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1. Masculinization of the X-chromosome in aphid soma and gonads

Author

Jaquiéry, Julie, Simon, Jean-Christophe, Robin, Stéphanie, Richard, Gautier, Peccoud, Jean, Boulain, Hélène, Legeai, Fabrice, Tanguy, Sylvie, Prunier-Leterme, Nathalie, and Letrionnaire, Gaël

Subjects
Archaeology, CC1-960, Science
Abstract

Males and females share essentially the same genome but differ in their optimal values for many phenotypic traits, which can result in intra-locus conflict between the sexes. Aphids display XX/X0 sex chromosomes and combine unusual X chromosome inheritance with cyclical parthenogenesis. Theoretical and empirical works support the hypothesis that the large excess of male-biased genes observed on the aphid X chromosome compared to autosomes evolved in response to sexual conflicts, by restricting the products of sexually antagonistic alleles to the sex they benefits. However, whether such masculinization of the X affects all tissues (as expected if it evolved in response to sexual conflicts) or is limited to specific tissues remains an open question. Here, we measured gene expression in three different somatic and gonadic tissues of males, sexual females and parthenogenetic females of the pea aphid. We observed a masculinization of the X in each of the studied tissues, with male-biased genes being 2.5 to 3.5 more frequent on the X than expected. We also tested the hypothesis that gene duplication can facilitate the attenuation of conflicts by allowing gene copies to neo- or sub-functionalize and reach sex-specific optima. As predicted, X-linked copies of duplicated genes having their other copies on autosomes were more frequently male-biased (40.5% of the genes) than duplicated autosomal genes (6.6%) or X-linked single-copy genes (32.5%). These results highlight a peculiar pattern of expression of X-linked genes in aphids at the tissue level and provide further support for sex-biased expression as a mechanism to attenuate intra-locus sexual conflicts.

Published
2022
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2. Dopamine pathway characterization during the reproductive mode switch in the pea aphid

Author

Le Trionnaire, Gaël, Hudaverdian, Sylvie, Richard, Gautier, Tanguy, Sylvie, Gleonnec, Florence, Prunier-Leterme, Nathalie, Gauthier, Jean-Pierre, and Tagu, Denis

Subjects
Archaeology, CC1-960, Science
Abstract

Aphids are major pests of most of the crops worldwide. Such a success is largely explained by the remarkable plasticity of their reproductive mode. They reproduce efficiently by viviparous parthenogenesis during spring and summer generating important damage on crops. At the end of the summer, viviparous parthenogenetic females perceive the photoperiod shortening and transduce this signal to their embryos that change their reproductive fate to produce sexual individuals: oviparous females and males. After mating, those females lay cold-resistant eggs. Earlier studies showed that some transcripts coding for key components of dopamine pathway were regulated between long days and short days conditions suggesting that dopamine might be involved in the transduction of seasonal cues prior to reproductive mode switch. In this study, we aimed at going deeper into the characterization of the expression dynamics of this pathway but also in the analysis of its functional role in this context in the pea aphid Acyrthosiphon pisum. We first analysed the level of expression of ten genes of this pathway in embryos and larval heads of aphids reared under long days (asexual producers) or short days (sexual producers) conditions. We then performed in situ hybridization experiments to localize in embryos the ddc and pale transcripts that are coding for two key enzymes in dopamine synthesis. Finally, Using CRISPR-Cas9 mutagenesis in eggs produced after the mating of sexual individuals, we targeted the ddc gene. We could observe strong melanization defaults in ddc mutated eggs, which confidently mimicked the Drosophila ddc phenotype. Nevertheless, such a lethal phenotype did not allow us to validate the involvement of dopamine as a signaling pathway necessary to trigger the reproductive mode switch in embryos.

Published
2022
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5. Disentangling the Causes for Faster-X Evolution in Aphids

Author

Jaquiéry, Julie, primary, Peccoud, Jean, additional, Ouisse, Tiphaine, additional, Legeai, Fabrice, additional, Prunier-Leterme, Nathalie, additional, Gouin, Anais, additional, Nouhaud, Pierre, additional, Brisson, Jennifer A, additional, Bickel, Ryan, additional, Purandare, Swapna, additional, Poulain, Julie, additional, Battail, Christophe, additional, Lemaitre, Claire, additional, Mieuzet, Lucie, additional, Le Trionnaire, Gael, additional, Simon, Jean-Christophe, additional, and Rispe, Claude, additional

Published
2018
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7. Genetic control of contagious asexuality in the pea aphid

