consider the infestation in each Drosophila species as
equal to 100%:
F= 100
-
DI
Rates of larval and pupal mortality and rate of successful parasitism were
weighted by the factor F (see below).
Secondly, control mortality was always substracted from experimental mortality, to take into account only the mortality which reflected the sensitivity of
Drosophila species to the parasite (whenRLh4 is less than RLMc, or RPM is less than
RPMc, we let RLM-RLMc-0 and RPM-RPMc=O).
Hence, a new rate of successful parasitism (nRSP),a new rate of mortality (nRM
and a new rate of host emergence (nRHE) can be calculated and symbolize
weighted results. They must be calculated from the number of larvae available at
the beginning of experiment.
Methodfor calculating the three weighted parameters
New rate ofmortdiQ (nRM)
Period from 0 h (hatching of Drosophila eggs) to 72 h
experimental larval mortality= RLM -RLMc
SUSCEPTIBILITY TO PARASITISM IN DROSOPHILA
23 1
weighted experimental larval mortality= F x ( 11,
i.e. F x (RLM-RLMc)
( 2)
percentage of larvae surviving after 7 2 h= 100-(2),
i.e. [lOO-Fx (RLM-RLMc)l
(3)
Period from 72 h to day 21
experimental pupal mortality= RPM -RPMc
(4)
weighted experimental pupal mortality= F x (41,
i.e. F x (RPM-RPMc)
(5)
Period from 0 h (hatching of Drosophila eggs) to day 21.
The weighted entire experimental mortality (nRM)must be calculated from the
number of larvae available at the beginning of experiment.
Considering that RPM was calculated from the number of surviving larvae at
72 h, the ‘true’ mortality from 72 h to day 21, calculated from the number of
larvae available at the beginning of experiments is equal to (3)x (51,
i.e. [lOO-Fx(RLM-RLMc)l x [ F x ( R P M - R P M c ) l
Consequently nRSP=(2) + ( 6 ) ,i.e.
nRSP=[Fx (RLM-RLMc)l+
“ 1 0 0 - F x (RLM-RRLMc)] x [ F x (RPM-RPMc)II
(6)
New rate of successful parasitism (nRSP)
Similarly to RPM, RSP was calculated without considering the larval mortality;
hence
nRSP=(3) x [ F x (RSPII
= [ ~ O O - F X ( R L M - R L M C ) IX [ F x (RSP)]
New rate ofhost emergence (nRHE)
nRHE=[lOO-(nRM +nRSP)I
RESULTS
Responses to theparasite during the host selectionprocess
Under the same experimental conditions, the rates of infestation of Drosophila
species varied from 44 to 93% (Table 1). I t appears that larvae of the different host
species, although very similar in size and shape can be distinguished at some
degree by the female wasp. We must point out that all host species were supplied
singly in these tests, and no choice between two or more host species was
attempted.
Mean numbers of eggs per Drosophila larvae, are given in Table 1 and show a
fairly broad range of variation ( 1.9 - 3.94). In fact, these variations are mainly
explained by variations of degree of infestation, since the two traits are highly
correlated (r=O, 66).
Degree ofthe immune cellular responses against the parasite
The production of an adult wasp from a parasitized Drosophila larvae depends
on two traits: larval mortality and defense capacity of the host.
, due to sting and perhaps venom, can be calculated from
between RLM and RLMc. A significant increase occurred
16
Table 1. Results obtained from the dissection, 72 h after the beginning of infestation. For the degree
of infestation (DZ)
the encapsulation rate (El?),the rate of larval mortality in experiments (RLM) and
control (RLMc), ranges in parentheses are 95% confidence limits. For the rate of mortality in
controls, the number of breeding larvae is also specified in parentheses.
