Richard Benton received his PhD in 2003 from the University of Cambridge, and was an EMBO/Heley Hay Whitney post-doctoral fellow at The Rockefeller University, New York. He joined the Center for Integrative Genomics in September 2007 as Assistant Professor and promoted to Associate Professor in August 2012. His group’s research has been recognised by award of several prizes, including the Eppendorf & Science Prize for Neurobiology (2009), Friedrich Miescher Award (2012), AChemS Young Investigator Award for Research in Olfaction (2012), the National Latsis Prize (2015), and the EMBO Gold Medal (2016). His research has been supported by the Swiss National Science Foundation, ERC Starting and Consolidator Grants, the EMBO Young Investigator Programme and an HFSP Young Investigator Award.
Our group is interested in the genetic, neural and evolutionary basis of sensory perception.
As a model, we investigate the chemosensory systems of the fruit fly, Drosophila melanogaster, which control many sophisticated behaviours, but are numerically simple and experimentally highly accessible. We take a multidisciplinary experimental approach, including bioinformatics, genetics, molecular and cellular biology, electrophysiology, optical imaging, and behavioural analysis.
Several conceptually diverse projects are currently being pursued, including the structural and molecular basis of chemosensory receptor function, the anatomical and physiological properties of chemosensory circuits in the brain, the genetic and ecological basis of chemosensory circuit evolution, and the neural underpinnings of chemosensory-dependent social behaviours.
Google Scholar Profile
Ramdya P, Thandiackal R, Cherney R, Asselborn T, Benton R, Ijspeert AJ and Floreano D. Climbing favors the tripod gait over alternative, faster insect gaits. Nature Communications, in press
Prieto-Godino LL, Rytz R, Cruchet S, Bargeton B, Abuin L, Silbering AF, Ruta V, Dal Peraro M and Benton R. Evolution of acid-sensing olfactory circuits in drosophilids. Neuron, in press
Sánchez-Alcañiz JA, Zappia G, Marion-Poll F and Benton R. A mechanosensory receptor required for food texture detection in Drosophila. Nature Communications, in press
Sutcliffe B*, Ng J, Auer TO, Pasche M, Benton R, Jefferis GSXE and Cachero S*. Second Generation Chemical Tags: Sensitivity, Versatility and Speed. bioRxiv (2016) doi.org/10.1101/095398 (*equal contribution)
Croset V, Schleyer M, Arguello JR, Gerber B and Benton R. A molecular and neuronal basis for amino acid sensing in the Drosophila larva. Scientific Reports (2016) doi:10.1038/srep34871
Uhlmann V*, Ramdya P*, Delgado-Gonzalo R, Benton R and Unser M. FlyLimbTracker: an active contour based approach for leg segment tracking in unmarked, freely behaving Drosophila. bioRxiv (2016) doi.org/10.1101/089714 (*equal contribution)
LeBoeuf AC, Waridel P, Brent CS, Gonçalves AN, Menin L, Ortiz D, Riba-Grognuz O, Koto A, Soares ZG, Privman E, Miska EA, Benton R* and Keller L*. Oral transfer of chemical cues, growth proteins and hormones in social insects. eLIFE (2016) doi.org/10.7554/eLife.20375 (*co-corresponding authors)
Prieto-Godino LL, Rytz R, Bargeton B, Abuin L, Arguello JR, Dal Peraro M and Benton R. Olfactory receptor pseudo-pseudogenes. Nature (2016) 539(7627):93-97
Knecht ZA*, Silbering AF*, Ni L*, Klein M*, Budelli G, Bell R, Abuin L, Ferrer AJ, Samuel ADT**, Benton R** and Garrity PA**. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. eLIFE (2016) doi.org/10.7554/eLife.17879 (*co-first authors; **co-corresponding authors).
