Skip to main content

Termite Phylogenetics and Co-cladogenesis with Symbionts

  • Chapter
  • First Online:
Biology of Termites: a Modern Synthesis

Abstract

Termites are key decomposer insects in numerous ecosystems in the tropics and beyond, and their unique social systems provide a major counterpoint to those of hymenopteran social insects. Our knowledge of the phylogenetics and systematics of the group have traditionally lagged behind those of other important insect groups, but significant progress has now been made. Here we review recent phylogenetic studies of relationships both among termites, and between termites, cockroaches and mantids. We also discuss studies of co-cladogenesis between termites and two groups of symbionts: cellulolytic hindgut flagellates, and Blattabacterium. A consensus has emerged that the sister-group of termites is the wood-feeding cockroach genus Cryptocercus, and that the digestion of wood by the common ancestor of these two groups was aided by cellulolytic hindgut flagellates. The basal phylogenetic position of Mastotermes darwiniensis among termites has been confirmed, however agreement on the phylogenetic positions of members of the Kalotermitidae, Termopsidae and Hodotermitidae has yet to be reached. Relationships between and within the Rhinotermitidae and Serritermitidae also remain to be settled. Key lineages of the major family Termitidae, however, are now fairly well established.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aanen DK, Eggleton P (2005) Fungus-growing termites originated in African rain forest. Curr Biol 15:851–855

    Article  PubMed  CAS  Google Scholar 

  • Aanen DK, Eggleton P, Rouland-Lefevre C et al (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A 99:14887–14892

    Article  PubMed  CAS  Google Scholar 

  • Ahmad M (1950) The phylogeny of termite genera based on imago-worker mandibles. Bull Am Mus Nat Hist 95:37–86

    Google Scholar 

  • Bandi C, Damiani G, Magrassi L et al (1994) Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B 257:43–48

    Article  CAS  Google Scholar 

  • Bandi C, Sironi M, Damiani G et al (1995) The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond B 259:293–299

    Article  CAS  Google Scholar 

  • Boudreaux HB (1979) Arthropod phylogeny with special reference to insects. John Wiley and Sons, New York, NY

    Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New York, NY

    Google Scholar 

  • Cancello EM, DeSouza O (2005) A new species of Glossotermes (Isoptera): reappraisal of the generic status with transfer from the Rhinotermitidae to the Serritermitidae. Sociobiology 45:31–51

    Google Scholar 

  • Clark JW, Hossain S, Burnside CA, Kambhampati S (2001) Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective. Proc R Soc Lond B 268:393–398

    Article  CAS  Google Scholar 

  • Cleveland LR, Hall SR, Saunders EP, Collier J (1934) The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem Am Acad Sci 17:185–342

    Google Scholar 

  • Cochran DG (1985) Nitrogen excretion in cockroaches. Annu Rev Entomol 10:29–39

    Article  Google Scholar 

  • Constantino R (1995) Revision of the neotropical termite genus Syntermes Holmgren (Isoptera: Termitidae). Univ Kans Sci Bull 55:455–518

    Google Scholar 

  • Crampton GC (1920) The terminal abdominal structures of the primitive Australian termite Mastotermes darwiniensis Froggatt. Trans R Entomol Soc Lond 1920:137–145

    Google Scholar 

  • Crampton GC (1923) A comparison of the terminal abdominal structures of an adult alate female of the primitive termite Mastotermes darwiniensis with those of the roach Periplaneta americana. Bull Brooklyn Entomol Soc 18:85–93

    Google Scholar 

  • Crampton GC (1938) The interrelationships and lines of descent of living insects. Psyche 45:165–181

    Article  Google Scholar 

  • Deitz LL, Nalepa CA, Klass KD (2003) Phylogeny of the Dictyoptera re-examined (Insecta). Entomol Abh 1:69–91

    Google Scholar 

  • DeSalle R, Gatesy J, Wheeler W, Grimaldi D (1992) DNA sequences from a fossil termite in Oligo-Miocene amber and their phylogenetic implications. Science 257:1933–1936

    Article  PubMed  CAS  Google Scholar 

  • Donovan SE, Jones DT, Sands WA, Eggleton P (2000) Morphological phylogenetics of termites (Isoptera). Biol J Linn Soc 70:467–513

    Article  Google Scholar 

  • Eggleton P (2001) Termites and trees: a review of recent advances in termite phylogenetics. Insectes Soc 48:187–193

