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Advances in
PARASITOLOGY
VOLUME
70
Parasitoids of Drosophila
SERIES EDITORS
D. ROLLINSON
Department of Zoology
The Natural History Museum
London, UK
S. I. HAY
Spatial Epidemiology and
Ecology Group
Tinbergen Building
Department of Zoology
University of Oxford
South Parks Road
Oxford OX1 3PS, UK
EDITORIAL BOARD
M. COLUZZI
Department of Public Health Sciences, Section of Parasitology
‘Ettore Biocca’ ‘Sapienza – Università di Roma’, 00185 Roma, Italy
C. COMBES
Laboratoire de Biologie Animale, Université de Perpignan, Centre
de Biologie et d’Ecologie Tropicale et Méditerranéenne, 66860
Perpignan Cedex, France
D. D. DESPOMMIER
Division of Tropical Medicine and Environmental Sciences,
Department of Microbiology, Columbia University, New York,
NY 10032, USA
J. J. SHAW
Instituto de Ciências Biomédicas, Universidade de São Paulo,
05508-990, Cidade Universitária, São Paulo, SP, Brazil
K. TANABE
Laboratory of Malariology, International Research Center of
Infectious Diseases, Research Institute for Microbial Diseases,
Osaka University, Suita 565-0871, Japan
Advances in
PARASITOLOGY
VOLUME
70
Parasitoids of Drosophila
Edited by
GENEVIÈVE PRÉVOST
Laboratoire de Biologie des Entomophages
Université de Picardie–Jules Verne
Amiens cedex, France
AMSTERDAM • BOSTON • HEIDELBERG • LONDON

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09 10 11 12 10 9 8 7 6 5 4 3 2 1
CONTENTS
Contributors xi
Preface xv
Introduction xvii
SECTION I. ECOLOGY OF DROSOPHILA PARASITOIDS 1
1. Ecology and Life History Evolution of Frugivorous

Drosophila Parasitoids 3
Frédéric Fleury, Patricia Gibert, Nicolas Ris, and Roland Allemand
Distribution, Community Structure and Ecological Interactions
1.1. 6
Drosophila Parasitoid Life Histories
1.2. 15
Geographical Differentiation and Local Adaptation
1.3. 28
Concluding Remarks
1.4. 33
References 35
2. Decision-Making Dynamics in Parasitoids of Drosophila 45

Andra Thiel and Thomas S. Hoffmeister
2.1.Introduction 46
2.2.Levels of Plasticity 46
2.3.Relative Value of Hosts and Patches 48
2.4.Host Patch Detection 50
2.5.Prepatch Experience and (Initial) Leaving Tendency 51
2.6.The Effects of Intrapatch Experience 54
2.7.The Patch-Leaving Decision 56
2.8.Genetic Differences in Searching Behavior 57
2.9.Predation and Starvation 59
2.10.Prospects and Implications 60
Acknowledgments 61
References 61
3. Dynamic Use of Fruit Odours to Locate Host Larvae:
Individual Learning, Physiological State and Genetic
Variability as Adaptive Mechanisms 67
Laure Kaiser, Aude Couty, and Raquel Perez-Maluf
3.1. Introduction 68
3.2. General Material and Methods 71
v
vi Contents
3.3.Dynamics of Odour Memory Displayed in Odour Choices 73

3.4.Dynamics of Odour Memory Displayed in Probing Behavior 77
3.5.Motivation Influences the Learned Searching Responses 81
3.6.Genetic Variability of the Learned Searching Response 83
3.7.Probing in Response to Fruit Odour: When is it Adaptive? 84
3.8.General Discussion and Conclusions 89
Acknowledgements 91
References 91
SECTION II. THE PHYSIOLOGY AND GENETICS OF IMMUNITY

RELATIONSHIPS BETWEEN PARASITOIDS AND THEIR
DROSOPHILA HOSTS 97
4. The Role of Melanization and Cytotoxic By-Products

in the Cellular Immune Responses of Drosophila
Against Parasitic Wasps 99
A. Nappi, M. Poirié, and Y. Carton
4.2. Hemocyte-Mediated Encapsulation 103
4.3. Melanization During the Drosophila Cellular Immune Reaction 103
4.4. Cytotoxic Molecules Associated with Melanization 107
4.5. The Prevention of Phenoloxidase Activity by Parasitoid
Virulence Factors 113
4.6. Conclusions 115
References 116
5. Virulence Factors and Strategies of Leptopilina spp.:

Selective Responses in Drosophila Hosts 123
Mark J. Lee, Marta E. Kalamarz, Indira Paddibhatla, Chiyedza Small,
Roma Rajwani, and Shubha Govind
5.2. The Host Range of L. boulardi and L. heterotoma 126
5.3. Origin of L. heterotoma/L. victoriae VLPs and their Effects
on Host Hemocytes 134
5.4. Host Gene Expression Changes After L. boulardi
and L. heterotoma Infection 138
5.5. Concluding Remarks 141
Acknowledgments 142
References 143
Contents vii
6. Variation of Leptopilina boulardi Success in Drosophila Hosts:

What is Inside the Black Box? 147
A. Dubuffet, D. Colinet, C. Anselme, S. Dupas, Y. Carton, and M. Poirié
6.1.Introduction 148
6.2.Dissection of the Natural Variation of Encapsulation 149
6.3.Host Resistance: Origin of Variation 158
6.4.Parasitoid Virulence: Origin of Variation 163
6.5.Discussion 174
Acknowledgments 183
References 183
7. Immune Resistance of Drosophila Hosts Against Asobara

Parasitoids: Cellular Aspects 189
Patrice Eslin, Geneviève Prévost, Sébastien Havard, and Géraldine Doury
7.2.The Immune System in D. melanogaster 191
7.3.Encapsulation: A Story Based on Quantities 195
7.4.But Does Quality Matter? The Case of the Obscura Group 207
7.5.Discussion and Concluding Remarks 208
Acknowledgment 212
References 212
8. Components of Asobara Venoms and their Effects on Hosts 217

Sébastien J.M. Moreau, Sophie Vinchon, Anas Cherqui,
and Geneviève Prévost
8.2. Anatomy of the Venom Apparatus within the
Asobara Genus 219
8.3. The Venom of A. tabida 224
8.4. The Venom of A. japonica 227
8.5. Expected Prospects from Studying Venoms
in the Asobara Genus 228
Acknowledgments 230
References 230
viii Contents
SECTION III. STRATEGIES AND EVOLUTION OF PARASITOID

VIRULENCE AND HOST RESISTANCE 233
9. Strategies of Avoidance of Host Immune Defenses

in Asobara Species 235
Geneviève Prévost, Géraldine Doury, Alix D.N.
Mabiala-Moundoungou, Anas Cherqui, and Patrice Eslin
9.2. Conformer Versus Regulator Strategy 237
9.3. Arms Developed by Asobara Parasitoids to Regulate or
Evade Host Immunity Defenses 246
9.4. Concluding Remarks and Prospects 250
References 251
10. Evolution of Host Resistance and Parasitoid

Counter-Resistance 257
Alex R. Kraaijeveld and H. Charles J. Godfray
Introduction
10.1. 258
10.2.Drosophila melanogaster and its Parasitoids 259
10.3.Geographic Variation 261
10.4.Experimental Evolution of Resistance and Counter-Resistance 264
10.5.Costs of Resistance and Counter-Resistance 268
10.6.Behavior Related to Resistance and Counter-Resistance 271
10.7.Parasitoids as Hosts 274
10.8.Genetics and Genomics 274
10.9.Concluding Remarks 276
References 277
11. Local, Geographic and Phylogenetic Scales of
Coevolution in Drosophila–Parasitoid Interactions 281
S. Dupas, A. Dubuffet, Y. Carton, and M. Poirié
11.2. The Local Coevolutionary Dynamics 284
11.3. The Components of the Geographic Mosaic of Coevolution 289
11.4. Hypothesis of Coevolutionary Diversification 291
11.5. Ancestral Traits and Phylogenetic Constraints
on Coevolution 292
11.6. Conclusion 292
References 293
Contents ix
SECTION IV. SYMBIOTIC ORGANISMS OF DROSOPHILA PARASITOIDS 297
12. Drosophila–Parasitoid Communities as Model Systems

for Host–Wolbachia Interactions 299
Fabrice Vavre, Laurence Mouton, and Bart A. Pannebakker
12.2. Pattern of Infection and Phylogenetic Diversity of
Wolbachia in Drosophila Parasitoids 302
12.3. Phenotypic Diversity of Wolbachia in Drosophila Parasitoids 308
12.4. Stability, Regulation and Consequences of Multiple
Wolbachia Infections 317
12.5. The Role of Wolbachia in the Interaction Between
Parasitoids and Hosts 320
Acknowledgments 325
References 325
13. A Virus-Shaping Reproductive Strategy in a Drosophila Parasitoid 333

Julien Varaldi, Sabine Patot, Maxime Nardin, and Sylvain Gandon
13.2. Main Effect and Transmission of LbFV 335
13.3. Adaptive Significance of Superparasitism Alteration:
A Modelization Approach 337
13.4. Effect of LbFV on Other Phenotypic Traits 340
13.5. Adaptive Significance of the Phenotypic Alteration Induced
(Except Superparasitism) 346
13.6. Evolution in Relation to the Frequency of Horizontal
Versus Vertical Transmission 348
13.7. Experimental Evolution in Relation to Transmission
Type (Horizontal or Vertical) 352
13.8. Other Viruses in the Drosophila–Parasitoid Community 355
References 359
Index 365
Contents of Volumes in This Series 373
Color Plate Section at the end of the Book
CONTRIBUTORS
Roland Allemand
Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie
Evolutive, F-69622 Villeurbanne, France
C. Anselme
Institut National de la Recherche Agronomique, INRA Sophia Antipolis,
UMR 1301; Centre National de la Recherche Scientifique, CNRS, UMR
6243; Université Nice Sophia Antipolis, UFR Sciences, France
Y. Carton
IRD, UR072 Laboratoire Evolution, Génomes et Spéciation/UPR9034,
CNRS 91198 Gif-sur-Yvette Cedex, France/Université Paris-Sud 11,
91405 Orsay Cedex, France
Anas Cherqui
Laboratoire de Biologie des Entomophages, EA 3900 BioPI, Université de
Picardie-Jules Verne, 33 rue Saint Leu, 80039 Amiens cedex, France
D. Colinet
Institut National de la Recherche Agronomique, INRA Sophia Antipolis,
UMR 1301; Centre National de la Recherche Scientifique, CNRS, UMR
6243; Université Nice Sophia Antipolis, UFR Sciences, France
Aude Couty
Unité de Recherche EA3900 BioPI-UPJV; Biologie des plantes et contrôle
des insectes ravageurs; Laboratoire de Biologie des Entomophages;
Faculté des Sciences, Ilot des Poulies, 33 rue Saint Leu, 80039 Amiens
Cedex, France
Géraldine Doury
A. Dubuffet
Institute of Integrative and Comparative Biology, Faculty of Biological
Sciences, University of Leeds, United Kingdom
xi
xii Contributors
S. Dupas
IRD, UR072 Laboratoire Evolution, Génomes et Spéciation/UPR9034,
CNRS 91198 Gif-sur-Yvette cedex, France/Université Paris-Sud 11,
91405 Orsay cedex, France; and Pontificia Universidad Católica del
Ecuador, Facultad de Ciencias Exactas y Naturales, Quito, Ecuador
Patrice Eslin
Frédéric Fleury
Sylvain Gandon
Centre d’Ecologie Fonctionnelles et Evolutives (CEFE) – UMR 5175, 1919
route de Mende, F-34293 Montpellier cedex 5, France
Patricia Gibert
H. Charles J. Godfray
Department of Zoology, University of Oxford, Oxford OX1 3PS, United
Kingdom
Shubha Govind
Department of Biology, The City College of New York, New York, NY
10031, USA; and The Graduate Center of the City University of New York,
New York, NY 10016, USA
Sébastien Havard
Thomas S. Hoffmeister
Institute of Ecology, University of Bremen, FB 02, D-28359 Bremen,
Germany
Laure Kaiser
INRA Centre de Versailles-Grignon; UMR 1272 Physiologie de l’Insecte
Signalisation et Communication, Route de St Cyr, 78026 Versailles
Cedex, France; and IRD, UR 072, c/o Laboratoire Evolution, Génomes et
Spéciation, UPR 9034, CNRS, 91198 Gif-sur-Yvette Cedex, France
Contributors xiii
Marta E. Kalamarz
Alex R. Kraaijeveld
University of Southampton, School of Biological Sciences, Southampton
SO16 7PX, United Kingdom
Mark J. Lee
Department of Biology, The City College of New York, New York,
NY 10031, USA
Sébastien J.M. Moreau

