Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Fine-scale mapping and BAC-FISH analysis of the social chromosome.
Figure 2: Expression of genes associated with Gp-9 genotype are overrepresented on the social chromosome.
Figure 3: Scaffolds lengths of the non-recombining region of the social chromosome (solid) and the rest of the genome (patterned) based on the genome assemblies of a Gp-9B (blue) and a Gp-9b (grey) male.

Accession codes

Primary accessions

Gene Expression Omnibus

Sequence Read Archive

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. Bourke, A. & Franks, N. Social Evolution in Ants (Princeton University Press, 1995)

    Google Scholar 

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

    CAS  Article  Google Scholar 

  3. Robinson, G. E., Fernald, R. D. & Clayton, D. F. Genes and social behavior. Science 322, 896–900 (2008)

    ADS  CAS  Article  Google Scholar 

  4. Krieger, M. J. B. & Ross, K. G. Identification of a major gene regulating complex social behavior. Science 295, 328–332 (2002)

    ADS  CAS  Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

  6. DeHeer, C. J., Goodisman, M. A. D. & Ross, K. G. Queen dispersal strategies in the multiple-queen form of the fire ant Solenopsis invicta. Am. Nat. 153, 660–675 (1999)

    Article  Google Scholar 

  7. Keller, L. & Ross, K. G. Selfish genes: a green beard in the red fire ant. Nature 394, 573–575 (1998)

    ADS  CAS  Article  Google Scholar 

  8. Ross, K. G. & Keller, L. Genetic control of social organization in an ant. Proc. Natl Acad. Sci. USA 95, 14232–14237 (1998)

    ADS  CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  10. Keller, L. & Ross, K. G. 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)

    Article  Google Scholar 

  11. Keller, L. & Ross, K. G. 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)

    Article  Google Scholar 

  12. Lawson, L. P., Vander Meer, R. K. & Shoemaker, D. 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)

    Article  Google Scholar 

  13. Krieger, M. J. B. & Ross, K. G. 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)

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  16. Clarke, C. A., Sheppard, P. M. & Thornton, I. W. The genetics of the mimetic butterfly Papilio memnon L. Philos. Trans. R. Soc. Lond. B 254, 37–89 (1968)

    ADS  Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

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

    ADS  Article  Google Scholar 

  19. Glancey, B. M., Romain, M. K. S. & Crozier, R. H. Chromosome numbers of red and black imported fire ants, Solenopsis invicta and Solenopsis richteri. Ann. Entomol. Soc. Am. 69, 469–470 (1976)

    Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  22. Blomquist, G. J. & Vogt, R. G. Insect Pheromone Biochemistry and Molecular Biology: the Biosynthesis and Detection of Pheromones and Plant Volatiles (Academic, 2003)

    Google Scholar 

  23. Charlesworth, B. & Charlesworth, D. Elements of Evolutionary Genetics (Roberts & Company, 2010)

    MATH  Google Scholar 

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

    CAS  Article  Google Scholar 

  25. Wang, J., Ross, K. G. & Keller, L. Genome-wide expression patterns and the genetic architecture of a fundamental social trait. PLoS Genet. 4, e1000127 (2008)

    Article  Google Scholar 

  26. Yang, Z. & Bielawski, J. P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–503 (2000)

    CAS  Article  Google Scholar 

  27. Feldman, M. W. & Liberman, U. An evolutionary reduction principle for genetic modifiers. Proc. Natl Acad. Sci. USA 83, 4824–4827 (1986)

    ADS  MathSciNet  CAS  Article  Google Scholar 

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

    Google Scholar 

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

    CAS  Article  Google Scholar 

  30. Nygaard, S. 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)

    CAS  Article  Google Scholar 

Download references

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

Authors and Affiliations

Authors

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.

Corresponding authors

Correspondence to John Wang, Yannick Wurm or Laurent Keller.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods and additional analysis, Supplementary References, Supplementary Figures 1-12 and Supplementary Tables 1-6. (PDF 1383 kb)

Supplementary Data

This zipped file contains Supplementary Tables 7-15. (ZIP 296 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wang, J., Wurm, Y., Nipitwattanaphon, M. et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668 (2013). https://doi.org/10.1038/nature11832

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11832

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing