Advertisement

Genetic Structure of Termite Colonies and Populations

  • Edward L. VargoEmail author
  • Claudia Husseneder
Chapter

Abstract

Increasingly, researchers are using molecular markers to investigate the genetic structure of termite colonies and populations. The studies are providing insights into the natural history and evolution of Isoptera in unprecedented detail. At the level of the colony, genetic studies reveal the breeding structure and degrees of inbreeding. In many species colonies are often headed by monogamous pairs of reproductives, although there is considerable variation in breeding structure within and between species in the proportions of colonies with multiple functional reproductives, usually containing inbreeding neotenics. Recent studies have identified negative consequences of inbreeding with important consequences for colony breeding structure. Genetic evidence does not support budding as a common mode of reproduction in termites. In most cases studied to date, alates appear to disperse far enough to promote extensive gene flow among populations within about 10 km, while populations at 50–100 km often show moderate to strong genetic differentiation. There has also been considerable progress in phylogeographic studies, relating differentiation among populations and speciation of termites to geological events. The few studies to date of invasive termite species suggest that some successful invaders (e.g. Reticulitermes flavipes) may undergo changes in breeding structure in the introduced range toward larger, unicolonial societies, whereas other introduced populations (e.g. Coptotermes formosanus) do not exhibit unicolonial characteristics. The powerful approach to termite colony and population genetics afforded by molecular markers will address a wide range of issues of fundamental importance to termite biology and evolution. With continued advancement in the tools for characterizing genetic variation, we anticipate rapid progress in termite colony and population genetics.

Keywords

Population Genetic Structure Termite Species Subterranean Termite Mating Flight Simple Family 
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. Aldrich BT, Kambhampati S (2004) Microsatellite markers for two species of dampwood termites in the genus Zootermopsis (Isoptera: Termopsidae). Mol Ecol Notes 4:719–721CrossRefGoogle Scholar
  2. Aldrich BT, Kambhampati S (2007) Population structure and colony composition of two Zootermopsis nevadensis subspecies. Heredity 99:443–451PubMedCrossRefGoogle Scholar
  3. Aluko GA, Husseneder C (2007) Colony dynamics of the Formosan subterranean termite in a frequently disturbed urban landscape. J Econ Entomol 100:1037–1046PubMedCrossRefGoogle Scholar
  4. Atkinson L, Adams ES (1997a) Double-strand conformation polymorphism (DSCP) analysis of the mitochondrial control region generates highly variable markers for population studies in a social insect. Insect Mol Biol 6:369–376PubMedCrossRefGoogle Scholar
  5. Atkinson L, Adams ES (1997b) The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proc R Soc Lond B 264:1131–1136CrossRefGoogle Scholar
  6. Atkinson L, Adams ES, Crozier RH (2007) Microsatellite markers for the polygamous termite Nasutitermes corniger (Isoptera: Termitidae). Mol Ecol Notes 7:299–301CrossRefGoogle Scholar
  7. Atkinson L, Teschendorf G, Adams ES (2008) Lack of evidence for nepotism by workers tending queens of the polygynous termite Nasutitermes corniger. Behav Ecol Sociobiol 62:805–812CrossRefGoogle Scholar
  8. Austin JW, Szalanski AL, Ghayourfar R et al (2006a) Phylogeny and genetic variation of Reticulitermes (Isoptera: Rhinotermitidae) from the Eastern Mediterranean and Middle East. Sociobiology 47:1–19Google Scholar
