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Social Insects: Are Ants Just Wingless Bees?

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Social Insects: Are Ants Just Wingless Bees? Dispatch R1011 11. Wu, Y., Vendome, J., Shapiro, L., Ben-Shaul, A., 13. Scott, J.A., Shewan, A.M., den Elzen, N.R., in the establishment of epithelial cell polarity and Honig, B. (2011). Transforming binding Loureiro, J.J., Gertler, F.B., and Yap, A.S. (2006). in Drosophila. J. Cell Biol. 167, 135–147. affinities from three dimensions to two with Ena/VASP proteins can regulate distinct modes application to cadherin clustering. Nature 475, of actin organization at cadherin-adhesive 510–513. contacts. Mol. Biol. Cell 17, 1085–1095. Department of Chemistry, University of 12. Shewan, A.M., Maddugoda, M., Kraemer, A., 14. Nagafuchi, A., Ishihara, S., and Tsukita, S. Illinois, 127 RAL, Box C-3, 600 South Stehbens, S.J., Verma, S., Kovacs, E.M., and (1994). The roles of catenins in the Mathews Avenue, Urbana IL 61801, USA. Yap, A.S. (2005). Myosin 2 is a key Rho cadherin-mediated cell adhesion: functional E-mail: [email protected] kinase target necessary for the local analysis of E-cadherin-alpha catenin fusion concentration of E-cadherin at molecules. J. Cell Biol. 127, 235–245. cell-cell contacts. Mol. Biol. Cell 16, 15. Harris, T.J., and Peifer, M. (2004). Adherens 4531–4542. junction-dependent and -independent steps http://dx.doi.org/10.1016/j.cub.2013.10.018 Social Insects: Are Ants Just Aculeata, and these studies have been based on a relatively small number of Wingless Bees? ‘standard’ phylogenetic markers [13,14]. No previous studies have attempted to analyze aculeate relationships based on New phylogenomic analyses suggest that ants and Apoidea (hunting wasps much larger transcriptomic or genomic and bees) are more closely related than we had previously believed. level data sets. Phylogenomics — the application Bryan N. Danforth evolutionary history of eusociality in the of large-scale (transcriptomic or group as a whole. genomic) data sets to phylogeny Wasps, bees, and ants — the stinging Before molecular data were used to reconstruction — has the potential to Hymenoptera — are an extraordinarily derive phylogenetic tress for wasps, revolutionize the way we do important group for understanding bees and ants — i.e. before the early phylogenetic studies. Rather than the evolutionary history of eusociality, 1990s — the predominant view was that analyze a small set of previously its origins and its loss. eusociality in Hymenoptera had arisen defined genes, high-throughput Eusociality — typically defined by the frequently (i.e., tens to hundreds of sequencing methods allow for more combination of overlapping times) across Aculeata. However, expansive coverage of mitochondrial generations, cooperative brood care, subsequent molecular phylogenetic genomes, expressed genes, conserved and reproductive division of labor — is studies have suggested a contrary view: regions of whole genomes, and whole a remarkable evolutionary innovation. eusociality has arisen rarely in bees and genomes [15–19]. Phylogenomic Some individuals, the workers, forego wasps, but reversals from eusociality studies can be based on hundreds to their own direct reproduction to serve back to solitary nesting are thousands of genes. While these as nurses, guards, foragers and common — rather than frequent origins methods have enormous potential for caretakers for the offspring of a single explaining the diversity of social phylogenetic analysis, they also pose reproductive individual, the queen. behavior, frequent losses of eusociality some serious challenges. Assembly Eusociality in Hymenoptera is (or reversals to solitary nesting) provide and annotation of non-model genomes restricted to stinging wasps, ants and much of the variation in sociality among can be difficult. Determining which bees, the groups referred to as closely related taxa. Eusociality has genes are true orthologues when ‘Aculeata’. Eusocial taxa in Aculeata been repeatedly lost in clades of conducting multiple alignments in include the ants (Formicidae [1]), ancestrally eusocial halictine bees [9], non-model organisms can also vespid wasps (Stenogastrinae, and reversals appear to be associated introduce problems in downstream Vespinae and Polistinae [2]), certain with species and populations at high analysis. Finally, such methods tend to bee groups (Allodapini, Halictinae, and elevations or latitudes [7].Recent put substantial limits on taxon corbiculate Apidae [3]), and studies of tribal relationships in the sampling, which we know is key to Microstigmus wasps (Crabronidae: largely social Xylocopinae (carpenter accurate phylogenetic resolution. Pemphredoninae [4]). A significant and allodapine bees) [11] have also Johnson and co-authors [10] apply amount of work has focused on supported the hypothesis