Carole Smadja | CNRS- Universite de Montpellier (original) (raw)

Books by Carole Smadja

Papers by Carole Smadja

Evolution, 2012

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The... more Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence. Here, we present a novel approach to the genetics of speciation, which should complement the commonly used approaches of quantitative trait locus mapping and genome-wide scans for selection. We present a large-scale candidate gene approach by means of sequence capture, applied to identifying the genetic changes underlying reproductive isolation in the pea aphid, a model system for the study of ecological speciation. Targeted resequencing enabled us to scale up the candidate gene approach, specifically testing for the role of chemosensory gene families in host plant specialization. Screening for the signature of divergence under selection at 172 candidate and noncandidate loci, we revealed a handful of loci that show high levels of differentiation among host races, which almost all correspond to odorant and gustatory receptor genes. This study offers the first indication that some chemoreceptor genes, often tightly linked together in the genome, could play a key role in local adaptation and reproductive isolation in the pea aphid and potentially other phytophagous insects. Our approach opens a new route toward the functional genomics of ecological speciation.

Trends in Ecology & …, Jan 1, 2010

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic... more Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of dist... more On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of distantly related plant taxa (Metrosideros, Howea and Coprosma; Proc. Natl Acad. Sci. USA 108, 2011, 13188). We now investigate whether the speciation processes were driven by divergent natural selection in each genus by examining the extent of ecological and genetic divergence. We present new and extensive, ecological and genetic data for all three genera. Consistent with ecologically driven speciation, outlier loci were detected using genome scan methods. This mechanism is supported by individualbased analyses of genotype-environment correlations within species, demonstrating that local adaptation is currently widespread on the island. Genetic analyses show that prezygotic isolating barriers within species are currently insufficiently strong to allow further population differentiation. Interspecific hybridization was found in both Howea and Coprosma, and species distribution modelling indicates that competitive exclusion may result in selection against admixed individuals. Colonization of new niches, partly fuelled by the rapid generation of new adaptive genotypes via hybridization, appears to have resulted in the adaptive radiation in Coprosmasupporting the 'Syngameon hypothesis'.

Journal of Evolutionary …, Jan 1, 2012

…, Jan 1, 2012

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The... more Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence.

Molecular Ecology, Jan 1, 2011

How common is speciation-with-gene-flow? How much does gene flow impact on speciation? To answer ... more How common is speciation-with-gene-flow? How much does gene flow impact on speciation? To answer questions like these requires understanding of the common obstacles to evolving reproductive isolation in the face of gene flow and the factors that favour this crucial step. We provide a common framework for the ways in which gene flow opposes speciation and the potential conditions that may ease divergence. This framework is centred on the challenge shared by most scenarios of speciation-withgene-flow, i.e. the need for coupling among different components of reproductive isolation. Using this structure, we review and compare the factors favouring speciation with the intention of providing a more integrated picture of speciation-with-gene-flow.

… Journal of the …, Jan 1, 2005

We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in... more We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in the hybrid zone between the house mouse subspecies Mus musculus domesticus and M. m. musculus in central Jutland. After determining the general orientation of the clines of allele frequencies, we analysed the cline shapes along the direction of maximum gradient. Eight of the ten clines are best described by steep central steps with coincident positions and an average width of 8.9 km (support limits 7.6-12.4) flanked by tails of introgression, indicating the existence of a barrier to gene flow and only weak selection on the loci studied. We derived estimates of migration from linkage disequilibrium in the centre of the zone, and by applying isolation by distance methods to microsatellite data from some of these populations. These give concordant estimates of s = 0.5-0.8 km generation -. The barrier to gene flow is of the order of 20 km (support limits 14-28), and could be explained by selection of a few per cent at 43-120 underdominant loci that reduces the mean fitness in the central populations to 0.45. Some of the clines appear symmetrical, whereas others are strongly asymmetrical, and two loci appear to have escaped the central barrier to gene flow, reflecting the differential action of selection on different parts of the genome. Asymmetry is always in the direction of more introgression into musculus , indicating either a general progression of domesticus into the musculus territory, possibly mediated by differential behaviour, or past movement of the hybrid zone in the opposite direction, impeded by potential geographical barriers to migration in domesticus territory.

