BJ Fischman

BM Sadd

EO Wilson

J Maynard Smith

J Roux

Laurent Keller

N Terrapon

P Christe

R Libbrecht

Romain Libbrecht

S Cremer

SM Barribeau

English

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Libbrecht and Keller Genome Biology  (2015) 16:75 DOI 10.1186/s13059-015-0635-zRESEARCH HIGHLIGHTThe making of eusociality: insights from twobumblebee genomesRomain Libbrecht1,2* and Laurent Keller1AbstractThe genomes of two bumblebee species characterizedby a lower level of sociality than ants and honeybeesprovide new insights into the origin and evolution ofinsect societies.The comparison of the honeybee and bumblebeegenomesBumblebees enter the genomic eraIn 1995, John Maynard Smith and Eörs Szathmáry classi-fied the transition from solitary to social life as one of themajor transitions in evolution, along with the transitionsfrom prokaryotes to eukaryotes, and from asexual tosexual reproduction [1]. The highest level of social orga-nization is found in eusocial insects (for example, ants,termites and some bees and wasps) that are characterizedby societies with overlapping generations, cooperativebrood care and the coexistence of fertile queens and func-tionally sterile workers [2]. It is common to differentiatetwo categories of eusociality: primitive eusociality, wherequeens are morphologically similar to workers, and ad-vanced eusociality, where queens and workers follow adifferent developmental pathway, resulting in marked dif-ferences between adults.Since the publication of the genome of the honeybeeApis mellifera in 2006, the genomes of two other honey-bee and nine ant species have been sequenced. Thesevaluable genomic resources provided insights into seve-ral key features of eusocial Hymenoptera, including thedevelopmental processes leading to queen and workercaste differentiation, division of labor, chemical commu-nication and immunity [3]. However, because honeybeesand ants show advanced eusociality, it has so far notbeen possible to investigate the molecular changes asso-ciated with the early stages of the evolution of social life.In this issue of Genome Biology, Sadd and colleagues[4] and Barribeau and colleagues [5] present and analyze* Correspondence: romain.libbrecht@gmail.com1Department of Ecology and Evolution, University of Lausanne, CH-1015,Lausanne, Switzerland2Rockefeller University, 1230 York Avenue, New York, NY 10065, USA© 2015 Libbrecht and Keller; licensee BioMedCreative Commons Attribution License (http:/distribution, and reproduction in any mediumDomain Dedication waiver (http://creativecomarticle, unless otherwise stated.the genomes of two bumblebee species - Bombus ter-restris and Bombus impatiens. These two primitivelyeusocial species are particularly interesting because theyshare a primitively eusocial ancestor with the honeybees.The honeybees and bumblebees belong to the Apidae, agroup of insects that are important pollinators and pos-sess a similar diet. However, these taxa exhibit markeddifferences in their life history and social organization.Honeybee colonies are perennial, typically containingtens of thousands of workers that cannot mate and aremorphologically different from the queen heading thecolonies. By contrast, bumblebees have a yearly cycle,with an overwintering queen starting a colony in spring.By the end of the season, when colonies can contain upto a few hundreds of workers at most, new queens andmales are produced. Bumblebee workers are usuallysmaller than the queen, but they are not morphologicallydifferent, and they can, in principle, mate.The comparison of the genomes of B. terrestris and B.impatiens revealed strong similarity. In particular, thegenetic architecture is very conserved, with high syntenyand less than 10 chromosomal rearrangements. This isstriking because these two species diverged 18 millionyears ago, and bumblebees are known for their high rateof recombination. The genomes of the honeybee andbumblebees were also found to share many similarities.They are all characterized by a low number and lowdiversity of repetitive elements, similar developmentalgene repertoire, biogenic amines and neuropeptide suite,a reduced set of detoxification enzymes, a similar num-ber of odorant and ionotropic receptor genes, and asimilar DNA methylation machinery.Despite these similarities, fine differences exist bet-ween the honeybee and bumblebees. Bumblebees show arecent expansion of gustatory receptor genes and achange in domain repeat numbers for proteins that havefunctions related to muscles, which could be associatedCentral. This is an Open Access article distributed under the terms of the/creativecommons.org/licenses/by/4.0), which permits unrestricted use,, provided the original work is properly credited. The Creative Commons Publicmons.org/publicdomain/zero/1.0/) applies to the data made available in thisLibbrecht and Keller Genome Biology  (2015) 16:75 Page 2 of 2with differences between honeybees and bumblebees intaste detection and muscle use during flight, respec-tively. The bumblebee genome contains two genes codingfor proteins that bind to juvenile hormone (JH) that donot have orthologs in the honeybee. This finding is inte-resting because the JH signaling pathway plays a key rolein regulating division of labor in eusocial Hymenoptera.Known to affect reproduction in solitary insects, JH mighthave been co-opted to regulate the