CR Biologies

Alexander V. Sirotkin

Andrej Benco

Milos Mlyncek

Jan Kotwica

Saleh Alwasel

Abdel Halim Harrath

Transcription factor p53 regulates healthy human ovarian cells function

Adriano-B. Kury

A new species of Discocyrtoides from southern Brazilian pine forest (Opiliones, Gonyleptidae, Mitobatinae)

Laurent Keller

258 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
Disclosure of interest The author declares that she has no
competing interest.
References
[1] F. Müller, Ituna and Thyridia: A remarkable case of mimicry
in butterflies, Proc. Entomol. Soc. Lond. (1879), xx–xxix.
[2] M. Elias, M. Joron, Mimicry in Heliconius and Ithomiini but-
terflies: the profound consequences of an adaptation, Bio
Web of Conferences 4 (2015) 00008.
[3] M. McClure, C. Clerc, C. Desbois, A. Meichanetzoglou, M. Cau,
L. Bastin-Héline, et al., Why has transparency evolved in
aposematic butterflies? Insights from the largest radiation
of aposematic butterflies, the Ithomiini, Proc. Biol. Sci. 286
(2019) 20182769.
https://doi.org/10.1016/j.crvi.2019.09.010
Session III. Social insects and other
10
Supergene, sex and sociality
Laurent Keller
Faculté de biologie et médecine, Département d’écologie et
évolution, Groupe Keller, Lausanne University, CH-1015,
Lausanne, Switzerland
E-mail address: laurent.keller@unil.ch
Intraspecific variability in social organization is common, yet
the underlying causes are rarely known. I will show that the
existence of two divergent forms of social organization in six
ant species is under the control of a pair of heteromorphic
chromosomes that have many of the key properties of sex
chromosomes. In particular, this social chromosome contains
a large (13 megabases) region in which recombination is com-
pletely suppressed via three large inversions (Fig. 1). These
findings highlight how genomic rearrangements can maintain
divergent adaptive social phenotypes involving many genes
acting together by locally limiting recombination.
Fig. 1 Fine scale mapping and BAC-FISH analysis of social
chromosome.
Disclosure of interest The author declares that he has no com-
peting interest.
Further reading
T. Schwander, R. Libbrecht, & L. Keller. Supergenes and complex
phenotypes, Curr. Biol. 24 (2014) R288–R294.
J. Wang, Y. Wurm, M. Nipitwanttanaphon, O. Riba-Grognuz, Y.-
C. Huang, D. Shoemaker & L. Keller. A Y-like social chromosome
causes alternative colony organization in fire ants, Nature 493
(2013) 664-668.
A.C. LeBoeuf, R. Benton & L. Keller, The molecular basis of social
behavior: models, methods and advances, Curr. Opin. Neurobiol.
23 (2013) 3-10.
https://doi.org/10.1016/j.crvi.2019.09.011
11
Termites: Soil engineers for
ecological engineering
Pascal Jouquet1,∗, Ajay Harit2, Sougueh Cheik1,3,
Saran Traoré4, Nicolas Bottinelli 1,3
1 UMR iEES-Paris, Centre IRD, Bondy, France
2 School of Environmental Sciences, Mahatma Gandhi University,
Kottayam, Kerala, India
3 Soils and Fertilizers Research Institute, Dong Ngac, Tu Liem,
Hanoi, Vietnam
4 UFR-ST, Université Nazi Boni (UNB), Bobo, Burkina Faso
∗ Corresponding author.
E-mail address: pascal.jouquet@ird.fr (P. Jouquet)
This communication assesses advances in our knowledge of
the beneficial influences of termites on ecosystem functioning
and services. Termites are amongst the main macroinverte-
brate decomposers in arid and semi-arid environments and
exert additional impacts through the creation of biostructures
(mounds, galleries, sheetings, etc.) with different soil physical
and chemical properties. Unfortunately, the positive ‘or bright’
role of termites is often overshadowed by their dark side, i.e.
their status as pests threatening agriculture in the tropics (635
vs. 164 articles referenced in WoS with termites and either pest
or ecosystem engineer as keywords. Source: WoS, April 2019).
Termite impacts on soil properties and water dynamics can
be differentiated at four different scales: (i) at the landscape
scale, where termites act as heterogeneity drivers; (ii) at the
soil profile scale, where termites act as soil bioturbators; (iii) at
the aggregate scale, where they act as aggregate reorganizers;
(iv) and last, at the clay mineral scale, where they can act as
weathering agents [1].
In this communication, two examples of ecosystem services
provided by termites are given.
The first describes the positive impact of termites on water
infiltration and nutrient guidance at small scale through the
production of foraging galleries in soil [2] and how this activity
can be used to improve agro-ecosystem functioning in arid and
semi-arid environments [3].
The second example deals with the construction of mounds and
sheeting by termites in “natural” environments [4] and how
these “patches of biodiversity and fertility” can be used in the
lower Mekong Basin to reduce food insecurity and to provide a
better access to health [5] (Fig. 1).
Finally, the perception of termite mounds in Southern Indian