  9. Austin JW, Szalanski AL, Gold RE, Foster BT (2004a) Genetic variation and geographic distribution of the subterranean termite genus Reticulitermes in Texas. Southwest Entomol 29:1–11Google Scholar
  10. Austin JW, Szalanski AL, Kard BM (2004b) Distribution and genetic variation of Reticulitermes (Isoptera: Rhinotermitidae) in Oklahoma. Fla Entomol 87:152–158CrossRefGoogle Scholar
  11. Austin JW, Szalanski AL, Scheffrahn RH et al (2005) Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Ann Entomol Soc Am 98:395–401CrossRefGoogle Scholar
  12. Austin JW, Szalanski AL, Scheffrahn RH et al (2006b) Genetic evidence for two introductions of the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae), to the United States. Fla Entomol 89:183–193CrossRefGoogle Scholar
  13. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MAGoogle Scholar
  14. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates Inc, Sunderland, MAGoogle Scholar
  15. Behura SK (2006) Molecular marker systems in insects: current trends and future avenues. Mol Ecol 15:3087–3115PubMedCrossRefGoogle Scholar
  16. Booth W, Lewis VR, Taylor RL et al (2008) Identification and characterization of 15 polymorphic microsatellite loci in the western dry-wood termite, Incisitermes minor (Hagen). Mol Ecol Resour 8:1102–1104PubMedCrossRefGoogle Scholar
  17. Brandl R, Hacker M, Bagine RKN, Kaib M (2001) Geographic variation of polygyny in the termite Macrotermes michaelseni (Sjöstedt). Insectes Soc 48:134–137CrossRefGoogle Scholar
  18. Brandl R, Hacker M, Bagine RKN, Kaib M (2004) Yearly variation in polygyny in the termite Macrotermes michaelseni (Sjöstedt). Insectes Soc 51:294–298CrossRefGoogle Scholar
  19. Brandl R, Hacker M, Epplen J, Kaib M (2005) High gene flow between populations of Macrotermes michaelseni (Isoptera, Termitidae). Insectes Soc 52:344–349CrossRefGoogle Scholar
  20. Broughton RE (1995) Mitochondrial DNA variation within and among species of termites in the genus Zootermopsis (Isoptera: Termopsidae). Ann Entomol Soc Am 88:120–128Google Scholar
  21. Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243CrossRefGoogle Scholar
  22. Calleri DV, Reid EM, Rosengaus RB et al (2007) Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proc R Soc Lond B 273:2633–2640CrossRefGoogle Scholar
  23. Calleri DV, Rosengaus RB, Traniello JFA (2005) Disease and colony foundation in the dampwood termite Zootermopsis angusticollis: The survival advantage of nestmate pairs. Naturwissenschaften 92:300–304PubMedCrossRefGoogle Scholar
  24. Clément J-L (1981) Enzymatic polymorphism in the European populations of various Reticulitermes species (Isoptera). In: Howse PE, Clément J-L (eds) Biosystematics of social insects. Academic Press, London and New York, NY, pp 49–61Google Scholar
  25. Clément J-L (1984) Diagnostic alleles and systematics in termite species of the genus Reticulitermes in Europe. Experientia 40:283–285CrossRefGoogle Scholar
  26. Clément J-L, Bagnères A-G, Uva P et al (2001) Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insectes Soc 48:202–215CrossRefGoogle Scholar
  27. Copren KA (2004) The genetic and social structure of the western subterranean termite, Reticulitermes hesperus (Isoptera: Rhinotermitidae). Ph.D. dissertation, University of California, Davis, CAGoogle Scholar
  28. Copren KA (2007) Characterization of microsatellite loci in the western subterranean termite Reticulitermes hesperus and cross-amplification in closely related cryptic species. J Insect Sci 7:17PubMedCrossRefGoogle Scholar
  29. Cornuet J-M, Piry S, Luikart G et al (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000PubMedGoogle Scholar