    Article  Google Scholar 

  • Eggleton P, Beccaloni G, Inward D (2007) Save Isoptera: a comment on Inward et al – response to Lo et al. Biol Lett 3:564–565

    Article  Google Scholar 

  • Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 3650:1–27

    Article  Google Scholar 

  • Engel MS, Krishna K (2004) Family-group names for termites (Isoptera). Am Mus Novit 3432:1–9

    Article  Google Scholar 

  • Gäde G, Grandcolas P, Kellner R (1997) Structural data on hypertrehalosaemic neuropeptides from Cryptocercus punctulatus and Therea petiveriana: how do they fit into the phylogeny of cockroaches? Proc R Soc Lond B 264:763–768

    Article  Google Scholar 

  • Gillott C (1995) Entomology. Plenum Press, New York, NY

    Google Scholar 

  • Goloboff PA, Farris JS, Nixon KC (2008) TNT, a free program for phylogenetic analysis. Cladistics 24:774–786

    Article  Google Scholar 

  • Grandcolas P (1994) Phylogenetic systematics of the subfamily Polyphaginae, with the assignment of Cryptocercus Scudder, 1862 to this taxon (Blattaria, Blaberoidea, Polyphagidae). Syst Entomol 19:145–158

    Google Scholar 

  • Grandcolas P (1996) The phylogeny of cockroach families: a cladistic appraisal of morpho-anatomical data. Can J Zool 74:508–527

    Article  Google Scholar 

  • Grimaldi D (1997) A fossil mantis (Insecta: Mantodea) in Cretaceous amber of New Jersey, with comments on the early history of the Dictyoptera. Am Mus Novit 3204:1–11

    Google Scholar 

  • Hennig W (1981) Insect phylogeny. John Wiley & Sons, New York, NY

    Google Scholar 

  • Hill GF (1926) Australian termites (Isoptera) Notes on Stolotermes, Calotermes and Coptotermes, with descriptions of new species. Proc R Soc Vic 38:192–214

    Google Scholar 

  • Hudson GB (1945) A study of the tentorium in some orthopteroid Hexapoda. J Entomol Soc South Afr 8:71–90

    Google Scholar 

  • Hudson GB (1947) Studies in the comparative anatomy and systematic importance of the hexapod tentorium II Dermaptera, Embioptera, and Isoptera. J Entomol Soc South Afr 9:99–108

    PubMed  CAS  Google Scholar 

  • Ikeda-Ohtsubo W, Brune A (2009) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and Candidatus Endomicrobium trichonymphae. Mol Ecol 18:332–342

    Article  PubMed  CAS  Google Scholar 

  • Imms AD (1920) On the structure and biology of Archotermopsis, together with descriptions of new species of intestinal protozoa, and general observations on the Isoptera. Philos Trans R Soc Lond B 209:75–180

    Article  Google Scholar 

  • Imms AD (1957) A general textbook of entomology. Methuen, London

    Google Scholar 

  • Inoue T, Kitade O, Yoshimura T, Yamaoka I (2000) Symbiotic associations with protists. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 275–288

    Google Scholar 

  • Inward D, Beccaloni G, Eggleton P (2007a) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335

    Article  PubMed  CAS  Google Scholar 

  • Inward DJ, Vogler AP, Eggleton PE (2007b) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44:953–967

    Article  PubMed  CAS  Google Scholar 

  • Jucci C (1932) Sulla presenza di batteriociti nel tessuto adiposo dei Termitidi. Boll Zool; Atti XI Congr Intern Zool Padova 1930 Arch Zool Ital 16:1422–1429

    Google Scholar 

  • Jucci C (1952) Symbiosis and phylogenesis in the Isoptera. Nature 169:837

    Article  PubMed  CAS  Google Scholar 

  • Kambhampati S (1995) A phylogeny of cockroaches and related insects based on DNA sequence of mitochondrial ribosomal RNA genes. Proc Natl Acad Sci U S A 92:2017–2020

    Article  PubMed  CAS  Google Scholar 

  • Kambhampati S, Eggleton P (2000) Taxonomy and phylogeny of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 1–23

    Google Scholar 

  • Kitade O (2004) Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes Environ 19:215–220