rural environments (Fig. 2) is discussed and used as example
of the cultural services that can be provided by termites in
some circumstances. The story of Valmiki, the author of the
Ramayana, is explained and used as a parable for highlighting
the interconnection between the “bright” and “dark” sides of
termites, and more generally that to get the bright we also need
the dark.
Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 259
Fig. 1 Termite mounds are conspicuous features of paddy
fields in Laos and Cambodia. Their soil is used as amendment
because it is enriched in organic matter and clay while its ani-
mal and plant diversity are used by the population as source
of food or medicine (Miyagawa et al., 2011) (Photo: P. Jouquet,
Cambodia, 2008).
Fig. 2 Termite mound made by Odontotermes obesus in South-
ern India (Photo: P. Jouquet, 2016). The offerings and the
statuette show that termite mounds are used as a means to
express one’s devotion to Shiva.
Disclosure of interest The authors declare that they have no
competing interest.
References
[1] P. Jouquet, N. Bottinelli, R.R. Shanbhag, T. Bourguignon, S.
Traoré, S.A. Abbasi, Termites: the neglected soil engineers
of tropical soils, Soil Sci. 181 (3/4) (2016) 157–165.
[2] S. Cheik, N. Bottinelli, M.T. Tran, T.T. Doan, P. Jou-
quet, Quantification of three dimensional characteristics of
macrofauna macropores and their effects on soil hydraulic
conductivity in northern Vietnam, Front. Environ. Sci.
(2019), http://dx.doi.org/10.3389/fenvs.2019.00031.
[3] E. Roose, V. Kabore, C. Guenat, Zai practice: a West African
traditional rehabilitation system for semiarid degraded
lands, a case study in Burkina Faso, Arid Soil Res. Rehab.
13 (4) (1999) 343–355.
[4] P. Jouquet, E. Chaudhary, A.R.V. Kumar, Sustainable use of
termite activity in agro-ecosystems with reference to earth-
worms. A review, Agron. Sustain. Dev. 38 (2018) 3.
[5] S. Miyagawa, Y. Koyama, M. Kokubo, Y. Matsushita, Y.
Adachi, S. Sivilay, N. Kawakubo, S. Oba, Indigenous utiliza-
tion of termite mounds and their sustainability in a rice
growing village of the central plain of Laos, J. Ethnobiol.
Ethnomed. 7 (2011) 24.
https://doi.org/10.1016/j.crvi.2019.09.012
12
Using contact networks and
next-generation sequencing for
wildlife epidemiology
Vincent Doublet ∗,1,2, Toby Doyle2, Isobel Refoy2,
Sophie Hedges2, Claire Carvell3, Mark J.F. Brown4,
Lena Wilfert2,5
1 Institute of Evolutionary Biology, University of Edinburgh, UK
2 College of Life and Environmental Sciences, University of Exeter,
Penryn Campus, UK
3 NERC Centre for Ecology & Hydrology, Wallingford, UK
4 Royal Holloway University of London, School of Biological
Sciences, UK
5 Institute of Evolutionary Ecology and Conservation Genomics,
University of Ulm, Germany
∗ Corresponding author.
E-mail address: vincent.bs.doublet@gmail.com
(V. Doublet)
Horizontal transmission of infectious diseases is strongly
determined by the contact network between hosts [1]. Envi-
ronmental and ecological variables that define the probability
of contacts between individuals, such as food resource quality
and quantity, have been largely neglected in models studying
the dynamics and epidemiology of wildlife diseases.
In this work, we used pollinators and their pathogens to study
the role of contact networks in a natural multi-host pathogen
community. In agricultural landscapes, wild flowers are the
most important food resources of insect pollinators such as
bees and flies. To boost yields of agricultural crops and ensure
pollinator conservation, the UK Environmental Stewardship
scheme prompted farmers to grow pollinator-friendly wild
flower margins along their fields (Fig. 1). Wild flower margins
(Fig. 1) have proven to be efficient to increase both density and
diversity of bees in agricultural areas, and to increase pollina-
tion success of surrounding crops.
As the rate of disease transmission should increase with host
density, we hypothesize that the success of wild flower margins
may generate hubs for pathogen exchange within the bee com-
munity. Several recent studies have illustrated the frequent
transmission of infectious diseases between managed and wild
bees, potentially via the shared use of flowers [2]. However,
the environmental and ecological drivers of disease dynamics
between pollinators remain uncharacterised [3]. To understand
the role of flower density and diversity for bee disease trans-
mission, we reconstructed high-resolution plant–insect visitor
networks from flower visitation data collected in ten farms in
Southern England (five farms participating in the scheme vs.
five control farms), as well as a record of bee pollen collec-
tion to describe the resource bees were exploiting (pollen vs.
nectar).
When analysing the plant–pollinator networks, we found that
flower density and diversity strongly define pollinator density
and foraging behaviour, and influence the structure of indi-


