CR Biologies

Michel Mitov

Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 249
in vivo (degradation, trapping, relocalization, etc.; Fig. 2). Sev-
eral cases in which such small, functionalized protein binders
have been used in Drosophila will be discussed, and a look into
the promising future of research with Drosophila will end the
presentation.
Disclosure of interest The author declares that he has no com-
peting interest.
References
[1] S. Harmansa, M. Affolter, Protein binders and their appli-
cations in developmental biology, Development 145 (2)
(2018), http://dx.doi.org/10.1242/dev.148874 [Review, pii:
dev148874].
[2] D. Bieli, I. Alborelli, S. Harmansa, S. Matsuda, E. Caussinus,
M. Affolter, Development and Application of Functional-
ized Protein Binders in Multicellular Organisms, Int. Rev.
Cell. Mol. Biol. 325 (2016) 181–213, http://dx.doi.org/10.
1016/bs.ircmb.2016.02.006 [Epub 2016 Mar 19, Review].
Further reading
E. Caussinus, O. Kanca, M. Affolter, Fluorescent fusion protein
knockout mediated by anti-GFP nanobody, Nat. Struct. Mol.
Biol. (1) (2011) 117–121, doi: 10.1038/nsmb.2180.
S. Harmansa, F. Hamaratoglu, M. Affolter, E. Caussinus,
Dpp spreading is required for medial but not for lateral
wing disc growth, Nature 527(7578) (2015) 317–322, doi:
10.1038/nature15712. Epub 2015 Nov 9.
https://doi.org/10.1016/j.crvi.2019.09.003
3
Insects as interactants in artists’
minds: Symbols and
anti-symbols
Yvan Rahbé1,∗, Edwige Keller-Rahbé2, Sibylle Orlandi2
1 INRA, France
2 Laboratoire MAP, UMR5240, Université Claude-Bernard Lyon-I,
bâtiment Lwoff, campus scientifique de La Doua, 43, boulevard
du 11-Novembre-1918, 69100 Villeurbanne, France
∗ Corresponding author.
E-mail address: yvan.rahbe@inra.fr (Y. Rahbé)
Insects, as small animals of frequent and easy access to humans,
at least under their non-flying larval stages, have always
been of interest to our species. The interest has probably
been nutritional, but also naturalistic and symbolic. Many
aspects of insects’ biology are of high symbolic potential,
among which biodiversity, metamorphosis or flight. These
three creative attributes of the insect orders, over the mam-
malian order at least–the self or reference class of human
life–, probably induced early interests in human societies.
This interest is indicated by folk classification of insects in
some indigene cultures of northern America or central Africa
[1]. Representation of insects in paleolithic art is scarce but
existing; one of the earliest attested records could be that
of “the buprestid” of Arcy-sur-Cure, revised as a ground
beetle–carabid–(Magdalenian III, ≈ 15000 years BP), or that of
“the grasshopper” of Enlène [2]. The first is sculpted in lig-
nite and could have served as a shamanic representation, while
the latter is more obviously naturalistic in nature, and carved
on bone. The more recently discovered Chauvet cave might
contain insect representations (a “butterfly” or a many-legged
animal), but no attested insects yet. Similarly, no insect men-
tion come yet from Sulawesi caves (late Mousterian, < 30,000
years BP).
Neolithic representations are much more numerous, as exem-
plified by bee hunting and bee rearing in Iberic or Egyptian
parietal and monumental arts. This trend culminated in Egyp-
tian jewellery and its quasi-industrial representations of scarab
or dung beetles. Noteworthy, most prehistoric representation
of insects lie on coleoptera and Hymenoptera, and associated
with symbolic features linked to colour, strength (beetles),
metamorphosis (all) or social and utility behaviours (bees,
ants). Aristotle himself did not clearly recognize aphids as a
group, as the ancient Greek word   ´ ı˛ did not differ-
entiate aphids and psyllids. Many mentions however, on the
reproduction of such insects, for example, show that he was
talking of aphids.
In line with these historical roots, insects have been associ-
ated with far eastern or Christian society arts [3]— in contrast,
Islamic and Jewish imaging or alimentary taboos having
banned them from visible representations in middle eastern
societies. A previous review on the subject gives an excellent
outline of our matter, restricted to European painting [4]. I will
here sketch a variant perspective, trying to uncover a hitherto
hidden monument of cultural entomology, with the case study
of the representation of aphids (Hemiptera: Aphididae) in var-
ious arts and all periods of history. Our purpose is to draw a
reflexive perspective on what such invisible insects, through
their invisibility, tell us of their representation in artists’ minds,
and more generally in any human mind (being he a reader, a
writer, a watcher, an actor, or in any position of the artistic
universe).
The first and archetypal position to be quoted in my survey of
invisible insects is the detail aphid. This position of a subject,
the detail, have been analysed thoroughly in the history of arts
[5]. It reflects both scientific and artistic mastery end precision
(it is painted because it exists), and a position of power of the
painter who is freely choosing low signification or even forbid-
den or non-codified subjects due to the act of freedom of the
artist (and art factories, often specialized in such very specific
matters); I paint it because I want/know it. This is characteristic
of the Flemish and Dutch renaissance, as visible in the Bou-
quet of flowers in a vase by Jan velvet Brueghel the Elder (Fig. 1).
In contrast to many of its fellow insects, cricket, coleoptera,
syrphid, the aphid is extremely difficult to localize (Fig. 1A),
and needs an intensive focus on its lily host-plant to be seen
(Fig. 1B). However, in spite of its minute size, it is precisely
depicted, and the crescent-marked lily aphid was recognized by
expert aphidologists (Colin Favret, pers. comm.). A non-expert
comparison between object and subject (Fig. 1B,C,D), be it liv-
ing (1 C) or mounted (1D) is edifying and informs us on the
naturalistic and observational abilities of the painter(s).
As one may imagine, such identification of aphids in European
classical painting is extremely difficult and has been only found
on three occasions and with the help of the G-art Gigapixel
project, apart from Fig. 1: in another still life by velvet Brueghel,
Flowers in a Vase displaying at the Antwerp museum of fine
arts, and in a third Chat renversant un vase de fleurs by Abraham
Mignon, Museum of Fine Arts, Lyon.
Fig. 1 Bouquet of flowers in a vase, by Jan Brueghel the Elder
(1608, oil on copper 65 × 45 cm); original (A) in the Pinacoteca
Ambrosiana (Milan, Italy), © with permission. Detail with an
aphid on a lily leaf (B) situated at the bottom-left corner of
the bouquet. Inferred species, with the help of Dr C. Favret:
Neomyzus circumflexus, quoted from Encyclop’aphid (C) with
its typical darkish crescent on the back (D).
250 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
All Dutch painters.
One easy case of naturalistic aphid lie in the paintings of Maria
