Insectes Sociaux

, Volume 65, Issue 4, pp 593–599 | Cite as

Caste-biased genes in a subterranean termite are taxonomically restricted: implications for novel gene recruitment during termite caste evolution

  • S. Behl
  • T. Wu
  • A. M. Chernyshova
  • G. J. Thompson
Research Article


The caste system of social insects presents a classic polyphenism in which widely divergent reproductive and non-reproductive phenotypes are expressed from the same genome. In termites, the sterile soldier caste is particularly divergent in phenotype and presumably evolved under selection for defensiveness. In this study, we use genomic phylostratigraphy to show that genes with soldier- and other caste-biased expression from the Eastern subterranean termite Reticulitermes flavipes are more taxonomically restricted on the tree of life than genes with no caste-biased expression. This pattern suggests that caste-biased genes are relatively young and implies past selection for novel gene recruitment during termite caste evolution. Moreover, a soldier-biased set of 74 genes contains a higher proportion of orphan genes with no known homology than does a nymph-biased set or any null gene sets. This again suggests that the termite caste—and soldiers in particular—makes disproportionate use of evolutionarily novel genes that are potentially recruited from non-coding regions of the genome. Given that Reticulitermes and most termite soldiers are sterile, any past selection for genetic novelty of this caste must have been indirect and mediated through reproducing relatives.


Sociogenomics Phylostrata Genetic novelty Orphan genes Reticulitermes 



We thank Justin Croft and all members of the Social Biology Group at Western University (Canada) for discussion and advice throughout this study. This work was funded by a Faculty of Science Undergraduate Pre-Thesis Award to SB and a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to GJT.

Supplementary material

40_2018_650_MOESM1_ESM.pptx (720 kb)
Supplementary On-line Material Figure S1. Cluster analysis of genes differentially expressed by caste (re-drawn from Wu et al. 2018). This heat map shows the n = 93 most differentially expressed genes from a total of 13,755 that have been provisionally assembled via RNA-Seq analysis for Reticulitermes flavipes. The top-most axis shows how castes (soldiers, nymphs, workers) and populations within castes (1, 2, 3) cluster based on pattern of gene expression. The left-most axis shows three co-expressed sets of genes that are I - uniquely up-regulated (red) in soldiers (n = 61), II- uniquely down-regulated (blue) in soldiers (n = 13) or III - uniquely up-regulated in nymphs (PPTX 720 KB)
40_2018_650_MOESM2_ESM.xlsx (45 kb)
Supplementary material 2 (XLSX 44 KB)