Supergene, sex and sociality

Ian Thomas Baldwin

262 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
Drosophila C Virus (DCV) and Cricket Paralysis Virus (CrPV)
in Drosophila. By contrast, the other components of the path-
way, including the regulatory subunit of the IKK kinase,
NEMO, do not appear to play a role in the resistance to infec-
tion by these viruses. Among the genes regulated by IKK
in virus-infected flies, we identified two genes involved in
the resistance to viral infection. The first one is the homo-
logue of the mammalian factor STING (Stimulator of Interferon
Genes), and we could show that it acts upstream of IKK and
Relish in a new signaling pathway (Fig. 2). The second one
encodes a new antiviral factor, that we called Nazo (meaning
“enigma” in Japanese) [3]. The STING-IKK -Relish signaling
cassette controls inducible expression of Nazo in response to
viral infection. Nazo results from a duplication of the gene
CG3740 in Drosophila species from the Sophophora subgenus. Of
note, CG3740 is not upregulated by viral infection, and ectopic
expression of the gene has no effect on replication of DCV or
CrPV, unlike expression of Nazo, which results in strong sup-
pression of viral replication. The discovery of Nazo provides
an excellent opportunity to decipher the genetics by which a
cellular gene acquires a new function in antiviral immunity.
Furthermore, the characterization of its mode of action against
picorna-like viruses may reveal novel angles of attack against a
family of viruses that include many serious human pathogens
(e.g., poliovirus).
In summary, the fantastic diversity of insects extends to the
viruses they carry, and to the genetic mechanisms they evolved
to control these viruses. This biodiversity provides a unique
opportunity to extend the repertoire of known antiviral mech-
anisms and to identify weak spots in the replication cycles of
viruses.
Disclosure of interest The author declares that he has no com-
peting interest.
References
[1] M. Shi, et al., Redefining the invertebrate RNA virosphere,
Nature 540 (2016) 539–543.
[2] E.R. Aguiar, et al., Sequence-independent characterization
of viruses based on the pattern of viral small RNAs produced
by the host, Nucl. Acids Res. 43 (2015) 6191–6206.
[3] A. Goto, et al., The kinase IKK regulates a STING- and NF-
 B- dependent antiviral response pathway in Drosophila,
Immunity 49 (2018) 225–234.
https://doi.org/10.1016/j.crvi.2019.09.015
15
Cassava mealybug biological
control delivers multi-faceted
societal benefits
Kris Wyckhuys
China Academy of Agricultural Sciences, China
E-mail address: kagwyckhuys@gmail.com
As core component of sustainable intensification, biological
control constitutes a tailor-made solution for the long-term
management of both endemic and invasive pests. Here, draw-
ing upon the example of the cassava mealybug (Phenacoccus
manihoti; Hemiptera), we illuminate the myriad benefits of
insect biological control.
In 2008, the above mealybug invaded Asia, where it inflicted
a 27% drop in aggregate cassava production and triggered
a 260% surge in starch prices. Mealybug-induced shocks in
Thailand’s cassava output were offset by a 300,000-ha expan-
sion of the agricultural frontier–accompanied with major
loss of intact tropical forest. Mealybug outbreaks were per-
manently resolved through the release of the neotropical
wasp Anagyrus lopezi (Hymenoptera). This minute parasitoid
effectively suppressed P. manihoti at a continent-wide scale,
restored food security, and delivered pest control services
worth US$ 200–700/ha. This same parasitic wasp had pre-
viously averted famine for ∼ 20 million people in Africa.
Our work emphasizes how beneficial (pest-controlling) insects
help meet food production needs while benefiting farmers’
pockets, global commodity trade, and the environment.
Disclosure of interest The author declares that he has no com-
peting interest.
Further reading
K.A. Wyckhuys, W. Zhang, S.D. Prager, D.B. Kramer, E. Delaquis,
C.E. Gonzalez, W. Van der Werf, Biological control of an invasive
pest eases pressures on global commodity markets, Environ.
Res. Lett. 13(9) (2018) 094005.
K.A.G. Wyckhuys, A.C. Hughes, C. Buamas, A.C. Johnson,
L. Vasseur, L. Reymondin, J.-P. Deguine, D. Sheil, Biologi-
cal control of an agricultural pest protects tropical forests,
Commun. Biol. 2 (2018); https://doi.org/10.1038/s42003-
018-0257-6.
K.A. Wyckhuys, P. Wongtiem, A. Rauf, A. Thancharoen, G.E.
Heimpel, N.T. Le, M.Z. Fanani, G.M. Gurr, J.G. Lundgren, D.D.
Burra, L.K. Palao, Continental-scale suppression of an invasive
pest by a host-specific parasitoid underlines both environ-
mental and economic benefits of arthropod biological control.
PeerJ., 6 (2018) e5796.
https://doi.org/10.1016/j.crvi.2019.09.016
16