Sibylla Meriam, a painter and entomologist of the seventieth
century who has painted aphids in numerous works, and both
entitled some of her paintings with the word, and depicted the
whole aphid ecosystem including all trophic levels in the global
picture (Rode akelei met bladwesp en bladluis, 1684).
One important item in our quest is the topos of the female
aphid (and eventually superfemale aphid). It probably did not
start with Charles Bonnet, but at least has fully expanded
after him. This talented Swiss student of Réaumur discovered,
described, and demonstrated parthenogenesis in what could be
called one of the first modern scientific papers in biology, its
Traité d’entomologie (1745). This signed a series of quasi-quotes
all over the following centuries, exemplifying the importance
of this reproductive trait in biology, as well as the impor-
tance of aphids as a model for this trait: this started by a
pejorative citation of Eugène Delacroix in a letter to a friend
in 1830 (“What a pity that such brilliant mind and man has
lost his time and eyes for understanding the venial sin of such
hideous animals”), followed by a real tribute to parthenogen-
esis in the masterpiece of Simone de Beauvoir, Le deuxième
sexe (Volume 1, Chapter 1, “The data of Biology”). One may
also quote in this very context the interesting parallel, made
by the contemporary art blog Quadrivia, between partheno-
genesis and the codified representation of “Sainte Anne
trinitaire” in the European religious sculpture of the late Mid-
dle Ages (https://quadriv.wordpress.com/2011/06/10/jesus-
aphids-and-parthenogenesis/). The sculptural code of Ste
Anne consisted in a triptychal representation of Virgin Mary,
her mother Anne, and child Jesus in a strange charac-
ter proportionality of adult (Anne), child-adult (Mary) and
child-child (Jesus). This invasion of the female-only char-
acter over the Holy Trinity was increasingly popular in
central Europe from the fortieth to the sixtieth century
(https://fr.wikipedia.org/wiki/Sainte Anne trinitaire), and was
only stopped by a specific canonical law codifying the Marial
cult, or hyperdulia, within the Council of Trento (1542–1563).
Although no aphid is represented in such topoi, of course,
the parallel between parthenogenesis and viviparity, somehow
unique to aphids, and the mystery of immaculate conception
ought to be underlined.
Already exemplified by Eugene Delacroix, cited above, the
recurrent and frequent topos of the evil aphid has been used
many times in French literature. Victor Hugo listed the vile
aphid among a list of biological fearsome fellows (Les Contem-
plations, T3 L6 26, p. 467 as appears in the Frantext database).
However, the complimentary figure of the humble aphid is
also present in post-ninetieth-century occurrences, typically
shown in Maurice Carême’s poem entitled Le Puceron.
Coming to modern art, the appearance of aphids tends
to explode, and I will only quote two examples. One
is what could be called the surrealistic oulipian aphid by
Boris Vian (Fig. 2), the other being the situationist aphid
of the musical theme of the Polish artist Duy Gebord in
the well-named Mildew album (https://duygebord.bandcamp.
com/album/mildew). The former merits a short outline, as it
is emblematic of the mosaic Carollian style of Boris Vian (Les
Fourmis, Fig. 2A). The prose starts as a very standard description
of a explicitly boring subject, to fall out into the final black-
hole of Oulipian fantasy (which translates as “The rearing of the
Tyrolian ‘gnatlet’or the milking of woolly aphids”). The induced
image explicitly (again) looks as Fig. 2A, driving the reader in a
universe of gentle and poetic madness typical of Vian’s prose.
It should be noted that the French mouchetis tyrolien (trans-
lated as Tyrolian gnatlet) does not refer, as it seems through
subtle juxtaposition, to an insect: instead it refers to an indus-
trial painting technique, also typical of the universe of engineer
Boris Vian, who started as fonctionnaire of the French normal-
ization agency AFNOR (as did Albert Einstein with the Swiss
patent agency). . .
We hope that our short survey of a hitherto boring subject has
driven the reader on the wild side of the history of arts and
sciences, and that the final references will allow him to escape
even more, at night, from its truly exciting daytime highways
Fig. 2 The milking of woolly aphids, as cited by Boris Vian
in Les Fourmis (Gallimard, La Pléiade) and reported on the left,
with a possible representation on the right: Le Génie des alpages,
F’Murr, Casterman.
of insect science. This compendium and conference is part of
an ongoing project, involving the aphid BAPOA community for
data collection, and partially published by Encyclopaphid [6].
The full corpus contains more than 100 entries and the present
outline is thus only the hidden part of the iceberg, to be fully
published soon.
This conference is quoted in the CNRS repository HAL as:
https://hal.archives-ouvertes.fr/hal-02069668.
Disclosure of interest The authors declare that they have no
conflict of interest.
References
[1] B. Morris, Insects and human life, Berg, Oxford, New York,
2004 [317 p.].
[2] P.G. Bahn, R.K. Butlin, in: J. Clottes (dir.), L’art des objets
au Paléolithique, colloque international. Foix, Le Mas-d’Azil,
Foix, 16–21 novembre 1987 sous la dir. de Jean Clottes, Min-
istère de la culture de la communication, Paris, 1987, pp.
247–253.
[3] C.L. Hogue, Annu. Rev. Entomol. 32 (1987) 181–199.
[4] M. Dicke, Am. Entomol. 46 (2000) 228–237.
[5] D. Arasse, Le détail, in: Pour une histoire rapprochée de la
peinture, Flammarion, Paris, 2009 [1 vol. (380 p.)].
[6] Y. Rahbé, E. Keller-Rahbé, S. Orlandi, P. Senges, C.-
A Dedryver, Aphids in art, a borderless outline. An
anniversary section of Encyclopaphid (GBR edition), in:
J.-C. Simon, M. Hullé, E. Turpeau (Eds.), Encyclopaphid,
INRA, Rennes, 2018 [https://www6.inra.fr/encyclopedie-
pucerons eng/].
https://doi.org/10.1016/j.crvi.2019.09.004
4
The shining world of beetles
Michel Mitov
Centre d’élaboration de matériaux et d’études structurales,
CEMES, CNRS, Toulouse, France
Twisted liquid-crystalline organizations are ubiquitous in liv-
ing matter [1,2]. Many insects own a tessellated carapace with
bumps, pits, indentations, stripes or spots (Fig. 1). These geo-
metric variation often exhibit iridescent colors, which are the
consequence of a complex twist of chitin macromolecules. Such
optical information with vivid structural colors might be of
paramount importance in the life and the evolution of most
day-living insects. Many biological functions are yet debated.
They are related to conspecific or intra-species communication,
thermoregulation, camouflage, survival or navigation [1,3].
For example, the cuticle of the scarab beetle Chrysina glo-
riosa exhibits two bands (Fig. 2). The green band serves as a
wavelength-selective (green) diffuser due to the set of polygons