  30. Darlington JPEC (1985) Multiple primary reproductives in the termite Macrotermes michaleseni (Sjöstedt). In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Caste differentiation in social insects. Pergamon Press, Oxford, pp 187–200Google Scholar
  31. Davis RB, Baldauf SL, Mayhew PJ (2009) Eusociality and the success of the termites: insights from a supertree of dictyopteran families. J Evol Biol 22:1750–1761PubMedCrossRefGoogle Scholar
  32. DeHeer CJ, Kamble ST (2008) Colony genetic organization, fusion and Inbreeding in Reticulitermes flavipes from the Midwestern U.S. Sociobiology 51:307–325Google Scholar
  33. DeHeer CJ, Kutnik M, Vargo EL, Bagnères A-G (2005) The breeding system and population structure of the termite Reticulitermes grassei in Southern France. Heredity 95:408–415PubMedCrossRefGoogle Scholar
  34. DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441PubMedCrossRefGoogle Scholar
  35. DeHeer CJ, Vargo EL (2006) An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav Ecol Sociobiol 59:753–761CrossRefGoogle Scholar
  36. DeHeer CJ, Vargo EL (2008) Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the termite Reticulitermes flavipes. Insectes Soc 55:190–199CrossRefGoogle Scholar
  37. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  38. Dronnet S, Bagnères A-G, Juba TR, Vargo EL (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol Ecol Notes 4:127–129CrossRefGoogle Scholar
  39. Dronnet S, Chapuisat M, Vargo EL et al (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol Ecol 14:1311–1320PubMedCrossRefGoogle Scholar
  40. Dupont L, Roy V, Bakkali A, Harry M (2009) Genetic variability of the soil-feeding termite Labiotermes labralis (Termitidae, Nasutitermitinae) in the Amazonian primary forest and remnant patches. Insect Conserv Divers 2:53–61CrossRefGoogle Scholar
  41. Fang R, Huang L, Zhong JH (2008) Surprising low levels of genetic diversity of Formosan subterranean termites in south China as revealed by the COII gene (Isoptera: Rhinotermitidae). Sociobiology 51:1–20Google Scholar
  42. Fei HX, Henderson G (2003) Comparative study of incipient colony development in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insectes Soc 50:226–233CrossRefGoogle Scholar
  43. Fisher ML, Gold RE, Vargo EL, Cognato AI (2004) Behavioral and genetic analysis of colony fusion in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 44:565–576Google Scholar
  44. Fuchs A, Heinze J, Reber-Funk C, Korb J (2003) Isolation and characterization of six microsatellite loci in the drywood termite Cryptotermes secundus (Kalotermitidae). Mol Ecol Notes 3:355–357CrossRefGoogle Scholar
  45. Global Invasive Species Database (2010) Coptotermes formosanus (insect). Available from: http://www.issg.org/database/species/ecology.asp?si=61&fr=1&sts=&lang=EN [Accessed 1 Jan 2010]
  46. Goodisman MAD, Crozier RH (2002) Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56:70–83PubMedGoogle Scholar
  47. Goodisman MAD, Evans TA, Ewen JG, Crozier RH (2001) Microsatellite markers in the primitive termite Mastotermes darwiniensis. Mol Ecol Notes 1:250–251CrossRefGoogle Scholar
  48. Hacker M, Kaib M, Bagine RKM et al (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14:1527–1532PubMedCrossRefGoogle Scholar
  49. Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232CrossRefGoogle Scholar
  50. Hamilton WD (1978) Evolution and diversity under bark. In: Mound LA, Waloff N (eds) Diversity of insect faunas. Blackwell Scientific Publications, London, pp 154–175Google Scholar
  51. Harry M, Roose CL, Garnier-Sillam E, Solignac M (2001) Microsatellite markers in soil-feeding termites (Cubitermes subarquatus, Isoptera, Termitidae, Termitinae). Mol Ecol Notes 1:226–228CrossRefGoogle Scholar
