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Termite Phylogenetics and Co-cladogenesis with Symbionts

  • Nathan Lo
  • Paul Eggleton
Chapter

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.

Keywords

Sister Group Horizontal Transfer Cladistic Analysis Malpighian Tubule Sister Group Relationship 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aanen DK, Eggleton P (2005) Fungus-growing termites originated in African rain forest. Curr Biol 15:851–855PubMedCrossRefGoogle Scholar
  2. 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 99:14887–14892PubMedCrossRefGoogle Scholar
  3. Ahmad M (1950) The phylogeny of termite genera based on imago-worker mandibles. Bull Am Mus Nat Hist 95:37–86Google Scholar
  4. Bandi C, Damiani G, Magrassi L et al (1994) Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B 257:43–48CrossRefGoogle Scholar
  5. 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 259:293–299CrossRefGoogle Scholar
  6. Boudreaux HB (1979) Arthropod phylogeny with special reference to insects. John Wiley and Sons, New York, NYGoogle Scholar
  7. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New York, NYGoogle Scholar
  8. 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 45:31–51Google Scholar
  9. 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 268:393–398CrossRefGoogle Scholar
  10. 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 17:185–342Google Scholar
  11. Cochran DG (1985) Nitrogen excretion in cockroaches. Annu Rev Entomol 10:29–39CrossRefGoogle Scholar
  12. Constantino R (1995) Revision of the neotropical termite genus Syntermes Holmgren (Isoptera: Termitidae). Univ Kans Sci Bull 55:455–518Google Scholar
  13. Crampton GC (1920) The terminal abdominal structures of the primitive Australian termite Mastotermes darwiniensis Froggatt. Trans R Entomol Soc Lond 1920:137–145Google Scholar
  14. 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 18:85–93Google Scholar
  15. Crampton GC (1938) The interrelationships and lines of descent of living insects. Psyche 45:165–181CrossRefGoogle Scholar
  16. Deitz LL, Nalepa CA, Klass KD (2003) Phylogeny of the Dictyoptera re-examined (Insecta). Entomol Abh 1:69–91Google Scholar
  17. DeSalle R, Gatesy J, Wheeler W, Grimaldi D (1992) DNA sequences from a fossil termite in Oligo-Miocene amber and their phylogenetic implications. Science 257:1933–1936PubMedCrossRefGoogle Scholar
  18. Donovan SE, Jones DT, Sands WA, Eggleton P (2000) Morphological phylogenetics of termites (Isoptera). Biol J Linn Soc 70:467–513CrossRefGoogle Scholar
  19. Eggleton P (2001) Termites and trees: a review of recent advances in termite phylogenetics. Insectes Soc 48:187–193CrossRefGoogle Scholar
  20. Eggleton P, Beccaloni G, Inward D (2007) Save Isoptera: a comment on Inward et al – response to Lo et al. Biol Lett 3:564–565CrossRefGoogle Scholar
  21. Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 3650:1–27CrossRefGoogle Scholar
  22. Engel MS, Krishna K (2004) Family-group names for termites (Isoptera). Am Mus Novit 3432:1–9CrossRefGoogle Scholar
  23. 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 264:763–768CrossRefGoogle Scholar
  24. Gillott C (1995) Entomology. Plenum Press, New York, NYGoogle Scholar
  25. Goloboff PA, Farris JS, Nixon KC (2008) TNT, a free program for phylogenetic analysis. Cladistics 24:774–786CrossRefGoogle Scholar
  26. Grandcolas P (1994) Phylogenetic systematics of the subfamily Polyphaginae, with the assignment of Cryptocercus Scudder, 1862 to this taxon (Blattaria, Blaberoidea, Polyphagidae). Syst Entomol 19:145–158Google Scholar
  27. Grandcolas P (1996) The phylogeny of cockroach families: a cladistic appraisal of morpho-anatomical data. Can J Zool 74:508–527CrossRefGoogle Scholar
  28. 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 3204:1–11Google Scholar
  29. Hennig W (1981) Insect phylogeny. John Wiley & Sons, New York, NYGoogle Scholar
  30. Hill GF (1926) Australian termites (Isoptera) Notes on Stolotermes, Calotermes and Coptotermes, with descriptions of new species. Proc R Soc Vic 38:192–214Google Scholar