Silbering AF, Bell R, Münch D, Cruchet S, Gomez-Diaz C, Laudes T, Galizia CG and Benton R. Ir40a neurons are not DEET detectors. Nature (2016) 534:E5–E7
Gomez-Diaz C, Bargeton B*, Abuin L*, Bukar N, Reina J, Bartoi T, Graf M, Ong H, Ulbrich MH, Masson JF and Benton R. A CD36 ectodomain mediates insect pheromone detection via a putative tunnelling mechanism. Nature Communications (2016) 7:11866 (*equal contribution)
Arguello JR, Cardoso-Moreira M, Grenier JK, Gottipati S, Clark AG and Benton R. Extensive local adaptation within the chemosensory system following Drosophila melanogaster’s global expansion. Nature Communications (2016) 7:11855
Auer, TO and Benton R. Sexual circuitry in Drosophila. Current Opinion in Neurobiology (2016) 38:18-26
Chen C*, Buhl E*, Xu M, Croset V, Rees J, Lilley KS, Benton R, Hodge JJL, Stanewsky R. Drosophila Ionotropic Receptor 25a mediates circadian clock resetting by temperature. Nature (2015) 527(7579):516-520 (*equal contribution)
Maesani A*, Ramdya P*, Cruchet S, Gustafson K, Benton R** and Floreano D**. Fluctuation-driven neural dynamics reproduce Drosophila locomotor patterns. PLOS Computational Biology (2015) 11(11):e1004577 (*equal contribution; **joint senior authors)
Benton R. Multigene family evolution: perspectives from insect chemoreceptors. Trends in Ecology and Evolution (2015) 30(10):590-600
Saina M, Busengdal H, Sinigaglia C, Petrone L, Oliveri P, Rentzsch F and Benton R. A cnidarian homologue of an insect gustatory receptor functions in developmental body patterning. Nature Communications (2015) 6:6243 doi:10.1038/ncomms7243
Hopf TA, Morinaga S, Ihara S, Touhara K, Marks DS and Benton R. Amino acid coevolution reveals three-dimensional structure and functional domains of insect odorant receptors. Nature Communications (2015) 6:6077 doi:10.1038/ncomms7077
Ramdya P, Lichocki P, Cruchet S, Frisch L, Tse W, Floreano D and Benton R. Mechanosensory Interactions Drive Collective Behaviour in Drosophila. Nature (2015) 519(7542):233-6
Gomez-Diaz C, Reina JH, Cambillau C, and Benton R. Ligands for pheromone-sensing neurons are not conformationally-activated odorant binding proteins. PLOS Biology (2013) 11(4):e1001546
LeBoeuf A, Benton R* and Keller L*. The molecular basis of social behavior: models, methods and advances. Current Opinion in Neurobiology (2013) 23(1):3-10 (*co-corresponding authors)
Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GSXE and Benton R. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature (2011) 478(7368), 236-40
Silbering AF*, Rytz R*, Grosjean Y*, Abuin L, Ramdya P, Jefferis GSXE and Benton R. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. The Journal of Neuroscience (2011) 31(38):13357-13375 (*equal contribution)
Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S and Benton R. Functional architecture of olfactory ionotropic glutamate receptors. Neuron (2011) 69, 44-60
Ai M, Min S, Grosjean Y, Leblanc C, Bell R, Benton R, Suh, GSB. Acid sensing by the Drosophila olfactory system. Nature (2010) 468, 691-695
Croset V*, Rytz R*, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ and Benton R. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLOS Genetics (2010) 6(8): e1001064 (*equal contribution)
Ramdya P, Benton R. Evolving olfactory systems on the fly. Trends in Genetics (2010), 26(7):307-16
Benton R. Evolution and revolution in odor detection. Science (2009) 326, 382-383
Benton R, Vannice KS, Gomez-Diaz C and Vosshall LB. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell (2009) 136(1):149-162
Structure, function, and evolution of chemosensory receptors
We have a longstanding interest in the molecular basis of odour detection by the Ionotropic Receptor (IR) family of chemosensory receptors, which have derived from the ancestral ionotropic glutamate receptor family of ligand-gated ion channels. Through comprehensive comparative bioinformatic analyses of IR repertoires in animal genomes, we have studied the evolutionary origin, expansion and diversification of this family of chemosensory receptors, and how this relates to individual species’ chemosensory ecology. Using electrophysiological and cell biological approaches in vivo and heterologous cells, we have studied IR complex formation and stoichiometry, and their trafficking, ion conduction and ligand-recognition properties. Our results provide insights into the conserved and distinct architecture of these chemosensory receptors and their synaptic ancestors. In current work, we collaborate with structural biologists Rongsheng Jin and Chun Tang to visualise the three-dimensional organisation and dynamics of the apo and odour-bound IR ligand-binding domain by X-ray crystallography and Nuclear Magnetic Resonance to understand the molecular basis and evolution of their odour recognition properties.