  52. Harry M, Roy V, Mercier A et al (2007) Isolation and characterization of microsatellite markers in Labiotermes labralis (Isoptera, Termitidae, Nasutitermitinae). Mol Ecol Notes 7:121–123CrossRefGoogle Scholar
  53. Hayashi Y, Kitade O, Gonda M et al (2005) Diverse colony genetic structures in the Japanese subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Sociobiology 46:175–184Google Scholar
  54. Hayashi Y, Kitade O, Kojima J-I (2002) Microsatellite loci in the Japanese subterranean termite, Reticulitermes speratus. Mol Ecol Notes 2:518–520CrossRefGoogle Scholar
  55. Holway DA, Lach L, Suarez AV et al (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  56. Husseneder C, Brandl R, Epplen C et al (1998) Variation between and within colonies in the termite: morphology, genomic DNA, and behaviour. Mol Ecol 7:983–990CrossRefGoogle Scholar
  57. Husseneder C, Brandl R, Epplen C et al (1999) Within-colony relatedness in a termite species: genetic roads to eusociality? Behaviour 136:1045–1063CrossRefGoogle Scholar
  58. Husseneder C, Grace JK (2001a) Evaluation of DNA fingerprinting, aggression tests and morphometry as tools for colony delineation of the Formosan subterranean termite. J Insect Behav 14:173–186CrossRefGoogle Scholar
  59. Husseneder C, Grace JK (2001b) Similarity is relative: hierarchy of genetic similarities in the Formosan subterranean termite (Isoptera: Rhinotermitidae) in Hawaii. Environ Entomol 30:262–266CrossRefGoogle Scholar
  60. Husseneder C, Grace JK, Messenger MT et al (2003a) Describing the spatial and social organization of Formosan subterranean termite colonies in Armstrong Park, New Orleans. Sociobiology 41:61–65Google Scholar
  61. Husseneder C, Messenger MT, Su N-Y et al (2005) Colony social organization and population genetic structure of an introduced population of Formosan subterranean termite from New Orleans, Louisiana. J Econ Entomol 98:1421–1434PubMedCrossRefGoogle Scholar
  62. Husseneder C, Powell JE, Grace JK et al (2008) Worker size in the Formosan subterranean termite in relation to colony breeding structure as inferred from molecular markers. Environ Entomol 37:400–408PubMedCrossRefGoogle Scholar
  63. Husseneder C, Simms DM (2008) Size and heterozygosity influence partner selection in the Formosan subterranean termite. Behav Ecol 19:764–773PubMedCrossRefGoogle Scholar
  64. Husseneder C, Simms DM, Riegel C (2007) Evaluation of treatment success and patterns of reinfestation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 100:1370–1380PubMedCrossRefGoogle Scholar
  65. Husseneder C, Simms DM, Ring DR (2006) Genetic diversity and genotypic differentiation between the sexes in swarm aggregations decrease inbreeding in the Formosan subterranean termite. Insectes Soc 53:212–219CrossRefGoogle Scholar
  66. Husseneder C, Vargo EL, Grace JK (2003b) Molecular genetic methods: new approaches to termite biology. In: Goodell B, Schultz TP, Nicholas DD (eds) Wood deterioration and preservation: advances in our changing world. American Chemical Society Symposium Series 845. American Chemical Society, Washington, DC, pp 358–370CrossRefGoogle Scholar
  67. Indrayani Y, Matsumura KEI, Yoshimura T et al (2006) Development of microsatellite markers for the drywood termite Incisitermes minor (Hagen). Mol Ecol Notes 6:1249–1251CrossRefGoogle Scholar
  68. Jeffreys AJ, Wilson V, Thein SL (1985) Inidividual-specific “fingerprints” of human DNA. Nature 316:76–79PubMedCrossRefGoogle Scholar
  69. Jenkins TM, Basten CJ, Kresovich S, Forschler BT (1999) Mitochondrial gene sequence questions Reticulitermes sp. social structure (Isoptera: Rhinotermitidae). Sociobiology 34:161–172Google Scholar