Insects and their microbial
partners: The Drosophila case
study
François Leulier
Institute de génomique fonctionnelle de Lyon, École normale
supérieure de Lyon, University of Lyon, France
E-mail address: francois.leulier@ens-lyon.fr
Metazoans establish reciprocal interactions with their com-
mensal bacterial communities. Despite recent progress, a
clear view of the physiological benefits associated with
host/microbiota relationship remains elusive. Hence the
molecular mechanisms through which the microbiota exerts its
beneficial influences are still largely undefined. In this line, we
aim at deciphering the molecular dialogue governing the mutu-
alistic interaction between intestinal bacteria and their host. To
Fig. 1 Lactobacillus plantarum (associated with blue food and
feces) colonizes the host intestine (in both adults and larvae)
and is transmitted vertically to progenies (note the contami-
nation of an egg being laid) and promotes larval growth (note
the size difference of L. plantarum associated individuals (lar-
vae with blue intestine) vs. non colonized larvae (no blue in
the intestine) when grown for six days on a low nutrient diet).
© François Leulier.
Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 263
this end, we are using a genetically tractable gnotobiotic ani-
mal model: Drosophila melanogaster, which is mono-associated
with one of its natural dominant commensal, Lactobacillus
plantarum (Fig. 1). We are developing multiscale functional
approaches to identify the mechanisms that underlie their
mutualistic relationship, which results in the promotion of host
juvenile growth upon chronic undernutrition. Our approaches
aim at identifying both the bacterial and host genetic networks
required to sustain their mutualistic relationship.
Disclosure of interest The author declares that he has no com-
peting interest.
Further reading
M.E. Martino, P. Joncour, R. Leenay, H. Gervais, M. Shah, S.
Hughes, B. Gillet, C. Beisel, F. Leulier, Bacterial Adaptation to
the Host’s Diet Is a Key Evolutionary Force Shaping Drosophila-
Lactobacillus Symbiosis. Cell Host Microbe 24. Published online
28 June 2018, 10.1016/j.chom.2018.06.001.
G. Storelli, M. Strigini, T. Grenier, L. Bozonnet, M. Schwarzer,
C. Daniel, R. Matos, F. Leulier, Drosophila Perpetuates Nutri-
tional Mutualism by Promoting the Fitness of Its Intestinal
Symbiont Lactobacillus plantarum, Cell Metab. (2017), doi:
10.1016/j.cmet.2017.11.011.
R.C. Matos, M. Schwarzer, H. Gervais, P. Courtin, P. Joncour,
B. Gillet, D. Ma, A.L. Bulteau, M.E. Martino, S. Hughes, M.P.
Chapot-Chartier, F. Leulier, d-Alanylation of teichoic acids
contributes to Lactobacillus plantarum-mediated Drosophila
growth during chronic undernutrition, Nat. Microbiol. (2017),
doi: 10.1038/s41564-017-0038-x.
https://doi.org/10.1016/j.crvi.2019.09.017
17
What five insects told us about
how a native plant copes with
real-world problems
Ian Thomas Baldwin
Max Planck Institute for Chemical Ecology, Jena, Germany
E-mail address: baldwin@ice.mpg.de
Five native insects have taught us about traits that are essential
for the survival of a native tobacco plant, Nicotiana attenu-
ata, which lives in the Great Basin Desert of the USA. The
five insects come from different feeding guilds, attack different
tissues at different developmental stages and have revealed dif-
ferent traits that are essential for plant survival. For example,
this plant recognizes attack from a specialized Lepidopteran
herbivore (Manduca sexta) by the particular chemistry of the
herbivore’s saliva, and uses this recognition to tailor a compli-
cated 6-layered defense response that involves a remodeling of
the plant’s transcriptome, metabolome and proteome, as well
as some of its life history traits. The plant traits revealed by the
remaining four insects will be described below, and how these
insects will be used as high-through-put (HTP) screeners of
large plantations of transformed and recombinant inbred lines
of this native plant, to reveal the function of genes required for
survival in nature. Insects are some of the best plant biologists
on our planet and it behooves plant biologists to rediscover the
lost art of natural history discovery to take advantage of the
unique skill-sets of insects.
The plant and its insect herbivore community
Nicotiana attenuata (coyote tobacco: Solanales: Solanaceae) is
a diploid tobacco native to the Great Basin Desert of North
America. It enjoys a unique position scientifically, because hun-
dreds of transgenic lines have been studied over the past two
decades to understand the fitness consequences of precisely
defined changes in gene expression for plants growing in their
native habitats. For more than 30 years, the plant has been an
ecological model system to study the complex plant-mediated