The shining world of beetles

Markus Gildenhardt

Elena Levashina

Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 269
Session V. Vector insects and transmission
of diseases
21
Do we have to get rid of
mosquitoes to eliminate
malaria?
Markus Gildenhardt , Elena Levashina ∗
Vector Biology Unit, Max Planck Institute for Infection Biology,
Berlin, Germany
∗ Corresponding author.
E-mail address: levashina@mpiib-berlin.mpg.de
(E. Levashina)
Malaria is a local disease with global impact. The fitness of
vector-borne Plasmodium parasites, the causative agents of
malaria, is closely linked to the ecology and evolution of its
mosquito vector. Ongoing adaptive radiation and introgression
diversify mosquito populations in Africa. However, whether
the genetic structure of vector populations impacts malaria
transmission remains unknown.
We discuss below new approaches that gauge the contribution
of mosquito species to Plasmodium abundance in nature, with a
particular focus on time-series analyses in the context of popu-
lation genetics and epidemiology [1]. Our data highlighted the
importance of focusing vector control strategies on mosquito
species that drive malaria dynamics.
Using time-series collections and the econometric approach
Granger causality, we demonstrated that the abundance of
Plasmodium-infected mosquitoes in a field site in Mali was
driven by only one of the two sympatric vectors (Fig. 1). This
mosquito species carried a susceptible allele of the known
antiparasitic gene TEP1 [2,3], and until now it was resistant to
colonization efforts and, therefore, is not the target of current
gene drive applications.
Extending such studies to other key components of vecto-
rial capacity and epidemiological and parasitological surveys
should ultimately identify patterns, tipping points, and gen-
eral laws that describe dynamics, emergence, and resurgence
of mosquito-borne diseases.
Fig. 1 Granger causality.
Disclosure of interest The authors declare that they have no
competing interest.
References
[1] M. Gildenhard, E.K. Rono, A. Diarra, et al., Mosquito
microevolution drives Plasmodium falciparum dynamics,
Nat. Microbiol. 4 (6) (2018) 941–947.
[2] S. Blandin, S.-H. Shiao, L.F. Moita, C.J. Janse, A.P. Waters, F.C.
Kafatos, et al., Complement-like protein TEP1 is a determi-
nant of vectorial capacity in the malaria vector Anopheles
gambiae, Cell 116 (2004) 661–670.
[3] S.A. Blandin, R. Wang-Sattler, M. Lamacchia, J. Gagneur, G.
Lycett, Y. Ning, et al., Dissecting the genetic basis of resis-
tance to malaria parasites in Anopheles gambiae, Science 326
(2009) 147–150.
https://doi.org/10.1016/j.crvi.2019.09.022
22
Human activities and climate
change in the emergence of
vector-borne diseases
Anna-Bella Failloux
Arboviruses and Insect Vectors Laboratory, Department of
Virology, Institut Pasteur, Paris, France
E-mail address: anna-bella.failloux@pasteur.fr
Because of human population expansion and activities,
arthropod-borne viruses (arboviruses) have increased in
importance during these last decades. Arboviruses are main-
tained by alternate replication in both vertebrate hosts and
arthropod vectors. Successful transmission relies on a complex
life cycle in the vector, which starts when a competent arthro-
pod ingests an infectious blood meal from a viremic vertebrate
host. Following an extrinsic incubation time during which the
virus replicates in the vector midgut, followed by systemic viral
dissemination to the salivary glands, the vector can transmit
the virus to a new naïve host. Whereas they typically cause self-
limiting, acute infections in their vertebrate hosts, arboviruses
establish persistent infections in their vectors.
Arboviruses are typically maintained within an enzootic cycle
between wild animals and vectors. As human populations
encroach on regions where these diseases are endemic,
spillover transmission to humans and domestic animals can
lead to large-scale disease outbreaks affecting millions of peo-
ple. Dengue, chikungunya, Zika, and yellow fever mainly use
humans as amplification hosts. Extensive urbanization com-
bined with increased commerce and travel give rise to the
mosquitoes Aedes aegypti and Aedes albopictus, both highly
adapted to the human environment. The high densities of these
human-biting mosquitoes that proliferate in highly populated
cities made the bed to explosive outbreaks of arboviral dis-
eases. As insects are ectothermic organisms, climate change
may affect the geographical distribution of vectors, with con-
sequences on the transmission of arboviruses.
Yellow fever (YF) is a good example of an emerging arbovirus,
as it illustrates three main steps in the emergence: (i) introduc-
tion of a new pathogen in a new environment causing urban
outbreaks, (ii) spillback of this pathogen into the wild initiating
an enzootic cycle, and (iii) the spillover of this pathogen from
an enzootic cycle to initiate an urban cycle (Fig. 1).
YF (YFV, Flavivirus, Flaviviridae) is a disease endemic to tropical
regions of Africa and South America. There are seven lineages:
five in Africa and two in America. Each year, 200,000 cases and
30,000 deaths were reported. In 2016, YFV emerged in Angola
and imported cases were detected outside Africa, posing the
threat of emergence of this virus outside Africa and Americas
(Amraoui et al. Euro Surveill 2016).
YFV was introduced into the New World during the slave trade,
causing devastating outbreaks in several American countries,
including cities like New York City and Boston. Once Carlos
Finlay and Walter Reed had demonstrated that the YFV was
transmitted by a mosquito, Ae. aegypti, eradication campaigns
of the vector were initiated, leading to the control of YF.
In Brazil, Ae. aegypti was eradicated in 1954. YF disappeared
from cities and only persisted in a sylvatic cycle where YFV
circulated between zoophilic mosquitoes (Hemagogus and
Sabethes) and non-human primates. Using experimental infec-
tions, we showed that the zoophilic mosquitoes (Hemagogus
leucocelaenus and Sabethes albiprivus) were able to transmit
YFV at very high rates (Couto-Lima et al. Sci Rep 2017). With
the relaxation of control measures in Brazil, Ae. aegypti was
reintroduced in 1967 and Ae. albopictus in 1986. We showed
that Ae. aegypti and Ae. albopictus were highly susceptible to
YFV. We also demonstrated that using a protocol of experi-
270 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
mental selection, we were able to select a YFV well adapted to
a transmission by Ae. albopictus (Amraoui et al. Sci Rep 2018).
This result should alert about the potential of YFV to initiate an
urban cycle in Brazil, like in the past.
Fig. 1 The three main steps in the emergence of an arbovirus.
Disclosure of interest The author declares that she has no
competing interest.
https://doi.org/10.1016/j.crvi.2019.09.023
23
Benefits and limitations of
emerging techniques for
mosquito vector control
Catherine Golstein ∗,1, Pascal Boireau1,2,
Jean-Christophe Pagès1,3,
on behalf of the Scientific Committee of the High Council for
Biotechnology in France
1 Haut Conseil des biotechnologies (HCB, High Council for
Biotechnology), Paris, France
2 Anses, Maisons-Alfort, France
3 François Rabelais University, Tours, France
∗ Corresponding author.
E-mail address:
catherine.golstein@hautconseildesbiotechnologies.fr
(C. Golstein)
In response to a broad governmental referral, the French High
Council for Biotechnology has published an opinion on the use
of genetically modified (GM) mosquitoes for vector control [1].
Emerging techniques of vector control were developed to over-
come (i) the lack of therapies, preventive treatments and
vaccines for most mosquito-borne diseases, and (ii) the limi-
tations of existing vector control techniques (the situation is
particularly critical regarding insecticides: in France, essen-
tially only one insecticide is used against adult mosquitoes
(deltamethrin), and its efficacy decreases due to resistance evo-
lution in mosquito populations).
To date, only one GM mosquito-based technique has been
developed to an operational level, Oxitec’s RIDL technique,
which seeks to reduce a mosquito population by repeated mass
releases of sterilising transgenic males [2]. Two other tech-
niques under development rely on CRISPR-based gene drive,
seeking to spread a genetic trait in a wild population, either to
eliminate the population by spreading sterility [3] or to make
the target mosquitoes incapable of transmitting pathogens [4].
To identify the specific benefits and limitations of the different
GM mosquito-based techniques, a cross-analysis of different
vector control techniques was conducted with respect to possi-
ble objectives, efficacy and sustainability, technical constraints
and risks to health and the environment. Consideration was
given to both existing techniques (chemical, biological, phys-
ical, and environmental) and emerging techniques based on
release of mosquitoes, whether GM (RIDL and the different
gene drive techniques) or non-GM–irradiated (standard sterile
insect technique (SIT)) or carrying Wolbachia1 (incompatible
insect technique (IIT) and spread of pathogen interference (PI)
technique).
As specified by the referral, we considered the mosquito-borne
diseases and vector species present across France, including
overseas territories. The French territories being dispersed
across the world, the most notable mosquito-borne diseases
worldwide were considered, namely dengue, chikungunya,
Zika, yellow fever, West Nile fever, for the viral diseases, and
malaria and lymphatic filariasis for the parasitic diseases. We
focused on the corresponding local vector species: mainly
Aedes aegypti and Aedes albopictus, and species of Anopheles
and Culex.
These vector species have very distinct features, not only
in distribution and vector competence, but also in bio-
ecology (reproduction modes, potential for survival, host
preferences, peaks and sites of aggressiveness, invasive
potential. . .). The vector systems themselves (the triad
mosquito/pathogen/vertebrate host), as well as the diversity of
situations encountered across the territories add another layer
of complexity. This overall complexity must be understood and
taken into account in order to design the most appropriate
vector control strategy.
Cross-analysis of the different vector control techniques has
been conducted in great detail and has made it possible to
identify specific features and relative benefits and limitations
of each of these techniques. Detailed results are developed in
HCB’s opinion (HCB, 2017).
At a more general level, we found:
– no divide between GM and non-GM techniques or between
emerging and existing techniques (Fig. 1);
– shared characteristics within different sets of techniques,
i.e. (i) techniques based on release of mosquitoes, (ii) pop-
ulation reduction techniques2 vs. population modification
techniques3, (iii) self-limiting techniques4 vs self-sustaining
techniques5;
– complementarity of the techniques.
Lastly, we found that the benefits and limitations of these vec-
tor control techniques cannot be treated in a generic manner,
but will depend on the target vector species, the intended
objective, and the broader context (epidemiological, environ-
mental and socio-economic context, including available human
and financial resources).
Key highlights for each of these broad conclusion points are
developed below.
Fig. 1 Possible objectives and sustainability potential of exist-
ing and emerging vector control techniques (Insects Grand
Conference Talk, C. Golstein and P. Boireau, 14 March 2019).
Most exist. tech.: Most existing vector control techniques,
including use of chemical insecticides; SIT: standard Sterile
Insect Technique (mostly based on irradiated mosquitoes);
RIDL: Release of Insects carrying a Dominant Lethal (GM-
mosquito based technique); IIT: Wolbachia-mediated Incom-
patible Insect Technique; GD: Gene Drive techniques, for
population elimination or modification (GM-mosquito based
techniques in this report); Wb-PI: Wolbachia-mediated spread
of pathogen interference; wMel Pop and wMel: two different
strains of Wolbachia.