  70. Jenkins TM, Dean RE, Forschler BT (2002) DNA technology, interstate commerce, and the likely origin of Formosan subterranean termite (Isoptera: Rhinotermitidae) infestation in Atlanta, Georgia. J Econ Entomol 95:381–389PubMedCrossRefGoogle Scholar
  71. Jenkins TM, Dean RE, Verkerk R, Forschler BT (2001) Phylogenetic analyses of two mitochondrial genes and one nuclear intron region illuminate European subterranean termite (Isoptera: Rhinotermitidae) gene flow, taxonomy, and introduction dynamics. Mol Phylogenet Evol 20:286–293PubMedCrossRefGoogle Scholar
  72. Jenkins TM, Jones SC, Lee C-Y et al (2007) Phylogeography illuminates maternal origins of exotic Coptotermes gestroi (Isoptera: Rhinotermitidae). Mol Phylogenet Evol 42:612–621PubMedCrossRefGoogle Scholar
  73. Johnson RN, Starks PT (2004) A surprising level of genetic diversity in an invasive wasp: Polistes dominulus in the northeastern United States. Ann Entomol Soc Am 97:732–737CrossRefGoogle Scholar
  74. Jones SC, La Fage JP, Howard RW (1988) Isopteran sex ratios: phylogenetic trends. Sociobiology 14:89–118Google Scholar
  75. Kaib M, Hacker M, Brandl R (2001) Egg-laying in monogynous and polygynous colonies of the termite Macrotermes michaelseni (Isoptera, Macrotermitidae). Insectes Soc 48:231–237CrossRefGoogle Scholar
  76. Kaib M, Hacker M, Over I et al (2000) Microsatellite loci in Macrotermes michaelseni (Isoptera: Termitidae). Mol Ecol 9:502–504PubMedCrossRefGoogle Scholar
  77. Kaib M, Husseneder C, Epplen C et al (1996) Kin-biased foraging in a termite. Proc R Soc Lond B 263:1527–1532CrossRefGoogle Scholar
  78. Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol Evol 12:99–103PubMedCrossRefGoogle Scholar
  79. Kitade O, Hayashi Y, Kikuchi Y, Kawarasaki S (2004) Distribution and composition of colony founding associations of a subterranean termite, Reticulitermes kanmonensis. Entomol Sci 7:1–8CrossRefGoogle Scholar
  80. Kolbe JJ, Glor RE, Schettino LR et al (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  81. Kutnik M, Uva P, Brinkworth L, Bagnères A-G (2004) Phylogeography of two European Reticulitermes (Isoptera) species: the Iberian refugium. Mol Ecol 13:3099–3113PubMedCrossRefGoogle Scholar
  82. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive species. Proc Natl Acad Sci USA 104:3883–3888PubMedCrossRefGoogle Scholar
  83. Lefebvre T, Châline N, Limousin D et al (2008) From speciation to introgressive hybridization: the phylogeographic structure of an island subspecies of termite, Reticulitermes lucifugus corsicus. BMC Evol Biol 8:38PubMedCrossRefGoogle Scholar
  84. Leniaud L, Dedeine F, Pichon A et al (2010) Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae). Biol Invasions 12:1389–1402CrossRefGoogle Scholar
  85. Lenz M, Barrett RA (1982) Neotenic formation in field colonies of Coptotermes lacteus (Froggatt) in Australia, with comments on the roles of neotenics in the genus Coptotermes (Isoptera, Rhinotermitidae). Sociobiology 7:47–59Google Scholar
  86. Lenz M, Runko S (1993) Long-term impact of orphaning on field colonies of Coptotermes lacteus (Froggatt) (Isoptera: Rhinotermitidae). Insectes Soc 40:439–456CrossRefGoogle Scholar
  87. Lepage M, Darlington JPEC (2000) Population dynamics of termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 333–361Google Scholar
  88. Loxdale HD, Lushai G (1998) Molecular markers in entomology. Bull Entomol Res 88:577–600CrossRefGoogle Scholar
  89. Luchetti A, Marini M, Mantovani B (2005) Mitochondrial evolutionary rate and speciation in termites: data on European Reticulitermes taxa (Isoptera, Rhinotermitidae). Insectes Soc 52:218–221CrossRefGoogle Scholar
