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

Nature volume 493, pages 664–668 (2013)Cite this article

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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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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 GSM1031731–GSM1031746, GSM1031779–GSM1031794, GSM1040938–GSM1040947, GSM1049807–GSM1049816 and GSM1049903–GSM1049912); sequence data are available at the NCBI Sequence Read Archive (accessions SRA061944, SRP017299, SRP017317 and SRP017322).

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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.

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Author notes

  1. John Wang and Yannick Wurm: These authors contributed equally to this work.

Authors and 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.

Corresponding authors

Correspondence to John Wang, Yannick Wurm or Laurent Keller.

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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)

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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

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