UMR 6035 CNRS, Institut de Recherche sur la Biologie de l’Insecte,
Faculté des Sciences et Techniques, Université François-Rabelais, Parc
Grandmont, 37200 Tours, France
Alix D.N. Mabiala-Moundoungou

Laurence Mouton
A. Nappi
Department of Biology, Loyola University of Chicago, Chicago, IL 60525,
USA
Maxime Nardin
Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1; CNRS;
UMR 5558, 43 boulevard du 11 novembre 1918, F-69622 Villeurbanne,
France
Indira Paddibhatla
Bart A. Pannebakker
Evolutionary Genetics, Centre for Ecological and Evolutionary Studies,
University of Groningen, P.O. Box 14, NL-9750 AA Haren, The Netherlands
xiv Contributors
Sabine Patot
UMR 5558, 43 boulevard du 11 Novembre 1918, F-69622 Villeurbanne, France
Raquel Perez-Maluf
Laboratório de Zoologia, DNC/UESB, Estrada do Bem Querer KM 04,
Vitoria da Conquista, 45000 BA, Brazil
M. Poirié
UMR Interactions Biotiques et Santé Végétale, Institut Agrobiotech, 06 903
Sophia Antipolis, France. INRA, UMR 1301/CNRS UMR 6243/Université
Nice Sophia Antipolis, 28, avenue de Valrose, 06103 Nice Cedex 2, France
Geneviève Prévost
Roma Rajwani
10031, USA
Nicolas Ris
Centre INRA de Sophia Antipolis, Unité Expérimentale 1254 ‘‘Lutte
Biologique’’, BP 167, F-06903 Sophia-Antipolis, France
Chiyedza Small
Andra Thiel
Institute of Ecology, University of Bremen, FB 02, D-28359 Bremen, Germany
Julien Varaldi
UMR 5558, 43 boulevard du 11 novembre 1918, F-69622 Villeurbanne, France
Fabrice Vavre
Sophie Vinchon
PREFACE
Extensive studies have been conducted on various parasitoid species, and

almost all different approaches of the biology of parasitoids have been, at
least once, studied on parasitoids of Drosophila. Originally, this particular
interest for species parasitizing Drosophila hosts has been motivated by
the exceptional knowledge we have on Drosophila species themselves, and
particularly on Drosophila melanogaster. Benefiting from this knowledge,
the research conducted on Drosophila parasitoids has covered very diver-
sified topics, such as physiological and immunity relationships with
hosts, reproduction strategies, the role of symbiotic microorganisms,
behavioral and chemical ecology, genetics, population dynamics, evolu-
tionary biology, the different approaches of which include field surveys,
and laboratory experiments. As a result, we now benefit from a particu-
larly vast and extended knowledge of the biology of these parasitoid
species and of their relationships with their Drosophila hosts.
Thanks to the authors who kindly contributed to the writing of this
special volume, the book highlights the diversity of the fields of research
that have been explored on Drosophila parasitoids. It also points out that
this biological model is of particular interest for an evolutionary approach
to parasitism.
Due to circumstances beyond our control, Professor Jacques J.M. Van

Alphen (University of Leiden, the Netherlands) could not contribute to
this volume in the section 1 on the ecology of Drosophila parasitoids.
Because of the particularly important work of Pr. J.J.M. Van Alphen on
the evolution of life histories and foraging behaviour in larval parasitoids
of Drosophila, I strongly recommend to study his amazing bibliography.
GENEVIÈVE PRÉVOST
xv
INTRODUCTION
Although for a long time parasitoid insects have received much attention,
most former studies were focused on their interest as biocontrol agents.
Now, however, academic research on parasitoid insects has developed
and reached a full and very promising maturity.
As studies led to a better balance between the classic applied and
academic sides, researchers turned to other insect species, correlatively,
and as well as species of agricultural importance, new biological models
progressively obtained increasing favor due to their suitability for labora-
tory and field studies. Obviously, Hymenopteran Drosophila parasitoids
offer exceptional advantages in all respects and despite their lack of
interest for agriculture, they have been adopted as biological models by
more and more, mainly European, teams.
In 1986, they were included in Ashburner’s monumental treatise
on Drosophila spp., and the chapter written by Y. Carton, M. Boulétreau,
J. van Lenteren and J. van Alphen in vol. 3e synthesized previous data,
together with current work. More than 20 years ago, this paper highlighted
a number of questions that, hopefully, Drosophila parasitoids could help
to answer. It is time now to restate the field, and owing to her enthusiasm
and energy, Professor Geneviève Prévost has succeeded in convincing a
number of outstanding authors to contribute to the challenge.
Section I considers the ‘‘preovipositional’’ relationships of parasitoids
with their Drosophila hosts; this encompasses all the steps (mainly ecolog-
ical and behavioral) that precede the actual physical contact between the
parasitoid and its host individual, and which thus correspond to the
classic ecological and encounter filters of parasitologists. Populations
and communities submit to a number of particular constraints from
their common environment that are not evenly distributed over time
and space. Chapter 1 considers the temporal and spatial organization of
communities on different scales. The seasonal and the daily organization
of activities reveal a fine interspecific tuning which could enhance the
probability of parasitoids encountering suitable hosts, and also mediate
competition among parasitoid species, thus promoting their coexistence
and enhancing the stability of the whole community. Comparative stud-
ies bring to light significant variations of populations and communities on
a narrow geographic scale, suggesting fine local adaptation to ecological
conditions that are mainly climatic. Genetic analysis establishes the role
of natural selective pressures in shaping life-history traits, suggesting a
xvii
xviii Introduction
dynamic equilibrium of populations and communities with their local

environmental constraints, which is likely to be open to adaptive varia-
tion as a response to predictable long-term climatic changes.
At the individual level, behavioral relationships of parasitoids with
their hosts have reached an extreme degree of sophistication, probably
unmatched among the whole invertebrate phylum. Two chapters are
devoted to this field, each of them taking a particular approach. Under-
standing of the individual relationships between a parasitoid and its hosts
necessarily takes into account the immediate external context where they
are living. Behavior leading to host infestation is not a fixed pattern, but
will depend first of all on several external conditions that need to be
considered on different scales, both spatial and temporal. Those directly
arising from insects themselves are of special interest. Among others, host
diversity and suitability, host abundance and distribution, the presence of
potential competitors, whether conspecific or not, will strongly influence
the foraging female and orientate her behavioral decisions. Second, the
inner state of the female herself, both physiological and informational,
will also change her decision when faced with a given external context.
Field observations, experimental analysis and mathematical modeling
generally confirm the theoretical prediction that the female behaves so
as to optimize her own fitness. That leads us to credit females with a
surprising analysis/integration capacity, which is logically taken as
resulting from natural selection; however, the origin and acquisition of
such a capacity remain doubtful and clearly call for further studies.
Both chapters deal with behavioral phenomenology: which cues,
which receptors are involved, and how parasitoids use information to
successfully reach and discriminate their hosts. We are not surprised by
the specificity of responses to cues emanating from the host habitat and
from the host itself, but we discover the complexity of the integrative
process that results in a precise decision made by females under given
circumstances. Memory; experience; assortative learning; estimates of
space, of time and perhaps of numbers; and decision-making have long
been considered as a prerogative of vertebrates, but it is now clear that
insects are also capable of such achievements. In this field, Drosophila
parasitoids demonstrate incredible performances, ending in highly effi-
cient host infestation strategies. Adaptiveness of such behaviors is quite
obvious, and their variation, whether epigenetic or genetic, allows
females to adapt to the precise situation they are faced with perfectly,
on the immediate individual scale and on the ecological and evolutionary
ones. The consistency of these chapters is mostly based on their common
evolutionary approach, which is the actual thread of the whole book.
Obviously, the authors have made the most of using Drosophila parasi-
toids in their studies, whereas scattering their efforts over various para-
sitoids would not have made for such consistency.
Introduction xix
Section II is devoted to ‘‘postovipositional’’ host–parasitoid relation-

ships, that is the compatibility filter. In the absence of any study of the
physiologic components of the filter (e.g., biochemical, hormonal or devel-
opmental), this section focuses on the immunological host–parasitoid
relationships. We can regret that only endoparasitoids of host larvae are
considered: no reference can be found to the immunological situation of
endopupal parasitoids, or to any possible conflict between the host pupa
and its ectoparasitoids. That means that the studies only deal with ‘‘koi-
nobiotic parasitoids,’’ those species which spare their host’s survival as
long as they need it for their own development, and thus behave like ‘‘true
parasites’’ for a while. We can, however, wonder whether ‘‘idiobiotic
parasitoids,’’ which generally kill their host at the earliest stages of their
own development, suffer any kind of defense from their host. To be
honest, the boundary between ‘‘host killers’’ and ‘‘host savers’’ is some-
what fuzzy, and furthermore we perfectly understand and share the
special attention that koinobionts have received, since only their biology
allows immunological conflicts to take place for a significant duration.
In this immunological field, Drosophila parasitoids offer the unique
opportunity for researchers to put a symmetrical effort into studying both
hosts and parasites. As far as we know, no other insect system allows such
a comprehensive analysis of the whole immunological race. Three main
parasitoid species are studied: Leptopilina boulardi, Leptopilina heterotoma
and Asobara tabida, which belong to different Hymenoptera families:
Figitidae and Braconidae, respectively, and which exploit a few Drosophila
spp., mainly frugivorous, often in sympatry. They have rather similar
within-host developmental strategies: infestation at the very beginning of
the larval host life, then solitary endoparasitic development until host
pupation, and finally saprophytic consumption of the host pupa tissues
before nymphosis. Free pharate imagos emerge from the mummified host
puparium, the envelope that the host larva had built for its own protec-
tion before metamorphosis. The immunological reaction of the host and
the reciprocal counter-reaction of the parasitoid occur at an early stage of
infestation, and mostly address parasitoid eggs. It is worth keeping in
mind that compared to most other host–parasite systems, survival of both
the host and the parasite is quite impossible: either the host succeeds in
killing its parasite and then survives, perhaps at some cost to itself but
with the benefit of life, or the parasitoid evades or overcomes the host’s
defenses, then carries on with its own development. The alternative is
terrible and suffers no exception, at least in Drosophila parasitoids. We
thus understand that such a vital challenge results in drastic selection
pressure on both partners, and has elicited powerful defense and counter-
defense mechanisms. Chapters 4–8 explore the biochemical and physio-
logical mechanisms involved in host ‘‘resistance’’ (its ability to survive
infestation) and parasitoid counter-resistance or ‘‘virulence’’ (its ability to
xx Introduction
survive the host’s defenses). In hosts, authors give a thorough analysis of

the sequence of events, be they molecular, biochemical or cellular, that are
elicited by the infestation and will end in parasite elimination. More than
one path exists, and the outcome can result from the synergic interplay of
several of them. Moreover, different parasitoid species can trigger differ-
ent defense processes in the same host species. For parasitoids, evading or
overcoming the host’s defense is an absolute prerequisite, and we under-
stand that they have evolved efficient protective strategies that the
females themselves put into operation to protect their descent. At the
time of infestation, they inject into the host, together with their eggs,
various immunodepressive or immunosuppressive factors that they
have developed, and which can consist either of venom (mostly proteinic)
and/or of structural entities (virus-like particles). Acting independently
or in a coordinated manner, sometimes reinforced by specific surface
properties of the parasitoid egg, these ‘‘virulence factors’’ inhibit or anni-
hilate the host’s defense either by changing the expression of some spe-
cific host genes, or by direct effect on their effectors, or through other
mechanisms, which can be quantitative or qualitative. It is worth noting
that in all cases, immunoprotection, which is so vital for the parasitic
stages, is mostly the duty of their mothers, which thus pay all costs and do
not benefit directly from their own investment.
Given the drastic consequences of these processes on the host’s and
parasitoid’s fitness, the question of their specificity and their variability
immediately arises, together with their possible genetic determinisms.
That is the condition for selective and evolutionary processes to take
place. Here again, Drosophila parasitoids provide unequalled facilities.
Comparative studies reveal that the intensity and specificity of the Dro-
sophila defense against parasitoids (their ‘‘resistance’’) can vary within
species and are controlled by a few genes, some of which could be
specifically oriented against a given parasitoid species. Reciprocally, the
‘‘virulence’’ of parasitoids can vary within species, and appears to be
under the control of a few genes that could be specific toward the defense
reactions of different host species. Obviously, the hypothesis of resis-
tance- and virulence-genes being species specific, based on the absence
of clear cross-resistance and cross-virulence among the only few species
so far studied, is strengthened when more species are analyzed, especially
among the very rich and diverse tropical Drosophila–parasitoid commu-
nities. In any case, we have the demonstration that in all partners, several
genetic systems are in operation, each specialized in a certain immuno-
logical path or combination of paths. Thus, the Drosophila–parasitoid
system offers exceptional conditions for the study of evolution and coevo-
lution of host–pathogen systems.
Section III deals with the evolution of host–parasitoid relationships.
This classical chapter of evolutionary parasitology receives special
Introduction xxi
attention here, thanks to the unique evolutionary and genetic status of

