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

Journal name:
Nature
Volume:
493,
Pages:
664–668
Date published:
DOI:
doi:10.1038/nature11832
Received
Accepted
Published online

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 13megabases (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.

At a glance

Figures

  1. Fine-scale mapping and BAC-FISH analysis of the social chromosome.
    Figure 1: Fine-scale mapping and BAC-FISH analysis of the social chromosome.

    a, Fine-scale linkage map of the SB social chromosome derived from RADseq analysis of male offspring from a monogyne Gp-9BB queen (M013). Genetic positions in centimorgans (below) and RAD marker names (above) are indicated. Each genetic marker has a prefix (brc_m013_) and a number based on its serial position on the map. Multiple markers that have the same map position are indicated using ‘firstlast’ marker notation. The positions of Gp-9, BAC probes and the extent of the non-recombining region in Gp-9Bb queens are indicated. Genetic maps for all seven families are in Supplementary Figs 1–7 and precise genetic and physical positions of genetic markers are in Supplementary Tables 8–14. LG, linkage group. b, BAC-FISH identifies an inversion between the SB and Sb social chromosomes. Social chromosomes from a Gp-9B haploid male (SB chromosome, left) and Gp-9b haploid male (Sb chromosome, right). The bottom panel shows a schematic interpretation of hybridization patterns as well as BAC positions on the SB genetic map. Images with all chromosomes of the respective cells are in Supplementary Fig. 8. c, BAC-FISH on full chromosome complement from one cell of a diploid Gp-9Bb female (SB/Sb chromosomes). Both orientations corresponding to SB (arrow) and Sb (arrowhead) can be observed. Magnified views of respective social chromosomes are on right. Chromosomes are counterstained with 4′,6-diamidino-2-phenylindole (DAPI; white) and hybridized with fluorescently labelled BAC probes: A22 (red, b), E17 (green, b, c) and E03 (blue, b, c). Scale bars, 5μm.

  2. Expression of genes associated with Gp-9 genotype are overrepresented on the social chromosome.
    Figure 2: Expression of genes associated with Gp-9 genotype are overrepresented on the social chromosome.

    The outer circle depicts the S. invicta chromosome ideograms. The social chromosome (S) is subdivided into the non-recombining (orange) and recombining (tan) regions. Genes differentially expressed between individuals of alternative Gp-9 genotypes in mature adult workers25, young adult queens and male pupae are plotted as squares according to their genomic location. The relative expression level (log2-transformed) of Gp-9BB to Gp-9Bb (worker and queens) or Gp-9B to Gp-9b (male) is also indicated, with squares closer to the circle centre having greater expression in Gp-9BB or Gp-9B individuals. Colours highlight direction of gene expression: green, expression in Gp-9BB (or Gp-9B) > Gp-9Bb (or Gp-9b); and purple, reversed. ***P<0.001, hypergeometric test.

  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.
    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.

    Box-and-whisker plots of scaffold lengths: the top and bottom of the box are the first and third quartiles, respectively; the horizontal bar within the box is median; whiskers extend from the box to the most extreme scaffold length within 1.5× of the interquartile range of the box; data beyond the whiskers are outliers and plotted as points. Tukey’s honestly significant difference (HSD) comparisons among groups marked (1) are non-significant (P>0.05), the comparison between (1) and (3) is significant (P<10−7), and the comparison between (2) and (3) is also significant (P<10−4).

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Author information

  1. These authors contributed equally to this work.

    • John Wang &
    • Yannick Wurm

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

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 financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

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).

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