Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Dec;165(4):1853–1867. doi: 10.1093/genetics/165.4.1853

Alternative genetic foundations for a key social polymorphism in fire ants.

Kenneth G Ross 1, Michael J B Krieger 1, D DeWayne Shoemaker 1
PMCID: PMC1462884  PMID: 14704171

Abstract

Little is known about the genetic foundations of colony social organization. One rare example in which a single major gene is implicated in the expression of alternative social organizations involves the presumed odorant-binding protein gene Gp-9 in fire ants. Specific amino acid substitutions in this gene invariably are associated with the expression of monogyny (single queen per colony) or polygyny (multiple queens per colony) in fire ant species of the Solenopsis richteri clade. These substitutions are hypothesized to alter the abilities of workers to recognize queens and thereby regulate their numbers in a colony. We examined whether these same substitutions underlie the monogyny/polygyny social polymorphism in the distantly related fire ant S. geminata. We found that Gp-9 coding region sequences are identical in the polygyne and monogyne forms of this species, disproving our hypothesis that one or a few specific amino acid replacements in the protein are necessary to induce transitions in social organization in fire ants. On the other hand, polygyne S. geminata differs genetically from the monogyne form in ways not mirrored in the two forms of S. invicta, a well-studied member of the S. richteri clade, supporting the conclusion that polygyny did not evolve via analogous routes in the two lineages. Specifically, polygyne S. geminata has lower genetic diversity and different gene frequencies than the monogyne form, suggesting that the polygyne form originated via a founder event from a local monogyne population. These comparative data suggest an alternative route to polygyny in S. geminata in which loss of allelic variation at genes encoding recognition cues has led to a breakdown in discrimination abilities and the consequent acceptance of multiple queens in colonies.

