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
Sánchez-Alcañiz JA, Zappia G, Marion-Poll F and Benton R. A mechanosensory receptor required for food texture detection in Drosophila. Nature Communications (2017) doi:10.1038/ncomms14192
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 (2017) doi.org/10.1016/j.neuron.2016.12.024
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
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
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 - PhD Student
Raquel Alvarez Ocaña 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 joined our group in February 2016, first as a Master student, and before staying on for her PhD, to perform a comparative analysis of olfactory pathways in drosophilids.
|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.
Alexandre Cergneux - Summer student
|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.
|Kaan Mika - PhD 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, before beginning his PhD in the group in Dec 2015.
|Sean McKenzie - Post-doctoral Fellow
Sean obtained his PhD in social evolution and behaviour from the Rockefeller University in 2018. His PhD research in Daniel Kronauer's lab examined genomic adaptations facilitating communication and behavioural coordination in social insects, especially chemosensory genes used in pheromone perception. Sean started a Marie Curie post-doctoral research fellowship at the University of Lausanne in February 2018, working jointly in our lab and in Laurent Keller’s lab in the Department of Ecology and Evolution. His is currently researching the evolutionary development of the insect olfactory system, using various insect models including silkmoths and ants to work on questions that have proven difficult to study in the standard insect model Drosophila melanogaster.
|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.
|Pedro Tan - Summer Undergraduate Research programme student
Pedro is a biomedical undergraduate student from the Federal University of Rio de Janeiro (UFRJ), Brazil. At UFRJ he has worked with mouse models to study the role of replicative stress signalling during retinal development under the supervision of Professor Rodrigo Alves Portela Martins. As a 2018 SUR student in our lab, he is working with Kaan Mika on Drosophila olfactory receptor expression regulation.
|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.
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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. Genetics (2017) doi:10.1534/genetics.116.199281 URL (*equal contribution) (*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. PLOS ONE (2017) 12(4):e0173433 URL (*equal contribution)
Open Labware / 3D Printing
Through her work with TReND in Africa, Lucia Prieto-Godino 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. PLOS Biol (2015) 13(3):e1002086 URL
Maia Chagas A, Prieto-Godino L, Arrenberg AB and Baden T. The 100 € lab: A 3-D printable open source 1 platform for fluorescence microscopy, optogenetics and accurate temperature control during behaviour of zebrafish, Drosophila and C. elegans. bioRXiv (2017) doi.org/10.1101/122812
Some of the 3D printed object designs we use in the research in our group 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)
Rencontre avec Richard Benton (RTS - CQFD)
Im Kopf von Fruchtfliegen - Migros Magazin (auf deutsch)
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 Wire