Drosophila spp. Predictably, the authors focus on the immunological pro-
cesses involved in host resistance and parasitoid counter-resistance
(or ‘‘virulence’’). Indeed, these traits do decide which partner will survive
the infestation, resulting in drastic – but nonsymmetrical – selective
pressures. Their crucial involvement in individual fitness, together with
the rather clear genetic basis of their within- and between-population
variations, make them ideal targets for evolutionary and coevolutionary
processes. Comparative analysis, field data and experimental results fuel
exciting discussions that keep within – and illustrate – current theories on
host–parasite coevolution. However, we must admit that the diversity of
the mechanisms involved in host resistance and the reciprocal parasitoid
counter-resistance, the variety of specificity levels among the species
studied here, the complexity of population structures and of ecological
situations as yet poorly documented, do not lead to clear and definitive
conclusions. The cost of being resistant (for hosts) and of being counter-
resistant (for parasitoids), tradeoffs with other unrelated traits that are
either physiological, or behavioral, etc., are likely to play a major role in
the evolution of immunological traits and need many more studies. In my
opinion, forthcoming analysis of the evolution of a given trait – here
immunological relationships – benefits from keeping within inclusive com-
prehension of the whole selective and evolutionary process including life
styles of species, their reproductive strategies, ecological and behavioral
features, population structures, local histories and many other factors that
act on a variety of scales.
Clearly, this fascinating topic is far from being exhausted. We do not
expect a unique conclusion, and only the patient accumulation of concrete
data and of conflicting hypotheses will bring more and more light in
the field.
Section IV approaches a new topic: the association of Drosophila para-
sitoids with symbiotic prokaryotes. We now know that a number of insect
species, perhaps most of them, harbor Wolbachia, those astonishing intra-
cellular bacteria which interfere with their host’s reproduction in different
ways, all of which enhance their own transmission rate. Thus, it is not
surprising that most Drosophila parasitoids are infected. However, the
study of their interaction with Wolbachia is of special interest in several
respects. First, Hymenopteran parasitoids reproduce parthenogeneti-
cally. Interference of Wolbachia with their haplo-diploid sex determination
leads to a variety of consequences on offspring sex-ratio, ranging from all
female to all male progeny, with or without differential mortality of sexes.
Such diversity goes far beyond what has been described in any other
insect group. Second, we benefit here from the fact that Drosophila is
among the best-documented Wolbachia partners. Predictably, host–
parasitoid relationships are an ideal ground for horizontal transmission
xxii Introduction
to take place. Indeed, the Drosophila–parasitoid communities provide a

well-documented demonstration that in evolutionary times, Wolbachia
could transfer from hosts to parasitoids, and furthermore that parasitoids
did ‘‘accumulate’’ the different Wolbachia strains they acquired from
different host species. That accounts for the high frequency of multi-
infection among parasitoids, which creates fascinating situations of intra-
cellular microbial ecology, with numerous questions about the evolution
of virulence. Readers also learn about the consequences of Wolbachia
infection on the dynamics of parasitoid populations, on the individual
host–parasitoid relationships, and on the physiology of the infected
female, with this astonishing result: Asobara is totally dependent on
Wolbachia infection for egg production. Again, the unique status of
Drosophila allows the authors to develop molecular and genomic pro-
grams which, hopefully, will soon bring about a better understanding
of insect–Wolbachia relationships, from both the mechanistic and the
evolutionary points of view.
Viruses also infect a number of insect species, causing a wide range of
pathogenic effects ranging from near triviality to harsh lethality. Strains of
L. boulardi have proved to be infected with a strange filamentous virus,
vertically transmitted, which causes no severe pathology physiologically-
speaking, but which induces a deep change in a critical behavioral step of
parasitoid females. While uninfected females discriminate already para-
sitized host larvae and reject them, which is taken as an optimal behavior
that avoids the death of supernumerary parasites and egg wastage,
infected ones do accept superparasitism. In doing so, they doom most of
their progeny to death and bring down their own offspring production
and fitness. Obviously, such behavioral dysfunction is prejudicial to
parasitoids, but as far as we understand it benefits the virus which proved
able to transfer from one parasitoid larva to another within the same
superparasitized Drosophila host, and thus to colonize new parasitoid
lineages that otherwise would not be reached. Theoretical studies show
that adding horizontal transmission to vertical transmission, even
casually, allows the virus to invade parasitoid populations and can be
considered as an efficient reproductive strategy. Until now, the general-
ity, the mechanisms and the evolution of this new virus–parasitoid asso-
ciation have been poorly understood, but we can wonder whether such
manipulation of the female’s behavior by viruses questions current the-
ories about the possible adaptiveness of behavioral decisions of wasps
that deviate from the expected optimization.
Clearly, microorganisms associated with parasitoids are a very excit-
ing and promising research area, to which Drosophila parasites are
bringing an outstanding contribution.
It is a pleasure for me to advise entomologists and parasitologists to
read this book carefully. Predictably, Drosophila parasitoids have allowed
Introduction xxiii
the authors to bring new data and/or new hypotheses to a number of

fields, most of which extend to other parasitoids. While not exhaustive,
the contributions brought together here are essential to the understanding
of the functioning and evolution of host-parasitoid relationships, and thus
are very helpful to entomologists involved in academic or agricultural
research. They are also important for the whole field of parasitology, since
they document a number of current theories dealing with the evolution of
symbiotic relationships, with the evolution of virulence–resistance inter-
play, with the dynamics of host–parasite communities and their possible
evolution in response to climatic change. Considering the genetic and
molecular mechanisms that underlie host–parasite relationships, the
unique status of Drosophila makes it likely that, provided a reasonable
effort is made to study the genomics of parasitoids (including microbes),
our knowledge will soon make huge strides forward.
Finally, we now have a clear demonstration that with or without the
help of associated microorganisms, insect parasitoids have established
highly sophisticated relationships with their hosts. If it is possible that the
obligatory death inflicted by parasitoids on their hosts does not basically
differ from the severe and possibly lethal harmful effects ‘‘true’’ parasites
inflict on hosts, then the popular discrimination between parasitoids and
parasites starts to seem less and less obvious.
MICHEL BOULÉTREAU
UNIVERSITÉ LYON 1
VILLEURBANNE, FRANCE
CHAPTER 1
Ecology and Life History
Evolution of Frugivorous
Drosophila Parasitoids
Frédéric Fleury,* Patricia Gibert,* Nicolas Ris,†
and Roland Allemand*
Contents 1.1. Distribution, Community Structure and Ecological

Interactions 6
1.1.1. Diversity, biogeography and phylogeny 6
1.1.2. Spatial and seasonal variations of communities 8
1.1.3. Intensity of parasitism, competition and
coexistence 10
1.2. Drosophila Parasitoid Life Histories 15
1.2.1. Host range and specialization 17
1.2.2. Effect of developmental host on parasite life
histories 19
1.2.3. Adult parasitic strategies and life history
covariation 21
1.2.4. Effects of temperature and overwintering 26
1.3. Geographical Differentiation and Local Adaptation 28
1.3.1. Geographical variations and host–parasitoids
relationship 28
1.3.2. Small scale geographical variations
and competitive interaction 30
1.4. Concluding Remarks 33
References 35
* Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622,

Villeurbanne, France
{
Centre INRA de Sophia Antipolis, Unité Expérimentale 1254 ‘‘Lutte Biologique’’, BP 167, F-06903
Sophia-Antipolis, France
Advances in Parasitology, Volume 70 # 2009 Elsevier Ltd.

ISSN 0065-308X, DOI: 10.1016/S0065-308X(09)70001-6 All rights reserved.
3
4 Frédéric Fleury et al.
Abstract Parasitoids and their hosts are linked by intimate and harmful
interactions that make them well suited to analyze fundamental
ecological and evolutionary processes with regard to life histories
evolution of parasitic association. Drosophila aspects of what para-
sitoid Hymenoptera have become model organisms to study aspects
that cannot be investigated with other associations. These include the
genetic bases of fitness traits variations, physiology and genetics of
resistance/virulence, and coevolutionary dynamics leading to local
adaptation. Recent research on evolutionary ecology of Drosophila
parasitoids were performed mainly on species that thrive in ferment-
ing fruits (genera Leptopilina and Asobara). Here, we review informa-
tion and add original data regarding community ecology of these
parasitoids, including species distribution, pattern of abundance and
diversity, host range and the nature and intensity of species interac-
tions. Biology and the evolution of life histories in response to
habitat heterogeneity and possible local adaptations leading to
specialization of these wasps are reported with special emphasis
on species living in southern Europe. We expose the diversity and
intensity of selective constraints acting on parasitoid life history traits,
which vary geographically and highlight the importance of considering
both biotic and abiotic factors with their interactions to understand
ecological and evolutionary dynamics of host-parasitoid associations.
Within the huge diversity of host–parasite interactions, parasitoidism

occupies the higher level of virulence because successful development of
parasites classically leads to the host death. Reuter (1913) first used the
term ‘‘parasitoid’’ to name this particular way of life observed in about
10–20% of insect species, mainly Hymenoptera, Diptera and Coleoptera
(Godfray, 1994). Parasitoidism is however not restricted to the Arthropod
taxa and encompasses a large variety of organisms such as parasitic
nematodes, bacteria or certain viruses (bacteriophages) that also kill
their host as a consequence of parasite multiplication (Forde et al., 2004;
Gomez-Gutierrez et al., 2006; Kaya and Gaugler, 1993). The fact that
parasitoids and their hosts are linked by tightly and harmful interactions
makes the system particularly suited to analyze fundamental ecological
and evolutionary processes with regard to life histories evolution of both
partners, local adaptation, coevolutionary arms race, maintenance of
species and genetic diversity, as well as demographic mechanisms of
host population regulation (Boulétreau, 1986; Godfray and Shimada,
1999; Hassel and Waage, 1984; Jessup and Forde, 2008; Rosenheim,
1998). Parasitoids insects overwhelmingly attracted most attention in
these fields with studies performed on a wide diversity of associations
(Godfray, 1994). Classically, parasitoid insects are free-living as adults
and only their larvae develop as parasites of a single insect host that is
killed. A number of species were studied with applied goals evaluating
Ecology and Life History Evolution of Frugivorous Drosophila Parasitoids 5
their potential to control phytophagous insect populations and their

possible use in pest management programs.
With more fundamental objectives, Drosophila parasitoid Hymenop-
tera arose as model organisms to study all aspects of host–parasitoid
relationships, particularly those that are hard to investigate in others
systems, mainly the genetic bases and variations of fitness traits or pro-
cesses underlying coevolutionary dynamic and local adaptation. Indeed,
as their Drosophila host, Drosophila parasitoids cumulate many advantages
such as rearing facilities and ease of experimental and field works that
make them particularly suited to disentangle physiological, genetic and
ecological interactions occurring among partners of host–parasitoid asso-
ciation. Moreover, research can benefit from data available on Drosophila
biology and genetics. In return, parasitoid knowledge may also contribute
to understand Drosophila ecology and evolution that cannot miss out the
possible impact of parasites. Since the synthesis of Carton et al. (1986), our
understanding of Drosophila parasitoid biology progressed in all fields of
parasitic interactions but clearly most attention was paid to host immune
resistance, factors of parasitoid virulence and their possible pleiotropic
effects (see other chapters in this volume). Field ecology of Drosophila
parasitoids including species distribution, pattern of abundance and
diversity, host range, nature and intensity of interactions in natural com-
munities, evolution of life histories with regard to habitat heterogeneity
and possible local adaptations leading to specialization have been inves-
tigated less. According to Carton et al. (1986), approximately 50 hyme-
nopterous parasite species of Drosophila belonging to four families and at
least 16 genera are recognized: the larval parasites Braconidae (Asobara,
Aphaereta, Phaenocarpa, Tanycarpa, Aspilota, Opius) and Eucoilidae (Leptopi-
lina, Ganaspis, Kleidotoma, Dicerataspis), the pupal parasites Diapriidae (Tri-
chopria, Spilomicrus) and Pteromalidae (Pachycrepoideus, Spalangia,
Trichomalopsis, Toxomorpha). Research over these last 20 years on Drosophila
parasitoid ecology has been performed mainly on species attacking Drosoph-
ila larvae living in fermenting substrates (rotting fruits, sap fluxes, decaying
plants and mushrooms) and by far most knowledge was obtained from
frugivorous Drosophila parasitoids of the genera Leptopilina and Asobara,
and among them the wasp species Leptopilina heterotoma, Leptopilina boulardi
and Asobara tabida that share common hosts (Drosophila melanogaster, D.
simulans, D. subobscura). Of these associations, complex patterns of geo-
graphical and genetic variation of resistance and virulence with their asso-
ciated costs and benefits were described (Dubuffet et al., 2007; Fellowes et al.,
1999a; Fellowes and Godfray, 2000; Kraaijeveld and Godfray, 1999;
Kraaijeveld et al., 1998), but clearly present results cannot be fully under-
stood without a good knowledge of the ecology of interacting species.
In this article, we review information and add original data about
community ecology, biology and evolution of these wasp species with
special emphasis on the complex Leptopilina/Asobara/Drosophila living in

rotting fruits in southern Europe. We show evidence of the intensity of
selective constraints acting on parasitoid life history traits that show
geographical pattern of variations and highlight the importance to con-
sider both biotic and abiotic factors with their interactions to better
understand ecological and evolutionary dynamics of the community.
1.1. DISTRIBUTION, COMMUNITY STRUCTURE

