Letter | Published:

A Y-like social chromosome causes alternative colony organization in fire ants

Nature volume 493, pages 664668 (31 January 2013) | Download Citation

Abstract

Intraspecific variability in social organization is common, yet the underlying causes are rarely known1,2,3. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene4,5,6,7,8. Here we characterize the genomic region responsible for this important social polymorphism, and show that it is part of a pair of heteromorphic chromosomes that have many of the key properties of sex chromosomes. The two variants, hereafter referred to as the social B and social b (SB and Sb) chromosomes, are characterized by a large region of approximately 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromosomes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differentiation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations, including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between individuals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.

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Accessions

Data deposits

The microarray expression data are available at the NCBI Gene Expression Omnibus (accessions GSM1031731GSM1031746, GSM1031779GSM1031794, GSM1040938GSM1040947, GSM1049807GSM1049816 and GSM1049903GSM1049912); sequence data are available at the NCBI Sequence Read Archive (accessions SRA061944, SRP017299, SRP017317 and SRP017322).

References

  1. 1.

    & Social Evolution in Ants (Princeton University Press, 1995)

  2. 2.

    Social life – the paradox of multiple-queen colonies. Trends Ecol. Evol. 10, 355–360 (1995)

  3. 3.

    , & Genes and social behavior. Science 322, 896–900 (2008)

  4. 4.

    & Identification of a major gene regulating complex social behavior. Science 295, 328–332 (2002)

  5. 5.

    & Phenotypic basis of reproductive success in a social insect: genetic and social determinants. Science 260, 1107–1110 (1993)

  6. 6.

    , & Queen dispersal strategies in the multiple-queen form of the fire ant Solenopsis invicta. Am. Nat. 153, 660–675 (1999)

  7. 7.

    & Selfish genes: a green beard in the red fire ant. Nature 394, 573–575 (1998)

  8. 8.

    & Genetic control of social organization in an ant. Proc. Natl Acad. Sci. USA 95, 14232–14237 (1998)

  9. 9.

    & Ecology and evolution of social-organization: insights from fire ants and other highly eusocial insects. Annu. Rev. Ecol. Syst. 26, 631–656 (1995)

  10. 10.

    & Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta. J. Evol. Biol. 12, 672–680 (1999)

  11. 11.

    & Gene by environment interaction: effects of a single-gene and social-environment on reproductive phenotypes of Fire Ant queens. Funct. Ecol. 9, 667–676 (1995)

  12. 12.

    , & Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta. Proc. R. Soc. Lond. B 279, 3217–3222 (2012)

  13. 13.

    & Molecular evolutionary analyses of the odorant-binding protein gene Gp-9 in fire ants and other Solenopsis species. Mol. Biol. Evol. 22, 2090–2103 (2005)

  14. 14.

    & Genetic regulation of colony social organization in fire ants: an integrative overview. Q. Rev. Biol. 82, 201–226 (2007)

  15. 15.

    The genetical architecture of heterostyly in Primula sinensis. Evolution 4, 340–352 (1950)

  16. 16.

    , & The genetics of the mimetic butterfly Papilio memnon L. Philos. Trans. R. Soc. Lond. B 254, 37–89 (1968)

  17. 17.

    et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011)

  18. 18.

    et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376 (2008)

  19. 19.

    , & Chromosome numbers of red and black imported fire ants, Solenopsis invicta and Solenopsis richteri. Ann. Entomol. Soc. Am. 69, 469–470 (1976)

  20. 20.

    et al. The genome of the fire ant Solenopsis invicta. Proc. Natl Acad. Sci. USA 108, 5679–5684 (2011)

  21. 21.

    et al. Are all sex chromosomes created equal? Trends Genet. 27, 350–357 (2011)

  22. 22.

    & Insect Pheromone Biochemistry and Molecular Biology: the Biosynthesis and Detection of Pheromones and Plant Volatiles (Academic, 2003)

  23. 23.

    & Elements of Evolutionary Genetics (Roberts & Company, 2010)

  24. 24.

    & Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr. Biol. 21, 1470–1474 (2011)

  25. 25.

    , & Genome-wide expression patterns and the genetic architecture of a fundamental social trait. PLoS Genet. 4, e1000127 (2008)

  26. 26.

    & Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–503 (2000)

  27. 27.

    & An evolutionary reduction principle for genetic modifiers. Proc. Natl Acad. Sci. USA 83, 4824–4827 (1986)

  28. 28.

    Die Rolle der männlichen Keimzellen bei der Geschlechtsbestimmung der gynodiöecischen Pflanzen. Ber. Deut. Bot. Ges. 26A, 686–701 (1908)

  29. 29.

    Expression profile of a degenerating neo-Y chromosome in Drosophila. Curr. Biol. 16, 1694–1699 (2006)

  30. 30.

    et al. The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res. 21, 1339–1348 (2011)

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Acknowledgements

We thank C. Stoffel, C. La Mendola, N.-C. Chang, C.-Y. Kao and C.-C. Lee for helping with genotyping and molecular biology; the DEE-UNIL animal caretakers for ant husbandry; E. Johnson and P. Etter for RADseq advice; R. Nichols, J. Meunier and R. Verity for statistical advice; K. Harshman and M.-Y. Lu for Illumina sequencing support; R. Wang for FISH support; and B. Charlesworth, D. Charlesworth, H. Kaessmann, L. Ometto, J. Pannel, N. Perrin, M. Reuter, P. Reymond and K. Ross for comments. Some computations were performed at the Vital-IT (http://www.vital-it.ch) Center for high-performance computing (HPC) of the SIB Swiss Institute of Bioinformatics and the EPSRC-funded MidPlus HPC centre. This work was supported by the Biodiversity Research Center (Academia Sinica, Taiwan), Taiwan NSC grant 100-2311-B-001-015-MY3, grants from NERC and the BBSRC (BB/K004204/1), a USDA grant, several grants from the Swiss NSF and an ERC Advanced Grant.

Author information

Author notes

    • John Wang
    •  & Yannick Wurm

    These authors contributed equally to this work.

Affiliations

  1. Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland

    • John Wang
    • , Yannick Wurm
    • , Mingkwan Nipitwattanaphon
    • , Oksana Riba-Grognuz
    •  & Laurent Keller
  2. Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan

    • John Wang
    •  & Yu-Ching Huang
  3. School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK

    • Yannick Wurm
  4. Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland

    • Yannick Wurm
    •  & Oksana Riba-Grognuz
  5. USDA-ARS Center for Medical, Agricultural, and Veterinary Entomology, 1600/1700 Southwest 23rd Drive, Gainesville, Florida 32608, USA

    • DeWayne Shoemaker

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Contributions

J.W., Y.W. and L.K. designed the study and contributed to all stages of the project. M.N., D.D.S. and J.W. prepared samples. J.W. performed RAD sequencing, and J.W. and Y.W. performed genetic analyses. M.N. performed microarray experiments and analysed the data. O.R.-G. and Y.W. analysed RNA-seq and SNP data. J.W. and Y.W. analysed chromosomal locations of differentially expressed genes. Y.W. performed sequence assembly, genome comparisons, and molecular evolution analyses. Y.-C.H. performed FISH experiments. L.K., Y.W. and J.W. wrote the paper with input from other authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to John Wang or Yannick Wurm or Laurent Keller.

Supplementary information

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    Supplementary Information

    This file contains Supplementary Methods and additional analysis, Supplementary References, Supplementary Figures 1-12 and Supplementary Tables 1-6.

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    This zipped file contains Supplementary Tables 7-15.

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DOI

https://doi.org/10.1038/nature11832

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