Pheromone signal transduction
Pheromones form one of the major sensory mechanisms by which animals communicate with members of their own species. These signals are often chemically distinct from other environmental chemical cues, because they derive from internal metabolic pathways, such as those for lipids or peptides. Consistently, the molecular machinery that detects pheromones also appears to be highly specialised. In previous work, we and others have characterised a set of proteins, including the olfactory receptor OR67d, the CD36-related transmembrane protein SNMP, and the extracellular Odorant Binding Protein, LUSH, which are each required for detection of the fatty acid-derived Drosophila sex pheromone cis -vaccenyl acetate (cVA). We are investigating the role of these proteins in mediating the sensitive and specific neuronal responses to cVA through in vivo structure-function and biochemical analysis.
Chemical biosensor development
Harnessing our knowledge of chemosensory receptors, we are involved in developing novel types of chemical biosensors as part of the Nano-tera Envirobot project. Our aim is to integrate known chemosensory receptors or custom-designed receptors of desired specificity into a chemosensing robot to enable remote and real time tracking of environmental pollutants.
Neuroanatomy and physiological functions of chemosensory circuits
We have completed a comprehensive neuroanatomical and physiological analysis of the IR olfactory circuits, in which we have identified odour ligands and central circuit organization for the vast majority of IR olfactory pathways. By comparing our findings with the properties of the circuits expressing Odorant Receptors (ORs), we can begin to explain how and why two complementary olfactory subsystems have evolved in insects. Recently, we have shown that a large number of IRs are selectively expressed in small subpopulations of neurons in peripheral and internal gustatory neurons, suggesting roles for these receptors in taste detection and internal food assessment. We are currently defining the ligands detected by these sensory pathways, identifying their higher order circuit elements and exploring the taste-evoked behaviours they underlie.
Olfactory circuit evolution
Much of our current work focuses on obtaining mechanistic explanations for how novel olfactory pathways evolve, through two main approaches. First, we are performing comparative transcriptomics analyses of olfactory subsystems, as well as of individual olfactory pathways within these subsystems, to identify and characterise loci that have driven the developmental and functional diversification of these sensory circuits. Second, we are expanding our efforts to genetic, physiological and behavioural analysis of drosophilid species that have distinct chemosensory preferences to D. melanogaster, to identify the genetic basis of their ecologically-important olfactory adaptations. Together these studies will provide general insights into the mechanisms of, and constraints on, brain evolution. Moreover, we anticipate that understanding how brains have been finely sculpted through random mutation and natural selection in the past may enable future directed manipulation of the connectivity and activity of neural circuits.
Chemosensory and social behaviours in flies and ants
We have used simple chemosensory preference assays to define the innate behaviours mediated by a number of olfactory and gustatory pathways. We have also examined the role of chemosensory signals in controlling sexual behaviours. Current efforts are directed towards development of novel behavioural assays in which we can precisely control the temporal pattern of odour stimuli, and video-track single or groups of flies in a high-throughput manner, together with the group of Dario Floreano (EPFL). These technical advances are allowing us to describe previously unobservable individual and group behaviours. Finally, in a new research direction, we are collaborating with Laurent Keller (DEE-UNIL) to study how chemical communication can control social organisation in a social insect, the carpenter ant Camponotus floridanus.
Liliane Abuin - Technician
Liliane obtained her Diplôme de Technicienne en Analyses Biomédicales from the Ecole Cantonale Vaudoise de Laborantins et Laborantines Médicaux. During 1996-2007 she worked in the group of Susanna Cotecchia in the Department of Pharmacology and Toxicology at the University of Lausanne.
