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 2012 and Full Professor in 2018. 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, Consolidator and Advanced 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.
Prieto-Godino LL*, Silbering AF*, Khallaf MA**, Cruchet S**, Bojkowska K, Pradervand S, Hansson BS, Knaden M and Benton R. Functional integration of “undead” neurons in the olfactory system. bioRxiv (2019) doi: 10.1101/623488 (*equal contribution; **equal contribution)
Auer TO, Khallaf MA, Silbering AF, Zappia G, Ellis K, Hansson BS, Jefferis GSXE, Caron S, Knaden M, and Benton R. The making of an olfactory specialist. bioRxiv (2019) doi: 10.1101/546507
Chai PC, Cruchet S, Wigger L and Benton R. Sensory neuron lineage mapping and manipulation in the Drosophila olfactory system. Nature Communications (2019) 10:64
Sánchez-Alcañiz JA, Silbering AF*, Croset V*, Zappia G*, Sivasubramaniam AK, Abuin L, Sahai SY, Münch D, Steck K, Auer TO, Cruchet S, Neagu-Maier GL, Sprecher SG, Ribeiro C, Yapici N and Benton R. An expression atlas of variant ionotropic glutamate receptors identifies a molecular basis of carbonation sensing. Nature Communications (2018) 9:4252
Sánchez-Alcañiz JA, Zappia G, Marion-Poll F and Benton R. A mechanosensory receptor required for food texture detection in Drosophila. Nature Communications (2017) 8:14192
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) 93(3):661-67
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
We 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 experimentally highly accessible. Below we highlight some of our recent discoveries and on-going projects.
Evolutionary origin of insect chemosensory receptors
We have used comparative genomics to explore the origin of the insect chemosensory receptor superfamily, comprising the Odorant Receptors (ORs) and Gustatory Receptors (GRs). Although originally thought to be insect-specific genes, we identified distant relatives (“GR-like” (GRL) genes) in diverse animals, including non-Bilateria, as well as in plants. These findings indicate a very early origin of this gene family. Interestingly, expression and functional studies of GRLs in the sea anemone and sea urchin suggest that GRLs play developmental functions, arguing that the ancestral role of these proteins may not have been in chemosensation.
Chemosensory receptor population genetics
We have investigated the evolutionary forces affecting patterns of genetic variation over short-time scales within chemosensory gene repertoires (including OR, GRs and the Ionotropic Receptors (IRs)), using genome-wide data from geographically diverse populations. By couching population genomic analyses of these families within parallel analyses of other large gene families, we have demonstrated that chemosensory proteins are not outliers for adaptive divergence (between closely-related drosophilids), contrary to widespread belief that they are unusually rapidly evolving. However, chemosensory families often display the strongest genome-wide signals of recent selection within D. melanogaster, as genetic “first responders” to new ecological niches.
Olfactory receptor “pseudo-pseudogenes”
In the course of our analysis of the molecular evolution of IRs across drosophilids, we made an unexpected discovery: the functionality of a presumed pseudogenised receptor locus. This gene, Drosophila sechellia IR75a, bears a premature termination codon (PTC) that appears to be fixed in the population, but encodes a functional receptor due to efficient translational readthrough of the PTC. We identified several other examples of functional PTC-containing genes, suggesting that such “pseudo-pseudogenes” represent a widespread phenomenon that might include non-olfactory loci.
Pheromone signal transduction
Pheromones form one of the main mechanisms by which animals communicate with conspecifics, but how such signals are detected with specificity and sensitivity remains unclear. An important in vivo paradigm for this process is the detection mechanism of the sex pheromone cis-vaccenyl acetate (cVA), which involves a CD36-related transmembrane protein SNMP1, and the receptor OR67d. Through in vivo structure/function analysis of SNMP1, combined with protein homology modelling, and pheromone binding assays, we have provided evidence that SNMP1 forms a tunnel that “funnels” pheromone molecules from the extracellular fluid into the ligand-binding pocket of OR67d in the sensory membranes.
Expanding functions of IRs in gustation, hygrosensation and thermosensation
Through our own and collaborative work, we have continued to characterise the functions, circuits and behaviours mediated by members of the IR family. Though first identified for their role as olfactory receptors, we have shown that the IR family contributes to a remarkable range of sensory modalities, include taste recognition of amino acids, detection of humidity gradients, cool sensing and temperature-entrainment of the circadian clock. Future work is aimed at determining the molecular mechanism by which members of this protein family can respond to such diverse sensory stimuli.