AND ECOLOGICAL INTERACTIONS
1.1.1. Diversity, biogeography and phylogeny
Geographical distribution, host range and taxonomy are insufficiently
documented for the four major groups of Drosophila parasitoids (Braconi-
dae, Figitidae, Diapriidae and Chacidoidea) with a few exceptions (Carton
et al., 1986). Samplings in tropical regions of America or Africa suggest that
the fauna is poorly known and that many other new species remain to be
described (Carton and Lachaise, personal observations). Parasitoids that
attack frugivorous Drosophila are diverse but the most important species
are the larval parasites of the genus Leptopilina and Asobara and the pupal
parasites Spalangia, Pachycrepoideus and Trichopria (Allemand et al., 1999;
Carton et al., 1991; Rohlfs and Hoffmeister, 2004; Wertheim et al., 2006).
Tanycarpa punctata and Aphaereta scaptomyzae can be locally abundant in
some associations with L. heterotoma and A. tabida in fruit or sap fluxes
(Hardy and Godfray, 1990; Janssen, 1989).
Leptopilina is the best-known genus (Allemand et al., 2002;
Nordlander, 1980; Schilthuizen et al., 1998) ahead of Asobara
(Belokobylskij, 1998) or Spalangia (Boucek, 1963) and very few data are
available for other genera of Drosophila parasitoids. The taxonomic diffi-
culties can be partly solved using molecular tools that also give the
possibility to establish phylogenies. In the Leptopilina genus, molecular
phylogenies agreed with morphological traits (Allemand et al., 2002;
Schilthuizen et al., 1998), and separate three groups of species (longipes,
boulardi and heterotoma groups), which correlate with their distribution,
ecology or associations with symbiotic microorganisms (Chapter 12 by
Vavre et al.). The longipes group consists of six described species
(L. longipes, L. clavipes, L. fimbriata, L. australis, L. cupulifera and L. mahensis)
specialized on fungi and decaying plant materials (Driessen and
Hemerik, 1991; Janssen et al., 1988; van Alphen et al., 1991; van Dijken
and van Alphen, 1998; Vet and van Alphen, 1985; Wertheim et al., 2000).
The other two groups are species living mainly in fermenting fruits.
Taxonomy, recently revisited by Allemand et al. (2002), separates a
L. boulardi group including two newly described species originating
from tropical Africa (L. orientalis and L. freyae) and extends the L. heteroma
group to five species (L. heteroma, L. victoriae, L. rufipes, L. atraticeps and the
newly described L. guineaensis). To date, precise information on the ecol-
ogy and geographical distribution of these species is available for L.
heterotoma and L. boulardi only.
L. heterotoma is clearly the most generalist parasitoid among all other
Leptopilina species. It colonizes fermenting fruits but also sap fluxes and
decaying plant materials in a wide holarctic distribution but seems absent in
the afro-tropical region (Carton et al., 1986; Hardy and Godfray, 1990;
Janssen et al., 1988; Mitsui et al., 2007; Norlander, 1980; van Alphen et al.,
1991). To date, there is no record of this species in the austral hemisphere.
In contrast, L. boulardi, a specialist of frugivorous Drosophila, is recorded
worldwide in Mediterranean and intertropical climates including southern
Europe, Africa, North and South America, and the West Indies (Allemand
et al., 2002; Barbotin et al., 1979; Carton et al., 1991; Chabora et al., 1979;
Hertlein, 1986; Nordlander, 1980). The northern limit of the L. boulardi
geographical range in Europe is precisely localized around 45 N latitude,
separating the continental and Mediterranean climates. Its southern limit
remains largely unknown but records have been obtained from South Africa
and Brazil. The niches of L. heterotoma and L. boulardi overlap in a number
of countries of the Mediterranean areas where they compete for D. melano-
gaster and D. simulans during part of the season (Allemand et al., 1999;
Carton et al., 1991; Fleury et al., 2004). Both species were also sympatric
in the New World both in the east and west of North America (Schlenke
et al., 2007).
L. heterotoma and L. boulardi also interact with parasitoids of the
genus Asobara, which draw together at least nine species among
which A. tabida, A. citri, A persimilis, A. japonica and A. gahanii thrive
in rotting fruits ( Janssen et al., 1988; Mitsui et al., 2007; Vet and van
Alphen, 1985; Vet et al., 1984). By far, A. tabida is the most thoroughly
studied species and has become a model for life history evolution,
chemical and behavioral ecology, coevolutionary interactions of host
resistance and parasitoid virulence, and infection by endosymbiotic
microorganisms (Dedeine et al., 2001; Ellers et al., 2001; Green et al.,
2000; Kraaijeveld and Godfray, 1997, 1999; Pannebakker et al., 2007;
Prévost et al., 2005; Vet and van Alphen, 1985). A. tabida shows a wide
holarctic distribution with reports from the northwest of America
(Hoang, 2002), Japan (Mitsui et al., 2007) and all Europe from the
Mediterranean cost to northern Scandinavia (Carton et al., 1986). Niche
separation among A.tabida, L. heterotoma and L. boulardi is not clearly
established and probably varies throughout the season, geographical
sites and local conditions.
If distribution of these three main frugivorous Drosophila parasitoid
species is approximately known, there are very few data available on their
relative abundance on different fermenting substrates and intensity of

competitive interactions among them. By collecting fermenting fruits in
Tunisia over several months, Carton et al. (1991) observed the presence of
L. heterotoma and L. boulardi only with moderate levels of abundance but
species are not present at the same time of the season probably because
L. boulardi excludes L. heterotoma from April to December as a consequence
of its higher competitive ability. In contrast, fieldwork performed by
Hardy and Godfray (1990) in England showed that the northern Europe
parasitoid community is dominated by L. heterotoma, A. tabida and Tany-
carpa punctata with similar level of abundance and a synchronization of
their activity from May to September. In southern France where distribu-
tion of the three main Drosophila parasitoids overlaps, we sampled during
all the warm season (from April to September) several sites distributed
along a transect of 300 km by collecting standardized rotting fruits, mainly
bananas or apples, submitted to natural colonization by insects over
2 weeks (Allemand et al., 1999). Collected materials were brought back to
the laboratory and incubated at 21 C and all emerging Drosophila and
parasitoids were identified to the species level. Overall, species composi-
tion and abundance reveal a complex community structure in rotting fruits
that involved at least seven Drosophila spp. dominated by D. melanogaster,
D. simulans and D. immigrans with approximately the same level of
abundance (Fig. 1.1). Two pupal parasitoids coexist with three larval
parasitoids among which a very weak representation of A. tabida compared
to L. heterotoma and L. boulardi (Fig. 1.1). Clearly in this area, rotting fruits
are colonized by a very high density of Drosophila and parasitoids, thus
suggesting intense interactions within and among trophic levels that raise
the question of mechanisms responsible for the maintenance of this diver-
sity. These high population densities also suggest that Drosophila probably
experience crowded conditions in the field that can make possible the
expression of the cost of resistance genes demonstrated under laboratory
condition in both A. tabida et L. heterotoma spp. (Fellowes et al., 1998;
Kraaijeveld and Godfray, 1997). High densities of hosts and parasites,
however, did not reach the same level according to localities and ecological
conditions that vary among orchards or woodland, as shown by Wertheim
et al. (2006), thus resulting in a geographical mosaic of selective pressures
that can lead to local adaptation.
1.1.2. Spatial and seasonal variations of communities

In natural conditions, frugivorous Drosophila and their parasitoids are
present throughout the year except during the colder season. Species
are all polyvoltine, their diversity and abundance vary according to the
habitat, the available resources and their thermal tolerance. For
instance, the patchy distribution of mushrooms result in lower insects
Drosophila (n = 195,724)
D. melanogaster
D. simulans
D. immigrans
D. subobscura
D. hydei
D. buskii
D. testacea
Parasitoids (n = 118,979)
L. boulardi
L. heterotoma
Asobara tabida
Pachycrepoideus
Trichopria
FIGURE 1.1 Relative abundance of Drosophila and parasitoids emerging from standar-
dized fruits (bananas) deposited in orchards in the Saône-Rhône valley (southern France).
Data are pooled from about 480 fruits (six sites, five periods between April and
September, 16 replicates by site and period).
density (Driessen and Hemerik, 1991) that contrasts with the continuous
distribution of fruits (peaches, pears or apples in orchards) where impor-
tant populations of Drosophila breed and develop (Fleury et al., 2004;
Wertheim et al., 2006). Among studies focusing on Drosophila and their
parasitoid wasps that develop in fermenting fruits, very few reported how
natural assemblage of species varies in space and during the season.
Janssen et al. (1988) recorded presence/absence of Drosophila species and
their parasitoids in various fermenting substrates sampled in several
woods in The Netherlands but unfortunately without the composition of
local community. However, they noticed high levels of parasitism that
reach 50%. A more quantitative study performed on stinkhorn fungi in the
same woodlands showed the evidence of short temporal refuge for hosts
throughout the season that can stabilize the community experiencing high
rates of parasitism rising up 100% in July (Driessen et al., 1990). Hertlein
(1986) followed overwintering populations in citrus orchards of California
from fall to spring and observed rapid growth of populations for all
members of the community, here restricted to D. melanogaster, D. simulans

and L. boulardi only. However a lack of synchrony among hosts and
parasites was observed as a consequence of longer periods of inactivity
of parasites (5 months) that enter hibernal diapause whereas hosts over-
winter in a state of quiescence. Reproductive activity of hosts that occurs
2–3 months before parasites allows Drosophila populations to build up
high levels of densities and cope with high mortality rates induced by
parasitoids. Similar pattern of host–parasitoids asynchrony also appears
in Tunisia where Drosophila hosts thrive in prickly pears of Opuntia during
the winter, when parasitoids populations fall to very low level abundance
(Carton et al., 1991).
In southeastern France, we performed a more detailed survey of
Drosophila-parasitoid communities from April to the end of October in
4 orchards distributed along a north–south axis at the edge of L. boulardi
geographical range (Fig. 1.2, see Fleury et al., 2004 for more details). In the
north above 45 N latitude (area around Lyon), D. melanogaster always
overtook other Drosophila spp., whereas in the south D. simulans was
dominant during all the season. At intermediate sites, a progressive
replacement of D. melanogaster by D. simulans was observed that may
be interpreted as a consequence of increased competitive interactions
among Drosophila spp., due to climate conditions becoming favorable for
D. simulans or to an effect of parasitoid community composition that also
varies within the season. Indeed interestingly, parasitoid species show
parallel spatial and seasonal variations. L. heterotoma predominates in the
north where it develops mainly on D. melanogaster whereas its abundance
diminishes to only a few percent in the south. The coexistence of L.
heterotoma facing the competitive superiority of L. boulardi in the south
may partly result from parasitoid seasonal asynchrony and precedence
of L. heterotoma that is active several weeks before L. boulardi. This proba-
bly results from their different thermal requirement and overwintering
strategy that occurs as prepupal diapause in L. boulardi (Claret and
Carton, 1980; Hertlein, 1986) but as adult quiescence in L. heterotoma
(Eijs, 1999). Clearly in this area, sharp variation of community structure
is observed at low spatial and temporal scales that results in a geographi-
cal mosaic of selective pressures giving potential for local adaptations.
However, this phenomenon may be impeded by a high amplitude of
seasonal variation.
1.1.3. Intensity of parasitism, competition and coexistence