Raquel Alvarez Ocana - Masters Student
Raquel obtained her Bachelors in Biology from the Autonomous University of Madrid in 2015. During her degree, she worked in Isabel Correas’s laboratory on biochemical and functional characterization of 4.1/Coracle protein in Drosophila, and in Ana Busturia’s laboratory investigating MDM2 expression and p53-dependent apoptotic factors in Drosophila melanogaster cells. In September 2015 she started her Masters in Medical Biology at UNIL, working in Angela Ciuffi’s group for her First Steps Project on the resurrection of a zebrafish endogenous retrovirus. She will join our lab in February 2016 for her Masters project, to perform a comparative analysis of olfactory pathways in drosophilid species, under the supervision of Thomas Auer and Roman Arguello.
J. Roman Arguello - Post-doctoral Fellow
Roman obtained his PhD in evolutionary genetics from the University of Chicago (Committee on Evolutionary Biology) in 2008, while working with Prof. Manyuan Long's Group. His research focused on the molecular evolution and population genetics of gene families (including chemoreceptor families) and the rarely recombining fourth chromosome in the D. melanogaster subgroup. Following his PhD, he carried out a post doc with Prof. Andrew Clark's Group at Cornell where he was involved in generating and analyzing population genomic data sets designed to investigate the forces leading to genetic and phenotypic divergence between geographically diverse D. melanogaster populations. Roman joined the lab in Jan 2013 with the aim of bridging his evolutionary genomics background with functional studies of Drosophila taste evolution. His initial interests are in the role that taste receptor duplication events play in altering sensory neural networks between species, and in the evolution of oviposition preference, supported by a Novartis Foundation grant. See his personal workpage for more information.
Jan Armida - PhD Student
Jan obtained his Bachelors in Biology from the University of Lausanne in 2011. He worked in the lab during Oct-Dec 2011 for his First Steps project as part of his Masters in Medical Biology, under the supervision of Carol Gomez-Diaz, before joining Nicolas Toni's group at the Department of Fundamental Neuroscience for his Master's Thesis. He returned to our lab in June 2013 to begin his PhD research.
Thomas Auer - Post-doctoral Fellow
Thomas obtained his Bachelor and Master degrees from the Ruprecht-Karls-University Heidelberg where he was working on cis-regulation in the teleost fish Medaka in the lab of Joachim Wittbrodt. After a short research stay in Okazaki, Japan he started his PhD as a joint project between the labs of Joachim Wittbrodt and Filippo Del Bene at the Institut Curie in Paris. There he was developing genome editing tools in zebrafish and studied the role of axonal transport in visual system development. He joined our lab in April 2015 to work on the genetic basis of olfactory circuit evolution, supported by an HFSP Long-Term Fellowship.
Benoîte Bargeton - Post-doctoral Fellow
Benoîte obtained her Masters in Biology at the Pierre and Marie Curie University (Paris VI, FR). During her PhD thesis in Stephan Kellenberger's lab at the Department of Pharmacology and Toxicology at UNIL she studied a mammalian neural sodium channel, and began a collaboration with our lab to study Ionotropic Receptor function in Xenopus oocytes. She continued this work in our group during Sep 2010-Feb 2011, before joining Francisco Bezanilla's lab at the University of Chicago. She return to the lab to work on our HFSP project on IR ligand recognition in Sep 2012.
Phing Chian Chai - Post-doctoral Fellow
Phing Chian obtained his BSc from the National University of Singapore, where he studied the role of free radicals and proteasomal functions in biological systems under the supervision of Barry Halliwell. He then joined William Chia's lab in Temasek Life Sciences Laboratory (Singapore) for his PhD. During his PhD, he was co-supervised by Yu Cai to study the actions of Hedgehog and Notch pathways in the development of the Drosophila central nervous system. He joined our group in April 2014 to pursue his research interest in the evolution of neural circuits for olfactory perception from a developmental perspective.
|Iris Marouani - Administrative Assistant|
Steeve Cruchet - Technician
Steeve obtained his Diploma of Technician in Biomedical Analysis from the Ecole Cantonale Vaudoise de Laborantins et Laborantines Médicaux. From 2007 to 2010 he worked in the group of Thierry Pedrazzini in the Unity of Experimental Cardiology at the University Hospital of Lausanne. He joined the lab in March 2011.