Do we have to get rid of mosquitoes to eliminate malaria?

Alastair A. Macdonald

Cheek tooth erosion in male babirusa (genus <i>Babyrousa</i>)

Pascale Cossart

Jules Hoffmann

C. R. Biologies 342 (2020) 247–278
Contents lists available at ScienceDirect
Comptes Rendus Biologies
www.sc iencedi rec t .com
Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles
Talk summaries
Résumés des interventions
Session I. Insects as model organisms in
biology
1
How flies contribute to the
discovery of human diseases
and their pathogenic
mechanisms
Hugo Bellin
Howard Hughes Medical Institute, Baylor College of Medicine,
Houston, TX, USA
E-mail address: hbellen@bcm.edu
An area of research that has developed rapidly in the past five
years is the use of Drosophila to facilitate the diagnoses of rare
human diseases. The technical developments in sequencing
human genomes using whole exome (WES) or whole genome
sequencing (WGS) have completely changed the landscape of
human genetics. It is estimated that there are approximately 30
million people in the US and 400 million worldwide with rare
diseases. Many of the patients who have these diseases undergo
a diagnostic odyssey and remain undiagnosed for many years.
By sequencing their genomes and those of their relatives we
can now discover genetic variations in patients that are rare
or ultrarare. However, considering that there are many poly-
morphisms in the population, assessing which variant(s) is/are
related to the observed symptoms has remained a challenge.
This is precisely where model organisms can contribute and
Drosophila is now playing a prominent role in this strategy.
Although there are nearly 4,000 genes annotated in OMIM, the
pace of gene discovery has not shown any evidence of slowing
down in the past few years.
The NIH launched the Undiagnosed Diseases Network (UDN)
four years ago. Its goal is to enroll patients with undiagnosed
diseases and try to determine their causes, which are typically
genetic in origin. The patients who are enrolled are the most
challenging cases in medicine, and 12 clinical sites, a sequenc-
ing center, a metabolomics core and two Model Organisms
Screening Centers (MOSC) are supported to develop diagnoses.
To date, over 3,000 patients have applied and about 30% of the
accepted patients have been diagnosed by combining clinical
phenotyping, WES or WGS of the proband and 2–3 mem-
bers of the family, and performing functional studies in a
model organism. The MOSC Drosophila Core at Baylor College
of Medicine (BCM) has played a prominent role in this ven-
ture and has provided critical data for many human genetic
diseases [1]. The MOSC at BCM has also collaborated with the
Center for Mendelian Genomics to assess variant function using
Drosophila and facilitate the discovery of new human disease-
causing genes.
The first project discussed in this presentation was driven by
WES of a patient and his parents and the discovery of a de novo
point mutation in ACOX 1 (Acyl-CoA oxidase 1). ACOX1 encodes
the rate-limiting enzyme in very-long-chain fatty acid (VLCFA)
 -oxidation, and produces H2O2 in peroxisomes [2]. The
proband was diagnosed at age 11 and now uses a wheelchair
at age 18. Another patient with the same point mutation was
diagnosed at age 9 and is now comatose at age 15. By studying
the function of the ACOX1 gene in flies using strains devel-
oped in my lab, we showed that homozygous loss-of-function
mutations cause lethality and an autoimmune phenotype in
which the animals activate their cellular and humoral immune
responses. A comparison with the vertebrate literature sug-
gests that autoimmunity may also be the main reason infants
with an ACOX1 deficiency die at a very young age, prior to the
age of 5.
We then created flies with the patient’s point mutation and
observed a very different phenotype. Flies eclosed and died
within one or two days but were able to survive, fly, mate,
and live for extended periods of time when kept on food with
a potent antioxidant, N-acetylcysteine. This is consistent with
the fact that ACOX1 produces ROS in peroxisomes and that the
point mutation is a gain-of-function mutation. However, we
were surprised by the potency of the suppression. In addition,
just expressing the variant in Drosophila wrapping glia but not
any other tissue, is sufficient to kill animals, showing that the
toxicity is mainly due to an expression of the mutant protein in
glial cells. Importantly, expressing catalase in glia suppresses
this lethality. We were therefore able to demonstrate that fly
ACOX1 is indeed abundantly expressed and mostly restricted
to wrapping glia.
We then turned to rats and showed that ACOX1 is abun-
dantly expressed in Schwann cells (not in neurons). In addition,
expression of the patient de novo mutation kills cultured
Schwann cells and the antioxidant AD4 fully suppresses cell
1631-0691/
248 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
death. Finally, nerve biopsies of the patient, who suffered
severe axonal loss, showed that surviving Schwann cells are
morphologically (TEM) and functionally aberrant (electrophys-
iology). This prompted the physicians to provide the patient
with high doses of N-acetylcysteine and this new treatment is
associated with a clear improvement in motility.
A second project was driven by a forward mutagenesis screen in
Drosophila in which we previously identified variants in the fly
Ankle2 gene. We discovered that loss-of-function mutations of
the human ortholog of ANKLE2 cause microcephaly in a child
[3]. We then discovered, in collaboration with Nevan Krogan
and Priya Shah, that a Zika virus protein, NS4A, interacts with
and inhibits Ankle2 [4,5]. Our studies in Drosophila combined
with human genetic studies allowed us to uncover a pathway
that implicates several genes associated with primary micro-
cephaly in human.
We identified five additional microcephaly patients with
variants in ANKLE2 and showed that these variants act as
loss-of-function alleles in flies. Our data show that Ankle2 is
an ER-localized protein essential for proper ER and nuclear
envelope structure. Mutations in Ankle2 affect cell division,
spindle alignment, and localization of asymmetric determi-
nants including the proteins of the Par complex. Ankle2
strongly interacts with the nuclear kinase Ballchen, the
homolog of human VRK1, an established microcephaly locus.
Ankle2 mutants fail to maintain Ballchen/VRK1 in the nucleus,
and we propose that this leads to a “gain-of-function” phe-
notype where Ballchen/VRK1 can ectopically interact with
targets that it normally does not interact with. This results in
severely reduced aPKC phosphorylation, which has previously
been shown to have reduced kinase activity. The Ankle2 path-
way also physically and genetically interacts with L(2)gl, an
inhibitor of aPKC activity, which is consistent with the observed
aPKC defects noted in Ankle2 mutants. Finally, we show that
expression of NS4A, which binds to and inhibits the function
of Ankle2, phenocopies Ankle2 mutant defects in neuroblasts,
and these defects can be rescued by modulation of the Ankle2
pathway [3] (Link et al., 2019).
Our work highlights an important pathway required for proper
human brain development: ANKLE2 and VRK1 are both asso-
ciated with microcephaly; a member of the Par complex has
been linked to brain defects in mice; and LLGL1, the homolog of
L(2)gl, maps to the critical region of Smith Magenis Syndrome, a
disease associated with microcephaly. Furthermore, we identi-
fied many novel variants associated with microcephaly in many
of the human homologues of the fly genes described in this
study.
Disclosure of interest The author declares that he has no com-
peting interest.
References
[1] H.J. Bellen, M.F. Wangler, S. Yamamoto, The fruit fly at the
interface of diagnosis and pathogenic mechanisms of rare
and common human disease, Hum. Mol. Genet. [submitted].
[2] H. Chung, M.F. Wangler, P.C. Marcogliese, J. Jo, T.A. Raven-
scroft, S. Sadeghzadeh, et al., Loss of peroxisomalACOX1
induces autoimmunity whereas a de novo gain-of-function
variant induces elevated ROS and Schwann cell loss [in
preparation].
[3] S. Yamamoto, M. Jaiswal, W.L. Charng, T. Gambin, E. Karaca,
G. Mirzaa, et al., A Drosophila genetic resource of mutants to
study mechanisms underlying human genetic diseases, Cell
159 (2014) 200–214 [PMCID: PMC4298142].
[4] P.S. Shah, N. Link, G.M. Jang, P.P. Sharp, T. Zhu, D.L.
Swaney, et al., Comparative flavivirus-host protein inter-
action mapping reveals mechanisms of dengue and Zika
virus pathogenesis, Cell 175 (2018) 1931–1945 [PMCID:
PMC6474419].
[5] N. Link, H.L. Chung, A. Jolly, M. Withers, B. Tepe, B.R.
Arenkiel, et al., ANKLE2, a target of Zika virus, controls asym-
metric cell division of neuroblasts and uncovers a novel
microcephaly pathway, Biorxiv (2019) [611384].
https://doi.org/10.1016/j.crvi.2019.09.002
2
Drosophila research: From the
genome to the proteome
Markus Affolter
Departement Biozentrum, University of Basel, Switzerland
E-mail address: markus.affolter@unibas.ch
Starting from 1900, Drosophila melanogaster has been studied in
the laboratory by scientists interested in many different aspects
of animal development, physiology, and evolution. Over much
of this more than hundred year period, genetic analyses have
been at the basis of most studies, also those who led to the
Nobel prices attributed to scientists working with Drosophila.
More recently, fluorescent proteins and optogenetic tools have
been added to the ever-expanding genetic toolbox allowing for
a better understanding of basic cellular processes underlying
complex developmental processes.
Even more recently, a novel approach is being added to the
toolbox. Small protein binders can be used to directly tar-
get and manipulate proteins in their native environment, in
cells of the living organism. The development of numerous
antibody- and non-antibody-based scaffolds of protein binders
(Fig. 1) has allowed the rapid identification of such small bind-
ing domain, recognizing virtually any target protein of interest.
Such binding molecules can then be functionalized in many dif-
ferent ways, allowing for acute and direct protein manipulation
Fig. 1 A–H: Different protein binder scaffolds that can be used
in developmental biology studies (see [1]).
Fig. 2 Protein binders can be expressed as functionalized pro-
teins in vivo (see [2]).


Insects: Friends, foes, and models

Markus Affolter

<i>Drosophila</i> research: From the genome to the proteome

Marianne Elias

256 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
Fig. 2 The MEKRE93 pathway. A. Expression patterns of
Krüppel homolog 1 (Kr-h1), E93 and Broad complex (BR-C)
in hemimetabolan insects (Blattella germanica). B. Expres-
sion patterns of Kr-h1, E93 and BR-C in holometabolan
insects (Tribolium castaneum). C. The MEKRE93 pathway in
hemimetabolan and holometabolan species. See the text for
additional information and sources.
interactions, and additionally discovered that BR-C and Kr-
h1 are reciprocally activated. In sharp contrast, and as shown
mainly by the group of Riddiford in the decade of 1990, BR-
C triggers the formation of the pupal stage in holometabolan
species, where JH inhibits the expression of BR-C during larval
stages and stimulates BR-C expression after pupal commitment
(Fig. 2B). In 2019, Chafino and co-workers showed that E93
is involved in triggering the pupal stage, as it promotes BR-C
expression in T. castaneum. The whole data indicates that the
MEKRE93 pathway is conserved in the holometabolan species,
which added the E93/BR-C interaction loop to the ancestral
(hemimetabolan) pathway during the evolutionary transition
from hemimetaboly to holometaboly (Fig. 2C).
Disclosure of interest The author declares that he has no com-
peting interest.
References
[1] M. Jindra, X. Belles, T. Shinoda, Molecular basis of juvenile
hormone signaling, Curr. Opin. Insect Sci. 11 (2015) 39–46,
http://dx.doi.org/10.1016/j.cois.2015.08.004.
[2] Q. Ou, K. King-Jones, What goes up must come down:
transcription factors have their say in making ecdysone
pulses, Curr. Top. Dev. Biol. 103 (2013) 35–71, http://dx.
doi.org/10.1016/B978-0-12-385979-2.00002-2.
[3] X. Belles, C.G. Santos, The MEKRE93 (Methoprene tolerant-
Krüppel homolog 1-E93) pathway in the regulation of
insect metamorphosis, and the homology of the pupal
stage, Insect Biochem. Mol. Biol. 52 (2014) 60–68,
http://dx.doi.org/10.1016/j.ibmb.2014.06.009.
https://doi.org/10.1016/j.crvi.2019.09.009
9
Evolution of aposematism and
mimicry in butterflies: Causes,
consequences and paradoxes
Marianne Elias
Institut de systématique, évolution, biodiversité, CNRS, Muséum
national d’histoire naturelle, Sorbonne Université, EPHE,
Université des Antilles, France
E-mail address: marianne.elias@mnhn.fr
Insects represent valuable food for many predators, and as
such they have evolved a large panel of anti-predator adap-
tations. While deceptive adaptations such as camouflage and
masquerade rest on avoiding detection by predators, aposema-
tism relies on advertising chemical defenses with conspicuous
warning signals, such as colorful patterns. Because the effi-
ciency of a warning signal increases with its own local
abundance, multiple aposematic prey exposed to the same
predators benefit from converging on the same warning sig-
nal, a phenomenon originally observed by Henri Bates and
Alfred Wallace and later understood and formalized by the Ger-
man naturalist Fritz Müller [1] and called Müllerian mimicry.
Convergence in warning signal is therefore due to positive
frequency-dependent selection, leading to a ‘strength in num-
bers’ effect. Species sharing the same warning are said to be
co-mimetic and interact mutualistically (i.e. individuals from
either species benefit from the presence of individuals of co-
mimetic species), and form mimicry rings.
Müllerian mimicry exists in a variety of organisms, includ-
ing frogs, wasps, millipedes and beetles, but it has been best
studied in butterflies (Fig. 1). Two neotropical butterfly clades
have attracted considerable attention: the genus Heliconius (43
species) and the tribe Ithomiini (393 species).
Here, I review recent genetic and ecological results on Helico-
nius and Ithomiini butterflies that advance our knowledge on
the proximal and ultimate drivers of mimicry, and on the evo-
lutionary and ecological consequences of mimicry in terms of
speciation, genetic architecture and ecological niche evolution.
I also present recent results that help us understanding two
apparent paradoxes: the embarrassing diversity of mimicry
patterns despite strong selection for convergence, and the evo-
lution of transparent wing patterns in aposematic butterflies,
where conspicuous signals are supposed to be favored.
Fig. 1 A. A common mimicry ring in the Andean foothills. Left
column, from top to bottom: Hypothyris mansuetus (Nymphali-
dae: Ithomiini), Hyposcada anchiala (Nymphalidae: Ithomiini),
Chetone sp. (Erebidae: Arctiinae). Right column, from top
to bottom: Mechanitis messenoides (Nymphalidae: Ithomiini),
Heliconius numata (Nymphalidae: Heliconiini), Melinaea moth-
one (Nymphalidae: Ithomiini). Photo credit: Mathieu Joron.
B. Co-mimetic subspecies of Heliconius melpomene (top) and
H. erato (bottom) in three different regions of their common
range, showing geographic variation in wing colour pattern.
Photo credit: Jim Mallet. C. An illustration of microhabitat seg-
regation of predators and mimicry rings. Illustration credits:
Nicolas Chazot (trees) and Marianne Elias (birds); photo cred-
its: Keith Willmott.
Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 257
Selection on convergent wing colour pattern among mimetic
butterflies is obviously strong, as illustrated by the strik-
ing similarity among distantly related species (Fig. 1A). Such
convergent selection is expected to reduce warning signal
diversity. Yet, diversity in warning signals is pervasive, at sev-
eral geographical scales (Fig. 1B,C). Is this diversity transient,
or is it stable? If so, what maintains it? Convergence in warn-
ing signal is driven by local predation pressure. Therefore,
prey exposed to different communities of predators are not
expected to converge on the same warning signal, as shown
by theoretical models. In practice, geographical subspecies
of mimetic butterflies, which occur in different regions, are
exposed to different suites of predators and often harbour dif-
ferent colour patterns (Fig. 1B). At a much smaller scale, it
has been shown that predators are segregated by microhabitat
locally (for instance, some live in the canopy while other occupy
the understorey), such that distinct mimicry rings can be main-
tained in different microhabitats (Fig. 1C). Therefore, mimicry
diversity at various ecological scales can be maintained due to
predator segregation [2].
Mimicry is also believed to be a driver of speciation. Indeed,
in species harbouring multiple subspecies with distinct colour
patterns (Fig. 1B), hybrids between subspecies typically have a
recombinant, non-mimetic colour pattern, and suffer increased
predation. Colour pattern is also often used as a mating
cue such that mimetic butterflies mate assortatively, a likely
consequence of selection against non-mimetic hybrids (rein-
forcement). Therefore, shifts in mimicry pattern causes both
post- and pre-mating reproductive isolation, and, ultimately,
speciation [2]. Mimicry may therefore be one of the factors
explaining the high diversity of Müllerian mimetic butterflies.
Mimicry raises the question of how convergent phenotypes are
produced in different species. Are the same genes involved?
Comparative analyses of genomic architectures controlling
mimicry patterns in Heliconius reveal that homologous chro-
mosomal regions, the “wing patterning toolkit” control much
of mimicry variations in most species [2]. Some of the
genes involved have now been characterized, and include
the transcription factor optix, the morphogen WntA, the cell-
cycle regulator cortex and the transcription factor Aristaless1.
Mimicry between Heliconius lineages has occurred through
parallel evolution (independent recruitment of the same
genes), except in a few cases where there is evidence for adap-
tive introgression of wing pattern genes [2]. Mimicry can also
incur strong selection on the genetic architecture of genes con-
trolling colour pattern variation, as has been shown in the
species H. numata. This species is unusual in that it is poly-
morphic within populations. Unlike other Heliconius species
that embrace multiple species with distinct colour patterns,
crosses between individuals harbouring different colour pat-
terns that co-occur in H. numata never produce offspring with
intermediate colour pattern. Instead, offspring look like either
of their parents. Recent genetic and behavioural studies have
shown that all variation is controlled at a single locus contain-
ing tightly linked genes (i.e. a supergene), and that different
colour patterns correspond to different supergene haplotypes,
which are characterized by different inversions of chromosome
fragments within the supergene. Therefore, recombination
between morphs is strongly reduced. Moreover, there is a strict
series of dominance among morphs that co-occur. Both mech-
anisms prevent the formation of intermediate colour pattern,
and have likely evolved as a response to selection against indi-
viduals with such intermediate, non-mimetic colour patterns
[2].
Selection incurred by mimicry can also affect multiple eco-
logical dimensions. Indeed, mimicry rings are segregated by
microhabitat and habitat, and theoretical work and phyloge-
netic comparative analyses on Ithomiini butterflies have shown
that the association between mimicry and (micro)habitat is
adaptive, i.e. it is not due to shared ancestry, but most likely to
selection for convergence on both colour pattern and ecological
niche [2]. Moreover, since larval hostplants are also likely seg-
regated ecologically, co-mimetic species tend to use the same
hostplant more often than expected at random. Therefore,
mimicry, a kind of mutualistic interaction, drives convergence
along multiple ecological dimensions, not only colour pattern.
Finally, although the efficiency and memorability of a warning
signal increases with its conspicuousness, the vast majority of
Ithomiini species are transparent to some degrees, although
all of them have conspicuous pattern elements (Fig. 2). Why
has transparency evolved in aposematic butterflies? Bird
vision modelling and detectability and palatability tests with
bird predators have shown that transparent species are less
detectable than opaque species; yet, they are no less unpalat-
able, and in fact they may even be more unpalatable [3].
Transparent species probably make the best of both worlds:
they suffer less attacks from naïve predators because they are
less often detected and, if they are detected by an ‘educated’
predator, they are not attacked because they are recognized
as unpalatable. However, all else being equal, the predator
learning process is expected to take longer with transparent
than with opaque butterflies. Since increased unpalatability
increases predator learning rate, we hypothesize that trans-
parency can only evolve in highly unpalatable lineages, where
it is less costly in terms of predator learning, which is consis-
tent with the observation that all transparent species studied
thus far are highly unpalatable.
In conclusion, Müllerian mimicry is a compelling example
of the power of natural selection, where the evolution of
defences against predators drives the evolution of conspicu-
ous warning signals, which in turn drives convergence in those
signals. Evolutionary implications of mimicry go well beyond
warning signal convergence, since mimicry also affects the evo-
lution of the ecological niche at various scales, and the genetic
architecture of warning signals. The apparent paradox of the
maintenance of mimicry diversity is now well understood, but
the origin of diversity in the first place is still puzzling, since
new warning signal are initially rare and should be selected
against. However complex cognitive strategies of predators,
such as the optimal sampling strategy, may protect rare warn-
ing signals, thereby enabling them to increase in frequency
until they are common enough to be recognized and avoided by
a large number of predators, and may be part of the explanation
of the origin of diversity.
Finally, another apparent paradox, the evolution of transpar-
ent wing colour patterns in aposematic butterflies is also now
understood. Yet, transparent wings, which entail a reduction
in membrane coverage by scales and a reduction in wing pig-
mentation, may incur costs in terms of thermoregulation and
hydrophobicity, which remain to be explored.
Fig. 2 Pagyris cymothoe, a species with transparent wings har-
bouring some conspicuously coloured pattern elements, and
less detectable than opaque relatives. Photo credits: Marianne
Elias.
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.