interactions that occur in nature and to elucidate the genetic
basis of traits important for the Darwinian fitness of plants.
The choice of this diploid, largely selfing plant as a model sys-
tem is grounded in its natural history and unusual germination
behavior. Dormant seeds, survivors of decades or even cen-
turies of microbial challenges in soil, germinate synchronously
into the nitrogen-rich, competition-free environments that are
commonly found after fires. Dense N. attenuata populations
then develop, in which plants are exposed not only to intense
conspecific competition, but also to attack from as many as
34 different herbivore and pathogen taxa that colonize these
post-fire populations from adjacent unburned areas.
These are the ecological conditions in which agriculture
started, as slash-and-burn agriculture, and are the conditions
that all our crops face. However, most crop taxa have not origi-
nated from post-fire adapted native species and are unlikely to
be pre-adapted to the conditions of the agricultural niche. By
understanding the specific traits that this native tobacco plant
has evolved to optimize its fitness in the post-fire environment
in which it times its germination and growth from long-lived
seedbanks, we hope to learn what will be required to make our
crop plants more self-sufficient, less dependent on agricultural
inputs.
Nicotiana attenuata hosts a diverse insect herbivore community
that includes several specialists on the Solanaceae: Corime-
laena extensa (Hemiptera: Thyreocoridae), Epitrix hirtipennis,
and E. subcrintia (Coleoptera: Chrysomelidae), two sympatric
sibling species of Trichobaris, T. compacta, and T. mucorea
(Coleoptera: Curculionidae), Tupiocoris notatus, (Hemiptera:
Miridae), Manduca quinquemaculata, and M. sexta (Lepidoptera:
Sphingidae) as well as the generalist herbivores Spodoptera
spp. (Lepidoptera: Noctuidae), Trimerotropis spp. (Orthoptera:
Acrididae), and Oecanthus spp. tree crickets (Orthoptera: Grylli-
dae) and the opportunistic generalist herbivores Empoasca spp.
(Hemiptera: Cicadellidae) and Heliothis spp. (Lepidoptera: Noc-
tuidae). Geocoris pallens is a common predator of herbivores on
N. attenuata.
Five of these insects (four herbivores and one predator) have
proven to be very useful in eliciting and responding to plant
traits, characteristics that make them very useful as High-
Through-Put (HTP) screeners and sentinel insects for large
forward-genetic Recombinant Inbred Line (RIL) populations
that will be described after these five insects are introduced.
The herbivores: Manduca, Empoasca, Tupiochorus, and Tri-
chobarus spp
Manduca spp. The tobacco and tomato hornworms (M. sexta
and M. quinquemaculata) have evolved an unprecedented
capacity to detoxify the signature defense metabolite of the
genus, Nicotiana, namely: nicotine. These nicotine-adapted
larvae excrete the vast majority of the nicotine that they ingest
with their food, but also co-opt a small fraction of the ingested
nicotine for their own defense [1]. M. sexta larvae are found
on N. attenuata plants because the adult moths oviposit while
nectaring on the flowers. Hence, this insect plays dual roles in
the lives of N. attenuata plants, as a devastating herbivore dur-
ing the larval stages and as an important pollinator as an adult,
vectoring gametes among the spatially separated plant popu-
lations that occur after fires, likely adding important genetic
diversity to the seeds that must survive the decades of dor-
mancy in the seed banks. Attack from these nicotine-adapted
larvae is specifically recognized by the plant, when fatty acid
amino acid conjugates (FACs) in the larval oral secretions
are introduced into wounds when the larvae feed. This FAC-
mediated recognition by the plant results in a six-layered suite
of defense, avoidance, and tolerance responses (summarized
in an iBiology talk available at https://www.ibiology.org/
plant-biology/studying-plants-ecological-interactions-
genomics-era-story-nicotiana-attenuata/#part-2), which
engages all aspects of the plant’s physiology. As such, Manduca
larvae are ideal elicitors of ecologically important plant phe-
notypes and these phenotypes can be elicited by introducing
larval oral secretions into plant wounds, a treatment that
can be readily accomplished in a HTP manner for the large
numbers of plants in a MAGIC population.
Empoasca spp. These piercing-sucking leafhoppers “eavesdrop”
on the jasmonate (JA)-mediated signaling capacities of their
host plants, preferentially selecting those hosts that are defi-
cient in jasmonate accumulations [2]. Given that JA signaling
mediates the vast majority of plant defenses, it is particularly
intriguing that this natural phenotyping “bloodhound” specif-