Adria Le Boeuf - Post-doctoral Fellow
Adria obtained her B.A. from the University of California, Santa Barbara where she studied the contributions of microtubule dynamics to neurodegenerative disease. For her PhD work in Jim Hudspeth's lab of Sensory Neuroscience at the Rockefeller University, she studied the biophysical and mechanical contributions of electrostatics to the mechanosensory organelles of the inner ear, and was granted a National Research Service Award from the NIDCD, receiving her PhD in 2011. Since June 2011, she is pursuing her post-doctoral research jointly in our lab and that of Laurent Keller in the Department of Ecology and Evolution on ant chemosensory genetics and behavior. Outside the lab, Adria is Artistic Director of The Catalyst, a Science-Theater Collective.
Laura Lucia Prieto Godino - Post-doctoral Fellow
Lucia obtained her B.A. from the Universidad Autonoma de Madrid, where she did her research thesis on olfactory processing in flies in the lab of Gonzalo Garcia de Polavieja. After a summer working on vision evolution in box jellyfish in the lab of Dan Nilsson at Lund University, she joined Michael Bate's group at the University of Cambridge for her PhD. During her PhD she studied the embryonic development of the Drosophila olfactory system, receiving her PhD in 2011. She was awarded a FEBS long-term post-doctoral fellowship to study the genetic basis of olfactory pathway evolution in Drosophila in our lab. She joined the lab in March 2012. Outside the lab, Lucia founded and runs TReND (Teaching and Research in Natural Sciences for Development) in Africa.
Kaan Mika - Visiting Student
Kaan obtained his Bachelors in Molecular Biology and Genetics from Istanbul Technical University in 2012, where he studied the effect of Nuclear Factor 1 family transcription factors on hind brain development under the supervision of Aslı Kumbasar. During his degree, he studied two semesters at Roskilde University where he worked on two independent projects under the supervision of Kim Furbo Rewitz and Birgit Koch, respectively. He then obtained his Masters in Molecular Biology and Genetics from Boğaziçi University in 2014 working in the laboratory of Arzu Çelik, where he focused on the development of the Drosophila olfactory system. He joined our lab as a visiting student in Jan 2015, working with Lucia Prieto.
Juan Antonio Sánchez Alcañiz - Post-doctoral Fellow
Juan obtained his MS in Biochemistry from the University Miguel Hernández of Elche (Spain). He obtained his PhD in 2010 in the lab of Prof. Óscar Marín at the Institute of Neurosciences of Alicante (Spain), studying the intracortical migration of GABAergic interneurons in the mouse neocortex. He joined the lab in August 2012 to study gustatory circuitry in Drosophila, funded by EMBO, FEBS and HFSP Long Term Fellowships.
Marta Scalzotto - PhD Student
Marta obtained her Masters degree from the University of Padova, Italy, in 2014, performing her thesis research at the University of Leicester, UK, as an Erasmus student. There she worked with Ezio Rosato and Flaviano Giorgini to characterise the activity of a light-switchable transgene system in Drosophila. She joined our lab in September 2014.
Ana Florencia Silbering - Post-doctoral Fellow
Ana obtained her Masters in Biology at the University of Buenos Aires. During her PhD thesis in Giovanni Galizia's lab she studied odour coding in the olfactory system of Drosophila. She received her PhD in 2007 from the Free University of Berlin. She joined the lab in September 2008 and will focus on the characterisation of neural circuits underlying olfactory behaviour.
Giovanna Zappia - Technician
Giovanna obtained her MS in Pharmaceutical Biotechnology from the University of Milan, Italy, where she studied the role of ADAM10, a metalloprotease involved in the physiological functioning, brain development and pathogenesis of Alzheimer's disease. In 2010 she joined the Andrea Volterra's Lab in the Department of Fundamental Neuroscience at UNIL where she investigated the role of TNFα on the astrocytes in pathological conditions, particularly in experimental autoimmune encephalomyelitis (EAE), a mouse model of Multiple Sclerosis. She joined our group in Oct 2013.
The Benton lab is active in developing, optimising and documenting a number of diverse experimental methods we (and others) use in our research. Please see below for links to published articles.
