Simola, Daniel F.3; Wissler, Lothar13; Donahue, Greg3; Waterhouse, Robert M.14; Helmkampf, Martin6; Roux, Julien15; Nygaard, Sanne16; Glastad, Karl M.8; Hagen, Darren E.9; Viljakainen, Lumi17; Reese, Justin T11; Hunt, Brendan G11; Graur, Dan11; Elhaik, Eran11; Kriventseva, Evgenia V11; Wen, Jiayu18; Parker, Brian John19; Cash, Elizabeth11; Privman, Eyal11; Childers, Christopher P11; Muñoz-Torres, Monica C11; Boomsma, Jacobus Jan16; Bornberg-Bauer, Erich11; Currie, Cameron R11; Elsik, Christine G11; Suen, Garret11; Goodisman, Michael A D11; Keller, Laurent11; Liebig, Jürgen11; Rawls, Alan11; Reinberg, Danny11; Smith, Chris D11; Smith, Chris R11; Tsutsui, Neil11; Wurm, Yannick11; Zdobnov, Evgeny M11; Berger, Shelley L11; Gadau, Jürgen11
1 Ecology and Evolution, Department of Biology, Faculty of Science, Københavns Universitet2 Computational and RNA Biology, Department of Biology, Faculty of Science, Københavns Universitet3 University of Pennsylvania4 University of Munster5 University of Geneva6 Arizona State University7 University of Lausanne8 Georgia Institute of Technology9 Georgetown University10 University of Oulu11 unknown12 Department of Mathematical Sciences, Faculty of Science, Københavns Universitet13 University of Munster14 University of Geneva15 University of Lausanne16 Ecology and Evolution, Department of Biology, Faculty of Science, Københavns Universitet17 University of Oulu18 Computational and RNA Biology, Department of Biology, Faculty of Science, Københavns Universitet19 Department of Mathematical Sciences, Faculty of Science, Københavns Universitet
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.
Genome Research, 2013, Vol 23, Issue 8, p. 1235-1247