D . mehogaster
7 20
360
78.9
(75-84)
2.14
0.7
(0-2)
4.2
(2-8)
D . sinnclmrr
640
315
75.6
(71-81)
2.67
29.8
(25-36)
1.6
(0-4)
44.1
(38-49)
1.9
30.5
(25-36)
4.5
(1-5)
( 1-41
5.0
(3-8)
(360)
1.6
( 1-41
(320)
D . mmrrilmtia
640
320
1.6
(sm)
D . erecla
880
160
77.5
(70-84)
2.71
21.8
(16-49)
63.9
(56-72)
32.5
(28-37)
D. OTCM
640
157
92.6
(87-96)
3.94
47.9
(40-56)
52.5
(44-60)
36.4
(31-42)
D. gahuba
640
309
68.6
(62-73)
3.74
85.4
(82-90)
2.7
( 1-5)
D. rcirsicri
640
294
53.1
(47-59)
1.9
90.4
5.9
(4-9)
(440)
(320)
3.7
(2-6)
(320)
(86-93)
6.9
(4-10)
(320)
233
SUSCEPTIBILITY TO PARASITISM IN DROSOPHILU~
only in two species ( D . erectu and D. orma) which present a high susceptibility. In
all other species, the mortality w a s not higher than in the controls. According to
current theory, a host is said to be immune if it displays defense mechanisms
which suppress parasite development (active immunity). This process takes the
form of a cellular effect, resulting in the formation of a cellular pigmented capsule around the parasite egg. The encapsulation rate ( E N varied from 0.7 to
loo
A
f"
50
h1' Z
T
Do
0
0
100
Dma
50
0
3
50
too
Encapsulation rate (%)
Figure 1. Rate of successful parasitism as an inverse function ofthe cehlar immune reaction for each
sibling species of Drosophila. A. Experimental results. B. Weighted results. (De, D.erccta; Dm,
D . mlano~aster;Dma, D . mauritiana; Do, D . OTCM;Ds, D . simulmrr; Dt, D . triSsini;Dy, D . yahuba(the bars
indicate 95% contidence limits).
Y. CARTON AND H. KITANO
234
90.4%.Three categories of immune responses have been observed among the
seven host species (Figs lA, 2A):D . melunogustcz being characterized by no encapsulative activity, D. ycutuba and D . teisssicn' by a high encapsulation rate. The four
other species have an intermediate state.
This classification agrees with the three groups demonstrating polytene
chromosome affinities (Lemeunier& Ashbumer, 1976).
0
50
loo
Encapsulation mto (Ye)
Figure 2. Rate ot'host emergence as a function of the cellular immune reaction for each sibling
species of Drosophila. A. Experimental mulo. B. Weighted mulo. Abbreviations a8 in Fig. 1.
SUSCEPTIBILITY TO PARASITISM IN DROSOPHILA
235
From the results obtained on day 21, we can show that effective parasitism
(evaluated by the rate of successful parasitism, i.e. RSP) varies with the host
species in a similar pattern of affinities (Fig. 1A).
The emergence of parasites is inversely related to the degree of cellular response of hosts (Fig. 1A).For all species, except D . mauritianu, it is observed that a
more intense immune response resulted in a lower degree of successful parasitization. In D . mauritiana, the cellular reaction against the parasite was not sufficient
to inhibit parasite development.
In the same way, the emergence of flies is positively correlated to the intensity
of cellular immunity (Fig. 2A). In Figs 1A & 2A, the various Drosophila species
seem to follow the order:
-
Dm < DszDe < Do< Dy Dt
We can observe a similar relationship with weighted data (Figs IB, 2B)which
take only into consideration physiological aspects of infestation. In this linear
arrangement, D . melanogaster is assigned to one end and D . teissieri to the other.
The remaining information about the susceptibility of the sibling species to the
parasite concerns their ability to develop up to pupariation with a parasitic larva
in the coelomic cavity. In fact, only D . simulans seems to present a high sensitivity
during parasite development, the experimental mortality rate being sharply
higher than in controls (Table 2).
A synthesis of all these results is given in Fig. 3A.This representation integrates
the three parameters : successful parasitization, host emergence and mortality.
Excluding D . mauritianu, the six other sibling species are distributed within the
following three groups:
( 1) D . melanogmter.
(2) D . simulans, D . erecta, D . orena.
(3) D . yakuba, D . teissieri.
A similar graphic distribution of Drosophila species is obtained with weighted
results (Fig. 3B). However, D . orena is now located near D . yakuba and D . teisszen'
because its high control mortality rate is now dismissed. For D. mauritiana which
reacts like D . melanogaster, successful parasitization is higher because the degree of
infestation is similar for all species (DZ= 100%) in weighted results.
DISCUSSION
0ther Cynipid parasites of Drosophila and especially Leptopilina heterotoma, previously known as Pseudeucoila bochei (Nordlander, 19801,have already been tested
on several species (Jenni, 1951). For example, in six nearctic species of the D .
melanica group, a great number of parasite eggs failed to hatch and many larvae
died in the first stage (Nap i, 1970;Nappi & Streams, 1970).Curiously, examination of the dead parasites ailed to show any encapsulation by hemocytes. On the
other hand, a defence encapsulation process was observed in other Drosophila
species, such as D . hydei (Schlegel-Oprecht, 1953),some strains of D . melanogaster
(Walker, 19591,D . simulans (Hadorn & Grassman, 19621,D . busckii (Streams, 1968)
and D . algonquin (Nappi, 1973).We can notice from these former studies involving
L . heterotoma that none of the Drosophila species examined up till now were
completely immune to this parasite due to their encapsulation capacity. We can
P
m
D . ltissieri
D.