Behavioral Ecology, Jan 1, 2002

Mate choice is the outcome of sexual preference for partners carrying specific signals. Thus, mat... more Mate choice is the outcome of sexual preference for partners carrying specific signals. Thus, mating among conspecifics (homogamy) depends on the occurrence of species recognition systems. We asked what happens if populations diverge, and we investigated female sexual preference between two subspecies of the house mouse in populations from the borders of a hybrid zone ( Jutland, Denmark). We used choice tests to analyze the occurrence of recognition signals and to locate these signals in soiled bedding and urine. Our results show that populations of the two subspecies can be discriminated on the basis of urinary signals, suggesting that the latter have diverged. Additionally, these signals seem to have similar features in populations of different geographical origins, suggesting that subspecific differentiation occurs. This is the first demonstration that subspecific recognition through urinary signals occurs in the house mouse. However, while Mus musculus domesticus does not display a preference, we show that Mus musculus musculus females tend to mate with males of the same subspecies. We discuss the different factors that could explain these discrepancies between females of the two taxa: differences in signal perception, evolution at a different pace, or evolution under different selective pressures in their area of contact. Further, we propose that the divergence in male signal was at least partly initiated in allopatry and discuss different evolutionary scenario that may explain the patterns observed in Denmark and their relevance to isolation between the two taxa.

Biological Journal of …, Jan 1, 2005

Molecular biology and …, Jan 1, 2009

Gaining insight into the mechanisms of chemoreception in aphids is of primary importance for both... more Gaining insight into the mechanisms of chemoreception in aphids is of primary importance for both integrative studies on the evolution of host plant specialization and applied research in pest control management because aphids rely on their sense of smell and taste to locate and assess their host plants. We made use of the recent genome sequence of the pea aphid, Acyrthosiphon pisum, to address the molecular characterization and evolution of key molecular components of chemoreception: the odorant (Or) and gustatory (Gr) receptor genes. We identified 79 Or and 77 Gr genes in the pea aphid genome and showed that most of them are aphid-specific genes that have undergone recent and rapid expansion in the genome. By addressing selection within sets of paralogous Or and Gr expansions, for the first time in an insect species, we show that the most recently duplicated loci have evolved under positive selection, which might be related to the high degree of ecological specialization of this species. Although more functional studies are still needed for insect chemoreceptors, we provide evidence that Grs and Ors have different sets of positively selected sites, suggesting the possibility that these two gene families might have different binding pockets and bind structurally distinct classes of ligand. The pea aphid is the most basal insect species with a completely sequenced genome to date. The identification of chemoreceptor genes in this species is a key step toward further exploring insect comparative genetics, the genomics of ecological specialization and speciation, and new pest control strategies.

Molecular Ecology, Jan 1, 2008

Understanding how speciation can take place in the presence of homogenizing gene flow remains a m... more Understanding how speciation can take place in the presence of homogenizing gene flow remains a major challenge in evolutionary biology. In the early stages of ecological speciation, reproductive isolation between populations occupying different habitats is expected to be concentrated around genes for local adaptation. These genomic regions will show high divergence while gene exchange in other regions of the genome should continue relatively unimpaired, resulting in low levels of differentiation. The problem is to explain how speciation progresses from this point towards complete reproductive isolation, allowing genome-wide divergence. A new study by Via and West (2008) on speciation between host races of the pea aphid, Acyrthosiphon pisum, introduces the mechanism of 'divergence hitchhiking' which can generate large 'islands of differentiation' and facilitate the build-up of linkage disequilibrium, favouring increased reproductive isolation. This idea potentially removes a major stumbling block to speciation under continuous gene flow.

Trends in Ecology & …, Jan 1, 2010

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic... more Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

Behavioral Ecology, Jan 1, 2008

PLOS …, Jan 1, 2010

Aphids are important agricultural pests and also biological models for studies of insect-plant in... more Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont.

Journal of Evolutionary Biology, Jan 1, 2005

Journal of Evolutionary …, Jan 1, 2004

Although selection against hybridization is expected to generate prezygotic divergence in unimoda... more Although selection against hybridization is expected to generate prezygotic divergence in unimodal hybrid zones, such a pattern has been seldom described. This study aims to better understand how prezygotic mechanisms may evolve in such zones. We investigated prezygotic divergence between populations of two subspecies of mice (Mus musculus musculus and M. m. domesticus) located at the edges of their unimodal hybrid zone in Denmark, and we developed an original multiple-population choice-test design, which allows assessment of within and between subspecies variation. Our study demonstrates that a strong assortative preference characterises one of the two subspecies (musculus) and that urinary signals are involved in this subspecies recognition. Taking into account the specific genetic and geographical characteristics of the Danish hybrid zone, we discuss the influence of the above pattern on its fate and the mechanisms that could have favoured this prezygotic divergence, among which the role of recombined populations constituting the core of the zone.

