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Genetic basis of alternative social organizations in fire ants

Titel Englisch Genetic basis of alternative social organizations in fire ants
Gesuchsteller/in Keller Laurent
Nummer 156732
Förderungsinstrument Projektförderung (Abt. I-III)
Forschungseinrichtung Département d'Ecologie et d'Evolution Faculté de Biologie et de Médecine Université de Lausanne
Hochschule Universität Lausanne - LA
Hauptdisziplin Zoologie
Beginn/Ende 01.01.2015 - 31.12.2017
Bewilligter Betrag 1'461'149.15
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Alle Disziplinen (2)

Disziplin
Zoologie
Oekologie

Keywords (3)

population genetics; behaviour; ant

Lay Summary (Französisch)

Lead
Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ants have emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element.The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species.
Lay summary

Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ant Solenopsis invicta has emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element. In the monogyne social form, colonies always contain a single queen while in the polygyne social form, colonies contain many (sometimes hundreds) queens. These two social forms also differ in a host of colony- and individual-level traits, many of which relate to their different strategies of colony founding. All these differences are completely associated with allelic variation at the gene Gp-9. In the monogyne social form all individuals bear only the B allele at this locus while polygyne colonies always comprise individuals with the alternate b allele. Results obtained recently from linkage mapping show that Gp-9 resides within a large (~13 Mb) genomic region in which recombination is completely suppressed. Thus, it is part of a “supergene” comprising an epistatic network of tightly linked genes that are resistant to being broken up and that regulate various aspects of the social syndromes. A perfect association between colony social organization and Gp-9 genotypic composition also occurs in the five closest relatives of S. invicta (i.e., S. macdonaghi, S. megergates, S. quinquecuspis, S. richteri, and the undescribed “S. species X”). Although this pattern has been interpreted as a trans-species polymorphism in which the b allele was retained across multiple speciation events, it is also possible that such a variant arose relatively recently and has spread among the related species by hybridization and introgression. The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species. Comparative analyses will then be conducted to characterize the gene content, putative regulatory regions, and extent of synteny in the supergene among species. We will also determine the number and identity of the genes being in complete linkage disequilibrium with one another and with colony social form in each species. Finally, we will determine the routes and mechanisms of gene gain/loss and identify the nature of selection acting on the genes in the nonrecombining region. The proposed studies will thus permit to reconstruct the evolutionary history of a supergene involved in mediating a major social innovation and provide a foundation for testing hypotheses on the evolution of supergenes, which, in other species, underlie such important and diverse evolutionary phenomena as the origin of sex chromosomes, mimicry, and self-incompatibility.

Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ant Solenopsis invicta has emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element. In the monogyne social form, colonies always contain a single queen while in the polygyne social form, colonies contain many (sometimes hundreds) queens. These two social forms also differ in a host of colony- and individual-level traits, many of which relate to their different strategies of colony founding. All these differences are completely associated with allelic variation at the gene Gp-9. In the monogyne social form all individuals bear only the B allele at this locus while polygyne colonies always comprise individuals with the alternate b allele. Results obtained recently from linkage mapping show that Gp-9 resides within a large (~13 Mb) genomic region in which recombination is completely suppressed. Thus, it is part of a “supergene” comprising an epistatic network of tightly linked genes that are resistant to being broken up and that regulate various aspects of the social syndromes. A perfect association between colony social organization and Gp-9 genotypic composition also occurs in the five closest relatives of S. invicta (i.e., S. macdonaghi, S. megergates, S. quinquecuspis, S. richteri, and the undescribed “S. species X”). Although this pattern has been interpreted as a trans-species polymorphism in which the b allele was retained across multiple speciation events, it is also possible that such a variant arose relatively recently and has spread among the related species by hybridization and introgression. The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species. Comparative analyses will then be conducted to characterize the gene content, putative regulatory regions, and extent of synteny in the supergene among species. We will also determine the number and identity of the genes being in complete linkage disequilibrium with one another and with colony social form in each species. Finally, we will determine the routes and mechanisms of gene gain/loss and identify the nature of selection acting on the genes in the nonrecombining region. The proposed studies will thus permit to reconstruct the evolutionary history of a supergene involved in mediating a major social innovation and provide a foundation for testing hypotheses on the evolution of supergenes, which, in other species, underlie such important and diverse evolutionary phenomena as the origin of sex chromosomes, mimicry, and self-incompatibility.

Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ant Solenopsis invicta has emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element. In the monogyne social form, colonies always contain a single queen while in the polygyne social form, colonies contain many (sometimes hundreds) queens. All these differences are completely associated with allelic variation at the gene Gp-9. In the monogyne social form all individuals bear only the B allele at this locus while polygyne colonies always comprise individuals with the alternate b allele. Results obtained recently from linkage mapping show that Gp-9 resides within a large  genomic region in which recombination is completely suppressed. Thus, it is part of a “supergene” comprising an epistatic network of tightly linked genes that are resistant to being broken up and that regulate various aspects of the social syndromes. A perfect association between colony social organization and Gp-9 genotypic composition also occurs in the five closest relatives of S. invicta (i.e., S. macdonaghi, S. megergates, S. quinquecuspis, S. richteri, and the undescribed “S. species X”).  The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species. The proposed studies will thus permit to reconstruct the evolutionary history of a supergene involved in mediating a major social innovation and provide a foundation for testing hypotheses on the evolution of supergenes, which, in other species, underlie such important and diverse evolutionary phenomena as the origin of sex chromosomes, mimicry, and self-incompatibility

 

Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ant Solenopsis invicta has emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element. In the monogyne social form, colonies always contain a single queen while in the polygyne social form, colonies contain many (sometimes hundreds) queens. These two social forms also differ in a host of colony- and individual-level traits, many of which relate to their different strategies of colony founding. All these differences are completely associated with allelic variation at the gene Gp-9. In the monogyne social form all individuals bear only the B allele at this locus while polygyne colonies always comprise individuals with the alternate b allele. Results obtained recently from linkage mapping show that Gp-9 resides within a large (~13 Mb) genomic region in which recombination is completely suppressed. Thus, it is part of a “supergene” comprising an epistatic network of tightly linked genes that are resistant to being broken up and that regulate various aspects of the social syndromes. A perfect association between colony social organization and Gp-9 genotypic composition also occurs in the five closest relatives of S. invicta (i.e., S. macdonaghi, S. megergates, S. quinquecuspis, S. richteri, and the undescribed “S. species X”). Although this pattern has been interpreted as a trans-species polymorphism in which the b allele was retained across multiple speciation events, it is also possible that such a variant arose relatively recently and has spread among the related species by hybridization and introgression. The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species. Comparative analyses will then be conducted to characterize the gene content, putative regulatory regions, and extent of synteny in the supergene among species. We will also determine the number and identity of the genes being in complete linkage disequilibrium with one another and with colony social form in each species. Finally, we will determine the routes and mechanisms of gene gain/loss and identify the nature of selection acting on the genes in the nonrecombining region. The proposed studies will thus permit to reconstruct the evolutionary history of a supergene involved in mediating a major social innovation and provide a foundation for testing hypotheses on the evolution of supergenes, which, in other species, underlie such important and diverse evolutionary phenomena as the origin of sex chromosomes, mimicry, and self-incompatibility.



Direktlink auf Lay Summary Letzte Aktualisierung: 24.09.2014

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Publikationen

Publikation
Camponotus fellah queens are singly mated
Mersch D., La Mendola C., Keller L. (2017), Camponotus fellah queens are singly mated, in Insectes Sociaux, 64, 269-276.
Convergent evolution of social hybridogenesis in Messor harvester ants.
laurent keller, J Romiguier, A Fournier, SH Yek, L Keller (2017), Convergent evolution of social hybridogenesis in Messor harvester ants., in Molecular Ecology, 28, 1108-1117.
Gene expression is more strongly influenced by age than caste in the ant Lasius niger
Lucas E. R., Romiguier J., Keller L. (2017), Gene expression is more strongly influenced by age than caste in the ant Lasius niger, in Molecular Ecology, 26, 5058-5073.
Genetics and evolution of social behavior in insects
Weitekamp C., Libbrecht R., Keller L. (2017), Genetics and evolution of social behavior in insects, in Annual Reviews Genetics, 51, 219-239.
Lifespan differences between queens and workers are not explained by rates of molecular damage.
laurent keller, ER Lucas, M Augustyniak, A K\kedziorski, L Keller (2017), Lifespan differences between queens and workers are not explained by rates of molecular damage., in Experimental Gerontology, 92, 1-6.
Polydomy enhances foraging performance in ant colonies.
laurent keller, N Stroeymeyt, P Joye, L Keller (2017), Polydomy enhances foraging performance in ant colonies., in Proceedings of the Royal Society, London B, 284, 1853.
Recent human history governs global ant invasion dynamics
Bertelsmeier C., Ollier S., Liebhold A., Keller L. (2017), Recent human history governs global ant invasion dynamics, in Nature Ecology & Evolution, 1, 0184.
Sexual selection shapes development and maturation rates in Drosophila.
laurent keller, B Hollis, L Keller, TJ Kawecki (2017), Sexual selection shapes development and maturation rates in Drosophila., in Evolution, 71, 304-314.
Short-term activity cycles impede information transmission in ant colonies
Richardson T. O., Liechti J. I., Stroeymeyt N., Bonhoeffer S., Keller L. (2017), Short-term activity cycles impede information transmission in ant colonies, in Plos Computational Biology, 1005527.
The GAGA Consortium
Boomsma J. J., Brady S. G., Dunn R. R., Gadau J., Heinze J., Keller L., Moreau C. S., Sanders N. J., Schrader L., Schultz T. R., Sundström L., Ward P. S., Wcislo W. T., Zhang G. (2017), The GAGA Consortium, in Myrmecological News, 25, 61-66.
Evolutionary stability of jointly evolving traits in subdivided populations
Mullon C., Keller L., Lehmann L. (2016), Evolutionary stability of jointly evolving traits in subdivided populations, in American Naturalist, 188(2), 175-195.
Higher expression of somatic repair genes in long-lived ant queens than workers.
laurent keller, ER Lucas, E Privman, L Keller (2016), Higher expression of somatic repair genes in long-lived ant queens than workers., in Aging, 8, 1940-1951.
Inter-caste communication in social insects
Grüter C., Keller L. (2016), Inter-caste communication in social insects, in Current Opinion in Neurobiology, 38, 6-11.
Oral transfer of chemical cues, growth proteins and hormones in social insects.
laurent keller, AC LeBoeuf, P Waridel, CS Brent, AN Gonçcalves, L Menin, D Ortiz, O Riba-Grognuz, A Koto, ZG Soares, E Privman, EA Miska, R Benton, L Keller (2016), Oral transfer of chemical cues, growth proteins and hormones in social insects., in eLife, 5, e20375.
Phylogenomics controlling for base compositional bias reveals a single origin of eusociality in corbiculate bees
Romiguier J., Cameron S.A., Woodard S.H., Fischman B.J., Keller L., Praz C.J. (2016), Phylogenomics controlling for base compositional bias reveals a single origin of eusociality in corbiculate bees, in Molecular Biology and Evolution, 33(3), 670-678.
Robust DNA methylation in the clonal raider ant brain
Libbrecht R., Oxley P.R., Keller L., Kronauer D.J.C. (2016), Robust DNA methylation in the clonal raider ant brain, in Current Biology, 26(3), 391-395.
Expression of foraging and Gp-9 are associated with social organization in the fire ant Solenopsis invicta
Lucas C., Nicolas M., Keller L. (2015), Expression of foraging and Gp-9 are associated with social organization in the fire ant Solenopsis invicta, in Insect Molecular Biology, 24(1), 93-104.
No evidence that within-group male relatedness reduces harm to females in Drosophila
Hollis B., Kawecki T.J., Keller L. (2015), No evidence that within-group male relatedness reduces harm to females in Drosophila, in Ecology and Evolution, 5(4), 979-983.
Social isolation causes mortality by disrupting energy homeostasis in ants
Koto A., Mersch D., Hollis B., Keller L. (2015), Social isolation causes mortality by disrupting energy homeostasis in ants, in Behavioral Ecology and Sociobiology, 69(4), 583-591.
The making of eusociality: Insights from two bumblebee genomes
Libbrecht R., Keller L. (2015), The making of eusociality: Insights from two bumblebee genomes, in Genome Biology, 16(1), 16:75.
Co-evolution of dispersal with social behaviour favours social polymorphism
Mullon C., Keller L., Lehmann L., Co-evolution of dispersal with social behaviour favours social polymorphism, in Nature Ecology & Evolution.
Low number of fixed somatic mutations in a long-lived oak tree
Schmid-Siegert E., Sarkar N., Iseli C., Calderon Copete S., Gouhier-Darimont C., Chrast J., Cattaneo P., Schütz F., Farinelli L., Pagni M., Schneider M., Voumard J., Jaboyedoff M., Fankhauser C., Hardtke C., Keller L., Pannell J., Reymond A., Robinson-Rechavi M., Xenarios I., Reymond P., Low number of fixed somatic mutations in a long-lived oak tree, in Nature Plants.