Author

Jaquiéry, Julie, Peccoud, Jean, Ouisse, Tiphaine, Legeai, Fabrice, Prunier-Leterme, Nathalie, Gouin, Anaïs, Nouhaud, Pierre, Brisson, Jennifer, Bickel, Ryan, Purandare, Swapna, Poulain, Julie, Battail, Christophe, Lemaitre, Claire, Mieuzet, Lucie, Le Trionnaire, Gaël, Simon, Jean-Christophe, Rispe, Claude, Ecosystèmes, biodiversité, évolution [Rennes] (ECOBIO), Université de Rennes (UR)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR), Université de Rennes (UR)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Centre National de la Recherche Scientifique (CNRS), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Ecologie et biologie des interactions (EBI), Université de Poitiers-Centre National de la Recherche Scientifique (CNRS), Ecologie, Evolution, Symbiose (EES), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), University of Veterinary Medicine [Vienna] (Vetmeduni), University of Rochester [USA], Multidisciplinary Center for Advance Research and Studies (MCARS ), Jamia Milia Islamia University [New Delhi] (JMI), Institut de Génomique d'Evry (IG), Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Centre National de Génotypage (CNG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Biologie, Epidémiologie et analyse de risque en Santé Animale (BIOEPAR), Institut National de la Recherche Agronomique (INRA)-École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), The Swiss National Science Fundation (grants PBLAA-122658 & PA00P3-139720 to JJ, http://www.snf.ch/fr/Pages/default.aspx), INRA-AIP BioRessources (project Poly-Express to DT, http://www.international.inra.fr/), The Fondation pour la Recherche pour la Biodiversité FRB (AAP-IN-2009-020 to JCS, http://www.fondationbiodiversite.fr/), The Genoscope (http://www.genoscope.cns.frspip/spip.php?lang = en), ANR-11-BSV7-0005,SPECIAPHID,Génétique de l'adaptation trophique et mécanismes d'isolement reproducteur chez les pucerons(2011), ANR-09-GENM-0017,GW-Aphid,Génomique et transcriptomique des populations pour l'identification de gènes contrôlant la variation du mode reproducteur chez le puceron du pois(2009), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Centre National de la Recherche Scientifique (CNRS), GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Université de Bretagne Sud (UBS)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-Télécom Bretagne-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Rennes (UNIV-RENNES)-CentraleSupélec-Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria), This study was supported by the Swiss National Science Fundation (grants PBLAA-122658 & PA00P3-139720 to JJ, http://www.snf.ch/fr/Pages/default.aspx), INRA-AIP BioRessources (project Poly-Express to DT, http://www.international.inra.fr/), the Fondation pour la Recherche pour la Biodiversite´ FRB (AAP-IN-2009-020 to JCS, http://www.fondationbiodiversite.fr/), the Genoscope (http://www.genoscope.cns.frspip/spip.php?lang = en) and ANR (grant ANR-09-GENM-017-001 to DT, grant ANR-11-BSV7-005-01 to JCS and grant ANR-11-BSV7-007 to SS, Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Centre National de la Recherche Scientifique (CNRS)-Université de Poitiers, Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Institut de Biologie François JACOB (JACOB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, and Institut National de la Recherche Agronomique (INRA)

Subjects
0106 biological sciences, Male, Cancer Research, Parthenogenesis, Population genetics, Asexual reproduction, Signatures of Natural Selection, 01 natural sciences, Natural Selection, Ecological Selection, Genetics (clinical), Genetics, 0303 health sciences, education.field_of_study, Reproduction, Chromosome Mapping, Genomics, Genome Scans, Female, Anatomy, Research Article, Evolutionary Processes, lcsh:QH426-470, Gene Transfer, Horizontal, Population, Quantitative Trait Loci, Biology, 010603 evolutionary biology, Asexuality, 03 medical and health sciences, Asexual Reproduction, Reproduction, Asexual, Animals, Allele, education, Molecular Biology, Ecology, Evolution, Behavior and Systematics, Crosses, Genetic, 030304 developmental biology, Evolutionary Biology, Obligate, Peas, Reproductive System, Biology and Life Sciences, Computational Biology, Genome Analysis, Sexual reproduction, lcsh:Genetics, Genetics, Population, Aphids, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Population Genetics
Abstract

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages., Author Summary Asexual lineages occur in most groups of organisms and arise from loss of sex in sexual species. Yet, the genomic bases of these transitions remain largely unknown. Here, we combined quantitative genetic and population genomic approaches to unravel the genetic control of shifts towards permanent asexuality in the pea aphid, which conveniently shows coexisting sexual and asexual lineages. We identified one main genomic region responsible for this transition located on the X chromosome. Also, our population genetic data indicated substantial gene exchange between these reproductively distinct lineages, potentially leading to the conversion of some sexual lineages into asexual ones in a contagious manner. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual lineages.

Published
2014

8. Masculinization of the X Chromosome in the Pea Aphid

Author

Jaquiéry, Julie, primary, Rispe, Claude, additional, Roze, Denis, additional, Legeai, Fabrice, additional, Le Trionnaire, Gaël, additional, Stoeckel, Solenn, additional, Mieuzet, Lucie, additional, Da Silva, Corinne, additional, Poulain, Julie, additional, Prunier-Leterme, Nathalie, additional, Ségurens, Béatrice, additional, Tagu, Denis, additional, and Simon, Jean-Christophe, additional

Published
2013
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9. Large-scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera)

Author

Sabater-Muñoz, Beatriz, Legeai, Fabrice, Rispe, Claude, Bonhomme, Joël, Dearden, Peter, Dossat, Carole, Duclert, Aymeric, Gauthier, Jean-Pierre, Ducray, Danièle, Hunter, Wayne, Dang, Phat, Kambhampati, Srini, Martinez-Torres, David, Cortes, Teresa, Moya, Andrès, Nakabachi, Atsushi, Philippe, Cathy, Prunier-Leterme, Nathalie, Rahbé, Yvan, Simon, Jean-Christophe, Stern, David, Wincker, Patrick, and Tagu, Denis

Published
2006

10. Genetic control of contagious asexuality in the pea aphid.

Author

Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, Bonhomme J, Mahéo F, Legeai F, Gauthier JP, Prunier-Leterme N, Tagu D, and Simon JC

Subjects
Animals, Aphids physiology, Chromosome Mapping, Crosses, Genetic, Female, Genetics, Population, Male, Parthenogenesis genetics, Quantitative Trait Loci, Reproduction genetics, Aphids genetics, Gene Transfer, Horizontal, Pisum sativum parasitology, Reproduction, Asexual genetics
Abstract

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼ 300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.

Published
2014
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