    Article  Google Scholar 

  • Kjer KM (2004) Aligned 18S and insect phylogeny. Syst Biol 53:506–514

    Article  PubMed  Google Scholar 

  • Klass K-D (1995) Die Phylogeny der Dictyoptera PhD thesis, Ludwig Maximilians Universität

    Google Scholar 

  • Klass K-D (2001) Morphological evidence on blattarian phylogeny: “phylogenetic histories and stories” (Insecta, Dictyoptera). Dtsch Entomol Z 48:223–265

    Google Scholar 

  • Klass K-D, Meier R (2006) A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomol Abh 63:3–50

    Google Scholar 

  • Klass K-D, Nalepa CA, Lo N (2008) How useful are the wood-feeding cockroaches Cryptocercus and Perisphaeria boleiriana as models of termite evolution (Insecta: Dictyoptera). Mol Phylogenet Evol 46:809–817

    Article  PubMed  Google Scholar 

  • Koch A (1938) Symbiosestudien, 3: Die intrazellulare symbiose von Mastotermes darwiniensis Froggatt. Z Morph Okol Tiere 34:384–609

    Article  Google Scholar 

  • Kristensen NP (1995) Forty years’ insect phylogenetic systematics. Zool Beitr 36:83–124

    Google Scholar 

  • Laurentiaux D (1951) Le problème des blattes paléozoiques a ovipositeur externe. Ann Paleontol 37:187–194

    Google Scholar 

  • Legendre F, Whiting MF, Bordereau C et al (2008) The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol Phylogenet Evol 48:615–627

    Article  PubMed  CAS  Google Scholar 

  • Lo N, Bandi C, Watanabe H, Beninati T (2003) Evidence for co-cladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20:907–913

    Article  PubMed  CAS  Google Scholar 

  • Lo N, Beninati T, Stone F et al (2007a) Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola. Biol Lett 3:327–330

    Article  PubMed  CAS  Google Scholar 

  • Lo N, Engel MS, Cameron S et al (2007b) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–563

    Article  PubMed  Google Scholar 

  • Lo N, Kitade O, Miura T et al (2004) Molecular phylogeny of the Rhinotermitidae. Insectes Soc 51:365–371

    Article  Google Scholar 

  • Lo N, Tokuda G, Watanabe H et al (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804

    Article  PubMed  CAS  Google Scholar 

  • Marks EP, Lawson FA (1962) A comparative study of the Dictyoptera ovipositor. J Morphol 111:139–171

    Article  Google Scholar 

  • Maynard Smith J, Szathmary E (1997) The major transitions in evolution. Oxford University Press, Oxford

    Google Scholar 

  • McKittrick FA (1964) Evolutionary studies of cockroaches. Mem Cornell Univ Agr Exp Stn 389:1–197

    Google Scholar 

  • McKittrick FA (1965) A contribution to the understanding of cockroach – termite affinities. Ann Entomol Soc Am 58:18–22

    PubMed  CAS  Google Scholar 

  • Nalepa CA (1984) Colony composition, protozoan transfer and some life-history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae). Behav Ecol Sociobiol 14:273–279

    Article  Google Scholar 

  • Nalepa CA (1988a) Reproduction in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae) – mating, oviposition, and hatch. Ann Entomol Soc Am 81:637–641

    Google Scholar 

  • Nalepa CA (1988b) Cost of parental care in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae). Behav Ecol Sociobiol 23:135–140

    Article  Google Scholar 

  • Nalepa CA (1991) Ancestral transfer of symbionts between cockroaches and termites: an unlikely scenario. Proc R Soc Lond B 246:185–189

    Article  CAS  Google Scholar 

  • Nalepa CA, Bandi C (2000) Characterising the ancestors: paedomorphosis and termite evolution. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 53–76

    Google Scholar 

  • Nalepa CA, Lenz M (2000) The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc Biol Sci 267:1809–1813

    Article  PubMed  CAS  Google Scholar 

  • Nobre T, Eggleton PE, Aanen DK (2010) Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites? Proc R Soc Lond B 277:359–365

    Article  CAS  Google Scholar 

  • Noda S, Kitade O, Inoue T et al (2007) Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp), their hosts, and their bacterial endosymbionts. Mol Ecol 16:1257–1266

    Article  PubMed  CAS  Google Scholar 

  • Noirot C (1995) The gut of termites (Isoptera) – comparative anatomy, systematics, phylogeny. 1 Lower termites. Ann Soc Entomol Fr 31:197–226