Full Text

The Full Text of this article is available as a PDF (324.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ben-Shahar Y., Robichon A., Sokolowski M. B., Robinson G. E. Influence of gene action across different time scales on behavior. Science. 2002 Apr 26;296(5568):741–744. doi: 10.1126/science.1069911. [DOI] [PubMed] [Google Scholar]
  2. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Crozier R. H., Kaufmann B., Carew M. E., Crozier Y. C. Mutability of microsatellites developed for the ant Camponotus consobrinus. Mol Ecol. 1999 Feb;8(2):271–276. doi: 10.1046/j.1365-294x.1999.00565.x. [DOI] [PubMed] [Google Scholar]
  4. Dewayne Shoemaker D., Keller Gwen, Ross Kenneth G. Effects of Wolbachia on mtDNA variation in two fire ant species. Mol Ecol. 2003 Jul;12(7):1757–1771. doi: 10.1046/j.1365-294x.2003.01864.x. [DOI] [PubMed] [Google Scholar]
  5. Galindo K., Smith D. P. A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics. 2001 Nov;159(3):1059–1072. doi: 10.1093/genetics/159.3.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Garza J. C., Williamson E. G. Detection of reduction in population size using data from microsatellite loci. Mol Ecol. 2001 Feb;10(2):305–318. doi: 10.1046/j.1365-294x.2001.01190.x. [DOI] [PubMed] [Google Scholar]
  7. Giraud Tatiana, Pedersen Jes S., Keller Laurent. Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci U S A. 2002 Apr 16;99(9):6075–6079. doi: 10.1073/pnas.092694199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Glazier Anne M., Nadeau Joseph H., Aitman Timothy J. Finding genes that underlie complex traits. Science. 2002 Dec 20;298(5602):2345–2349. doi: 10.1126/science.1076641. [DOI] [PubMed] [Google Scholar]
  9. Hekmat-Scafe Daria S., Scafe Charles R., McKinney Aimee J., Tanouye Mark A. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res. 2002 Sep;12(9):1357–1369. doi: 10.1101/gr.239402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Helms Cahan Sara, Vinson S. Bradleigh. Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution. 2003 Jul;57(7):1562–1570. doi: 10.1111/j.0014-3820.2003.tb00364.x. [DOI] [PubMed] [Google Scholar]
  11. Holway DA, Suarez AV, Case TJ. Loss of intraspecific aggression in the success of a widespread invasive social insect . Science. 1998 Oct 30;282(5390):949–952. doi: 10.1126/science.282.5390.949. [DOI] [PubMed] [Google Scholar]
  12. Hughes William O. H., Sumner Seirian, Van Borm Steven, Boomsma Jacobus J. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci U S A. 2003 Jul 23;100(16):9394–9397. doi: 10.1073/pnas.1633701100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hung A. C., Vinson S. B. Interspecific hybridization and caste specificity of protein in fire ant. Science. 1977 Jun 24;196(4297):1458–1460. doi: 10.1126/science.196.4297.1458. [DOI] [PubMed] [Google Scholar]
  14. Hunt G. J., Guzmán-Novoa E., Fondrk M. K., Page R. E., Jr Quantitative trait loci for honey bee stinging behavior and body size. Genetics. 1998 Mar;148(3):1203–1213. doi: 10.1093/genetics/148.3.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kimmel M., Chakraborty R., King J. P., Bamshad M., Watkins W. S., Jorde L. B. Signatures of population expansion in microsatellite repeat data. Genetics. 1998 Apr;148(4):1921–1930. doi: 10.1093/genetics/148.4.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Krieger Michael J. B., Ross Kenneth G. Identification of a major gene regulating complex social behavior. Science. 2001 Nov 15;295(5553):328–332. doi: 10.1126/science.1065247. [DOI] [PubMed] [Google Scholar]
  17. Leberg P. L. Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol. 2002 Nov;11(11):2445–2449. doi: 10.1046/j.1365-294x.2002.01612.x. [DOI] [PubMed] [Google Scholar]
  18. Osborne KE, Oldroyd BP. Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim Behav. 1999 Aug;58(2):267–272. doi: 10.1006/anbe.1999.1139. [DOI] [PubMed] [Google Scholar]
  19. Pelosi P., Maida R. Odorant-binding proteins in insects. Comp Biochem Physiol B Biochem Mol Biol. 1995 Jul;111(3):503–514. doi: 10.1016/0305-0491(95)00019-5. [DOI] [PubMed] [Google Scholar]
  20. Robinson G. E., Fahrbach S. E., Winston M. L. Insect societies and the molecular biology of social behavior. Bioessays. 1997 Dec;19(12):1099–1108. doi: 10.1002/bies.950191209. [DOI] [PubMed] [Google Scholar]
  21. Robinson GE. Integrative animal behaviour and sociogenomics. Trends Ecol Evol. 1999 May;14(5):202–205. doi: 10.1016/s0169-5347(98)01536-5. [DOI] [PubMed] [Google Scholar]
  22. Ross K. G., Keller L. Genetic control of social organization in an ant. Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14232–14237. doi: 10.1073/pnas.95.24.14232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ross K. G., Krieger M. J., Shoemaker D. D., Vargo E. L., Keller L. Hierarchical analysis of genetic structure in native fire ant populations: results from three classes of molecular markers. Genetics. 1997 Oct;147(2):643–655. doi: 10.1093/genetics/147.2.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ross K. G. Multilocus evolution in fire ants: effects of selection, gene flow and recombination. Genetics. 1997 Apr;145(4):961–974. doi: 10.1093/genetics/145.4.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ross K. G., Shoemaker D. D., Krieger M. J., DeHeer C. J., Keller L. Assessing genetic structure with multiple classes of molecular markers: a case study involving the introduced fire ant Solenopsis invicta. Mol Biol Evol. 1999 Apr;16(4):525–543. doi: 10.1093/oxfordjournals.molbev.a026134. [DOI] [PubMed] [Google Scholar]
  26. Tsutsui N. D., Case T. J. Population genetics and colony structure of the Argentine ant (Linepithema humile) in its native and introduced ranges. Evolution. 2001 May;55(5):976–985. doi: 10.1554/0014-3820(2001)055[0976:pgacso]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  27. Tsutsui N. D., Suarez A. V., Holway D. A., Case T. J. Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5948–5953. doi: 10.1073/pnas.100110397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tsutsui Neil D., Suarez Andrew V., Grosberg Richard K. Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci U S A. 2003 Jan 21;100(3):1078–1083. doi: 10.1073/pnas.0234412100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Turelli M., Hoffmann A. A., McKechnie S. W. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics. 1992 Nov;132(3):713–723. doi: 10.1093/genetics/132.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Young L. J., Nilsen R., Waymire K. G., MacGregor G. R., Insel T. R. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature. 1999 Aug 19;400(6746):766–768. doi: 10.1038/23475. [DOI] [PubMed] [Google Scholar]
  31. Zhang De-Xing, Hewitt Godfrey M. Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol. 2003 Mar;12(3):563–584. doi: 10.1046/j.1365-294x.2003.01773.x. [DOI] [PubMed] [Google Scholar]
  32. Zhou W., Rousset F., O'Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998 Mar 22;265(1395):509–515. doi: 10.1098/rspb.1998.0324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van der Hammen T., Pedersen J. S., Boomsma J. J. Convergent development of low-relatedness supercolonies in Myrmica ants. Heredity (Edinb) 2002 Aug;89(2):83–89. doi: 10.1038/sj.hdy.6800098. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES