Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

  1. Jürgen Gadau5,24
  1. 1Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA;
  2. 2University of Pennsylvania Epigenetics Program, Philadelphia, Pennsylvania 19104, USA;
  3. 3Institute for Evolution and Biodiversity, University of Münster, 48149 Münster, Germany;
  4. 4Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland;
  5. 5School of Life Sciences, Arizona State University, Tempe, Arizona 85287, USA;
  6. 6Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland;
  7. 7Centre for Social Evolution, University of Copenhagen, 2100 Copenhagen, Denmark;
  8. 8School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA;
  9. 9Department of Biology, Georgetown University, Washington, DC 20057, USA;
  10. 10Department of Biology, University of Oulu, 3000 Oulu, Finland;
  11. 11Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204, USA;
  12. 12The Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland 21205, USA; The Johns Hopkins University, School of Medicine, Baltimore, Maryland 21205, USA;
  13. 13The Bioinformatics Centre, University of Copenhagen, 2100 Copenhagen, Denmark;
  14. 14Department of Bacteriology, University of Wisconsin–Madison, Madison, Wisconsin 53706, USA;
  15. 15Department of Biochemistry, New York University, New York, New York 10003, USA; Howard Hughes Medical Institute, New York University, New York, New York 10003, USA;
  16. 16Center for Computing for Life Science, San Francisco State University, San Francisco, California 94117, USA;
  17. 17Department of Biology, Earlham College, Richmond, Indiana 47374, USA;
  18. 18Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720, USA;
  19. 19Department of Biology and Department of Genetics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA

    1. ↵20 These authors contributed equally to this work.

    • ↵Present addresses: 21Department of Human Genetics, University of Chicago, Chicago, IL 60637, USA;

    • ↵22 Divisions of Animal and Plant Sciences, University of Missouri, Columbia, MO 65211, USA;

    • ↵23 School of Biology & Chemistry, Queen Mary University of London, London E1 4NS, UK.

    Abstract

    Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor–binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the “socio-genomes” of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.

    Footnotes

    • Received January 24, 2013.
    • Accepted April 24, 2013.

    This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.

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    1. Published in Advance May 1, 2013, doi: 10.1101/gr.155408.113 Genome Res. 23: 1235-1247 © 2013, Published by Cold Spring Harbor Laboratory Press

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