Mechanosensory basis of collective behaviour
During establishment of high-resolution behavioural assays, we discovered a previously unobserved collective behavioural phenomenon in Drosophila, in which group density has a strong influence upon an individual’s response to odours. We showed that this collective behaviour depends upon specific mechanosensory neurons and receptors, which mediate fly-fly encounter-induced locomotion. These findings highlight the importance of social context in the sensory responses of a solitary species, and pave the way to a neural circuit-level understanding of collective behaviour in animal groups.
Chemical communication by trophallaxis in ants
Beyond our Drosophila studies we have investigated a novel type of chemical communication in a social insect, the Florida carpenter ant. Like other eusocial insects, these ants engage in trophallaxis, a behaviour that permits mouth-to-mouth liquid transfer between members of a colony, which is widely considered to be a simple food-sharing mechanism between adults and from adults to larvae. Through analysis of the protein, RNA and small molecule contents of trophallaxis fluid, we have identified a number of endogenous ant proteins implicated in regulation of juvenile hormone (JH) levels, as well as JH itself. By providing to colonies food supplemented with JH, we found that trophallaxis-mediated “external” hormone supplements can influence brood development. This work raises the possibility that trophallaxis underlies a novel mechanism of inter-individual communication in social insects controlling colony-level phenotypes.
Evolution of olfaction
Much of our on-going work aims to define the genetic basis of neural circuit and behavioural evolution. Towards this goal, we compare the olfactory pathways of closely related but ecologically distinct drosophilids, in particular D. simulans and D. sechellia. Like D. melanogaster, D. simulans is distributed worldwide and attracted to diverse fermenting vegetal substrates. By contrast, D. sechellia is endemic to the Seychelles archipelago, and is an ecological “specialist” that is attracted to, and feeds and breeds exclusively on the acid-rich fruit of Morinda citrifolia. We have identified changes in the odour-recognition properties and expression of acid-sensing receptors in D. sechellia and are currently defining the molecular basis of these differences. We are also visualising the neural pathways in which these receptors are expressed, to identify modifications in circuit organisation; subsequently we will use quantitative trait locus mapping to locate the genes responsible for adaptations in circuit development. Finally, we have applied genome-editing technologies to D. sechellia and D. simulans to test the contribution of these olfactory pathways and their species-specific structural and functional properties to the distinct host preferences of these drosophilids.
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. She has worked in the lab since October 2007.
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.
|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.
Jérôme Mermet - Post-doctoral Fellow
Jérôme obtained his Bachelor and Master degrees from University of Toulouse in France where he studied epigenetic regulation of gene expression in breast cancer cells in the lab of Kerstin Bystricky. He then joined the lab of Félix Naef at the EPFL, Switzerland, to study the dynamics of the three-dimensional organisation of chromatin across the circadian cycle and its function for circadian-clock gene transcription in mouse tissues. He joined our lab in April 2019 to investigate molecular mechanisms modulating olfactory circuit architecture during development in Drosophila.
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.
Hayden Schmidt - Post-doctoral Fellow
Hayden received his Bachelor’s degree from Whittier College in 2014, where he worked with Dr. Erica Fradinger studying the effects of organophosphate pesticides on zebrafish development. He also assessed use of zebrafish as a model for testing chemical antidotes for organophosphate poisoning, in collaboration with Drs. Palmer Taylor and Zoran Radić at the University of California San Diego. Afterwards, he started his PhD at Harvard University where he joined the laboratory of Dr Andrew Kruse. There, Hayden studied the structural pharmacology and biochemistry of σ1 and σ2 receptors, a pair of enigmatic membrane proteins that are notable for their broad pharmacological profiles and promise as drug targets for several conditions. He will join our lab in June 2019 to work on the structural pharmacology of insect chemoreceptors, with the hope of applying the principles of structure-based drug design to characterise receptor-ligand interactions and develop novel, environmentally sustainable forms of agricultural pest control.
Suguru Takagi - Post-doctoral Fellow
Suguru obtained his BEng from the Department of Applied Physics, University of Tokyo, where he studied the properties of shot noise in interferometry using power modulated laser beam. He then obtained his MS and PhD from the Department of Physics, the University of Tokyo, where he studied the circuit mechanisms and their molecular underpinnings of action selection in Drosophila melanogaster larvae, in collaboration with investigators in HHMI Janelia Research Campus and RIKEN BSI. He will join the lab in September 2019 to carry out cross-species comparisons of central olfactory circuits in drosophilids.
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 3D-printable open-source platform for fluorescence microscopy, optogenetics, and accurate temperature control during behaviour of zebrafish, Drosophila, and Caenorhabditis elegans. PLOS Biol (2017) 15(7):e2002702 URL
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