1.1.3.1. Impact of parasitoids on Drosophila populations
Most studies agreed that Drosophila parasitoids induce a high rate of
mortality on their host populations despite the fact that the level of
parasitism varies according to breeding site, the local situation and the
North
Uchizy 46.5°N
Species frequency 1 1
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0 0
Lyon (south) 45.4°N
1 1
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0 0
Valence 44.9°N
1 1
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0 0
Avignon 43.9°N
1 1
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0 0
South June July Aug Sept May June July Aug Sept
D. melanogaster D. immigrans L. heterotoma Pachycrepoideus
D. simulans Others L. boulardi Others
FIGURE 1.2 Seasonal variation of the relative abundance of Drosophila species (left)
and their parasitoids (right) in four sites distributed along a north–south axis in the
Saône-Rhône valley (southern France).
season. At the fruit scale, a high percentage of parasitized Drosophila

larvae (up to 80%) has been observed in Australia (Parsons, 1977), The
Netherlands (Driessen et al., 1990; Janssen et al., 1988), Tunisia
(Boulétreau et al., 1991) and in southern France (Fleury et al., 2004).
Most often, the natural average rate of parasitism varies between 5%
and 40% in midsummer under favorable climate conditions, that is, 30%
in temperate woodland of The Netherlands on various fermenting sub-
strates ( Janssen et al., 1988), around 15% on plums in northern Germany
(Rohlfs and Hoffmeister, 2004), 16% in peaches and 22% in apples sam-
pled in the same orchard in France (Wertheim et al., 2006) and up to 80%
in some sites of southern France (Fleury et al., 2004). These high values of
parasitism with their local variations indicate that parasitoids may be one
of the main factors of mortality in fly populations and thus constitute a
selective force acting on their hosts. To date, there is no indication how
parasitoids may have shaped Drosophila life history traits in the wild, even
for the evolution of host resistance, which has been studied mainly under
laboratory condition. In experimental cages, we know that selective pres-
sure of parasitoids can modify the polymorphic equilibrium of different
genotypes of D. melanogaster (Boulétreau, 1986). With some markers, like
the sepia gene, the evolution of allelic frequency is modified by the pres-
ence of parasitoids and the effect is not caused by a discriminatory
destruction of one genotype but by indirect effects on population density.
Parasitism is favored by the ability of parasitoid females to use chemi-
cal stimuli from the host itself such as larval excrements or feeding traces
(Dicke et al., 1985; Galis and van Alphen, 1981; Vet, 1985a; Vet and Bakker,
1985; Vet and van der Hoeven, 1984; Vet et al., 1993) or those from the host
habitat such as odors of decaying plant materials (Dicke et al., 1984; van
Alphen et al., 1991; Vet, 1985b; Vet et al., 1984). Moreover, responses to
cues could be learnt by parasitoids thus enhancing their efficiency in
microhabitat and host location. Associative learning was demonstrated
for several species of Asobara (Vet and van Opzeeland, 1984), L. heterotoma
(Vet and van Opzeeland, 1985, Vet et al., 1998) and L. boulardi (De Jong
and Kaiser, 1991; Poolman et al., 1992; Vet, 1985a). Drosophila parasitoids
also spy on the communication systems of their hosts to locate favorable
sites since aggregation pheromones of flies are used by both L. heterotoma
and L. boulardi (Couty et al., 1999; Hedlund et al., 1996; Wertheim et al.,
2003; Wiskerke et al., 1993). A positive dose-dependant response to aggre-
gation pheromones may explain higher aggregation of wasps in patches
of higher larval density, and thus the positive density-dependent parasit-
ism observed in some situations (Driessen and Hemerik, 1991; Hertlein
and Thorarinsson, 1987; Wertheim et al., 2003). Such a clumped distribu-
tion of hosts and parasitoids with positive functional response may con-
tribute to the stability of host/parasitoid associations as shown
theoretically (Hassel and May, 1973, 1974; Lett et al., 2003; Pacala et al.,
1990). However, this pattern of density-dependent parasitism risk is not

the rule and it varies according to the Drosophila breeding substrates. For
example, Rohlfs and Hoffmeister (2004) showed that both L. heterotoma
and A. tabida express positive density-dependent parasitism on sloes,
inverse density-dependent on plums, and a hump-shaped relationship
among a proportion of parasitized larvae and host density on apples
observed also in other sites (Wertheim et al., 2006). These variations
could be explained by the nature of breeding substrates that allow, or
not, a proportion of larvae to burrow within the fruits’ tissues, thus
escaping parasitism as a result of their concealment. The fact that risk of
parasitism is decreased with increasing host density may provide an
adaptive hypothesis to Drosophila aggregation and thus the evolution of
aggregation pheromones (Rohlfs and Hoffmeister, 2004). However, spa-
tial aggregation probably also leads to an increased intraspecific competi-
tion as suggested by lower fitness traits values observed on individuals
emerging from high-density patches (Wertheim et al., 2006). The adaptive
significance of Drosophila aggregation thus results from a benefit–cost
balance between refuge against parasitoids and mortality due to den-
sity-dependent competition, thus underlying the key role that parasitoids
may have played in the evolutionary outcome of this trait.
At the interspecific level, intraspecific aggregation across fragmented
resources may promote local diversity as suggested by several authors
(Atkinson and Shorrocks, 1984; Sevenster and van Alphen, 1996; Toda
et al., 1999). However, mechanisms of species coexistence are obviously
multifactorial and it is likely that parasitoids also participate to the species
diversity of their host community as suggested by results from laboratory
experiments (Boulétreau et al., 1991; Davis et al., 1998; Fleury et al., 2004).
Indeed, in simple experimental ecosystems, when parasitoids are absent,
D. melanogaster always eliminates D. simulans when they compete for
limited resources whatever the thermal regime (from 22 C to 28 C).
The outcome of competition is modified by the presence of parasitoids
and the issue varies according to temperature: D. simulans remains a poor
competitor at 28 C, but the frequency of this species increases until
the extinction of D. melanogaster at 22 C, and both species coexist at
25 C (Fleury et al., 2004). At 22 C, parasitoids invert the outcome of
competition and allow the coexistence of species that normally exclude
each other at 25 C, thus suggesting their role in the diversity of Drosophila
community.
1.1.3.2. Competition within parasitoids community

With regard to parasitoids, we also have evidence that competition is
severe among species in the wild, thus suggesting that horizontal inter-
actions are probably selective factors that also participate to shape the
whole Drosophila-parasitoid community. The first line of evidence results
from a high parasitization rate that sometimes exceeds 90%, which inevi-
tably leads to strong competitive interactions at least among individuals
of the same species. Convincing arguments were provided by field obser-
vations showing that a number of Drosophila larvae host more than one
parasitoid larva (superparasitism), although only one adult can emerge
from a single host (Fleury et al., 2004; Wertheim et al., 2003). The variation
of relative abundance of species across the season despite favourable
conditions also argues in favor of strong interspecific competition
among parasitoids. For instance, in southeastern France, L. heterotoma is
the main species early in the season but its density sharply decreases
when L. boulardi appears, probably as a result of competitive displace-
ment (Fig. 1.2). Indeed, both biotic and abiotic factors remain suitable for
L. heterotoma when populations persist, facing L. boulardi at very low
density over the whole season (Fauvergue et al., 1999), and the geograph-
ical range of L. heterotoma clearly includes wider habitat conditions than
those occurring when populations collapse (e.g., North Africa). A similar
pattern of seasonal abundance was observed in Tunisia (Carton et al.,
1991). Because intensity of competition is likely to vary geographically, it
is expected that competitive selective pressures result in a population
differentiation and local adaptation for a number of parasitoid traits and
reproductive strategies. How Drosophila parasitoids cope with competi-
tive interactions remains underinvestigated. Host range, habitat prefer-
ence, temporal as well as spatial refuge resulting from parasitoid
aggregation are all probably involved in reducing interspecific competi-
tion (Vet et al., 1984; Wertheim et al., 2000). However segregation of
realized niches in the field remains largely unknown. In some cases,
infochemicals can be used by Drosophila parasitoids to avoid patches
exploited by a superior competitor ( Janssen et al., 1995). The presence
of a conspecific on a patch also influences oviposition decisions of
L. heterotoma females less disposed to parasitize hosts (Visser, 1995).
Females are also able to recognize parasitized hosts and avoid superpara-
sitism (Bakker et al., 1990; van Alphen and Visser, 1990; van Lenteren,
1976) but to date there is no evidence that parasitoids discriminate hosts
attacked by another species and then multiparasitism might occur
(Turlings et al., 1985; van Strien-van Liempt and van Alphen, 1981).
Parasitoids such as Leptopilina and Asobara share the same habitat and
common hosts in rotting fruits and thus probably compete in the field.
However, intensity of interspecific competition may be softened by
fine-scale differences in species-specific life histories that can balance
competitive ability, thus promoting species coexistence as shown in Dro-
sophila ( Joshi and Thompson, 1996). For example, despite that the sea-
sonal phenology of frugivorous Drosophila parasitoid largely overlaps, all
species show different circadian rhythms, leading to fine temporal segre-
gation of activity within a day (Fleury et al., 2000a). Intrinsic inferior
competitors then take advantage to be active earlier, a temporal niche that

probably cannot exploit the superior competitor because of thermal con-
straints. Species also differ by host searching behavior and host detection
such as antennal or ovipositor searching, host location by vibrotaxis, or
the use of infochemicals, which may lead to exploit different microniches
or host species, thus contributing to coexistence (van Dijken and van
Alphen, 1998; Vet and Bakker, 1985). As the aggregation of parasitism
occurs at local scales (Driessen and Hemerik, 1991), microscale aggrega-
tion might also probably participate in reducing interspecific interactions.
This was clearly suggested in experimental observations where L. boulardi
and L. heterotoma alone or competing by pair (both intra- or interspecific
association) were allowed to parasitize four patches of Drosophila larvae in
a small Petri dish. Results clearly showed that when the female is alone,
both species aggregate their attacks mainly on one patch only (high value
of aggregation index) and the same result is observed with pair of conspe-
cific females (Fig. 1.3). In contrast, a very low aggregation index was
measured in heterospecific pairs (Fig. 1.3). Analysis of parasitoid emer-
gence indicated that observed overdispersion results from microscale spa-
tial segregation of heterospecific females that aggregate their infestation on
different patches. This probably might be mediated by infochemical repel-
lents or the consequence of physical contacts among females that drive
them on different patches. Thus, a number of factors contribute to micro-
niche differentiation among frugivorous Drosophila parasitoids in the wild
that might compensate intrinsic competitive differences among species.
However, according to the high rate of parasitism in some communities,
species differences are probably not broad enough to override competitive
interactions. This competition must constitute one of selective forces that
drive a large number of life history traits of Drosophila parasitoids.
1.2. DROSOPHILA PARASITOID LIFE HISTORIES

The adult and larval biology of Drosophila parasitoids are known from the
initial work of Jenni (1951) and Nöstvik (1954) on Leptopilina spp. and are
well reviewed by Carton et al. (1986). The biology of Asobara genus is less
carefully described. More recently, Melk and Govind (1999) described in
detail the biology of Ganaspis xanthopoda, which appears to be quite
similar to the Leptopilina genus. These species are all koinobiont and
solitary endoparasitoids that attack first and second stages of Drosophila
larvae. Under favorable conditions, with unlimited number of hosts,
L. heterotoma adult females deposit only one egg per host which hatch
2 days after oviposition in the host hemocele. The host tissues are
progressively consumed by second and third instars. Third-instar para-
sites become ectoparasites, consuming all host pupa, and metamorphosis
A L. boulardi B L. heterotoma
140 140 (P < 0.002)*

(P < 0.002)*
100 100
Count
Count
1
60 60
20 20
0.2 0.3 0.4 0.5 0.2 0.3 0.4 0.5
C D
140 (P < 0.002)* 140 (P < 0.002)*
100 100
Count
Count
2
60 60
20 20
0.2 0.3 0.4 0.5 0.2 0.3 0.4 0.5
L. boulardi + L. heterotoma
E
140 ( P = 0.056)
100
Count
60
20
0.2 0.3 0.4 0.5

Proportion of infestation
in the more infested patch
FIGURE 1.3 Aggregation of infestation by isolated or competing Leptopilina females.