What five insects told us about how a native plant copes with real-world problems

Luciano A. Moreira

Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 267
Un dernier aspect concerne le venin des parasitoïdes et le
potentiel d’évolution de la composition de ce venin en fonction
de paramètres abiotiques (température) ou biotique (résis-
tance de l’hôte, espèce ou souche hôte). Ainsi, un protocole
d’évolution expérimentale a été utilisé comme résumé ci-
dessous pour tester l’influence de la souche et espèce hôte
sur l’évolution de composition du venin. Deux souches de
L. boulardi différant par leur virulence et leur venin ont été
croisées dans les deux sens pour produire une F1 puis une
descendance F2, qui a ensuite été élevée en différents réplicas
et parallèlement sur des souches de D. melanogaster, D. yakuba
et D. simulans. L’expérience a été analysée en F3, F7 et F11 en
étudiant le taux de virulence du parasitoïde (réussite) et la
composition du venin. La méthode utilisée pour cette dernière
analyse a été développée et publiée en 2015 (Mathé-Hubert
et al., Mol. Ecol. Res.). Elle s’appuie sur la migration individu-
elle du venin et l’analyse des gels obtenus avec une méthode
semi-automatique à l’aide de Phoretix 1D. Elle permet d’obtenir
des bandes de référence calibrées et de produire un jeu de
données donnant l’intensité de chaque bande pour chaque indi-
vidu, cette intensité étant corrélée à la quantité de protéines.
Les résultats montrent une rapide augmentation de la viru-
lence du parasitoïde sur l’hôte de sélection et de la composition
du venin selon l’hôte et la génération. Trois à quatre généra-
tions suffisent pour observer des changements significatifs.
Les données suggèrent aussi un trade-off pour la virulence et
la composition du venin entre D. melanogaster et D. yakuba
(un changement dans un sens sur une espèce est corrélé à un
changement dans l’autre sens sur l’autre espèce). Enfin, il est
possible d’identifier les bandes dont le changement d’intensité
est responsable de l’évolution du venin sur un hôte donné.
On voit ainsi que toutes les bandes dont l’intensité a changé
sur D. yakuba sont spécifiques de cette espèce, montrant que
les protéines sélectionnées le sont également. En synthèse,
le venin évolue rapidement en fonction de l’hôte. En termes
de lutte biologique, des parasitoïdes locaux pourraient ainsi
s’adapter à un nouvel hôte invasif. Par ailleurs, l’élevage de par-
asitoïdes pour cibler un hôte donné se fait parfois sur un hôte
alternatif, ce qui peut induire une adaptation à cet hôte et un
échec ensuite sur l’hôte ciblé. En tous les cas, l’étude du venin
devrait permettre d’identifier les souches les plus efficaces et
de mener des contrôles qualité avant lâchers sur le terrain.
Déclaration de liens d’intérêts L’auteure déclare qu’elle n’a
pas de liens d’intérêts.
Pour en savoir plus
C. Kim-Jo, J.-L. Gatti, M. Poirié, Drosophila cellular immunity
against parasitoid wasps: a complex and time-dependent
process, Front. Invert. Physiol. 10 (2019) 603, doi:
10.3389/fphys.2019.00603.
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https://doi.org/10.1016/j.crvi.2019.09.019
19
When a bacterium fights
arboviruses
Luciano A. Moreira
Fiocruz Institute, Belo Horizonte, Brazil
E-mail address: luciano.andrade@fiocruz.br
Arboviruses or arthropod-borne viruses, such as dengue, Zika
and chikungunya represent a huge burden for tropical and sub-
tropical human populations. It has been estimated that, every
year, 390 million new cases of arboviruses occur in 128 coun-
tries and 3.9 billion people are at risk.
Vector control strategies are based on mechanical destruc-
tion of mosquito breeding sites and application of insecticides,
which, due to continuous and massive usage of different chem-
icals, have been contributing to the development of insect
resistance in many countries. Based on this complex scenario,
novel and sustainable strategies are urgently needed, which
can be used in an integrated control program by the gov-
ernments of affected countries. Biological control strategies,
involving mosquito pathogenic or pathogen-interfering orga-
nisms such as fungus or bacteria are possible, environmentally
friendly, candidates.
Wolbachia is an intracellular bacterium present in more than
60% of all insect species, worldwide. It manipulates the repro-
duction of insects, in order to be successfully maintained in
the system, through a mechanism called cytoplasmic incom-
patibility, or CI. When Wolbachia-infected males mate with
uninfected females, no progeny is produced. On the other hand,
females can mate with either infected or uninfected males and
will produce eggs, most frequently, 100% Wolbachia-infected,