Evolution, 2012

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The... more Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence. Here, we present a novel approach to the genetics of speciation, which should complement the commonly used approaches of quantitative trait locus mapping and genome-wide scans for selection. We present a large-scale candidate gene approach by means of sequence capture, applied to identifying the genetic changes underlying reproductive isolation in the pea aphid, a model system for the study of ecological speciation. Targeted resequencing enabled us to scale up the candidate gene approach, specifically testing for the role of chemosensory gene families in host plant specialization. Screening for the signature of divergence under selection at 172 candidate and noncandidate loci, we revealed a handful of loci that show high levels of differentiation among host races, which almost all correspond to odorant and gustatory receptor genes. This study offers the first indication that some chemoreceptor genes, often tightly linked together in the genome, could play a key role in local adaptation and reproductive isolation in the pea aphid and potentially other phytophagous insects. Our approach opens a new route toward the functional genomics of ecological speciation.

Trends in Ecology & …, Jan 1, 2010

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic... more Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of dist... more On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of distantly related plant taxa (Metrosideros, Howea and Coprosma; Proc. Natl Acad. Sci. USA 108, 2011, 13188). We now investigate whether the speciation processes were driven by divergent natural selection in each genus by examining the extent of ecological and genetic divergence. We present new and extensive, ecological and genetic data for all three genera. Consistent with ecologically driven speciation, outlier loci were detected using genome scan methods. This mechanism is supported by individualbased analyses of genotype-environment correlations within species, demonstrating that local adaptation is currently widespread on the island. Genetic analyses show that prezygotic isolating barriers within species are currently insufficiently strong to allow further population differentiation. Interspecific hybridization was found in both Howea and Coprosma, and species distribution modelling indicates that competitive exclusion may result in selection against admixed individuals. Colonization of new niches, partly fuelled by the rapid generation of new adaptive genotypes via hybridization, appears to have resulted in the adaptive radiation in Coprosmasupporting the 'Syngameon hypothesis'.

Journal of Evolutionary …, Jan 1, 2012

…, Jan 1, 2012

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The... more Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence.

Molecular Ecology, Jan 1, 2011

How common is speciation-with-gene-flow? How much does gene flow impact on speciation? To answer ... more How common is speciation-with-gene-flow? How much does gene flow impact on speciation? To answer questions like these requires understanding of the common obstacles to evolving reproductive isolation in the face of gene flow and the factors that favour this crucial step. We provide a common framework for the ways in which gene flow opposes speciation and the potential conditions that may ease divergence. This framework is centred on the challenge shared by most scenarios of speciation-withgene-flow, i.e. the need for coupling among different components of reproductive isolation. Using this structure, we review and compare the factors favouring speciation with the intention of providing a more integrated picture of speciation-with-gene-flow.

… Journal of the …, Jan 1, 2005

We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in... more We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in the hybrid zone between the house mouse subspecies Mus musculus domesticus and M. m. musculus in central Jutland. After determining the general orientation of the clines of allele frequencies, we analysed the cline shapes along the direction of maximum gradient. Eight of the ten clines are best described by steep central steps with coincident positions and an average width of 8.9 km (support limits 7.6-12.4) flanked by tails of introgression, indicating the existence of a barrier to gene flow and only weak selection on the loci studied. We derived estimates of migration from linkage disequilibrium in the centre of the zone, and by applying isolation by distance methods to microsatellite data from some of these populations. These give concordant estimates of s = 0.5-0.8 km generation -. The barrier to gene flow is of the order of 20 km (support limits 14-28), and could be explained by selection of a few per cent at 43-120 underdominant loci that reduces the mean fitness in the central populations to 0.45. Some of the clines appear symmetrical, whereas others are strongly asymmetrical, and two loci appear to have escaped the central barrier to gene flow, reflecting the differential action of selection on different parts of the genome. Asymmetry is always in the direction of more introgression into musculus , indicating either a general progression of domesticus into the musculus territory, possibly mediated by differential behaviour, or past movement of the hybrid zone in the opposite direction, impeded by potential geographical barriers to migration in domesticus territory.