  31. Hudson GB (1945) A study of the tentorium in some orthopteroid Hexapoda. J Entomol Soc South Afr 8:71–90Google Scholar
  32. 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 9:99–108PubMedGoogle Scholar
  33. Ikeda-Ohtsubo W, Brune A (2009) Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and Candidatus Endomicrobium trichonymphae. Mol Ecol 18:332–342PubMedCrossRefGoogle Scholar
  34. 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 209:75–180CrossRefGoogle Scholar
  35. Imms AD (1957) A general textbook of entomology. Methuen, LondonGoogle Scholar
  36. 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 275–288Google Scholar
  37. Inward D, Beccaloni G, Eggleton P (2007a) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335PubMedCrossRefGoogle Scholar
  38. Inward DJ, Vogler AP, Eggleton PE (2007b) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44:953–967PubMedCrossRefGoogle Scholar
  39. Jucci C (1932) Sulla presenza di batteriociti nel tessuto adiposo dei Termitidi. Boll Zool; Atti XI Congr Intern Zool Padova 1930 Arch Zool Ital 16:1422–1429Google Scholar
  40. Jucci C (1952) Symbiosis and phylogenesis in the Isoptera. Nature 169:837PubMedCrossRefGoogle Scholar
  41. 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 92:2017–2020PubMedCrossRefGoogle Scholar
  42. 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 1–23Google Scholar
  43. Kitade O (2004) Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes Environ 19:215–220CrossRefGoogle Scholar
  44. Kjer KM (2004) Aligned 18S and insect phylogeny. Syst Biol 53:506–514PubMedCrossRefGoogle Scholar
  45. Klass K-D (1995) Die Phylogeny der Dictyoptera PhD thesis, Ludwig Maximilians UniversitätGoogle Scholar
  46. Klass K-D (2001) Morphological evidence on blattarian phylogeny: “phylogenetic histories and stories” (Insecta, Dictyoptera). Dtsch Entomol Z 48:223–265Google Scholar
  47. Klass K-D, Meier R (2006) A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomol Abh 63:3–50Google Scholar
  48. 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 46:809–817PubMedCrossRefGoogle Scholar
  49. Koch A (1938) Symbiosestudien, 3: Die intrazellulare symbiose von Mastotermes darwiniensis Froggatt. Z Morph Okol Tiere 34:384–609CrossRefGoogle Scholar
  50. Kristensen NP (1995) Forty years’ insect phylogenetic systematics. Zool Beitr 36:83–124Google Scholar
  51. Laurentiaux D (1951) Le problème des blattes paléozoiques a ovipositeur externe. Ann Paleontol 37:187–194Google Scholar
  52. 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 48:615–627PubMedCrossRefGoogle Scholar
  53. Lo N, Bandi C, Watanabe H, Beninati T (2003) Evidence for co-cladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20:907–913PubMedCrossRefGoogle Scholar
  54. Lo N, Beninati T, Stone F et al (2007a) Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola. Biol Lett 3:327–330PubMedCrossRefGoogle Scholar
  55. Lo N, Engel MS, Cameron S et al (2007b) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–563PubMedCrossRefGoogle Scholar
  56. Lo N, Kitade O, Miura T et al (2004) Molecular phylogeny of the Rhinotermitidae. Insectes Soc 51:365–371CrossRefGoogle Scholar
  57. Lo N, Tokuda G, Watanabe H et al (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804PubMedCrossRefGoogle Scholar
  58. Marks EP, Lawson FA (1962) A comparative study of the Dictyoptera ovipositor. J Morphol 111:139–171CrossRefGoogle Scholar
  59. Maynard Smith J, Szathmary E (1997) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  60. McKittrick FA (1964) Evolutionary studies of cockroaches. Mem Cornell Univ Agr Exp Stn 389:1–197Google Scholar
  61. McKittrick FA (1965) A contribution to the understanding of cockroach – termite affinities. Ann Entomol Soc Am 58:18–22PubMedGoogle Scholar
  62. Nalepa CA (1984) Colony composition, protozoan transfer and some life-history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae). Behav Ecol Sociobiol 14:273–279CrossRefGoogle Scholar
