International Union for the Study of Social Insects (IUSSI2018), August 5-10, 2018 in Guarujá, Brazil.

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Comparative transcriptomics reveals the ancestral brain gene-network regulating caste differentiation in ants

Author(s):
Bitao Qiu, Bitao Qiu , Rasmus Stenbak Larsen , Ni-Chen Chang , John Wang , Jacobus J. Boomsma , Guojie Zhang
Institution(s):
Centre for Social Evolution, Department of Biology, University of Copenhagen, Denmark; Centre for Social Evolution, Department of Biology, University of Copenhagen, Denmark ; Centre for Social Evolution, Department of Biology, University of Copenhagen, Denmark ; Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan ; Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan ; Centre for Social Evolution, Department of Biology, University of Copenhagen, Denmark ; Centre for Social Evolution, Department of Biology, University of Copenhagen, Denmark; China National GeneBank, BGI-Shenzhen, China;State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, China
A superorganismal caste system with physically differentiated queens (inseminated) and workers (life-time-unmated) originated only once in the common ancestor of all ants. This implies that caste-specific gene-expression should have retained homologous ancestral characteristics, but the identity of the genetic regulatory network (GRN) reflecting the origin of superorganismality in ants has remained obscure. We analysed the caste-specific brain transcriptomes of five ant species from three subfamilies and show that the ancestral network for caste-specific gene regulation has indeed been maintained, but that signatures of common ancestry are obscured by later lineage-specific modifications. Adjusting for such differences, we identified a core set of genes that consistently display similar directions and degrees of caste-differentiated expression across ant species. Most of these genes have not been reported before as being involved in caste differentiation. We also show that these core caste-regulatory genes continue to exist in the genomes of two ant species that secondarily lost the queen caste, but that their expression differences in reproductive and sterile phenotypes are minor and similar to expression differences between egg-laying and sterile females of paper wasps where differentiated castes never evolved. Many of the core caste-regulating genes of ants also have caste-differentiated expression in the honeybee, but the directions of caste-expression-bias of these genes between ants and honeybees are uncorrelated. This is consistent with both lineages having used overlapping sets of toolkit genes to independently evolve irreversible transitions to superorganismality with a specialized fertile queen caste and a life-time unmated worker caste. 
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