Evolution of aposematism and mimicry in butterflies: Causes, consequences and paradoxes

Jean-Luc Imler

260 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
Fig. 1 Example of wild flower margin in one of our site. Photo:
Vincent Doublet.
rect ‘contact networks’ among pollinators (via the use of flower
species). Particularly, we found flower diversity to be posi-
tively correlated with the reduction of niche overlap between
insect species. This response of insect pollinators suggest that
wild flower margins with high plant species richness may
reduce insect competition for resources, and potentially reduce
the risk of inter-specific disease transmission by supporting
diverse diet for insects exploiting different flowers.
To test the effect of plant diversity on pathogen dynamics in
bees, we sampled pollinators on these farms and character-
ized their virome by deep transcriptome sequencing. We are
now combining these environmental data to virus discovery in
order to reveal the impact of the agri-environmental scheme on
viral dynamics. Ultimately, we aim to identify environmental
(flower density, agricultural practices) and ecological factors
(plant taxa, insect community assemblage) that significantly
enhance the transmission of plant and pollinator viral diseases
within our model to eventually improve agricultural practises
and wildlife management.
Disclosure of interest The authors declare that they have no
competing interest.
References
[1] M.E. Craft, Infectious disease transmission and contact
networks in wildlife and livestock, Phil. Trans. R. Soc. B. 370
(2015) [20140107].
[2] M.A. Fürst, D.P. McMahon, J.L. Osborne, R.J. Paxton, M.J.F.
Brown, Disease associations between honeybees and bum-
blebees as a threat to wild pollinators, Nature 506 (2014)
364–366.
[3] R. Manley, M. Boots, L. Wilfert, Emerging viral disease risk
to pollinating insects: ecological, evolutionary and anthro-
pogenic factors, J. Appl. Ecol. 52 (2015) 331–340.
https://doi.org/10.1016/j.crvi.2019.09.013
13
Microbial nutrient factories in
insects on extreme diets
Angela E. Douglas
Department of Entomology, Cornell University, Ithaca, NY, USA
E-mail address: aes326@cornell.edu
Insects are renowned for their capacity to specialize on a
wide diversity of diets, many of which are nutrient-poor or
nutritionally unbalanced. For example, various insects feed
through the life cycle on wood, vertebrate blood, plant sap and
other extreme diets that are variously deficient in vitamins,
sterols and essential amino acids. These insects circumvent
the fundamental “rules” of animal nutrition because they
possess symbiotic microorganisms that overproduce the lim-
iting dietary nutrients. Many associations between insects and
microorganisms are evolutionarily ancient and involve the
exquisite coevolution of metabolic function in the insect and
microbial partners, including the restructuring of microbial
metabolism as nutrient factories for the host (Fig. 1). These
insects include major pests and vectors of animal, human and
crop disease agents. Their dependence on specific microor-
ganisms offers novel routes for the control of these globally
important insect pests.
Fig. 1 Metabolic networks in xylem feeding insects.
Disclosure of interest The author declares that she has no
competing interest.
Further reading
N.Y.D. Ankrah, B. Chouaia, A.E. Douglas, The cost of metabolic
interactions in symbioses between insects and bacteria with
reduced genomes. mBio 9 (2018) e01433-18.
N.Y.D. Ankrah, A.E. Douglas, Nutrient factories: metabolic func-
tion of beneficial microorganisms associated with insects.
Environ. Microbiol. 20 (2018) 2002–2011.
A.E. Douglas, The multi-organismal insect: diversity and func-
tion of resident microorganisms, Annu. Rev. Entomol. 60 (2015)
17–34.
https://doi.org/10.1016/j.crvi.2019.09.014
Session IV. Interaction with other organisms
14
The insect reservoir of diversity
for viruses and antiviral
mechanisms
Jean-Luc Imler
Unité “Modèles insectes d’immunité innée” (M3i), Institut de
biologie moléculaire et cellulaire du CNRS, Université de
Strasbourg, France
E-mail address: jl.imler@ibmc-cnrs.unistra.fr
Insects originated more than 400 million years ago and have
undergone since then an extraordinary diversification, asso-
ciated with many spectacular innovations, such as flying or
establishment of social societies. They have colonized all ter-
restrial ecosystems, and are exposed to a broad range of
pathogens, including viruses, bacteria, fungi, and parasites. Like
all animals, insects rely on innate immunity to control infec-
tions. Innate immunity is the first layer in host-defense in
animals. It involves receptors sensing the presence of infec-
tious microorganisms and triggering signaling that leads to the
expression of genes coding effector molecules, which concur to
counter the infection. In vertebrates, a subset of genes induced
encode cytokines and coreceptors that activate a second layer


