Specialized queens and life-time unmated workers evolved once in the common ancestor of all ants, but whether caste development across ants continues to be at least partly regulated by a single core set of genes remains obscure. We analysed brain transcriptomes from five ant species (three subfamilies) and reconstructed the origins of genes with caste-biased expression. Ancient genes predating the Neoptera were more likely to regulate gyne (virgin queen) phenotypes, while the caste differentiation roles of younger, ant-lineage-specific genes varied. Transcriptome profiling showed that the ancestral network for caste-specific gene regulation has been maintained, but that signatures of common ancestry are obscured by later modifications. Adjusting for such differences, we identified a core gene-set that: (1) consistently displayed similar directions and degrees of caste-differentiated expression; and (2) have mostly not been reported as being involved in caste differentiation. These core regulatory genes exist in the genomes of ant species that secondarily lost the queen caste, but expression differences for reproductive and sterile workers are minor and similar to social paper wasps that lack differentiated castes. Many caste-biased ant genes have caste-differentiated expression in honeybees, but directions of caste bias were uncorrelated, as expected when permanent castes evolved independently in both lineages.
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RNA-Seq data have been deposited under BioProject accession number PRJNA427677 (https://www.ncbi.nlm.nih.gov/sra/SRP127971).
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Wheeler, W. M. The ant‐colony as an organism. J. Morphol. 22, 307–325 (1911).
Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120–1125 (2013).
Boomsma, J. J. & Gawne, R. Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation. Biol. Rev. 93, 28–54 (2018).
Ward, P. S. Ants. Curr. Biol. 16, R152–R155 (2006).
Gould, S. J. Ontogeny and Phylogeny (Harvard Univ. Press, Cambridge, 1977).
Wagner, G. P. Homology, Genes, and Evolutionary Innovation (Princeton Univ. Press, Princeton, 2014).
Simola, D. F. et al. Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 23, 1235–1247 (2013).
Morandin, C. et al. Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants. Genome Biol. 17, 1 (2016).
Toth, A. L. & Robinson, G. E. Evo-devo and the evolution of social behavior. Trends Genet. 23, 334–341 (2007).
Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008).
Arendt, D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868–882 (2008).
Barchuk, A. R. et al. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev. Biol. 7, 70 (2007).
Johnson, B. R. & Tsutsui, N. D. Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. BMC Genomics 12, 164 (2011).
Feldmeyer, B., Elsner, D. & Foitzik, S. Gene expression patterns associated with caste and reproductive status in ants: worker‐specific genes are more derived than queen‐specific ones. Mol. Ecol. 23, 151–161 (2014).
Sumner, S. The importance of genomic novelty in social evolution. Mol. Ecol. 23, 26–28 (2014).
Johnson, B. R. & Linksvayer, T. A. Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q. Rev. Biol. 85, 57–79 (2010).
Ding, Y., Zhou, Q. & Wang, W. Origins of new genes and evolution of their novel functions. Annu. Rev. Ecol. Evol. Syst. 43, 345–363 (2012).
Chen, S., Krinsky, B. H. & Long, M. New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 14, 645–660 (2013).
Warner, M. R., Mikheyev, A. S. & Linksvayer, T. A. Genomic signature of kin selection in an ant with obligately sterile workers. Mol. Biol. Evol. 34, 1780–1787 (2016).
Ward, P. S. The phylogeny and evolution of ants. Annu. Rev. Ecol. Evol. Syst. 24, 2047–2052 (2014).
Mank, J. E. The transcriptional architecture of phenotypic dimorphism. Nat. Ecol. Evol. 1, 0006 (2017).
Libbrecht, R., Oxley, P. R. & Keller, D. J. C. Robust DNA methylation in the clonal raider ant brain. Curr. Biol. 26, 391–395 (2016).
Wagner, G. P. The developmental genetics of homology. Nat. Rev. Genet. 8, 473–479 (2007).
Brawand, D. et al. The evolution of gene expression levels in mammalian organs. Nature 478, 343–348 (2011).
Roux, J., Rosikiewicz, M. & Robinson-Rechavi, M. What to compare and how: comparative transcriptomics for evo‐devo. J. Exp. Zool. B Mol. Dev. Evol. 324, 372–382 (2015).
Lucas, E. R., Romiguier, J. & Keller, L. Gene expression is more strongly influenced by age than caste in the ant Lasius niger. Mol. Ecol. 25, 5058–5073 (2017).
Patalano, S. et al. Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies. Proc. Natl Acad. Sci. USA 112, 13970–13975 (2015).
Monnin, T., Ratnieks, F., Jones, G. R. & Beard, R. Pretender punishment induced by chemical signalling in a queenless ant. Nature 419, 61–65 (2002).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 15, 550 (2014).
Frumhoff, P. C. & Ward, P. S. Individual-level selection, colony-level selection, and the association between polygyny and worker monomorphism in ants. Am. Nat. 139, 559–590 (1992).
Schwander, T., Rosset, H. & Chapuisat, M. Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav. Ecol. Sociobiol. 59, 215–221 (2005).