  63. Nalepa CA (1988a) Reproduction in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae) – mating, oviposition, and hatch. Ann Entomol Soc Am 81:637–641Google Scholar
  64. Nalepa CA (1988b) Cost of parental care in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera, Cryptocercidae). Behav Ecol Sociobiol 23:135–140CrossRefGoogle Scholar
  65. Nalepa CA (1991) Ancestral transfer of symbionts between cockroaches and termites: an unlikely scenario. Proc R Soc Lond B 246:185–189CrossRefGoogle Scholar
  66. 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 53–76Google Scholar
  67. Nalepa CA, Lenz M (2000) The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc Biol Sci 267:1809–1813PubMedCrossRefGoogle Scholar
  68. 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 277:359–365CrossRefGoogle Scholar
  69. 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 16:1257–1266PubMedCrossRefGoogle Scholar
  70. Noirot C (1995) The gut of termites (Isoptera) – comparative anatomy, systematics, phylogeny. 1 Lower termites. Ann Soc Entomol Fr 31:197–226Google Scholar
  71. Noirot C (2001) The gut of termites (Isoptera) comparative anatomy, systematics, phylogeny II – Higher termites (Termitidae). Ann Soc Entomol Fr 37:431–471Google Scholar
  72. 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 276:239–245CrossRefGoogle Scholar
  73. 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 31:701–710PubMedCrossRefGoogle Scholar
  74. 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 43:616–626PubMedCrossRefGoogle Scholar
  75. Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 106:19521–19526PubMedCrossRefGoogle Scholar
  76. Sacchi L, Nalepa CA, Bigliardi E et al (1998) Some aspects of intracellular symbiosis during embryo development of Mastotermes darwiniensis (Isoptera: Mastotermitidae). Parassitologia 40:309–316PubMedGoogle Scholar
  77. Sands WA (1972) The soldierless termites of Africa (Isoptera: Termitidae). Bull Br Mus Nat Hist (Entomol) Suppl 18:1–244Google Scholar
  78. Sands WA (1998) The identification of worker castes of termite genera from soils of Africa and the Middle East, CAB International, UK.Google Scholar
  79. 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 153:631–650CrossRefGoogle Scholar
  80. Seelinger G, Seelinger U (1983) On the social organization, alarm and fighting in the primitive cockroach Cryptocercus punctulatus Scudder. Z Tierpsychol 61:315–333Google Scholar
  81. Terry MD, Whiting MF (2005) Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21:240–257CrossRefGoogle Scholar
  82. Thompson GJ, Kitade O, Lo N, Crozier RH (2000a) On the origin of termite workers: weighing up the phylogenetic evidence. J Evol Biol 17:217–220CrossRefGoogle Scholar
  83. 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 17:419–429PubMedCrossRefGoogle Scholar
  84. Thorne BL (1990) A case for ancestral transfer of symbionts between cockroaches and termites. Proc R Soc Lond B 241:37–41CrossRefGoogle Scholar
  85. Thorne BL (1991) Ancestral transfer of symbionts between cockroaches and termites: an alternative hypothesis. Proc R Soc Lond B 246:191–195CrossRefGoogle Scholar
  86. Thorne BL, Carpenter JM (1992) Phylogeny of the Dictyoptera. Syst Entomol 17:253–268CrossRefGoogle Scholar
  87. 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 77–94Google Scholar
  88. Walker EM (1922) The terminal structures of orthopteroid insects: a phylogenetic study II The terminal abdominal structures of the male. Ann Entomol Soc Am 15:1–87Google Scholar
  89. 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 33:429–450CrossRefGoogle Scholar
  90. Wheeler WC, Whiting MF, Wheeler QD, Carpenter JM (2001) The phylogeny of the extant hexapod orders. Cladistics 17:113–169CrossRefGoogle Scholar

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© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Behaviour and Genetics of Social Insects LaboratorySchool of Biological Sciences, University of SydneySydneyAustralia
  2. 2.Termite Research Group and Soil Biodiversity Programme, Entomology DepartmentNatural History MuseumLondonUK

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