    Google Scholar 

  • Noirot C (2001) The gut of termites (Isoptera) comparative anatomy, systematics, phylogeny II – Higher termites (Termitidae). Ann Soc Entomol Fr 37:431–471

    Google Scholar 

  • Ohkuma M, Noda S, Hongoh Y et al (2009) Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc R Soc Lond B 276:239–245

    Article  CAS  Google Scholar 

  • Ohkuma M, Yuzawa H, Amornsak W et al (2004) Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol Phylogenet Evol 31:701–710

    Article  PubMed  CAS  Google Scholar 

  • Pellens R, D’Haese C, Belles X et al (2007) The evolutionary transition from subsocial to eusocial behaviour in Dictyoptera: phylogenetic evidence for modification of the “shift-in-dependent-care” hypothesis with a new subsocial cockroach. Mol Phylogenet Evol 43:616–626

    Article  PubMed  CAS  Google Scholar 

  • Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 106:19521–19526

    Article  PubMed  CAS  Google Scholar 

  • Sacchi L, Nalepa CA, Bigliardi E et al (1998) Some aspects of intracellular symbiosis during embryo development of Mastotermes darwiniensis (Isoptera: Mastotermitidae). Parassitologia 40:309–316

    PubMed  CAS  Google Scholar 

  • Sands WA (1972) The soldierless termites of Africa (Isoptera: Termitidae). Bull Br Mus Nat Hist (Entomol) Suppl 18:1–244

    Google Scholar 

  • Sands WA (1998) The identification of worker castes of termite genera from soils of Africa and the Middle East, CAB International, UK.

    Google Scholar 

  • Scholtz OI, Macleod N, Eggleton P (2008) Termite soldier defence strategies: a reassessment of Prestwich’s classification and an examination of the evolution of defence morphology using extended eigenshape analyses of head morphology. Zool J Linn Soc 153:631–650

    Article  Google Scholar 

  • Seelinger G, Seelinger U (1983) On the social organization, alarm and fighting in the primitive cockroach Cryptocercus punctulatus Scudder. Z Tierpsychol 61:315–333

    Google Scholar 

  • Terry MD, Whiting MF (2005) Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21:240–257

    Article  Google Scholar 

  • Thompson GJ, Kitade O, Lo N, Crozier RH (2000a) On the origin of termite workers: weighing up the phylogenetic evidence. J Evol Biol 17:217–220

    Article  Google Scholar 

  • Thompson GJ, Miller LR, Lenz M, Crozier RH (2000b) Phylogenetic analysis and trait evolution in Australian lineages of drywood termites (Isoptera, Kalotermitidae). Mol Phylogenet Evol 17:419–429

    Article  PubMed  CAS  Google Scholar 

  • Thorne BL (1990) A case for ancestral transfer of symbionts between cockroaches and termites. Proc R Soc Lond B 241:37–41

    Article  CAS  Google Scholar 

  • Thorne BL (1991) Ancestral transfer of symbionts between cockroaches and termites: an alternative hypothesis. Proc R Soc Lond B 246:191–195

    Article  CAS  Google Scholar 

  • Thorne BL, Carpenter JM (1992) Phylogeny of the Dictyoptera. Syst Entomol 17:253–268

    Article  Google Scholar 

  • Thorne BL, Grimaldi DA, Krishna K (2000) Early fossil history of the termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 77–94

    Google Scholar 

  • Walker EM (1922) The terminal structures of orthopteroid insects: a phylogenetic study II The terminal abdominal structures of the male. Ann Entomol Soc Am 15:1–87

    Google Scholar 

  • Ware JL, Litman J, Klass K-D, Spearman LA (2008) Relationships among the major lineages of Dictyoptera: the effect of outgroup selection on dictyopteran tree topology. Syst Entomol 33:429–450

    Article  Google Scholar 

  • Wheeler WC, Whiting MF, Wheeler QD, Carpenter JM (2001) The phylogeny of the extant hexapod orders. Cladistics 17:113–169

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathan Lo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Lo, N., Eggleton, P. (2010). Termite Phylogenetics and Co-cladogenesis with Symbionts. In: Bignell, D., Roisin, Y., Lo, N. (eds) Biology of Termites: a Modern Synthesis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3977-4_2

Download citation

Publish with us

Policies and ethics