title: A depauperate immune repertoire precedes evolution of sociality in bees.
abstract: BACKGROUND
  Sociality has many rewards, but can also be dangerous, as high population density and low genetic diversity, common in social insects, is ideal for parasite transmission. Despite this risk, honeybees and other sequenced social insects have far fewer canonical immune genes relative to solitary insects. Social protection from infection, including behavioral responses, may explain this depauperate immune repertoire. Here, based on full genome sequences, we describe the immune repertoire of two ecologically and commercially important bumblebee species that diverged approximately 18 million years ago, the North American Bombus impatiens and European Bombus terrestris.
  
  
  RESULTS
  We find that the immune systems of these bumblebees, two species of honeybee, and a solitary leafcutting bee, are strikingly similar. Transcriptional assays confirm the expression of many of these genes in an immunological context and more strongly in young queens than males, affirming Bateman's principle of greater investment in female immunity. We find evidence of positive selection in genes encoding antiviral responses, components of the Toll and JAK/STAT pathways, and serine protease inhibitors in both social and solitary bees. Finally, we detect many genes across pathways that differ in selection between bumblebees and honeybees, or between the social and solitary clades.
  
  
  CONCLUSIONS
  The similarity in immune complement across a gradient of sociality suggests that a reduced immune repertoire predates the evolution of sociality in bees. The differences in selection on immune genes likely reflect divergent pressures exerted by parasites across social contexts.
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. barribeaus14@ecu.edu.|Department of Biology, East Carolina University, Greenville, NC, 27858, USA. barribeaus14@ecu.edu.
authors.forename: Seth M
authors.initials: SM
authors.lastname: Barribeau
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. bmsadd@ilstu.edu.|School of Biological Sciences, Illinois State University, Normal, IL, 61790, USA. bmsadd@ilstu.edu.
authors.forename: Ben M
authors.initials: BM
authors.lastname: Sadd
authors.affiliation: Theoretical Biology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. louis.duplessis@env.ethz.ch.|Computational Evolution, Department of Biosystems Science and Evolution, ETH Zürich, 4058, Basel, Switzerland. louis.duplessis@env.ethz.ch.|Swiss Institute of Bioinformatics, 1211, Lausanne, Switzerland. louis.duplessis@env.ethz.ch.
authors.forename: Louis
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authors.lastname: du Plessis
authors.affiliation: School of Biological Sciences, Royal Holloway University of London, London, TW20 0EX, UK. mark.brown@rhul.ac.uk.
authors.forename: Mark J F
authors.initials: MJ
authors.lastname: Brown
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. severine.buechel@env.ethz.ch.
authors.forename: Severine D
authors.initials: SD
authors.lastname: Buechel
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium. kaat.cappelle@ugent.be.
authors.forename: Kaat
authors.initials: K
authors.lastname: Cappelle
authors.affiliation: Maynooth University Department of Biology, Maynooth University, Maynooth, Kildare, Ireland. james.carolan@nuim.ie.
authors.forename: James C
authors.initials: JC
authors.lastname: Carolan
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium. olchrist.christiaens@ugent.be.
authors.forename: Olivier
authors.initials: O
authors.lastname: Christiaens
authors.affiliation: Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, 2, Ireland. tcolgan@tcd.ie.|School of Biological and Chemical Sciences, Queen Mary University of London, E1 41NS, London, UK. tcolgan@tcd.ie.
authors.forename: Thomas J
authors.initials: TJ
authors.lastname: Colgan
authors.affiliation: Department of Apiculture and Sericulture, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Cluj-Napoca, 400372, Romania. silvio.erler@zoologie.uni-halle.de.|Institut für Biologie, Molekulare Ökologie, Martin-Luther-Universität Halle-Wittenberg, Wittenberg, 06120, Germany. silvio.erler@zoologie.uni-halle.de.
authors.forename: Silvio
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authors.affiliation: USDA-ARS Bee Research Laboratory, Beltsville, MD, 20705, USA. jay.evans@ars.usda.gov.
authors.forename: Jay
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authors.lastname: Evans
authors.affiliation: Institut für Biologie, Molekulare Ökologie, Martin-Luther-Universität Halle-Wittenberg, Wittenberg, 06120, Germany. sophie.helbing@zoologie.uni-halle.de.
authors.forename: Sophie
authors.initials: S
authors.lastname: Helbing
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. elke.karaus@env.ethz.ch.
authors.forename: Elke
authors.initials: E
authors.lastname: Karaus
authors.affiliation: Institut für Biologie, Molekulare Ökologie, Martin-Luther-Universität Halle-Wittenberg, Wittenberg, 06120, Germany. lattorff@zoologie.uni-halle.de.|German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 04103, Leipzig, Germany. lattorff@zoologie.uni-halle.de.|Institut für Biologie, Tierphysiologie, Martin-Luther-Universität Halle-Wittenberg, Wittenberg, 06099, Germany. lattorff@zoologie.uni-halle.de.
authors.forename: H Michael G
authors.initials: HM
authors.lastname: Lattorff
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. monika.marxer@env.ethz.ch.
authors.forename: Monika
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authors.lastname: Marxer
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium. ivan.meeus@ugent.be.
authors.forename: Ivan
authors.initials: I
authors.lastname: Meeus
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. kathrin.naepflin@env.ethz.ch.
authors.forename: Kathrin
authors.initials: K
authors.lastname: Näpflin
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium. jinzhi.niu@ugent.be.|College of Plant Protection, Southwest University, Chongqing, 400716, PR China. jinzhi.niu@ugent.be.
authors.forename: Jinzhi
authors.initials: J
authors.lastname: Niu
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. regula.schmid@env.ethz.ch.
authors.forename: Regula
authors.initials: R
authors.lastname: Schmid-Hempel
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, 9000, Ghent, Belgium. guy.smagghe@ugent.be.|College of Plant Protection, Southwest University, Chongqing, 400716, PR China. guy.smagghe@ugent.be.
authors.forename: Guy
authors.initials: G
authors.lastname: Smagghe
authors.affiliation: Swiss Institute of Bioinformatics, 1211, Lausanne, Switzerland. robert.waterhouse@unige.ch.|Department of Genetic Medicine and Development, University of Geneva Medical School, 1211, Geneva, Switzerland. robert.waterhouse@unige.ch.|Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA. robert.waterhouse@unige.ch.|The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA. robert.waterhouse@unige.ch.
authors.forename: Robert M
authors.initials: RM
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authors.forename: Na
authors.initials: N
authors.lastname: Yu
authors.affiliation: Swiss Institute of Bioinformatics, 1211, Lausanne, Switzerland. evgeny.zdobnov@unige.ch.|Department of Genetic Medicine and Development, University of Geneva Medical School, 1211, Geneva, Switzerland. evgeny.zdobnov@unige.ch.
authors.forename: Evgeny M
authors.initials: EM
authors.lastname: Zdobnov
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, ETH Zürich, CH-8092, Zürich, Switzerland. paul.schmid-hempel@env.ethz.ch.
authors.forename: Paul
authors.initials: P
authors.lastname: Schmid-Hempel
mesh_terms: D000818:Animals; D001516:Bees / Q000145:classification / Q000235:genetics* / Q000276:immunology*; D001522:Behavior, Animal; D019143:Evolution, Molecular; D005260:Female; D005786:Gene Expression Regulation; D017344:Genes, Insect; D014644:Genetic Variation; D008297:Male; D012641:Selection, Genetic; D012919:Social Behavior