D. wenu
D . crectu
D. tnaurilmrin
D . sirprulmu
D . mchgastcr
51.4
(297)
46.1
(204)
5.2
(308)
14.11
(298)
(315)
9.9
(342)
8.9
(315)
10.5
308
3 14
152
158
304
315
330
0
(0- 1)
34.2
(28-32)
24.7
( 18-32)
10.5
(6-16)
2.9
(1-6)
(12-40)
64.2
(58-69)
15.9
36.5
(31-42)
56.9
(51-62)
21.5
(15-28)
38.8
(31-47)
82.5
(79-87)
87.3
(82-90)
(9-17)
53.8
(46-62)
50.6
(42-59)
14.6
(11-19)
12.7
(6-12)
41.6
(41-52)
8.8
19.4
(16-25)
16.4
(12-21)
0
4.2
9.3
18.9
16.8
21.0
78.9
18.3
0
100.0
21.5
69.2
7 1.4
42.4
0.9
51.3
13.6
38.1
22.3
27.7
6.5
Weighted results (%)
Table 2. Results obtained on day 21 after the beginning of infestation (weighted results are obtained
with a 100% level of infestation, see t a t ) . Ranges in parentheses are 95%confidence limits. For the rate
of mortality in controls, the number of breeding larvae is also specified in parentheses.
P
N
W
01
SUSCEPTIBILITY TO PARASITISM I N DROSOPHILA
231
0
loo
I00
0
50
Successful parasitization (%)
B
50
0
Successful parasitiration (To)
Figure 3. Scheme giving the relative position of the seven DroJophila species with regard to their
response to the parasite. Each DroJophi& species is specified by the three biological parameters RSP,
RHE and RM (see text). Since RSP+ RHE+ R M = loo%, we utilized triangular coordinates. A.
Experimental results. 8. Weighted results. Abbreviations as in Fig. 1.
Y. CARTON AND H. KITANO
298
conclude that L. heterotoma has a low specificity since it develops more or less
successfully on a wide range of Drosophila species.
Leptopilina boulardi, which is mainly found in tropical and subtropical areas
(Nordlander, 1980) appears to have a much narrower specificity. The seven
Drosophila species of the D . melanogaster sub-group are considered by Lemeunier &
Ashburner (1976) as a complex of sibling species but, in spite of this relatedness,
their susceptibility to this arasite varies greatly from one species to another.
During the first ste s o infestation, where parasite behaviour is predominant,
no real significant di erences appear apart from D.mauritiana, which is infested
at a very low rate. However, striking differences are evident in the physiological
responses of these seven species and three categories can be distinguished. If the
degree of infestation is equal to 100%(weighted results, Fig. SB), we obtain the
following classification:
P P
nRSP
70-90%
1625%
&lo%
Category 1 (ER=0-20%)
Category 2 (ER= 2 1-50%)
Category 3 (ER=5 1-90%)
nRHE
0-20%
1040%
75-100%
nRM
&15%
2045%
&25%
Where ER= encapsulation rate; nRHE=rate of host emergence; nRM =rate of
mortality; nRSP=rate of successful parasitism, for a degree of infestation as equal
to 100%.
Host species falling in category 1 fit the definition of a ‘natural’ host, with a
high RSP and a low RM. Drosophila melanogaster belongs to this category. Drosophila
mauritianu is also included, in spite of its encapsulation rate equal to 29%;we may
suppose that immune reaction is not efficient(Fig. lB), so that the hatching of the
parasite egg is not prevented. On the other hand, in Mauritius, D . mauritianu is
endemic where L. boulurdi is perha s absent.
Drosophila simulans, D . erecta an D . o r m are included in category 2, which is
characterized by a moderate encapsulation rate and a high mortality. This high
mortality has already been observed experimentally on D. simulm infested by
L. boulurdi by Rouault (1979) who also observed in field conditions (Tunisia)that
29% of adult flies had a melanotic capsule in their abdomen. This percentage is in
good agreement with the encapsulation rate obtained in laboratory conditions.