Verbundene Projekte

Nummer Titel Start Förderungsinstrument
141063 The joint evolution of dispersal and altruism 01.10.2012 Interdisziplinäre Projekte
118194 Determinants of social organisation in ant colonies 01.10.2007 Projektförderung (Abt. I-III)
133121 The determinants of social organisation in ants 01.10.2010 Projektförderung (Abt. I-III)
130313 Population genomic survey of genes influencing fitness in a hybrid zone of fire ants 01.10.2010 ProDoc
176406 Genetic basis of alternative social organizations in fire ants 01.01.2018 Projektförderung (Abt. I-III)
160506 Spread of diseases in honey bee colonies 01.05.2015 Internationale Kurzaufenthalte

Abstract

Although studies of social organisms have demonstrated genetic influences on social organization, the specific genomic components or genetic/physiological networks involved remain largely unknown. The fire ant Solenopsis invicta has emerged as a model for such studies because a fundamental social trait is under the control of a single genomic element. In the monogyne social form, colonies always contain a single queen while in the polygyne social form, colonies contain many (sometimes hundreds) queens. These two social forms also differ in a host of colony- and individual-level traits, many of which relate to their different strategies of colony founding. All these differences are completely associated with allelic variation at the gene Gp-9. In the monogyne social form all individuals bear only the B allele at this locus while polygyne colonies always comprise individuals with the alternate b allele. Results obtained recently from linkage mapping show that Gp-9 resides within a large (~13 Mb) genomic region in which recombination is completely suppressed. Thus, it is part of a “supergene” comprising an epistatic network of tightly linked genes that are resistant to being broken up and that regulate various aspects of the social syndromes. A perfect association between colony social organization and Gp-9 genotypic composition also occurs in the five closest relatives of S. invicta (i.e., S. macdonaghi, S. megergates, S. quinquecuspis, S. richteri, and the undescribed “S. species X”). Although this pattern has been interpreted as a trans-species polymorphism in which the b allele was retained across multiple speciation events, it is also possible that such a variant arose relatively recently and has spread among the related species by hybridization and introgression. The major objective of the proposed research is to address this issue. This will be done by sequencing over 140 male (haploid) genomes from each of the six socially polymorphic species and three outgroup Solenopsis species. Comparative analyses will then be conducted to characterize the gene content, putative regulatory regions, and extent of synteny in the supergene among species. We will also determine the number and identity of the genes being in complete linkage disequilibrium with one another and with colony social form in each species. Finally, we will determine the routes and mechanisms of gene gain/loss and identify the nature of selection acting on the genes in the nonrecombining region. The proposed studies will thus permit to reconstruct the evolutionary history of a supergene involved in mediating a major social innovation and provide a foundation for testing hypotheses on the evolution of supergenes, which, in other species, underlie such important and diverse evolutionary phenomena as the origin of sex chromosomes, mimicry, and self-incompatibility.
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