  1. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. CrossRefGoogle Scholar
  2. Austin JW, Szalanski AL, Myles TG et al (2012) First record of Reticulitermes flavipes (Isoptera: Rhinotermitidae) from Terceira Island (Azores, Portugal). Fla Entomol 95:196–198CrossRefGoogle Scholar
  3. Barchuk AR, Cristino AS, Kucharski R et al (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol 7:70. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bourke AFG (2011) Principles of social evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  5. Chernyshova AM, Saraceni J, Thompson GJ (2018) Soldier-biased gene expression in a termite implies indirect selection for defensiveness. In: Kocher S, Sumner S, Zayed A (eds) Biology and genomics of social insects. Cold Spring Harbor, New York, p 42Google Scholar
  6. Crespi BJ, Yanega D (1995) The definition of eusociality. Behav Ecol 6:109–115. CrossRefGoogle Scholar
  7. Domazet-Loso T, Brajkovic J, Tautz D (2007) A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet 23:533–539CrossRefGoogle Scholar
  8. Drost HG, Gabel A, Grosse I, Quint M (2015) Evidence for active maintenance of phylotranscriptomic hourglass patterns in animal and plant embryogenesis. Mol Biol Evol 32:1221–1231. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Eggleton P, Beccaloni G, Inward D (2007) Response to Lo et al. Biol Lett 3:564–565. CrossRefPubMedCentralGoogle Scholar
  10. Feldmeyer B, Elsner D, Foitzik S (2014) 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. CrossRefPubMedGoogle Scholar
  11. Ferreira PG, Patalano S, Chauhan R et al (2013) Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol R 14:R20. CrossRefGoogle Scholar
  12. Gadau J, Fewell J (eds) (2009) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, CambridgeGoogle Scholar
  13. Grozinger CM, Fan YL, Hoover SER, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 16:4837–4848CrossRefGoogle Scholar
  14. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16CrossRefGoogle Scholar
  15. Harpur BA, Kent CF, Molodtsova D et al (2014) Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. Proc Natl Acad Sci USA 111:2614–2619. CrossRefPubMedGoogle Scholar
  16. Jasper WC, Linksvayer TA, Atallah J et al (2015) Large-scale coding sequence change underlies the evolution of postdevelopmental novelty in honey bees. Mol Biol Evol 32:334–346. CrossRefPubMedGoogle Scholar
  17. Johnson BR, Tsutsui ND (2011) Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. BMC Genom 12:164. CrossRefGoogle Scholar
  18. Khalturin K, Hemmrich G, Fraune S et al (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends Genet 25:404–413. CrossRefPubMedGoogle Scholar
  19. Kapheim KM (2016) Genomic sources of phenotypic novelty in the evolution of eusociality in insects. Curr Opin Insect Sci 13:24–32. CrossRefPubMedGoogle Scholar
  20. Korb J (2008) Termites, hemimetabolous diploid white ants? Front Zool 5:15. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lainé LV, Wright DJ (2003) The life cycle of Reticulitermes spp. (Isoptera: Rhinotermitidae): what do we know? Bull Entomol Res 93:267–278CrossRefGoogle Scholar
  22. Linksvayer TA, Wade MJ (2016) Theoretical predictions for sociogenomic data: the effects of kin selection and sex-limited expression on the evolution of social insect genomes. Front Ecol Evol 4:65CrossRefGoogle Scholar
  23. Long M, Betrán E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865–875. CrossRefPubMedGoogle Scholar
  24. NCBI Resource Coordinators (2017) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 45:D12–D17. CrossRefGoogle Scholar
  25. Noirot C, Pasteels JM (1987) Ontogenetic development and evolution of the worker caste in termites. Experientia 43:851–860CrossRefGoogle Scholar
  26. Pruitt KD, Tatusova T, Maglott DR (2005) NCBI reference sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–D504. CrossRefPubMedGoogle Scholar
  27. Perdereau E, Bagnères A-G, Bankhead-Dronnet S et al (2013) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol Ecol 22:1105–1119. CrossRefPubMedGoogle Scholar
  28. Raffoul M, Hecnar SJ, Prezioso S et al (2011) Trap response and genetic structure of eastern subterranean termites (Isoptera: Rhinotermitidae) in Point Pelee National Park, Ontario, Canada. Can Entomol 143:263–271. CrossRefGoogle Scholar
  29. Rehan SM, Toth AL (2015) Climbing the social ladder: the molecular evolution of sociality. Trends Ecol Evol 30:426–433. CrossRefPubMedGoogle Scholar
  30. Roisin Y (2000) Diversity and Evolution of Caste Patterns. In: Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 95–119CrossRefGoogle Scholar
  31. Roisin Y (1994) Intragroup conflicts and the evolution of sterile castes in termites. Am Nat 143:751–765. CrossRefGoogle Scholar
  32. Rust MK, Su NY (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375. CrossRefPubMedGoogle Scholar
  33. Scaduto DA, Garner SR, Leach EL, Thompson GJ (2012) Genetic evidence for multiple invasions of the eastern subterranean termite into Canada. Environ Entomol 41:1680–1686. CrossRefPubMedGoogle Scholar
  34. Scharf ME (2015) Omic research in termites: an overview and a roadmap. Front Genet 6:76. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Simola DF, Wissler L, Donahue G et al (2013) Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res 23:1235–1247. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Su N-Y, Ye W, Ripa R et al (2006) Identification of Chilean Reticulitermes (Isoptera: Rhinotermitidae) inferred from three mitochondrial gene DNA sequences and soldier morphology. Ann Entomol Soc Am 99:352–363.;2 CrossRefGoogle Scholar
  37. Sumner S (2014) The importance of genomic novelty in social evolution. Mol Ecol 23:26–28. CrossRefPubMedGoogle Scholar
  38. Tarver MR, Zhou X, Scharf ME (2010) Socio-environmental and endocrine influences on developmental and caste-regulatory gene expression in the eusocial termite Reticulitermes flavipes. BMC Mol Biol 11:28. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tautz D, Domazet-Lošo T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12:692CrossRefGoogle Scholar
  40. Thompson GJ, Hurd PL, Crespi BJ (2013) Genes underlying altruism. Biol Lett 9:20130395CrossRefGoogle Scholar
  41. Thompson GJ, Kitade O, Lo N, Crozier RH (2004) On the origin of termite workers: weighing up the phylogenetic evidence. J Evol Biol 17:217–220. CrossRefPubMedGoogle Scholar
  42. Thompson GJ, Richards MH (2016) Editorial: genetic effects on social traits: empirical studies from social animals. Front Ecol Evol 4:91. CrossRefGoogle Scholar
  43. Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proc Natl Acad Sci 100:12808–12813. CrossRefPubMedGoogle Scholar
  44. Thorne BL, Traniello JFA (2003) Comparative social biology of basal taxa of ants and termites. Annu Rev Entomol 48:283–306. CrossRefPubMedGoogle Scholar
  45. Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403. CrossRefPubMedGoogle Scholar
  46. Ware JL, Grimaldi DA, Engel MS (2010) The effects of fossil placement and calibration on divergence times and rates: an example from the termites (Insecta: Isoptera). Arthropod Struct Dev 39:204–219CrossRefGoogle Scholar
  47. Warner MR, Mikheyev AS, Linksvayer TA (2017) Genomic signature of kin selection in an ant with obligately sterile workers. Mol Biol Evol 34:1780–1787. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Watson JAL, Okot-Kotber BM, Noirot CH (1985) Caste differentiation in social insects. Pergamon Press, OxfordGoogle Scholar
  49. Weesner FM (1970) Termites of the Nearctic region. In: Krishna K, Weesner FM (eds) Biology of termites, vol 2. Academic Press, Cambridge, pp 477–525Google Scholar
  50. Wu T, Dhami GK, Thompson GJ (2018) Soldier-biased gene expression in a subterranean termite implies functional specialization of the defensive caste. Evol Dev 20:3–16. CrossRefPubMedGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Biology DepartmentWestern UniversityLondonCanada

Personalised recommendations