The insect reservoir of diversity for viruses and antiviral mechanisms

Marylène Poirié

Évolution et spécificité des interactions insectes hôtes–insectes parasitoïdes

Rod J. Dillon

272 Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278
They include techniques based on mosquito release (SIT, IIT, RIDL, gene
drive for elimination) or existing techniques (chemical, biological, phys-
ical and environmental control techniques), only RIDL and gene drive
techniques using GM mosquitoes.
3 Population modification techniques refer to techniques aiming at reduc-
ing vector competence and/or longevity. They include only techniques
based on mosquito release, namely gene drive for population modifica-
tion, using GM mosquitoes, and Wolbachia-mediated spread of PI.
4 Self-limiting techniques refer to vector control techniques with effects
that are limited in space and time unless application of the technique
is maintained. They include most existing vector control techniques (e.g.,
chemical control) as well as the sterile insect technique SIT and the derived
techniques RIDL and IIT.
5 Self-sustaining techniques refer to vector control techniques whose
effects spread across space and last over time without calling for any main-
tenance. They include some existing techniques such as biological control
(to an extent), gene drive techniques and Wolbachia-mediated spread of
PI. More rigorously, there is a continuum of techniques between these two
extremes of self-limiting and self-sustaining.
6 The objective of eradicating a species, which would be a specific feature
of gene drive techniques for elimination, is theoretical at this stage.
https://doi.org/10.1016/j.crvi.2019.09.024
24
A transdisciplinary
consideration of sand flies &
leishmaniasis
Rod J. Dillon
Biomedical and Life Sciences, Faculty of Health and Medicine,
Lancaster University, UK
E-mail address: r.dillon@lancaster.ac.uk
It has been hundred years since Phlebotomine sand flies were
first identified as transmitters of the medically important
parasites called Leishmania. The key players, investigated by
scientists during the first 60 years, were the insect, the par-
asite, and the mammalian host. Forty years ago, plants were
included as potentially influential players in the transmission
process. During the past ten years, we have witnessed a fur-
ther expansion to include bacteria and viruses as influencers
of transmission and the realisation that there is a fascinating
network of microbes interacting with surprising consequences
for the control of the leishmaniases.
This presentation focussed on the recent inclusion of the bac-
terial players in the sand fly–Leishmania drama. It was also a
personal reflection on the urgent need for entomologists and
other biologists to harness their creative endeavours to engage
with policy makers and the public about what insects can teach
us and the huge importance of insects and their microbes in a
human centred world.
Influence of gut microbiota on Leishmania interactions
I am very fond of the writing of US-based insect patholo-
gist, Ed Steinhaus, who wrote the following apt statement in
1960 “A comprehensive understanding of the biology of insects
requires that they be studied in an ecological context with
microorganisms as an important component of the system”.
There is certainly ample opportunity for Phlebotomine sand
flies to interact with elements of the microbial world. Adult
sand flies are plant feeders; the male only feeds on plants and
females require plants as well as blood for egg development.
The Leishmania parasite develops entirely inside the female gut
of the fly and is therefore exposed to the fly gut microbiota.
Hence microbes may be acquired during feeding on plants or
animals as well as being vertically transmitted via the larvae
and pupal stage. During the 1980’s and early 1990’s, the idea
that bacteria may have an important influence on Leishmania
was often met with some incredulity; experts even stated their
belief that the sand fly gut was ‘sterile’. The recognition of the
importance of bacterial interactions with Leishmania and the
sand fly vector finally started to gain some attention post 2010
after a few published studies on the sand fly gut microbiota.
Our work on the gut microbiota of sand flies was the first to
ask the important question: “Does the gut microbiota influence
Leishmania development in sand flies?” We examined the effect
of yeast and bacterial colonisation of the gut on the subsequent
development of Leishmania mexicana population in the gut of
the South American vector Lutzomyia longipalpis. We showed
that certain species of bacteria and yeast, previously isolated
from wild caught sand flies, significantly suppressed the Leish-
mania [1]. This demonstrated the potential for other microbes
already present in the sand fly to interfere with Leishmania
transmission. Kelly et al. [2] questioned whether some gut
microbes might be beneficial to Leishmania survival in the sand
fly. They showed that, although bacterial diversity decreased in
their model of Lu. longipalpis, there was a dominance of Ace-
tobacteraceae associated with an increase of the Leishmania
population. If we think of the sand fly gut as an ecological niche,
the initial occupation of that niche will therefore determine the
potential for Leishmania transmission and the potential of the
sand flies to act as successful vectors.
There are potential costs for the sand fly to harbour Leishmania
and we posed the question: “Does Leishmania infection of the
sand fly gut confer any benefit on the sand fly?” Are there cir-
cumstances under which Leishmania might protect the sand
fly during its occupation of the gut? We found that Leishmania
infected sand flies were able to survive for longer after being
fed with a bacterial insect pathogen compared to control flies
[1].
So, we finally understand that the gut microbiota are important
players in the activity of the sand flies as hosts of Leishmania. A
more recent study extended the influence of the fly microbiota
to include a role in the development of Leishmania in the mam-
malian host. When the female sand fly acquires a blood meal
through a bite, there is a transfer of Leishmania gut bacteria into
the wound [3]. The co-transfer of bacteria seemed to be signifi-
cant as the bacterial antigens primed the host immune system
by triggering the inflammasome, leading to an increase in Leish-
mania dissemination through the body of the mammalian host
[3]. These recent studies served to underline the importance
of the microbial ecology of insect vectors and the need to con-
sider the unseen players in predictive models for determining
transmission of medically important parasites and pathogens
by insects.
In the second part of my presentation I focussed on examples of
