My research focuses on speciation, a fundamental evolutionary and biological process responsible for the generation of novel forms and for the maintenance of biodiversity. My objective is to gain insights into the mechanisms of speciation and more specifically to understand the role of selection in the formation of new species (adaptive speciation). I use a comparative and integrative approach to address these interests by combining phenotypic and genomic analyses of divergence and traits involved in reproductive isolation. So far, I have been mainly focusing on mechanisms of divergence-with-gene-flow (in sympatry or secondary contact zones) to understand how reproductive isolation and non random mating build up in the face of homogenising gene flow. I pay a particular attention on the evolution of chemosensory traits responsible for the occurrence of premating isolation, the ultimate step of most speciation events. For the past few years, I have been dedicating most of my effort to the exploration of the genomics of speciation to describe and understand the pattern and dynamics of genomic differentiation as speciation unfolds. I take advantage of the recent development of Next-Generation Sequencing technologies to address genomic differentiation at very large scale (genome-wide, transcriptome-wide or large candidate gene families).
Selection, divergence-with-gene-flow and speciation
The evolution of reproductive isolation between two taxa, up to complete genome differentiation, relies on the evolution of associations among traits acting as barriers to gene flow. In allopatry, these associations automatically build up as a consequence of geographic isolation, but when gene flow occurs between the diverging taxa, the evolution and maintenance of trait associations is much more of a challenge, as gene flow tends to break down these associations. Under this scenario of gene flow, selection is often necessary for the build up of associations, and we therefore talk about adaptive speciation. I study populations experiencing gene flow under different geographical settings (hybrid zones (house mice); sympatric populations (pea aphids, Howea palms)) and try to understand how selective processes (natural and sexual selection) can facilitate divergence-with-gene-flow (see the review article Smadja & Butlin 2011). So far, my work on various systems has led me to address mechanisms of reinforcement in contact zones between diverging subspecies and ecological speciation between sympatric host races or incipient species, cases where selection against hybridisation and divergent ecological selection are the driving forces of speciation.
Inferring the role of selection in shaping divergence and promoting isolation is not straightforward and I use the combination of phenotypic, genetic, and theoretical analyses to address this question. For example, I am developing comparative analyses in natural populations to test for the role of selection in generating divergence by comparing populations occurring in different selective environments. Another approach is to assess the genetic basis of divergence and the genetic architecture of diverging genomes in order to test for the signature of selection in genes involved in reproductive isolation. In this context, I am interested in population genomics methods aiming at identifying loci under divergent selection, explored at the level of large candidate multigene families or whole genomes / transcriptomes.
Non-random mating and Chemosensory speciation
During a process of speciation, the evolution of prezygotic isolation (or non-random mating) is a key step as it is considered as the ultimate barrier to gene flow which prevents fertilisation between diverging taxa. Prezygotic barriers can evolve under direct selection (magic traits) or can evolve as a consequence of their association with postzygotic components of isolation (indirect selection). In my research, I have been paying particular attention to understanding how prezygotic barriers evolve especially in the face of gene flow and their coupling with other reproductive barriers. I have primarily been focusing on the evolution of behavioural traits responsible for the occurrence of premating isolation between populations among which mate choice (sexual isolation) and habitat choice (ecological isolation), although I also take part in a study addressing the evolution of flowering time shift in Howea palm trees (temporal isolation). My objectives are to test for a role of selection in shaping behavioural divergence and to identify the factors favouring the rapid evolution of non random mating (strength and modes of selection; cultural transmission; epigenetics; imprinting).
For the past few years, I have been particularly focusing my attention on organisms using chemical cues to choose their mates and their breeding habitat, analysing how the evolution of chemically-based behaviours and chemical signals play a role in speciation (see the review article Smadja & Butlin 2009 on “chemosensory speciation”). At the molecular level, the diversity and variability of chemoreceptors makes chemosensory systems prone to adaptive evolution. In the context of speciation with gene flow, where selection is key to the evolution of reproductive barriers, gaining insights into the evolution of chemosensory repertoires among taxa can tell us a great deal about the mechanisms underlying the origins of species. I explore the role of olfactory and gustatory receptors in speciation both in insects and mammals, using large scale genomics approaches to explore divergence at these large multigene families.
I combine behavioural ecology, chemical ecology and genomics to study barrier traits involved in prezygotic isolation and tackle the proximal and causal mechanisms shaping their evolution.
Genomics of speciation
New insights into the genetic basis of speciation can help to better understand the genetic architecture and the type genetic changes underlying reproductive barriers (protein, regulatory or structural changes), the origin of genetic variation (standing variation or novel mutation), but also the impact of selection on the genomes and the dynamics of genomic differentiation during speciation. Although these questions can and have been traditionally addressed using quantitative genetics methods, I mainly use population genomics and large scale candidate gene approaches to explore genomic differentiation and speciation genes. The recent availability of Next-Generation sequencing technologies provides a unique opportunity to address the genomics of speciation at very large scale.
I am particularly interested in understanding how genomic differentiation builds up as speciation unfolds, i.e. how islands of genomic divergence get formed and extend across the entire genome. In this context, I investigate how selection can promote genomic differentiation via hitchhiking and how the structure of the genome (rearrangements, recombination rate) affects the likelihood of genome differentiation.