Hopf TA, Morinaga S, Ihara S, Touhara K, Marks DS and Benton R. Amino acid coevolution reveals three-dimensional structure and functional domains of insect odorant receptors. Nature Communications (2015) 6:6077 doi: 10.1038/ncomms7077 URL
We have collaborated with Debbie Marks' lab at Harvard to generate the first de novo three-dimensional models of insect Odorant Receptors using EVfold-Transmembrane. You can find all the resources for this method on the EVfold webpage. The accuracy of these models can be improved by increasing the number of ORs in the sequence alignments (currently just under 6000), so we would be happy to incorporate any OR sequence resources being generated by the community (please contact Richard Benton).
Saina M and Benton R. Visualizing olfactory receptor expression and localization in Drosophila. in Methods in Molecular Biology (2013) Vol. 1003 URL
Greg Jefferis' lab at the MRC-LMB has developed powerful tools for chemical-tag based in situ labelling; we've shown that these work well also in peripheral appendages:
Sutcliffe B*, Ng J, Auer TO, Pasche M, Benton R, Jefferis GSXE and Cachero S*. Second Generation Chemical Tags: Sensitivity, Versatility and Speed. bioRxiv doi.org/10.1101/095398 URL (*equal contribution)
Benton R and Dahanukar A. Electrophysiological recording from Drosophila olfactory sensilla. Cold Spring Harbor Protocols (2011) doi: 10.1101/pdb.prot5630 URL
Benton R and Dahanukar A. Electrophysiological recording from Drosophila taste sensilla. Cold Spring Harbor Protocols (2011) doi: 10.1101/pdb.prot5631 URL
Benton R and Dahanukar A. Chemosensory coding in single sensilla. Cold Spring Harbor Laboratory Press - Drosophila Neurobiology: A Laboratory Manual (2010) URL
Silbering AF, Bell R, Galizia CG and Benton R. Calcium imaging in the Drosophila antennal lobe. Journal of Visualized Experiments (2012), 10.3791/2976 URL
Ramdya P, Schaffter T, Floreano D and Benton R. Fluorescence Behavioral Imaging (FBI) tracks identity in heterogeneous groups of Drosophila. PLOS ONE (2012) 7(11):e48381 URL
See also this resource page for FBI
Uhlmann V*, Ramdya P*, Delgado-Gonzalo R, Benton R and Unser M. FlyLimbTracker: an active contour based approach for leg segment tracking in unmarked, freely behaving Drosophila. bioRXiv (2016) doi.org/10.1101/089714 (*equal contribution)
Open Labware / 3D Printing
Through her work with TReND in Africa, Lucia Prieto-Godino in our group has been involved in development of 3D design and printing for labs:
Baden T, Chagas AM, Gage G, Marzullo T, Prieto-Godino LL, Euler T. Open Labware: 3-D printing your own lab equipment. PLoS Biol. 2015 Mar 20;13(3):e1002086. doi: 10.1371/journal.pbio.1002086. eCollection 2015 Mar URL
Some of the 3D printed object designs we use in our research are available through Thingiverse
Quelques articles/emissions sur notre recherche - Some articles/broadcasts about our research
Understanding the fruit fly's nose (SNF/Latsis) (en anglais, sous-titré en français)
Une mouche alliée de la science (RTS - CQFD)
What fruit flies can teach us about the science of smell (Podcast at swissinfo.ch)
Sa majesté des mouches (Le Temps)
The wisdom of the fly crowds (Ed Yong/National Geographic)
The world's first true aphrodisiac (NBC News)
An ant’s kiss may hide a sneaky form of communication - a comment in Science on our paper on trophallaxis and chemical communication in social insects; see also the Daily Mail and Wired
Visitez notre labo! - Visit our lab!
Si notre sujet de recherche vous intéresse, venez nous rendre visite pendant les journées portes ouvertes: Les Mystères de l'UNIL, le 30-31 mai 2015!
Visites de labos B2: Drosophile, du labo au champ… et le retour
If our research topic is of interest, come and visit us during the UNIL Open Doors Days: Les Mystères de l'UNIL on 30-31 May 2015!
Lab visit B2: Drosophila, from the lab to the field ... and back