the so-called, vertical transmission (Fig. 1). This mechanism,
among others caused by Wolbachia, promotes reproduction
advantage towards infected insects. Although present in sev-
eral mosquito species, the bacterium was never found in Aedes
aegypti, the main vector for dengue, Zika, and chikungunya,
worldwide. In the laboratory, back in 2005 in Australia, WMP
researchers were able to introduce a specific strain of this bac-
terium, into Aedes aegypti embryos, after having isolated it
from the fruit fly, Drosophila melanogaster. After this successful
transinfection, it has been discovered that, when the bacterium
is present in the mosquito, viruses do not replicate well, there-
fore reducing their transmission ability. This strategy does not
involve any kind of genetic modification.
An example of translational research
The World Mosquito Program (WMP) is a not-for-profit initia-
tive, working to protect the human population from mosquito-
borne diseases. WMP proposes an innovative method of
releasing Aedes aegypti mosquitoes into the environment with
Fig. 1 Representation of crosses between Wolbachia-infected
and uninfected mosquitoes, showing the mechanism of cyto-
plasmic incompatibility: when infected males mate with
uninfected counterparts, they produce no progeny.
268 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
the Wolbachia microorganism, which reduces the ability of the
mosquito to transmit dengue, Zika, and chikungunya. The Wol-
bachia method is safe, natural, and self-sustaining, and has the
potential to achieve significant public health impact in areas
endemic to these viruses.
WMP was formerly known as “Eliminate Dengue: Our Chal-
lenge.” The name has been changed due to rapid global program
expansion and also to reflect that the method works against
several diseases, not just dengue. WMP is active in 12 countries:
Australia, Vietnam, Indonesia, Pacific Islands (Fiji, Vanuatu,
Kiribati, New Caledonia), India, Sri Lanka, Colombia, Mexico,
and Brazil, and discussions are at an advanced stage with sev-
eral others. In Brazil, it has been conducted since 2012 by the
Fundação Oswaldo Cruz (Fiocruz), based in Rio de Janeiro.
The aim of WMP is to perform controlled releases of Aedes
aegypti containing Wolbachia, so there will be a gradient
substitution of local the Aedes aegypti population by Aedes
aegypti with Wolbachia. This is possible, through both the CI
mechanism and the vertical transmission, guaranteeing the
self-sustainability of the method.
Steps of Wolbachia Method
To achieve the goal of substitution of the local population of
Aedes aegypti with Aedes aegypti with Wolbachia, the actions of
WMP are divided into three main stages. (i) In the Community
Engagement phase, project teams interact with the population
and institutions (health clinics, schools, community leaders) for
disseminating information about the initiative. At this stage,
surveys are conducted to measure understanding and accep-
tance of the local population about the method. In addition,
a Community Reference Group is set up, a local committee
who monitors all actions taken in the locality, and communi-
cation channels are established with the community, including
telephone, e-mail, face-to-face interactions, and social media.
(ii) After the Community Engagement phase and community
approval begins the release of Aedes aegypti mosquitoes with
Wolbachia. Mosquitoes are bred in the Fiocruz insectary, which
has similar humidity and temperature characteristics as those
that mosquitoes encounter in the external environment. Adult
releases happen in the early hours of the morning and are
made by car. In some regions, this work is done on foot, by
health surveillance agents and community health agents of
the municipal governments of Rio de Janeiro and Niterói. (iii)
Monitoring of the Aedes aegypti population in these areas ini-
tiate during mosquito releases. Traps are installed in homes or
commercial establishments that voluntarily provide a location
for the traps. Weekly, technicians go to these sites to collect
mosquitoes. At the project facilities, the captured mosquitoes
are separated, identified and the Aedes aegypti are sent to the
Diagnostic Laboratory, where they are checked individually.
This analysis aims to identify the DNA of Wolbachia bacteria in
the mosquito organism and is an indicator of the establishment
of the local mosquito population with Wolbachia.
Large-scale expansion
WMP began preparative studies in Brazil in 2012 and ethical
and regulatory approvals. In 2014, releases began in the pilot
areas, Jurujuba, in Niterói-RJ, and Tubiacanga, in the city of
Rio de Janeiro. The last releases of mosquitoes at these sites