I also pay particular attention to the genetic basis of chemosensory-based barrier traits, in order to understand the genetic architecture of prezygotic isolation and the impact of selection on these traits, this time explored at the genomic level. At the molecular level, the diversity and variability of chemoreceptors makes chemosensory systems prone to adaptive evolution. I use this information to tackle the genetic basis of prezygotic isolation via candidate gene approaches, using sequence capture and NGS technologies to explore divergence at these large chemoreceptor multigene families.+++————————
Loire E, Tusso S, Camidade P, Severac D, Boursot P, Ganem G, Smadja CM (*joint first authors). Do changes in gene expression contribute to sexual isolation and reinforcement in the house mouse? 2017. Molecular Ecology DOI: 10.1111/mec.14212
Hurst JL, Beynon RJ, Armstrong SD, Davidson AJ, Roberts SA, Gómez-Baena G, Smadja CM, Ganem G. 2017. Molecular heterogeneity in major urinary proteins of Mus musculus subspecies: potential candidates involved in speciation. Scientific Reports 7, 44992
Eyres I, Duvaux D, Gharbi K, Tucker R, Simon JC, Ferrari J, Smadja CM, Butlin RK* (*joint last authors). 2017. Targeted re-sequencing confirms the importance of chemosensory genes in aphid host race differentiation. Molecular Ecology
Eyres I, Jaquiéry J, Sugio A, Duvaux L, Gharbi K, Zhou JJ , Legeai F, Nelson M, Simon JC, Smadja CM, Butlin RK, Ferrari J* (* joint last authors). 2016. Differential gene expression according to race and host plant in the pea aphid. Molecular Ecology 25(17):4197-4215
Hipperson H, Dunning LT, Baker WJ, Butlin RK, Hutton I, Papadopulos AST, Smadja CM, Wilson TC, Devaux C, Savolainen V. 2016. Ecological speciation in sympatric palms: 2. Pre- and post-zygotic isolation. Journal of Evolutionary Biology 29(11):2143-2156
Dunning LT, Hipperson H , Baker WJ, Butlin RK, Devaux C, Hutton I, Igea J, Papadopulos AST, Quan X, Smadja CM, Turnbull CGN, Savolainen V. 2016. Ecological speciation in sympatric palms: 1. Gene expression, selection and pleiotropy. Journal of Evolutionary Biology 29(8):1472-1487
Smadja CM, Loire E, Caminade P, Thoma M, Latour Y, Roux C, Thoss M, Penn DJ, Ganem G and Boursot P (* joint first authors). 2015. Seeking signatures of reinforcement at the genetic level: a hitchhiking mapping and candidate gene approach in the house mouse. Molecular Ecology 24 (16), 4222-4237
Duvaux L, Geissmann Q, Gharbi K, Zhou JJ, Ferrari J, Smadja CM and Butlin RK* (*joint last authors). 2015. Dynamics of copy number variation in host races of the pea aphid. Molecular Biology and Evolution 32 (1), 63-80
Peccoud J, de la Huerta M, Bonhomme J, Laurence C, Outreman Y, Smadja CM and Simon JC. 2014. Widespread ecological hybrid unfitness in the pea aphid species complex. Evolution 68 (10), 2983-2995
Latour Y, Perriat-Sanguinet M, Caminade P, Boursot P, Smadja CM and Ganem G. 2014. Sexual selection against natural hybrids: a barrier to gene flow in a house mouse hybrid zone? Proceedings of the Royal Society of London B. 281 (1776): 20132733
The FroSpects Gregynog Workshop. 2013. Hybridization and speciation. Target review. Journal of Evolutionary Biology 26(2):229-246
Smadja CM and RK Butlin. 2011. A framework for comparing processes of speciation in the presence of gene flow. Molecular Ecology 20:5123-5140
Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Benisson C, Ball AD, Beckerman A and Slate J. 2010. Adaptation genomics: the next generation. Trends in Ecology and Evolution 25(12):705-712
Smadja C and Butlin RK. 2009. Invited review: On the scent of speciation: the chemosensory system and its role in premating isolation. Special issue “Genetics of speciation”. Heredity 102(1): 77-97
Full list of PUBLICATIONS
MAIN RESEARCH PROJECTS :
Evolution of sexual isolation and reinforcement in the house mouseFunding: - ANR blanche ‘ASSORTMATE’ (2010-2016, PI : G. Ganem, France, C. Smadja: task coordinator) - Marie Curie Reintegration Grant (FP7 European commission) ‘SPECIATION GENOMICS’ (2010-2014, PI : C. Smadja, France)
Ecological speciation and host plant specialisation in the pea aphidFunding:
NERC British research council grant ‘Chemosensory genes and the evolution of aphid host races’ (2012-2016, PI : R. Butlin, UK, C. Smadja: project partner)
ANR blanche ‘SPECIAPHID’ (2012-2015, PI : JC Simon, France, C. Smadja: Co-I and task coordinator)
NERC British research council grant ‘Aphid host association’ (2010-2013, PI : R. Butlin, UK, C. Smadja: project partner)
Marie Curie EIF fellowship (FP6 European Commission) ‘Genetics of speciation in the pea aphid’ (2007-2009, PI: C. Smadja)
Other PROjects :ANR ADAPTOME (PI: R. Streiff). Mechanisms of host plant adaptation the European Corn Borer (Ostrinia nubilalis).
ANR HYBRIDADAPT (PI: P. Boursot). Demographic and selection inferences in the house mouse.