3 ( D . yakuba and D . teissim‘) is characterized by a very low rate or
Cat o successful parasitism mainly due to an efficient immune reaction.
absence
Grouping the seven species in three categories appears in some way to parallel
the phylogenic relationships established by chromosomal analysis (Lemeunier &
Ashburner, 1976); this is confirmed by allozyme comparison (Eisses et al., 1979)
and hemocyte study (Rizki & Rizki, 1980). The only discrepancy between phylogeny and parasite susceptibility concerns D . simulanr (Fig. SB) which, as a close
relative of D . melanogarter, should be included in category 1. It is ossible that this
difference is a more recent event, due to the usual sympatq o the two species,
resulting in a physiological character displacement.
Our results suggest that differences in susceptibility to the parasite are fairly
stable and that any genetic modification would need a long evolutionary period.
Such a conclusion seems to contradict the results of Hadorn & Walker ( 1960) who
claimed to observe a rapid change in the encapsulation rate of L. bterotoma by
D . melanogarter larvae. In fact, this conclusion does not seem well founded as the
authors selected a ‘pigment reaction’ (dispersed melanized hemocytes) which is
B
P
SUSCEPTIBILITY TO PARASITISM IN DROSOPHILA
239
not effective for encapsulation. The ability to make a capsule, on the other hand,
appears to have increased through selection by < 2% per generation.
We consider the capacity to encapsulate as a fairly stable characteristic. Bartlett
8c Ball (1966) previously reached a similar conclusion, showing that in several
cases, the encapsulation capacity evolves without the presence of a parasite and
“may have certain general limits of potency beyond which it cannot arise”.
Similarly, with L. boulardi, we have never observed, among the numerous
geographical strains of D . melanogarter studied, an encapsulation level up to 5%
(Carton, 1980).
Leptopilina boulardi appears very specific of D . melanogaster. The concept of
acquisition of host specificity by a predator or a parasite has been repeatly put
forward mostly on theoretical grounds by Levins (1968) and MacArthur (1972).
Specialization on a single host is possible and advantageous when the population
density of the host is high and stable, as in the case of tropical population of
D . melanogaster. In temperate countries, on the other hand, Drosophila populations
are submitted to high fluctuations (Baker, 1979). In this case it would be
advantageous for a parasite to enlarge its host spectrum (Levins, 1968;
MacArthur, 1972). Leptopilina heterotoma, with an holarctic distribution
(Nordlander, 1980), seems to fit this prediction since it successfully develops on a
fairly wide range of Drosophila species (see above and also Baker, 1979). This
different strategy could also ex lain why Hadorn & Walker ( 1960) were, to some
extent, able to increase the de ence reaction of D . melanogaster against this wasp
species. Leptopilina heterotom in temperate areas does not choose D . melanogaster as
its main host and is not strongly adapted to it (Baker, 1979). In the coevolution
process between host and parasite we must note that, according to the ecological
conditions, predictability of the environment and availability of resources,
parasitic wasps may exhibit different strategies, different capacities of adaptation
and different levels of genetic variability. Drosophila parasites, as a whole, should
be good model for checking such a hypothesis.
In a more speculative approach, the role of this parasite in the coexistence of
Drosophila related species is opened to discussion. Paine ( 19661,Janzen ( 1970) and
Connell (1970) have suggested that infestation on a superior competitor may
prevent it from eliminating inferior competitors. Leptopilinu boulardi may, to some
extent play such a role in natural populations. Furthermore, according to
Futuyma ( 19791, coexistence of sympatric host species in a stable environment is
more likely if they differ in their defence systems so that none of them are
subjected to the parasites harbored by the others. In some afrotropical areas
D . melanogaster, D . simulans, D . yakuba, D . teissieri and, more rarely, D . erecta and
D . orena, are found in sympatry (Tsacas & David, 1978; Lachaise, 1979; David &
Tsacas, 1980). All these species are fruit breeders and, like L. boulardi females
(Carton, 1978), are attracted by fermenting substrates. They are likely to be
competitors at least during larval development. It is also known that
D . melanogaster always eliminates D . simulans during competition in population
cages (Tantawy & Soliman, 1967). The two other abundant afrotropical species
(D.yakuba and D . teissieri) have even a lower reproductive potential than
D . simulans (David, pers. comm.) and would probably be more quickly eliminated.
Leptopilina boulardi, which appears specific of D . melanogaster, might play a
significant role in stabilizing these Drosophila communities by decreasing the
population size of the best competitor.
P
Y. CARTON AND H. KITANO
240
ACKNOWLEDGEMENTS
We wish to acknowledge the stimulating and pleasant discussionwith Professor
J. David. Sincere thanks are due Professor P. Chabora for his helpful criticism of
this manuscript.
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