creative projects featuring my work with microbes and insects.
The primary role of the bioscience researcher is to discover
more about life around us and to communicate our discoveries
firstly to our science peers but also to the public and decision
makers. However, I suggest that it is now more important than
ever for scientists including entomologists to engage in public
debate on issues that affect the health of the planet and all its
inhabitants, including insects. There are many ways to engage
with the public; clear factual presentations are useful, but the
audience may often be selective and narrow. I am interested
in engaging with audiences using artistic means, less directly,
through emotional engagement, often with playful elements.
Engagement may be through unexpected, novel interventions
or by modifying a ‘known’ commonplace activity. My presen-
tation gave three examples of projects developed through my
experience of working with insect vectors of disease.
My first example was the production of a children’s audio
story called Tropical Tales, done in collaboration with a group
of artists led by Bisakha Sarker, an Indian creative dance per-
former and choreographer. We developed a folk tale–very
loosely based on the story of Jonah and the Whale. In the tale, a
young Indian boy dreams that he was swallowed by a sand fly
where he fought with Leishmania inside a cavernous insect gut.
He then woke up and created a cure for his sisters leishmania-
sis after dreaming about a plant that kills Leishmania. This story
was presented as a series of cartoons (Fig. 1) and the user had
a ‘talking pen’(with which audio can be given in five different
languages) activated by touching each picture.
The second example took place in an art gallery in Liverpool.
Here we took part in a ‘Bed-In’–in celebration of the John
Lennon and Yoko Ono peace protest Bed-In. The intervention
was called ‘Bednets Not Bombs,’ which was meant to be a state-
ment about the funding available for research into tropical
diseases and insect control in comparison to the vast funding
Insects: Friends, foes, and models/Insectes : amis, ennemis et modèles / C. R. Biologies 342 (2020) 247–278 273
Fig. 1 Tropical Tales–children’s audio story about a child find-
ing a cure for leishmaniasis. Photo Copyright Eimear Kavanagh.
Fig. 2 Bed-In event in Liverpool; Bednets not Bombs, protest
about lack of funding for insect vector and bed nets research.
Photo Copyright Rod Dillon.
provided for military activity. My partner Viv Dillon and I spent
the day in bed covered with a mosquito net (Fig. 2). The instal-
lation included a video projected onto the bednet, containing
footage of sand flies and mosquitoes together with fighter air-
craft, overlayed with sounds of warfare, insects, children, and
electrical laboratory equipment.
Fig. 3 Parasiteseeing; The Departure Lounge. An art show
about travels from the perspective of Leishmania. Photo Copy-
right Erika Stevenson.
The final example was an interactive art show called ‘Para-
site-seeing; the Departure Lounge’. Artist Jen Southern and
myself were commissioned by Dundee University LifeSpace
Science Art Research Gallery UK and the Wellcome Centre for
Anti-infectives Research. In this show, we exploited the known
concept of an airport travel lounge and transformed it into a
place where the audience were invited to imagine life from the
perspective of a travelling Leishmania parasite. The interactive
exhibition started with visitors checking in at a check-in desk
with a Leishmania passport that they were instructed to stamp
as they walked through the exhibition (Fig. 3). Final board-
ing took place in a model area of a sand fly gut, with the final
exit being illustrated by a poem about a new anti-leishmanial
drug developed at the Wellcome Centre. The exhibition took
in many facets of research on Leishmania, including historical
aspects with many elements of social media following Leish-
mania travels in the wild and in the lab including a twitter feed
from @ldBOb72 a Leishmania parasite.
Disclosure of interest The authors declare that they have no
competing interest.
References
[1] M.R. Sant’Anna, H. Diaz-Albiter, K. Aguiar-Martins, W.S. Al
Salem, R.R. Cavalcante, V.M. Dillon, et al., Colonisation resis-
tance in the sand fly gut: Leishmania protects Lutzomyia
longipalpis from bacterial infection, Parasites and Vectors
7 (1) (2014) 329.
[2] P.H. Kelly, S.M. Bahr, T.D. Serafim, N.J. Ajami, J.F. Petrosino, C.
Meneses, et al., The gut microbiome of the vector Lutzomyia
longipalpis is essential for survival of Leishmania infantum,
MBio 8 (1) (2017) e01121–e1216.
[3] R. Dey, A.B. Joshi, F. Oliveira, L. Pereira, A.B. Guimarães-
Costa, T.D. Serafim, et al., Gut microbes egested during bites
of infected sand flies augment severity of leishmaniasis via
inflammasome-derived IL-1 , Cell host & microbe 23 (1)
(2018) 134–143.
https://doi.org/10.1016/j.crvi.2019.09.025
25
The trypanosome journey in the
tsetse fly
Philippe Bastin
Trypanosome Cell Biology Unit, Institut Pasteur, Inserm U1201,
Paris, France
E-mail address: pbastin@pasteur.fr
Trypanosoma brucei is a flagellated parasite responsible for
sleeping sickness in central Africa. It is transmitted from one
host to another via the bite of the tsetse fly (Glossina genus),
which is the major mode of contamination. The tsetse fly
(Fig. 1), both male and female, feeds exclusively on blood
and exhibits unique features such as viviparous reproduction
and lactation. It should be considered as a real host for try-
panosomes, since the parasites differentiate and proliferate in
several fly tissues such as the gut, the proventriculus, and the
salivary glands. Trypanosomes adapt to these various envi-
ronments by modifications in their cell surface composition,
metabolism, and morphogenesis. One of the most prominent
characteristics of trypanosomes is the presence of a flagellum
that is attached to the cell body and drives parasite movement,
but also dictates cell morphology. Its length varies according to
the life cycle stage, ranging from 3 to 30  m. This organelle is
essential for parasite survival. Here, we will discuss the differ-
ent aspects of trypanosome development in the tsetse fly, with
focus on flagellum function.
The disease and the parasite Human African Trypanosomiasis
is a disease characterised by two phases, one with rather unspe-
cific symptoms such as bouts of fever, headaches, weakness
or lymphadenopathy, and a second one with severe neuro-
logical symptoms including disruption of the sleeping pattern,
hence the historical name of the disease, sleeping sickness. It is
due to a parasitic protist called Trypanosoma brucei, with only
two subspecies being responsible for human infections: T. b.


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