Project

Back to overview

Genetic basis of alternative social organizations in fire ants

English title Genetic basis of alternative social organizations in fire ants
Applicant Keller Laurent
Number 156732
Funding scheme Project funding (Div. I-III)
Research institution Département d'Ecologie et d'Evolution Faculté de Biologie et de Médecine Université de Lausanne
Institution of higher education University of Lausanne - LA
Main discipline Zoology
Start/End 01.01.2015 - 31.12.2017
Approved amount 1'461'149.15
Show all

All Disciplines (2)

Discipline
Zoology
Ecology

Keywords (3)

population genetics; behaviour; ant

Lay Summary (French)

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.



Direct link to Lay Summary Last update: 24.09.2014

Responsible applicant and co-applicants

Employees

Publications

Publication
Encyclopedia of Social Insects
Kay Tomas, Lehmann Laurent, Keller Laurent (2020), Encyclopedia of Social Insects, Springer International Publishing, Cham.
Evolution of a supergene that regulates a trans-species social polymorphism
Yan Zheng, Martin Simon H., Gotzek Dietrich, Arsenault Samuel V., Duchen Pablo, Helleu Quentin, Riba-Grognuz Oksana, Hunt Brendan G., Salamin Nicolas, Shoemaker DeWayne, Ross Kenneth G., Keller Laurent (2020), Evolution of a supergene that regulates a trans-species social polymorphism, in Nature Ecology & Evolution, 4(2), 240-249.
Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in Drosophila GENOMIC BASIS OF DROSOPHILA LONGEVITY
Hoedjes Katja M., van den Heuvel Joost, Kapun Martin, Keller Laurent, Flatt Thomas, Zwaan Bas J. (2019), Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in Drosophila GENOMIC BASIS OF DROSOPHILA LONGEVITY, in Evolution Letters, 3(6), 598-609.
The co‐evolution of longevity and social life
Lucas Eric R., Keller Laurent (2019), The co‐evolution of longevity and social life, in Functional Ecology, 34(1), 76-87.
Coevolution of Genome Architecture and Social Behavior
Rubenstein Dustin R., Ågren J. Arvid, Carbone Lucia, Elde Nels C., Hoekstra Hopi E., Kapheim Karen M., Keller Laurent, Moreau Corrie S., Toth Amy L., Yeaman Sam, Hofmann Hans A. (2019), Coevolution of Genome Architecture and Social Behavior, in Trends in Ecology & Evolution, 34(9), 844-855.
Oral transfer of chemical cues, growth proteins and hormones in social insects
LeBoeuf Adria C, Waridel Patrice, Brent Colin S, Goncalves Andre N, Menin Laure, Ortiz Daniel, Riba-Grognuz Oksana, Koto Akiko, Soares Zamira G, Privman Eyal, Miska Eric A, Benton Richard, Keller Laurent (2019), Oral transfer of chemical cues, growth proteins and hormones in social insects, in eLife, 8, 1-6.
Insights and opportunities in insect social behavior
Gadagkar Raghavendra, Gordon Deborah, Keller Laurent, Michod Rick, Queller David, Robinson Gene E, Strassmann Joan, West-Eberhard Mary Jane (2019), Insights and opportunities in insect social behavior, in Current Opinion in Insect Science, 34, ix-xx.
Kin selection and altruism
Kay Tomas, Lehmann Laurent, Keller Laurent (2019), Kin selection and altruism, in Current Biology, 29(11), R438-R442.
Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster
Hollis Brian, Koppik Mareike, Wensing Kristina U., Ruhmann Hanna, Genzoni Eléonore, Erkosar Berra, Kawecki Tadeusz J., Fricke Claudia, Keller Laurent (2019), Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster, in Proceedings of the National Academy of Sciences, 116(17), 8437-8444.
Genes and Behaviour: Beyond Nature-Nurture
WeitekampC.A., KellerL. (2019), Genes and Behaviour: Beyond Nature-Nurture, in Wedell N., Hosken D.J., Hunt J. (ed.), Wiley, USA, 93-103.
Oxytocin/vasopressin-like peptide inotocin regulates cuticular hydrocarbon synthesis and water balancing in ants
Koto Akiko, Motoyama Naoto, Tahara Hiroki, McGregor Sean, Moriyama Minoru, Okabe Takayoshi, Miura Masayuki, Keller Laurent (2019), Oxytocin/vasopressin-like peptide inotocin regulates cuticular hydrocarbon synthesis and water balancing in ants, in Proceedings of the National Academy of Sciences, 116(12), 5597-5606.
Tissue- and sex-specific small RNAomes reveal sex differences in response to the environment
Bezler Alexandra, Braukmann Fabian, West Sean M., Duplan Arthur, Conconi Raffaella, Schütz Frédéric, Gönczy Pierre, Piano Fabio, Gunsalus Kristin, Miska Eric A., Keller Laurent (2019), Tissue- and sex-specific small RNAomes reveal sex differences in response to the environment, in PLOS Genetics, 15(2), e1007905-e1007905.
Isolation and characterization of novel microsatellite markers for a globally distributed invasive ant Paratrechina longicornis (Hymenoptera: Formicidae)
TSENG Shu-Ping, DARRAS Hugo, LEE Chow-Yang, YOSHIMURA Tsuyoshi, KELLER Laurent, YANG Chin-Cheng Scotty (2019), Isolation and characterization of novel microsatellite markers for a globally distributed invasive ant Paratrechina longicornis (Hymenoptera: Formicidae), in European Journal of Entomology, 116, 253-257.
Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour
Romiguier Jonathan, Rolland Jonathan, Morandin Claire, Keller Laurent (2018), Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour, in BMC Evolutionary Biology, 18(1), 40-40.
Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour
Romiguier Jonathan, Rolland Jonathan, Morandin Claire, Keller Laurent (2018), Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour, in BMC Evolutionary Biology, 18(1), 40-40.
Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid
LeBoeuf Adria C., Cohanim Amir B., Stoffel Céline, Brent Colin S., Waridel Patrice, Privman Eyal, Keller Laurent, Benton Richard (2018), Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid, in Scientific Reports, 8(1), 17830-17830.
Doublesex Evolution Is Correlated with Social Complexity in Ants
Jia Ling-Yi, Chen Li, Keller Laurent, Wang John, Xiao Jin-Hua, Huang Da-Wei (2018), Doublesex Evolution Is Correlated with Social Complexity in Ants, in Genome Biology and Evolution, 10(12), 3230-3242.
Social network plasticity decreases disease transmission in a eusocial insect
Stroeymeyt Nathalie, Grasse Anna V., Crespi Alessandro, Mersch Danielle P., Cremer Sylvia, Keller Laurent (2018), Social network plasticity decreases disease transmission in a eusocial insect, in Science, 362(6417), 941-945.
Caste ratio adjustments in response to perceived and realised competition in parasites with division of labour
Lagrue Clément, MacLeod Colin D., Keller Laurent, Poulin Robert (2018), Caste ratio adjustments in response to perceived and realised competition in parasites with division of labour, in Journal of Animal Ecology, 87(5), 1429-1439.
Positive selection on sociobiological traits in invasive fire ants
Privman Eyal, Cohen Pnina, Cohanim Amir B., Riba-Grognuz Oksana, Shoemaker DeWayne, Keller Laurent (2018), Positive selection on sociobiological traits in invasive fire ants, in Molecular Ecology, 27(15), 3116-3130.
Bridgehead Effects and Role of Adaptive Evolution in Invasive Populations
Bertelsmeier Cleo, Keller Laurent (2018), Bridgehead Effects and Role of Adaptive Evolution in Invasive Populations, in Trends in Ecology & Evolution, 33(7), 527-534.
Elevated expression of ageing and immunity genes in queens of the black garden ant
Lucas Eric R., Keller Laurent (2018), Elevated expression of ageing and immunity genes in queens of the black garden ant, in Experimental Gerontology, 108, 92-98.
New explanation for the longevity of social insect reproductives: Transposable element activity
Lucas Eric R., Keller Laurent (2018), New explanation for the longevity of social insect reproductives: Transposable element activity, in Proceedings of the National Academy of Sciences, 115(21), 5317-5318.
New explanation for the longevity of social insect reproductives: Transposable element activity
Lucas Eric R., Keller Laurent (2018), New explanation for the longevity of social insect reproductives: Transposable element activity, in Proceedings of the National Academy of Sciences, 115(21), 5317-5318.
Recurrent bridgehead effects accelerate global alien ant spread
Bertelsmeier Cleo, Ollier Sébastien, Liebhold Andrew M., Brockerhoff Eckehard G., Ward Darren, Keller Laurent (2018), Recurrent bridgehead effects accelerate global alien ant spread, in Proceedings of the National Academy of Sciences, 115(21), 5486-5491.
Social polymorphism is favoured by the co-evolution of dispersal with social behaviour
Mullon Charles, Keller Laurent, Lehmann Laurent (2018), Social polymorphism is favoured by the co-evolution of dispersal with social behaviour, in Nature Ecology & Evolution, 2(1), 132-140.
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.

Collaboration

Group / person Country
Types of collaboration
Dr. Dewayne Shomaker, USDA United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Kenneth G. Ross, University of Georgia United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Associated projects

Number Title Start Funding scheme
141063 The joint evolution of dispersal and altruism 01.10.2012 Interdisciplinary projects
118194 Determinants of social organisation in ant colonies 01.10.2007 Project funding (Div. I-III)
160506 Spread of diseases in honey bee colonies 01.05.2015 International short research visits
176406 Genetic basis of alternative social organizations in fire ants 01.01.2018 Project funding (Div. I-III)
133121 The determinants of social organisation in ants 01.10.2010 Project funding (Div. I-III)
130313 Population genomic survey of genes influencing fitness in a hybrid zone of fire ants 01.10.2010 ProDoc

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.
-