  90. Luchetti A, Marini M, Mantovani B (2007) Filling the European gap: biosystematics of the eusocial system Reticulitermes (Isoptera, Rhinotermitidae) in the Balkanic Peninsula and Aegean area. Mol Phylogenet Evol 45:377–383PubMedCrossRefGoogle Scholar
  91. Luchetti A, Trenta M, Mantovani B, Marini M (2004) Taxonomy and phylogeny of north Mediterranean Reticulitermes termites (Isoptera, Rhinotermitidae): a new insight. Insectes Soc 51:117–122CrossRefGoogle Scholar
  92. Luykx P (1993) Allozyme markers and formal Mendelian genetics of the termite Incisitermes schwarzi (Isoptera: Kalotermitidae). Sociobiology 21:185–192Google Scholar
  93. Marini M, Mantovani B (2002) Molecular relationships among European samples of Reticulitermes (Isoptera, Rhinotermitidae). Mol Phylogenet Evol 22:454–459PubMedCrossRefGoogle Scholar
  94. Matsuura K, Fujimoto M, Goka K (2004) Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Soc 51:325–332CrossRefGoogle Scholar
  95. Matsuura K, Nishida T (2001) Colony fusion in a termite: what makes the society “open”? Insectes Soc 48:378–383CrossRefGoogle Scholar
  96. Matsuura K, Vargo EL, Kawatsu K et al (2009) Queen succession through asexual reproduction in termites. Science 323:1687PubMedCrossRefGoogle Scholar
  97. Messenger MT, Mullins AJ (2005) New flight distance recorded for Coptotermes formosanus (Isoptera: Rhinotermitidae). Fla Entomol 88:99–100CrossRefGoogle Scholar
  98. Muirhead JR, Gray DK, Kelly DW et al (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035PubMedCrossRefGoogle Scholar
  99. Myles TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–87Google Scholar
  100. Nobre T, Nunes L, Bignell D (2008) Colony interactions in Reticulitermes grassei population assessed by molecular genetic methods. Insectes Soc 55:66–73CrossRefGoogle Scholar
  101. Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, NY, pp 233–282Google Scholar
  102. Pamilo P, Gertsch P, Thorén P, Seppä P (1997) Molecular population genetics of social insects. Annu Rev Ecol Syst 28:1–25CrossRefGoogle Scholar
  103. Park YC, Kitade O, Schwarz M et al (2006) Intraspecific molecular phylogeny, genetic variation and phylogeography of Reticulitermes speratus (Isoptera: Rhinotermitidae). Mol Cells 21:89–103PubMedGoogle Scholar
  104. Parman V, Vargo EL (2008) Population density, species abundance, and breeding structure of subterranean termite colonies in and around infested houses in central North Carolina. J Econ Entomol 101:1349–1359PubMedCrossRefGoogle Scholar
  105. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  106. Reilly LM (1987) Measurements of inbreeding and average relatedness in a termite population. Am Nat 130:339–349CrossRefGoogle Scholar
  107. Roisin Y (1993) Selective pressures on pleometrosis and secondary polygyny: a comparison of termites and ants. In: Keller L (ed) Queen number and sociality in insects. Oxford Science Publications, Oxford, pp 402–422Google Scholar
  108. Roisin Y, Lenz M (2002) Origin of male-biased sex allocation in orphaned colonies of the termite, Coptotermes lacteus. Behav Ecol Sociobiol 51:472–479CrossRefGoogle Scholar
  109. Roisin Y, Pasteels JM (1985) Imaginal polymorphism and polygyny in the Neo-Guinean termite Nasutitermes princeps (Desneux). Insectes Soc 32:140–157CrossRefGoogle Scholar
  110. Roisin Y, Pasteels JM (1986) Reproductive mechanisms in termites: polycalism and polygyny in Nasutitermes polygynus and Nasutitermes costalis. Insectes Soc 33:149–167CrossRefGoogle Scholar
  111. Rosengaus RB, Traniello JFA (1993) Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc Natl Acad Sci USA 90:6641–6645PubMedCrossRefGoogle Scholar
  112. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284PubMedCrossRefGoogle Scholar