Trible, W. & Kronauer, D. J. C. Caste development and evolution in ants: it’s all about size. J. Exp. Biol. 220, 53–62 (2017).
Nygaard, S. et al. Reciprocal genomic evolution in the ant–fungus agricultural symbiosis. Nat. Commun. 7, 12233 (2016).
Monnin, T. & Peeters, C. How many gamergates is an ant queen worth? Naturwissenschaften 95, 109–116 (2007).
Cronin, A. L., Molet, M., Doums, C., Monnin, T. & Peeters, C. Recurrent evolution of dependent colony foundation across eusocial insects. Annu. Rev. Entomol. 58, 37–55 (2013).
Heinze, J. The demise of the standard ant (Hymenoptera: Formicidae). Myrmecol. News 11, 9–20 (2008).
Rabeling, C. & Kronauer, D. J. C. Thelytokous parthenogenesis in eusocial Hymenoptera. Annu. Rev. Entomol. 58, 273–292 (2013).
Luo, W., Friedman, M. S., Shedden, K., Hankenson, K. D. & Woolf, P. J. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinform 10, 161 (2009).
Peters, R. S. et al. Evolutionary history of the Hymenoptera. Curr. Biol. 27, 1013–1018 (2017).
Corona, M. et al. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl Acad. Sci. 104, 7128–7133 (2007).
Vleurinck, C., Raub, S., Sturgill, D., Oliver, B. & Beye, M. Linking genes and brain development of honeybee workers: a whole-transcriptome approach. PLoS ONE 11, e0157980 (2016).
LaPolla, J. S., Dlussky, G. M. & Perrichot, V. Ants and the fossil record. Annu. Rev. Entomol. 58, 609–630 (2013).
Barden, P. & Grimaldi, D. A. Adaptive radiation in socially advanced stem-group ants from the Cretaceous. Curr. Biol. 26, 515–521 (2016).
Peeters, C. in The Evolution of Social Behaviour in Insects and Arachnids (eds Crespi, B. J. & Choe, J. C.) 372–391 (Cambridge Univ. Press, Cambridge, 1997).
Girardie, J., Boureme, D., Couillaud, F., Tamarelle, M. & Girardie, A. Anti-juvenile effect of neuroparsin A, a neuroprotein isolated from locust corpora cardiaca. Insect Biochem. 17, 977–983 (1987).
Toth, A. L. et al. Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proc. R. Soc. B 277, 2139–2148 (2010).
Mikheyev, A. S., Linksvayer, T. A. & Khaitovich, P. Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns. eLife 4, e04775 (2015).
Pantalacci, S. et al. Transcriptomic signatures shaped by cell proportions shed light on comparative developmental biology. Genome Biol. 18, 29 (2017).
Romiguier, J. et al. Phylogenomics controlling for base compositional bias reveals a single origin of eusociality in corbiculate bees. Mol. Biol. Evol. 33, 670–678 (2016).
Pontieri, L., Schmidt, A. M., Singh, R., Pedersen, J. S. & Linksvayer, T. A. Artificial selection on ant female caste ratio uncovers a link between female‐biased sex ratios and infection by Wolbachia endosymbionts. J. Evol. Biol. 30, 225–234 (2017).
Conesa, A. et al. A survey of best practices for RNA-Seq data analysis. Genome Biol. 17, 13 (2016).
Keilwagen, J. et al. Using intron position conservation for homology-based gene prediction. Nucleic Acids Res. 44, e89 (2016).
Lechner, M. et al. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinform. 12, 124 (2011).
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
Bourgon, R., Gentleman, R. & Huber, W. Independent filtering increases detection power for high-throughput experiments. Proc. Natl Acad. Sci. USA 107, 9546–9551 (2010).
Bolstad, B. M., Irizarry, R. A., Åstrand, M. & Speed, T. P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 107, 9546–9551 (2003).
Leek, J. T. svaseq: removing batch effects and other unwanted noise from sequencing data. Nucleic Acids Res. 42, e161 (2014).
Efron, B. in Breakthroughs in Statistics (eds Kotz, S. & Johnson, N. L.) 569–593 (Springer, New York, 1992).
Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B. & Pierce, N. E. Phylogeny of the ants: diversification in the age of angiosperms. Science 312, 101–104 (2006).
Ward, P. S., Brady, S. G., Fisher, B. L. & Schultz, T. R. The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst. Entomol. 40, 61–81 (2015).
This work was supported by grants from the Lundbeck Foundation (R190-2014-2827 to G.Z.), Carlsberg Foundation (CF16-0663 to G.Z.), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13000000 to G.Z.) and Biodiversity Research Center, Academia Sinica (100-2311-B-001-015-MY3, 103-2311-B-001-018-MY3 and 104-2314-B-001-009-MY5 to J.W.), as well as an Academia Sinica Career Development Grant (to J.W.) and an ERC Advanced Grant (323085 to J.J.B.). We thank C. Guo, H. Yu and Q. Li for coordination of the sequencing at BGI.
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Nature Ecology & Evolution (2018)