behavior of sterileworkers in advanced eusocial species such as the honey-bee. Finally, there were many more microRNAs in thehoneybee than in the bumblebees. This is exciting becausemicroRNAs are involved in the regulation of many aspectsof the honeybee social life. Whether those differences areactually associated with advanced eusociality remains tobe investigated.Social and individual immunity in beesInsect societies are usually characterized by high popula-tion density, frequent social contacts and high relatedness,which should make them particularly good targets for thespread of pathogens. However, eusocial insects haveevolved a suite of collective defenses, known as social im-munity, that comprise both prophylactic and activatedmeasures to protect themselves against pathogens. Suchmeasures include mechanical removal of parasites bygrooming, avoidance of infected individuals, waste man-agement and any behavior enhancing nest hygiene ingeneral [6]. A famous example is found in wood ants thatincorporate conifer resin into their nest, thus using theantimicrobial properties of the resin as a means of defenseagainst pathogenic microorganisms [7].The sequencing of the honeybee genome revealed a lownumber of immunity genes compared with the numberpresent in the fly and mosquito genomes. This led earlierauthors to suggest that social immunity might have de-creased the selective pressure on individual immunity,resulting in less immunity genes either by gene loss orlimited gene duplication. While this hypothesis has beensupported by the finding of a similarly small immune generepertoire in ant genomes, it has later been challenged byfurther genomic studies. First, a recent study showed noevidence for relaxed selection (as expected if social im-munity had reduced the selection pressure) on the im-mune gene repertoire in honeybees and ants [8]. Second,the genomes of the solitary wasp Nasonia vitripennis andthe solitary pea aphid Acyrtosiphon pisum also have a lownumber of immune genes, suggesting an expansion of theimmune gene repertoire in flies and mosquitoes ratherthan a reduction in the eusocial honeybees and ants [9].According to this hypothesis, a small repertoire of im-mune genes would be ancestral to eusociality.The genomes of the bumblebees provided Barribeauand colleagues [5] with the opportunity to test thisprediction in the bee lineage. They compared the sets ofimmunity genes across the advanced eusocial honeybee,the intermediate eusocial bumblebee and a solitary beethat diverged from the ancestor of honeybees and bum-blebees before it evolved eusociality. As expected, if thelow number of immune genes was the ancestral state,Barribeau et al. found comparable low numbers of im-munity genes, irrespective of the complexity of socialorganization. Thus, this result shows that, in the beelineage, the limited number of immunity genes is not aconsequence of, but rather predates, the evolution ofeusociality.Concluding remarksExciting times lie ahead for biologists interested in theorigin of eusociality, which evolved at least 10 times ininsects. There are a minimum of nine independent ori-gins of eusociality in Hymenoptera (five times in diffe-rent bee lineages, three times in different wasp lineagesand once in ants) and one in Isoptera (which gave riseto termites). The recent sequencing of a termite genome[10], as well as the imminent publication of a wasp gen-ome, give the opportunity to study two additional originsof eusociality in insects. It has been almost a decadesince the publication of the first eusocial insect genome,and each additional sequenced genome has been anotherstep towards unveiling the making of eusociality.AbbreviationJH: Juvenile hormone.Competing interestsThe authors declare that they have no competing interests.References1. Maynard Smith J, Szathmary E. The major transitions in evolution. USA:Oxford University Press; 1995.2. Wilson EO. The insect societies. Cambridge, MA: Harvard University Press;1971.3. Libbrecht R, Oxley PR, Kronauer D, Keller L. Ant genomics sheds light on themolecular regulation of social organization. Genome Biol. 2013;14:212.4. Sadd BM, Barribeau SM, Bloch G, de Graaf DC, Dearden P, Elsik CG, et al.The genomes of two key bumblebee species with primitive eusocialorganisation. Genome Biol. 2015;16:623.5. Barribeau SM, Sadd BM, du Plessis L, Brown MJF, Buechel SD, Cappelle K,et al. A depauperate immune repertoire precedes evolution of sociality inbees. Genome Biol. 2015;16:628.6. Cremer S, Armitage SA, Schmid-Hempel P. Social immunity. Curr Biol.2007;17:R693–702.7. Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M. Evidence forcollective medication in ants. Ecol Lett. 2003;6:19–22.8. Roux J, Privman E, Moretti S, Daub JT, Robinson-Rechavi M, Keller L. Patternsof positive selection in seven ant genomes. Mol Biol Evol. 2014;31:1661–85.9. Fischman BJ, Woodard SH, Robinson GE. Molecular evolutionary analyses ofinsect societies. Proc Natl Acad Sci U S A. 2011;108:10847–54.10. Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, et al. Moleculartraces of alternative social organization in a termite genome. Nat Commun.2014;5:3636.

The making of eusociality: insights from two bumblebee genomes

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The making of eusociality: insights from two bumblebee genomes

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