Behavioral Ecology, Jan 1, 2002

Mate choice is the outcome of sexual preference for partners carrying specific signals. Thus, mat... more Mate choice is the outcome of sexual preference for partners carrying specific signals. Thus, mating among conspecifics (homogamy) depends on the occurrence of species recognition systems. We asked what happens if populations diverge, and we investigated female sexual preference between two subspecies of the house mouse in populations from the borders of a hybrid zone ( Jutland, Denmark). We used choice tests to analyze the occurrence of recognition signals and to locate these signals in soiled bedding and urine. Our results show that populations of the two subspecies can be discriminated on the basis of urinary signals, suggesting that the latter have diverged. Additionally, these signals seem to have similar features in populations of different geographical origins, suggesting that subspecific differentiation occurs. This is the first demonstration that subspecific recognition through urinary signals occurs in the house mouse. However, while Mus musculus domesticus does not display a preference, we show that Mus musculus musculus females tend to mate with males of the same subspecies. We discuss the different factors that could explain these discrepancies between females of the two taxa: differences in signal perception, evolution at a different pace, or evolution under different selective pressures in their area of contact. Further, we propose that the divergence in male signal was at least partly initiated in allopatry and discuss different evolutionary scenario that may explain the patterns observed in Denmark and their relevance to isolation between the two taxa.

Biological Journal of …, Jan 1, 2005

Molecular biology and …, Jan 1, 2009

Gaining insight into the mechanisms of chemoreception in aphids is of primary importance for both... more Gaining insight into the mechanisms of chemoreception in aphids is of primary importance for both integrative studies on the evolution of host plant specialization and applied research in pest control management because aphids rely on their sense of smell and taste to locate and assess their host plants. We made use of the recent genome sequence of the pea aphid, Acyrthosiphon pisum, to address the molecular characterization and evolution of key molecular components of chemoreception: the odorant (Or) and gustatory (Gr) receptor genes. We identified 79 Or and 77 Gr genes in the pea aphid genome and showed that most of them are aphid-specific genes that have undergone recent and rapid expansion in the genome. By addressing selection within sets of paralogous Or and Gr expansions, for the first time in an insect species, we show that the most recently duplicated loci have evolved under positive selection, which might be related to the high degree of ecological specialization of this species. Although more functional studies are still needed for insect chemoreceptors, we provide evidence that Grs and Ors have different sets of positively selected sites, suggesting the possibility that these two gene families might have different binding pockets and bind structurally distinct classes of ligand. The pea aphid is the most basal insect species with a completely sequenced genome to date. The identification of chemoreceptor genes in this species is a key step toward further exploring insect comparative genetics, the genomics of ecological specialization and speciation, and new pest control strategies.

Molecular Ecology, Jan 1, 2008

Understanding how speciation can take place in the presence of homogenizing gene flow remains a m... more Understanding how speciation can take place in the presence of homogenizing gene flow remains a major challenge in evolutionary biology. In the early stages of ecological speciation, reproductive isolation between populations occupying different habitats is expected to be concentrated around genes for local adaptation. These genomic regions will show high divergence while gene exchange in other regions of the genome should continue relatively unimpaired, resulting in low levels of differentiation. The problem is to explain how speciation progresses from this point towards complete reproductive isolation, allowing genome-wide divergence. A new study by Via and West (2008) on speciation between host races of the pea aphid, Acyrthosiphon pisum, introduces the mechanism of 'divergence hitchhiking' which can generate large 'islands of differentiation' and facilitate the build-up of linkage disequilibrium, favouring increased reproductive isolation. This idea potentially removes a major stumbling block to speciation under continuous gene flow.

Trends in Ecology & …, Jan 1, 2010

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic... more Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

Behavioral Ecology, Jan 1, 2008

PLOS …, Jan 1, 2010

Aphids are important agricultural pests and also biological models for studies of insect-plant in... more Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont.

Journal of Evolutionary Biology, Jan 1, 2005

Journal of Evolutionary …, Jan 1, 2004

Although selection against hybridization is expected to generate prezygotic divergence in unimoda... more Although selection against hybridization is expected to generate prezygotic divergence in unimodal hybrid zones, such a pattern has been seldom described. This study aims to better understand how prezygotic mechanisms may evolve in such zones. We investigated prezygotic divergence between populations of two subspecies of mice (Mus musculus musculus and M. m. domesticus) located at the edges of their unimodal hybrid zone in Denmark, and we developed an original multiple-population choice-test design, which allows assessment of within and between subspecies variation. Our study demonstrates that a strong assortative preference characterises one of the two subspecies (musculus) and that urinary signals are involved in this subspecies recognition. Taking into account the specific genetic and geographical characteristics of the Danish hybrid zone, we discuss the influence of the above pattern on its fate and the mechanisms that could have favoured this prezygotic divergence, among which the role of recombined populations constituting the core of the zone.

Journal of Evolutionary …, Jan 1, 2004

Reinforcement: a process, not a pattern 183