Females were allowed to parasitize 4 patches of 50 Drosophila larvae in a small Petri dish
(5.5 cm diameter) during 24 h (25 C, LD 12:12). Each graph indicates the observed value of
aggregation index (arrow) compared to the simulated distribution of this index under the
hypothesis of random parasitoid attacks on all patches (500 simulations). Results show
that alone (A, B) or by conspecific pairs (C, D), both species aggregate their attacks
mainly on one patch only. In contrast, interaction between L. heterotoma and L. boulardi
females (E) results in overdispersion of parasitization.
occurs in Drosophila puparium approximately 2 weeks after oviposition.

Under laboratory conditions, adults emerge after about 3 weeks and
emergence spreads over 4–5 days at 25 C, with males emerging
1–2 days before females. Within the day, protandry is observed with
males emerging 1–2 h before females (Fauvergue et al., 1999). In the
field, development time can last 35 days in May–June but decreases
along the season with rising temperatures (Fauvergue et al., 1999). Devel-
opment time of the parasitoid is then approximately 1.5 to 2 times longer
than those of the unparasitized host. According to the conditions, the
preimaginal wasp development does not always succeed and the parasit-
ism may fail in three different ways: (1) a precocious parasite death
induced by the immune response of the host called encapsulation, as
described in different Drosophila–Leptopilina interactions, (2) the death of
the parasitoid eggs without any consequence to the adult Drosophila
(Nappi and Streams, 1970; Streams, 1968) and (3) a failure or ‘‘inade-
quacy’’, which leads to the death of both host and parasitoid. Both
L. heterotoma and Asobara parasitoids emerge with a number of mature
eggs ready to be laid but the degree of proovigeny varies among species.
Adult wasp fitness components thus may be experimentally estimated by
counting the number of oocytes in ovaries soon after the emergence.
Because Drosophila parasitoids are all haplodiploid species (haploid
males and diploid females produced respectively by unfertilized and
fertilized eggs), the offspring sex ratio may vary according to local con-
ditions. Isolated females of L. heterotoma produce around 20–30% of males
but females are able to modify the sex ratio when wasp densities increase
according to sex-allocation theories (Debout et al., 2002). Despite these
common characteristics, Drosophila parasitoids exhibit differences in sev-
eral life history traits such as host range, biological rhythms, overwinter-
ing strategies, host foraging behavior and thermal sensitivity.
1.2.1. Host range and specialization

Host range of larval Drosophila parasitoids differ significantly among
species even if they are phylogenetically closely related, such as L. hetero-
toma and L. boulardi. The host spectrum is predominantly determined
under laboratory conditions on the basis of host acceptation and parasite
developmental success. Clearly, the host range actually used in the field
by parasitoids needs to be determined. To date, authors agree that
L. boulardi is a specialist of D. melanogaster and D. simulans (Barbotin
et al., 1979; Carton and Nappi, 1991; Carton et al., 1981, 1987; Fleury
et al., 2004). However, particular African strains can develop in D. yakuba
(Dubuffet et al., 2008), and recent data suggest that L. boulardi can also
develop in D. subobscura and D. pseudoobscura at a low rate (Schlenke et al.,
2007). L. heterotoma is by far the more generalist species, since its
successful development has been recorded on numerous Drosophila (D.

busckii, D. funebris, D. kuntzei, D. melanogaster, D. obscura, D. phalerata, D.
simulans, D. subobscura and D. willistoni) or related genera (Chymomyza or
Scaptomyza) (Carton et al., 1986; Janssen, 1989; Jenni, 1951; Ris, personal
observations). To date, determinants of this large host range are not
precisely known but it should be hypothesized that this relies on the
ability of L. heterotoma to cope with different host defenses (Schlenke
et al., 2007) or its ability to cope with qualitatively and quantitatively
different host resources. A. tabida is considered rather as a specialist
species attacking D. subobscura, D. obscura and D. melanogaster mainly,
but can also develop on D. tristis (Janssen, 1989; Kraaijeveld et al., 1995).
Recently, Eslin and Prévost (1998) reported the successful development of
A. tabida in other species of the D. melanogaster subgroup, such as
D. sechellia (58%), D. simulans and D. mauritiana (18%) that could enlarge
the potential host spectrum of this species. However, other studies have
reported no development in D. simulans that expresses a complete resis-
tance to A. tabida, whose eggs are encapsulated (Kraaijeveld and van der
Wel, 1994), thus explaining the weak abundance of this species in orch-
ards of Mediterranean area where D. simulans is dominant. The origin of
such discrepancies remains unclear, but it is likely that variability results
from the origin of host or parasite strains. Indeed, a number of studies
reported genetic variability within or among populations in either host
suitability or the ability of a parasite to develop in a particular host species
(Boulétreau, 1986). For example, while suitability of D. subobscura is fairly
constant whatever the geographical origin of A. tabida, only southern
European wasp populations show a good survival rate in D. melanogaster
(40–80% compared to few percent). This is interpreted as an adaptation to
local conditions where D. melanogaster is more abundant (Kraaijeveld and
van der Wel, 1994). Genetic variability was also observed from the host
side on their ability to enable parasite development. Such variation was
reported mainly for D. melanogaster that show different suitability for
L. heterotoma (Boulétreau and Wajnberg, 1986), L. boulardi (Boulétreau
and Fouillet, 1982; Carton et al., 1989; Wajnberg et al., 1985) and A. tabida
(Kraaijeveld and van Alphen, 1995a). The origin of these variations relies
on both immunological resistance and parasite virulence ability (see for
a review Kraaijeveld and Godfray, 1999; Kraaijeveld et al., 1998 and this
volume) but can also result from physiological inadequacy of the host
with regard to parasite requirement (Boulétreau, 1986). Of course, a
number of other factors participate to larval survivorship of parasites in
a given host, mainly temperature, giving rise to complex interactions
(Fleury et al., 2004; Kraaijeveld and van der Wel, 1994; Ris et al., 2004).
Crowding appears also important since success of parasite development
could rise from 40% to 90% with increased larval density (Boulétreau and
Wajnberg, 1986; Wajnberg et al., 1990).
1.2.2. Effect of developmental host on parasite life histories

Besides the developmental success, host species can influence a number
of adult parasitoid traits either on emerging wasps as a result of pheno-
typic plasticity, or on offspring of these wasps by maternal effects. Hosts
also constitute a selective force that can genetically modify parasitoid
populations in a number of traits including parasite success. Surpris-
ingly, the extent to which host species influence parasitoid phenotype by
developmental plasticity was studied for a limited number of host–
parasite combinations. Moreover, complex interactions with other biotic
or abiotic factors such as temperature or crowding can mix up conclu-
sions, as well as the origin of the strains (Boulétreau and Wajnberg, 1986;
Fleury et al., 2004; Kraaijeveld and van der Wel, 1994). For example,
L. boulardi females produce many more offspring at 25 C after develop-
ment in D. melanogaster (mean total progeny 293) than on D. simulans
(mean total progeny 184). The lesser quality of D. simulans as a host was
confirmed for both L. boulardi and L. heterotoma at 25 C but the differ-
ence is sharply reduced at 22 C, where the quality of the two host
species is quite similar (Fleury et al., 2004; Ris et al., 2004). Moreover,
parasitoid genotype is also involved, since the southern genotype of
L. heterotoma performs much better in D. simulans than in northern
ones originating from the area where this host species is less abundant.
This indicates a possible local adaptation of the parasite to cope with the
most abundant host in local sites (Fleury et al., 2004). Traits other than
egg load or total offspring count such as preimaginal development time,
growth rate body size, adult longevity or fat reserve are also influenced
by developmental host species (Eijs and van Alphen, 1999). Using a
wider host range, we compared the influence of the five sympatric
Drosophila species potentially used as a host by L. heterotoma in the
southeast of France (21 C, photoperiod LD 16:8). Under experimental
condition, survival of all host species is high but they differ in size with
the following order using D. simulans as reference: D. melanogaster (120%
dry weight), D. subobscura (150%), D. immigrans (230%) and D. hydei
(310%) with the same trend observed for development time. These five
Drosophila species clearly do not offer the same developmental condi-
tions to L. heterotoma since D. melanogaster and D. simulans appear to be
as expected the two most suitable hosts, with almost 80% of parasite
survival, while D. subobscura and D. hydei show intermediate quality
(parasite survival ranging from 40% to 60%), and D. immigrans (20%)
clearly appears as a rather unsuitable hosts (Fig. 1.4). Parasitism failure
on D. immigrans is associated with the death of the parasitized host and
no encapsulation was observed. However, less suitable hosts for parasite
development give rise to females with higher egg loads, probably as a
consequence of a direct effect of host size on parasite size, which
Number of oocytes/ovary 150
130
0.64 ± 0.03 imm 0.63 ± 0.02
sub
(mean ± SD)
0.59 ± 0.02
110 0.67 ± 0.03 hyd mel

0.59 ± 0.02
sim
90
70
0 0.2 0.4 0.6 0.8 1.0
Preimaginal survival
(median ± interquartile)
FIGURE 1.4 Influence of five Drosophila hosts on preimaginal survival, egg load of
5-day-old females and the tibia length (values on the graph in mm, meanSD) of
Leptopilina heterotoma (sympatric strains). imm D. immigrans, hyd D. hydei, sub
D. subobscura, mel D. melanogaster, sim D. simulans. SD, standard deviation.
appears closely correlated. This negative correlation among parasite

development success and egg load calls for careful classification of
host quality. Interestingly, development time of parasitoid from egg to
adult follows more closely the ability of the host to give rise to an adult
parasite than host development time or host size themselves. This sug-
gests that despite L. heterotoma is a ‘‘conformer’’, with parasite traits
directly influenced by those of their host, host species cannot only be
viewed as a ‘‘temporal scheduler’’ and/or a ‘‘food resource’’, but more
complex physiological interactions are involved in the host–parasite
relationship. Future progress should better understand the physiological
determinants of this host suitability and, for instance, the puzzling
inadequacy of L. heterotoma to develop in D. immigrans.
Drosophila parasitoids probably switch from one host species to
another, as consequences of temporal or spatial variation of community
composition. In addition to the direct influence of the host on the
emerging parasitoid, the host species experienced by the parents could
also influence the phenotype of their progeny by maternal effects.
Surprisingly, such phenomenon remains poorly documented for koino-
biont parasitoids including Drosophila parasitoids. Influence of the paren-
tal host has been investigated for L. heterotoma using D. melanogaster and
D. immigrans, producing four combinations of developmental and paren-
tal hosts. Maternal effects were detected on two of three life history
parameters under study (Fig. 1.5). The egg load of 5-day-old females
hatching from D. melanogaster is lower when their mother had developed
in D. immigrans whereas such an effect is not observed when D. immigrans
is used as the developmental host. This demonstrates that host shift from
D. immigrans to D. melanogaster is clearly detrimental for the wasp with
possible consequence on host range evolution. More complex maternal
effects were also observed in wasp size (estimated by tibia length), with a
gain of size when the mother had developed on a different host species
than the daughters but no evident explanation arises about underlying
physiological processes involved. Only preimaginal parasitoid survival is
not influenced by maternal effect, but drastically drops when D. immi-
grans is used as the developmental host. These results clearly demonstrate
that the host of the parents can influence the L. heterotoma offspring as
already reported in other animals (Bernardo, 1996; Rossiter, 1996). The
physiological basis of this cross-generational phenotypical plasticity
remains however unknown insofar as both size and fecundity are not
affected in the same ways. These traits vary in opposite ways (in term of
fitness) when development occurs in D. melanogaster, which could be a
consequence of different allocation of the resources between size and
fecundity in response to environmental conditions.
1.2.3. Adult parasitic strategies and life history covariation

Faced with the multitude of factors that can modify wasp phenotype
including temperature, crowding, host species and the associated mater-
nal effect and given the fact that traits also vary according to both host and
parasite genotype, it is not realistic to review in detail life histories that
show wide phenotypic or genotypic variation such as fecundity, longev-
ity or size of Drosophila parasitoids. More interesting is our knowledge
about how parasitoids behave to locate, select and exploit an optimal host
(optimal foraging) and how they trade off the advantage to gain on one
trait by the cost sent back on another trait with regard to life histories
theory (Roff, 1992; Stearns, 1992).
1.2.3.1. Hosts finding