were carried out in January 2016, and since then monitoring
has revealed Wolbachia’s establishment of more than 90%. In
November 2016, large-scale expansion began for 28 neighbor-
hoods in Niterói, to protect 270,000 people.
In Rio de Janeiro, large-scale releases began in August 2017,
with the plan of reaching 19 neighborhoods, where 0.9 mil-
lion people live. Concomitantly with community engagement,
mosquito release and monitoring activities, an epidemiological
study is underway to measure the impact of our work in reduc-
ing disease transmission. Preliminary results show already a
reduction on the incidence of dengue, Zika, and chikungunya
in areas where Wolbachia is present.
Through a partnership with the city of Belo Horizonte, WMP
Brazil will start activities in an pilot area with 60,000 inhabi-
tants, probably in late 2019.
Regulatory and ethical approvals
For pilot projects, regulatory and ethical approvals were
granted in 2014. The Temporary Special Registry (Registro
Especial Temporário–RET–, in Portuguese) was granted after
evaluating the project simultaneously by three governmen-
tal areas: National Agency of Sanitary Surveillance–ANVISA–,
Ministry of Agriculture, Livestock and Supply–MAPA–, and
the Brazilian Institute of Environment and Renewable Natural
Resources–IBAMA. Ethical approval was also granted in early
2014, following a thorough evaluation by the National Commis-
sion for Research Ethics (CONEP). For the large-scale expansion,
all the regulatory documents have been renewed.
In February 2016, the Ministry of Health recommended the
Wolbachia method as promising in vector control in response
to Zika’s national emergency. This recommendation was rein-
forced in March of that year by the World Health Organization
(WHO) through its Vector Control Advisory Group (VCAG).
Funding
The project has been historically financed in Brazil by the
Ministry of Health, with an in-kind contribution from Fiocruz
and, internationally, by the Bill and Melinda Gates Foundation,
through Monash University, Australia. The municipalities of Rio
de Janeiro and Niterói provided an important contribution with
local infrastructure and human resources.
Disclosure of interest The author declares that he has no com-
peting interest.
Further reading
L.A. Moreira, I. Iturbe-Ormaetxe, J.A. Jeffery, G. Lu, A.T. Pyke,
L.M. Hedges, B.C. Rocha, S. Hall-Mendelin, A. Day, M. Riegler, L.E.
Hugo, K.N. Johnson, B.H. Kay, E.A. McGraw, A.F. van den Hurk,
P.A. Ryan, S.L O’Neill, A Wolbachia symbiont in Aedes aegypti
limits infection with dengue, Chikungunya, and Plasmodium,
Cell 139(7) (2009) 1268–1278.
H.L. Dutra, M.N. Rocha, F.B. Dias, S.B. Mansur, E.P. Caragata, L.A.
Moreira. Wolbachia Blocks Currently Circulating Zika Virus Iso-
lates in Brazilian Aedes aegypti Mosquitoes, Cell Host Microbe.
19(6) (2016) 771–774.
S.L. O’Neill, The Use of Wolbachia by the World Mosquito Pro-
gram to Interrupt Transmission of Aedes aegypti Transmitted
Viruses, Adv. Exp. Med. Biol. 1062 (2018) 355–360.
https://doi.org/10.1016/j.crvi.2019.09.020
20
Ecosystem services provided by
insects for achieving sustainable
developmental goals
Olivier Dangles
Département “Écologie, biodiversité et fonctionnement des
écosystèmes continentaux” (ECOBIO), Montpellier, France
E-mail address: olivier.dangles@ird.fr
Ecosystem services underpin all dimensions of human well-
being. As a consequence, it is crucial to integrate ecosystem
services into strategies for achieving Sustainable Develop-
ment Goals (SDGs). Because insects and other invertebrates
have profound and well-identified influences on many ecosys-
tems services (e.g., pollination and biological control) and
SDGs (e.g., crop pest and disease vectors), insect research and
development have a great potential to address current global
challenges. We argue that time is ripe to put more efforts in
developing integrated research on the ecosystem services pro-
vided by insects, as they may result in solutions to achieve
many SDGs. We provide evidence of insects’ utility to address
global challenges and propose a framework of the needed shift
in the perception of insects from enemies to allies, providers of
ecosystem services, and then to solutions to achieve SDGs. We
further advocate that making a place for SDG-relevant research
on insects’ ecosystem services requires transforming existing
academic knowledge into application-driven science, a poten-
tial upscaling of local solutions and socio-economic relevance.
Disclosure of interest The author declares that he has no com-
peting interest.
https://doi.org/10.1016/j.crvi.2019.09.021


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