of a reversal combined genomic and transcriptomic understanding phylogenetic to solitary nesting in one of the four data to the higher-level phylogeny of relationships within these diverse xylocopine tribes: Manueliini. And Aculeata. Their data set is derived from eusocial lineages [3,5–9] because recent molecular studies of corbiculate previously published genomes of three phylogenies provide an essential bees (honey bees and their relatives) bee and three ant species, plus de novo framework for inferring the evolutionary have indicated that the weakly social transcriptome data for ten additional history of eusociality. A recent study in orchid bees are likely derived from a taxa spanning nine aculeate wasp Current Biology by Johnson et al. [10], primitively eusocial ancestor [12].While families. The published genome of the based on a massive data set of phylogenetic studies have primarily parasitic wasp Nasonia vitripennis was transcriptomes and whole genomes, been carried out on eusocial groups, used as an outgroup. Based on provides some remarkable new such as Vespidae, Xylocopinae, bioinformatic analysis of the insights into the relationships among Halictinae, and corbiculate Apidae, few transcriptome and genome data, they the major branches of the aculeate tree studies have tackled the higher-level obtained multiple partitioned amino of life, and thus sheds light on the relationships among the major clades of acid matrices ranging from 300 genes Current Biology Vol 23 No 22 R1012 (over 175,000 amino acid sites) to over provisioning, and central-place foraging Anthophila: Halictidae). Mol. Phylo. Evol. 65, 926–939. 5000 genes (over 3 million amino acid have been identified as potential 10. Johnson, B.R., Borowiec, M.L., Chiu, J.C., sites). Based on partitioned maximum prerequisites for the evolutionary origins Lee, E.K., Atallah, J., and Ward, P.S. (2013). likelihood and Bayesian analyses of of eusociality — a view supported by Phylogenomics resolves evolutionary relationships among ants, bees, and wasps. their data sets, they obtained a strongly Johnson et al.’s [10] analysis. While the Curr. Biol. 23, 2058–2062. supported tree (all nodes are supported new phylgenomic results contradict 11. Rehan, S.M., Leys, R., and Schwarz, M.P. (2012). A Mid-Cretaceous origin of sociality in by 100% likelihood bootstrap values previous molecular and morphological xylocopine bees with only two origins of true and a posterior probability of 1.0). All studies in terms of the affinities of ants worker castes indicates severe barriers to analyses supported a novel result: ants and Apoidea, a recently described fossil eusociality. PLoS ONE 7, e34690. 12. Cardinal, S., and Danforth, B.N. (2011). The and Apoidea — the clade that includes [10] that has been alternatively placed in antiquity and evolutionary history of social four solitary hunting wasp families plus the ants and the basal Apoidea behavior in bees. PLoS ONE 6, e21086. 13. Pilgrim, E.M., von Dohlen, C.D., and Pitts, J.P. the bees — are sister groups. Previous (Ampulicidae) might suggest that ants (2008). Molecular phylogenetics of Vespoidea studies, based on both morphology [20] and Apoidea are more closely related indicate paraphyly of the superfamily and novel and molecular data [13,14] had than we had previously believed. This relationships of its component families and subfamilies. Zool. Scr. 37, 539–560. suggested that ants were more might just be a case where fossils and 14. Debevec, A.H., Cardinal, S., and Danforth, B.N. closely related to ectoparasitic wasps genomes converge on the same radical, (2012). Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an (such as Scoliidae, Tiphiidae, and anti-establishment view of aculeate emphasis on the superfamily Apoidea. Zool. Bradynobaenidae) than to the clade that phylogeny. Scr. 41, 527–535. includes hunting wasps and bees 15. Simon, S., and Hadrys, H. (2013). A comparative analysis of complete mitochondrial genomes (Apoidea). Johnson and co-authors’ References among. Hexapoda. Mol. Phylo. Evol. 69, analysis [10] suggests otherwise. 1. Ho¨ lldobler, B., and Wilson, E.O. (1990). The 393–403. Apoidea (including hunting wasps in the Ants (Cambridge: Harvard Univ. Press). 16. Hittinger, C.T., Johnson, M., Tossberg, J.T., 2. Ross, K.G., and Matthews, R.W. (1991). The and Rokas, A. (2010). Leveraging skewed families Heterogynaeidae, Ampulicidae, Social Biology of Wasps (Ithaca and London: transcript abundance by RNA-Seq to increase Sphecidae, and Crabronidae, plus bees) Comstock Publishing Associates). the genomic depth of the tree of life. Proc. Natl. 3. Danforth, B.N., Cardinal, S.C., Praz, C., Acad. Sci. USA 107, 1476–1481. and Formicidae appear to be sister Almeida, E., and Michez, D. (2013). Impact of 17. Lemmon, A.R., Emme, S.A., and Lemmon, E.M. groups. Likelihood-based
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