Because parasitoid searching behavior correlates directly with offspring
production, it is expected that host foraging by parasitoids is optimized
by natural selection solving the tremendous difficulty of finding hosts.
A number of studies reported adaptive foraging decisions observed in
Drosophila parasitic wasp. As previously discussed, parasitoids of frugiv-
orous Drosophila locate host habitat and select suitable hosts using a
number of cues, mainly infochemicals. Olfactory microhabitat selection
is mediated by the emanation of fermenting fruits, decaying plants or
A Preimaginal survival B Tibia length (mm) C Fecundity (oocytes/ovary)
median and interquartile mean and standard error mean and standard error
1.0 a a b b c b a b b c a,b a
0.69 140
0.8 0.66 130
0.6 0.63 120
0.4 0.60 110
0.2 0.57 100
0 0.54 90
Parental host mel imm mel imm mel imm mel imm mel imm mel imm
Developmental host mel imm mel imm mel imm
FIGURE 1.5 Influence of Drosophila immigrans (imm) and D. melanogaster (mel) as developmental host or parental host on the Leptopilina
heteroma phenotype. Sample sizes for the four combinations of parental and developmental hosts (from left to right on the figures) are (A) for
preimaginal survival: 7, 9, 6 and 11; (B) for tibia length: 54, 50, 42 and 27; (C) for fecundity: 56, 42, 46 and 26.
fungi. Laboratory experiments often showed that live baker’s yeast odor
is attractive (Vet, 1985a). L. heterotoma (Dicke et al., 1984; Papaj and Vet,
1990; Vet and van Opzeeland, 1985; Vet et al., 1998), L. boulardi (Carton,
1978; Couty et al., 1999; Vet, 1985a) and A. tabida (Kraaijeveld and van der
Wel, 1994; Vet et al., 1984) all perform olfactory microhabitat selection as
well as other Drosophila parasitoids (van Alphen et al., 1991). Odor habitat
alone is not spontaneously attractive and parasitoids must learn to mem-
orize the fruit odor by associative learning with host cues (Couty et al.,
1999; De Jong and Kaiser, 1992; Kaiser et al., 2003; Vet et al., 1998). Odors
of the host itself appear much more attractive than substance emanating
from the microhabitat. Several studies reported that most wasp species
show a very strong innate attraction to Drosophila aggregation pheromone
(Wertheim et al., 2003; Wiskerke et al., 1993). Molecule was identified as
(Z)-11-octadecenyl acetate produced by Drosophila male and transferred
to female during mating. In contrast to the innate response of Leptopilina,
A. tabida needs to learn this host’s odor source (Hedlund et al., 1996).
As we could expect, the generalist parasitoid L. heterotoma innately
responds to odor cues of all Drosophila species within its host range,
while the specialist L. boulardi is attracted by odors of a limited number
of Drosophila species, mainly those inhabiting fermenting fruit, among
which are its natural hosts, D. melanogaster and D. simulans (Hedlund
et al., 1996; Vet et al., 1993). The fact that L. boulardi responds also to
odor of nonhost species suggests common compounds in odor blend
emanating from host and nonhost species. Specialists and generalists
also might differ in their ability to learn, with a stronger learning capacity
in generalist species (Poolman et al., 1992).
1.2.3.2. Host patch exploitation

Once potential host batches are successfully localized, Drosophila parasi-
toids need to select suitable preys, that is, species of its host range and
healthy larvae. Drosophila parasitoids exhibit a species-specific searching
strategy to localize host larvae that classically involves the use of host-
induced vibrations transmitted by the substrate (vibrotaxis), ovipositor
searching (walking while probing), antennal searching and local arrest-
ment to perceive high concentration of kairomones (van Dijken and van
Alphen, 1998; Vet and Bakker, 1985; Vet and van Alphen, 1985). A. tabida
uses mainly vibrotaxis (Sokolowski and Turling, 1987; van Alphen and
Drijver, 1982) to detect its host that is thought to be the most efficient
strategy when hosts are scarce or buried deeply in the substrate.
However, this becomes confusing at high host density. L. heterotoma use
ovipositor searches (Vet and van Alphen, 1985) that can be more efficient
to find Drosophila larvae at high host density, a situation that is actively
sought by this species as suggested by its rapid departure from lower
density patches (van Lenteren and Bakker, 1978). L. boulardi shows an

intermediate strategy with mainly the use of ovipositor but also the
movement of larva as host detection cues (Vet and Bakker, 1985). The
difference in such searching behavior among species with overlapping
niches is thought to favor spatial partitioning of competing species and
thus their coexistence (van Dijken and van Alphen, 1998). This could also
participate in the choice of the most suitable host species for parasite
development in nature where several Drosophila species thrive in the
same fruits.
1.2.3.3. Hosts acceptation and superparasitism

The following step in the process of host selection that focused extensive,
empirical and theoretical studies is the distinction by the parasite among
parasitized and unparasitized hosts (Gandon et al., 2006; Godfray, 1992;
van Alphen and Visser, 1990; van Lenteren, 1981; Visser et al., 1992a).
Drosophila parasitoids were largely used to analyze the process of dis-
crimination between healthy and parasitized hosts, and superparasitism,
when a female accepts a previously parasitized host. Most results were
obtained on L. heterotoma, which clearly distinguishes and avoids para-
sitized hosts with the capacity to determine the number of parasite eggs in
a particular host (Bakker et al., 1972, 1990; Hemerik and van der Hoeven,
2003; van Lenteren, 1976). A. tabida also discriminates parasitized hosts
but lacks the ability to count the number of parasite eggs they contain
(Hemerik and van der Hoeven, 2003; van Alphen and Nell, 1982). Host
discrimination may prevent the waste of eggs, and it may be involved in
the time budget conservation and gives cues about patch quality used by
females to leave low profitability patches. However, the fact that super-
parasitism is often observed, probably arising from the female’s decision,
initiated theoretical works demonstrating the adaptive value of superpar-
asitism under competition, if there is a fitness pay-off from an egg laid in a
parasitized host (Gandon et al., 2006; Hemerik et al., 2002; van Alphen
and Visser, 1990; Visser et al., 1992b). Theoretical predictions were sup-
ported by results from experiments on L. heterotoma, which often behaves
as an optimal model of superparasitism (Visser, 1995; Visser et al., 1990,
1992b,c). However, this adaptive view of superparasitism was recently
called into question by results obtained on L. boulardi, which can show
very high level of clearly nonadaptive superparasitism. In this species,
excessive superparasitism is surprisingly triggered by a virus (LbFV), that
is vertically and horizontally (contagiously) transmitted (Varaldi et al.,
2003, 2006; Chapter 13 by Varaldi et al.). The differential adaptive interests
of the virus and the wasp can create a conflict that can deeply modify the
outcome of superparastism level (Gandon et al., 2006). To date, this viral
origin of superparasitism does not challenge adaptive interpretation of
this behavior made in other Drosophila parasitoid species since the LbFV
virus shows a strict specificity to L. boulardi (Patot et al., 2009). According
to all information gathered within a patch (host kairomone, oviposition
experience, patch depletion, time spent) and possible knowledge about
quality of the surrounding habitat, parasitoids are supposed to allocate
optimally their patch resident time, that can be reached by different
procedures (review in van Alphen et al., 2003). In A. tabida, ovipositions
increase patch resident time (incremental mechanism) and females use
several cues to optimize time allocation on a patch (Galis and van Alphen,
1981; van Alphen and Galis, 1983). L. heterotoma also shows an
incremental mechanism of oviposition whereas rejection of parasitized
hosts increases the patch leaving tendency, which is consistent with
aggregated distribution of Drosophila larvae (Haccou et al., 1991; Varaldi
et al., 2005). In contrast, oviposition and rejection have no effect on patch
resident time and leaving tendency in L. boulardi, thus suggesting a
different issue of selection, probably in response to the high level of
superparasitism induced by LbFV virus infection (Varaldi et al., 2005).
1.2.3.4. Virulence and resistance

The covariation of life histories and the underlying trade-off that can
balance overall parasitoid fitness with different combination of traits
according to life histories theory (Roff, 1992; Stearns, 1992) were far less
investigated and probably remains a promising issue for the future. More
results are available on Drosophila, particularly the cost to develop genetic
resistance against parasitoids (encapsulation) that can decrease fitness
related trait, among which the competitive ability of Drosophila, their
mating success and resistance to stresses (Fellowes et al., 1998; Hoang,
2001; Kraaijeveld and Godfray, 1997; Kraaijeveld et al., 2001, 2002; Rolff
and Kraaijeveld, 2003). With regard to parasitoids, enhanced virulence
obtained by artificial selection has only a very slight effect on egg stage
duration with no consequence on other fitness traits, but the difference
seems sufficient to potentially reduce survival probability in case of
superparasitism and then can be considered as an evolutionary trade-off
(Kraaijeveld et al., 2001). Extensive progress has been made since the late
1990s on immune response of Drosophila against parasitoids, and strate-
gies of wasps used to overcome host resistance, including factor of viru-
lence (Carton and Nappi, 1997, 2001). This aspect of host–parasitoid
relationship falls beyond the scope of this review (see section III this
volume), but it is, however, noticeable that mechanisms by which para-
sitoids defeat the Drosophila immune response vary hugely among spe-
cies. L. heterotoma suppresses host encapsulation of its egg by injecting
virus-like particles (VLPs) that cause cellular immune depression.
L. boulardi harbors morphologically different VLPs and uses virulence
factors present in the venom to weaken the immune competency of
their host. Virulence factors of these two Leptopilina species have quite
different effects on the up- and downregulation of transcriptional activity
of the Drosophila immune gene (Schlenke et al., 2007). In contrast, A. tabida
does not provoke any host immune depression but uses sticky eggs that
bind to host tissues allowing parasitoids to avoid encapsulation (Eslin
et al., 1996; Prévost et al., 2005). How and why these different strategies
have evolved remains an open question that could be solved only by
integrating precise knowledge about host range of parasitoids and com-
munity structure and functioning.
1.2.3.5. Adult life history traits

Whatever the mechanism of virulence used, it seems that the ability of
Drosophila parasitoids to overcome host immune responses is pervasive in
natural populations, giving the opportunity for natural selection to shape
other life history traits whose covariation remains poorly understood.
Using five Leptopilina species, Eijs and van Alphen (1999) studied the
correlation among several life history traits (development time, adult
life span, body size, egg load, growth rate and fat reserve) when para-
sitoids are reared on two host species. A classic correlation among body
size and egg load was observed in Leptopilina species that was previously
demonstrated for a number of other parasitoids whose fitness increased
with female size (Visser, 1994). The authors however failed to detect any
relationship between development time and adult life span, a classic
trade-off predicted by life history theory (Roff, 1992). This confirms earlier
findings in Hymenoptera parasitoids (Blackburn, 1991) and the authors
put forward the hypothesis that the particular way of life of parasitoids,
especially the growth rate of their immature stage that shows a host-
related plasticity, can explain this result. A. tabida also exhibits a positive
correlation between size and egg load (Ellers et al., 1998; Kraaijeveld and
van der Wel, 1994). Nevertheless, size–fitness relationships could change
during the season moderating even impeding selection for large indivi-
duals (Ellers et al., 2001).
1.2.4. Effects of temperature and overwintering

In all ectotherms, temperature plays a major role on phenotypic expres-
sion of traits and life histories (Cossins and Bowler, 1987; Leather et al.,
1993; Precht et al., 1973). Insect hosts and their parasitoids may show
different thermal requirements with complex and unexpected effects on
the nature of interaction and stability of the associations. Several studies
reported temperature-induced variation on phenotypic traits of
Drosophila parasitoids (Boulétreau et al., 1994; Kraaijeveld and van der
Wel, 1994), but very few analyzed precise reaction norms looking for
difference in thermal specialization of host and parasite. This is, however,
an important issue to understand the geographical distribution of species,

the community structure and the impact of climate change on the stability
of parasitic associations. Using a range of temperature from 14 C to 26 C
and the three main host species, Ris et al. (2004) showed that L. heterotoma
has a narrow thermal niche compared to all their host species (D. melano-
gaster, D. simulans and D. subobscura). This probably explains the variation
of species abundance throughout the season and probably participates to
the stability of host–parasitoid association. Interestingly, different geno-
types of L. heterotoma do not show the same ability to cope with tempera-
ture variation. Complex genotype-by-temperature interactions thus
appear, revealing local adaptation with southern strains more adapted
to warmer temperatures when the most common local host species is used
(D. simulans). These results illustrate how parasitoids genotypes could be
locally specialized to the host species, the temperature and their interac-
tion, thus suggesting that weak environmental variation may destabilize
the association. Another issue of parasitoid thermal biology lies in the
way species cope with cold temperatures during winter. L. boulardi and
A. tabida have been described as developing a larval diapause. Claret and
Carton (1980) demonstrated the occurrence of facultative diapause at the
prepupa stage of L. boulardi induced by a relatively low temperature,
which was also observed in other populations (Hertlein, 1986). Almost
98% of the larvae enter diapause at 17.5 C, 14% at 22.5 C and no
diapause is observed at 25 C. Diapause induction is independent of
photoperiod and thermoperiod. Diapause termination is hastened by
transferring larvae to 25 C. No indication of any genetic differentiation
between tropical and temperate populations has been found on diapause
induction in L. boulardi (Carton and Claret, 1982). In A. tabida, diapause
occurs as a prepupa inside the host’s puparium and the photoperiod
clearly influences diapause induction (Baker, 1979; Jenni, 1951). The
termination of diapause requires exposure to 4 C for at least 6 weeks.
Percentage diapause in A. tabida is influenced by host species with more
diapause in D. melanogaster than in D. subobscura (Kraaijeveld and
van Alphen, 1995b) and more in D. pseudoobscura than in D. subobscura,
D. ambigua and D. athabasca (Kraaijeveld and van Alphen, 1993). Diapause
in A. tabida is clearly influenced by both low (15 C) and high tempera-
tures (25 C) that both increase its occurence (Kraaijeveld and van Alphen,
1995b). In this species, diapause is associated with energetic costs such as
a substantial reduction in egg load, fat reserves and dry weight of the
emerging adult females (Ellers and van Alphen, 2002). As with L. boulardi,
no latitudinal geographical cline on percentage diapause has been observed
despite the variation that occurs among populations (Kraaijeveld and van
Alphen, 1995b). In contrast, L. heterotoma does not show larval or prepupal
diapause (Carton et al., 1991) but this species overwinters as an adult (Eijs,
1999). Overwintering females are readily active early in the season as soon
as favorable climatic conditions reappear. In spite of a high winter adult

mortality, by breeding early in the season, L. heterotoma is able to produce up
to four generations in temperate areas (Eijs, 1999).
1.3. GEOGRAPHICAL DIFFERENTIATION

AND LOCAL ADAPTATION
1.3.1. Geographical variations and host–parasitoids relationship

Abiotic factors and the structure of the Drosophila parasitoid community
and their interactions vary geographically even at a lower scale (e.g., the
situation in the southeast of France). Under the hypothesis that genetic
variations exist within populations, geographical differentiation and pos-
sible local adaptation are expected and important issues include identify-
ing the selective forces involved in the adaptive processes and what traits
actually respond to selection. Significant heritability of host and parasit-
oid features involved in the interaction, mainly host suitability and resis-
tance, has been revealed by the isofemale lines technique for L. boulardi
(Boulétreau and Fouillet, 1982; Boulétreau and Wajnberg, 1986;
Boulétreau et al., 1987; Carton and Nappi, 1991; Carton et al., 1989;
Wajnberg et al., 1985), L. heterotoma (Boulétreau and Wajnberg, 1986;
Boulétreau et al., 1987; Carton and Boulétreau, 1985; Delpuech et al.,
1994) and A. tabida (Mollema, 1991; Orr and Irving, 1997). Additive
genetic variance within populations was confirmed by artificial selection
experiments on traits such as host resistance (encapsulation) that can
show rapid response to selection (Fellowes et al., 1998; Hughes and
Sokolovski, 1996; Kraaijeveld and Godfray, 1997; see Fellowes and
Godfray, 2000 and Kraaijeveld and Godfray, 1999 for reviews). Few
investigations focused on genetic variability of parasitoid virulence
despite our knowledge that these variations do occur (Carton and
Nappi, 1991; Carton et al., 1989; Walker, 1962). These natural variations
were then used to identify the genetic basis of the immune response of
Drosophila and factors of parasitoid virulence which put forward candi-
date genes involved in the interaction (Benassi et al., 1998; Colinet et al.,
2007, 2009; Dubuffet et al., 2008; Dupas and Carton, 1999; Dupas et al.,
1998; Fellowes and Godfray, 2000; Labrosse et al., 2003; Nappi et al., 1991,
1992; Poirié et al., 2000; Vass et al., 1993). Unfortunately, in return, these
findings on resistance and virulence genes have not yet been used to
analyze how they may explain additive genetic variation observed within
a population or if these genes are involved in variation among natural
populations. A number of studies demonstrated that geographical popu-
lations can show marked differences, thus suggesting that local selective
forces acted to shape host and parasitoid traits. Virulence of L. boulardi,
that is, ability to evade D. melanogaster encapsulation, differs among

populations originating from Europe or central Africa (Carton and
Nappi, 1991), but subsequent studies failed to extend this variation to
worldwide populations that are clearly nearly all immunosuppressive
with the exception of those originating from Central Africa (Dupas and
Boscaro, 1999). In A. tabida, virulence on D. melanogaster shows a north–
south clinal variation across Europe (Kraaijeveld and van Alphen, 1994)
with a much higher virulence of southern Mediterranean populations.
The fact that these variations parallel geographical variation of the rela-
tive abundance of encapsulating (D. melanogaster) and nonencapsulating
(D. subobscura) hosts suggests a local adaptation of the parasitoid
to D. melanogaster, its main host species in the south. On the host side,
D. melanogaster also shows geographical variation of resistance against
both L. boulardi (Boulétreau, 1986; Boulétreau and Fouillet, 1982) and
A. tabida (Kraaijeveld and van Alphen, 1995a), without any correlation
between resistances against the two parasitoid species (Kraaijeveld and
Godfray, 1999). However, the significance of the geographical pattern of
resistance variation is unclear on an adaptive point of view.
Because the host community composition varies locally and the suit-
ability for parasitoid development also varies within one host species,
differential selective pressures may lead to local variation in host selection
behavior. By comparing choices made by females with those predicted by
optimal foraging models, it has been shown that parasitoids indeed
behave optimally with regard to host selection ( Janssen, 1989;
Kraaijeveld et al., 1995). Comparative studies revealed that this could
lead to genetic differentiation in the choice of the most suitable local
host. Due to geographical variation in the capacity of A. tabida to survive
in D. melanogaster, Kraaijeveld et al. (1995) demonstrated that the northern
population rejects this host and prefers to oviposit in D. subobscura,
whereas the southern populations accept both host species indistinctly
as expected in accordance with the to local abundance of host species.
A similar conclusion was drawn from a quite a different situation
bringing into play two L. boulardi strains that can develop either on
D. melanogaster (Mediterranean strain encapsulated by D. yakuba) or on
D. yakuba (Central Africa strain encapsulated by D. melanogaster).
In agreement with optimal foraging models, the Mediterranean strain
prefers D. melanogaster in choice experiments, whereas the other prefers
D. yakuba (Dubuffet et al., 2006). In this case, more precise information on
the local ecological situation is needed to interpret these results in terms of
local adaptations. Pannebakker et al. (2008) also showed genetic differen-
tiation in L. clavipes between northwestern and southern European
strains. Parasitoids from southern Europe accepted all tested Drosophila
species while northwestern parasitoids appeared to be more specialist
and preferred hosts that thrive in fungi, rejecting D. melanogaster.
This difference is interpreted by the authors as an adaptation to condi-

tions most often encountered by parasitoids in the field.
1.3.2. Small scale geographical variations

and competitive interaction
1.3.2.1. Geographical variation in southeastern France
The ecological situation followed in southeastern France (see section 1.1)
shows that selective forces other than single host–parasitoid interactions
act in natural communities – mainly competition. As community struc-
tures vary locally at low geographical scales (less than 4 of latitude),
mainly because this area encompasses the northern limit of L. boulardi
geographical range, other parasitoid species experience quite different
competitive interactions with higher selective pressure in the south, as
suggested by the rate of parasitized hosts (80% in some sites). We per-
formed a comparative analysis of life history traits of L. heterotoma by
sampling populations distributed along a north–south axis that included
different levels of competition. Strains were bred in the laboratory and
traits were measured under the same conditions (25 C, photoperiod
LD 12:12) to reveal the expression of genetic variation. Huge variations
were observed for a number of traits that correlate latitudinal variation
of Drosophila–parasitoid communities. Activity and its circadian rhythm
show genetic differentiation with southern populations active both at
the beginning and the end of the day with higher rate of activity, whereas
northern populations are less active only during the afternoon
(Fleury et al., 1995). These results were confirmed on a number of other
L. heterotoma populations (Fleury, unpublished observation) and could be
interpreted as a better capacity of southern population to disperse and
then to explore a more fragmented habitat also exploited by L. boulardi.
Populations of L. heterotoma also differ for fecundity with a very high,
significant effect of latitude. Populations from the north show a low
fecundity compared to populations from the south that produce almost
100 eggs more despite populations being separated by a distance of less
than 500 km. The fact that the variation of fecundity follows a cline that is
inverted compared to what is generally observed in insect responses to
temperature (Boulétreau-Merle, 1992; Capy et al., 1993; Karan et al., 1998;
Mitrovski and Hoffmann, 2001) suggested that other selective factors than
a direct response to temperature are involved. We put forward the
hypothesis that these variations result from high competitive interactions
induced by the presence of the superior competitor L. boulardi in the south
but absent in the north. Higher fecundity may increase the competitive
ability of L. heteroma and then balance the competitive ability of interact-
ing species, which could participates with other mechanisms of resource
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THE END
Transcriber’s Note: This story appeared in the November 15, 1927

issue of Adventure magazine.
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Advances in Parasitology 1st Edition Genevieve Prevost (Eds.) All Chapter Instant Download

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Advances in Parasitology First Edition Kirchhoff

Advances in Librarianship Volume 29 Advances in

Advances in Parasitology Volume 84 1st Edition D.

Advances in Parasitology Vol 66 1st Edition D.

Molecular Medical Parasitology 1st Edition Joseph Marr

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AMSTERDAM • BOSTON • HEIDELBERG • LONDON

First edition 2009

For information on all Academic Press publications

Printed and bound in UK

SECTION I. ECOLOGY OF DROSOPHILA PARASITOIDS 1

1. Ecology and Life History Evolution of Frugivorous

2. Decision-Making Dynamics in Parasitoids of Drosophila 45

3.3.Dynamics of Odour Memory Displayed in Odour Choices 73

SECTION II. THE PHYSIOLOGY AND GENETICS OF IMMUNITY

4. The Role of Melanization and Cytotoxic By-Products

5. Virulence Factors and Strategies of Leptopilina spp.:

6. Variation of Leptopilina boulardi Success in Drosophila Hosts:

7. Immune Resistance of Drosophila Hosts Against Asobara

8. Components of Asobara Venoms and their Effects on Hosts 217

SECTION III. STRATEGIES AND EVOLUTION OF PARASITOID

9. Strategies of Avoidance of Host Immune Defenses

10. Evolution of Host Resistance and Parasitoid

SECTION IV. SYMBIOTIC ORGANISMS OF DROSOPHILA PARASITOIDS 297

12. Drosophila–Parasitoid Communities as Model Systems

13. A Virus-Shaping Reproductive Strategy in a Drosophila Parasitoid 333

Sébastien J.M. Moreau

Alix D.N. Mabiala-Moundoungou

Extensive studies have been conducted on various parasitoid species, and

Due to circumstances beyond our control, Professor Jacques J.M. Van

dynamic equilibrium of populations and communities with their local

Section II is devoted to ‘‘postovipositional’’ host–parasitoid relation-

survive the host’s defenses). In hosts, authors give a thorough analysis of

attention here, thanks to the unique evolutionary and genetic status of

to take place. Indeed, the Drosophila–parasitoid communities provide a

the authors to bring new data and/or new hypotheses to a number of

Contents 1.1. Distribution, Community Structure and Ecological

* Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622,

Advances in Parasitology, Volume 70 # 2009 Elsevier Ltd.

Within the huge diversity of host–parasite interactions, parasitoidism

their potential to control phytophagous insect populations and their

special emphasis on the complex Leptopilina/Asobara/Drosophila living in

1.1. DISTRIBUTION, COMMUNITY STRUCTURE

relative abundance on different fermenting substrates and intensity of

1.1.2. Spatial and seasonal variations of communities

members of the community, here restricted to D. melanogaster, D. simulans

1.1.3. Intensity of parasitism, competition and coexistence

season. At the fruit scale, a high percentage of parasitized Drosophila

1990). However, this pattern of density-dependent parasitism risk is not

1.1.3.2. Competition within parasitoids community

competitors then take advantage to be active earlier, a temporal niche that

1.2. DROSOPHILA PARASITOID LIFE HISTORIES

140 140 (P < 0.002)*

0.2 0.3 0.4 0.5 0.2 0.3 0.4 0.5