  113. Ross KG, Keller L (1995) Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu Rev Ecol Syst 26:631–656CrossRefGoogle Scholar
  114. Schmidt AM, Trindl A, Korb J (2007) Isolation and characterization of 10 microsatellite loci in the magnetic termite, Amitermes meridionalis (Isoptera: Termitidae). Mol Ecol Notes 7:1045–1047CrossRefGoogle Scholar
  115. Shellman-Reeve JS (1996) Operational sex ratios and lipid reserves in the dampwood termite Zootermopsis nevadensis (Hagen) (Isoptera: Termopsidae). J Kans Entomol Soc 69:139–146Google Scholar
  116. Shellman-Reeve JS (1997) The spectrum of eusociality in termites. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 52–93Google Scholar
  117. Shellman-Reeve JS (2001) Genetic relatedness and partner preference in a monogamous wood-dwelling termite. Anim Behav 61:869–876CrossRefGoogle Scholar
  118. Simms D, Husseneder C (2009) Assigning individual alates of the Formosan subterranean termite to their colonies of origin within the context of an area-wide management program. Sociobiology 53:631–650Google Scholar
  119. Strong KL, Grace JK (1993) Low allozyme variation in Formosan subterranean termite (Isoptera: Rhinotermitidae) colonies in Hawaii. Pan Pac Entomol 69:51–56Google Scholar
  120. Su N-Y (2003) Overview of the global distribution and control of the Formosan subterranean termite. Sociobiology 41:7–16Google Scholar
  121. 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 99:352–363CrossRefGoogle Scholar
  122. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203PubMedCrossRefGoogle Scholar
  123. Syren RM, Luykx P (1977) Permanent segmental interchange complex in the termite Incisitermes schwarzi. Nature 266:167–168PubMedCrossRefGoogle Scholar
  124. Szalanski AL, Scheffrahn RH, Austin JW et al (2004) Molecular phylogeny and biogeography of Heterotermes (Isoptera: Rhinotermitidae) in the West Indies. Ann Entomol Soc Am 97:556–566CrossRefGoogle Scholar
  125. Thompson GJ, Hebert PDN (1998a) Population genetic structure of the neotropical termite Nasutitermes nigriceps (Isoptera: Termitidae). Heredity 80:48–55CrossRefGoogle Scholar
  126. Thompson GJ, Hebert PDN (1998b) Probing termite social systems through allozyme and mtDNA analysis: a case study of Nasutitermes nigriceps and Nasutitermes costalis (Isoptera, Termitidae). Insectes Soc 45:289–299CrossRefGoogle Scholar
  127. Thompson GJ, Lenz M, Crozier RH (2000) Microsatellites in the subterranean, mound-building termite Coptotermes lacteus (Isoptera: Rhinotermitidae). Mol Ecol 9:1932–1934PubMedCrossRefGoogle Scholar
  128. Thompson GJ, Lenz M, Crozier RH, Crespi BJ (2007) Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system. Aust J Zool 55:219–227CrossRefGoogle Scholar
  129. Thorne BL (1982) Polygyny in termites: multiple primary queens in colonies of Nasutitermes corniger (Motschuls) (Isoptera: Termitidae). Insectes Soc 29:102–117CrossRefGoogle Scholar
  130. Thorne BL (1984) Polygyny in the Neotropical termite Nasutitermes corniger: life history consequences of queen mutualism. Behav Ecol Sociobiol 14:117–136CrossRefGoogle Scholar
  131. Thorne BL (1985) Termite polygyny: the ecological dynamics of queen mutualism. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. G. Fischer, Stuttgart, New York, NY, pp 325–342Google Scholar
  132. 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 USA 100:12808–12813PubMedCrossRefGoogle Scholar
  133. Thorne BL, Traniello JFA, Adams ES, Bulmer M (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological and genetic studies. Ethol Ecol Evol 11:149–169CrossRefGoogle Scholar
  134. Tsutsui ND, Suarez AV, Grosberg RK (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci USA 100:1078–1083PubMedCrossRefGoogle Scholar
  135. Uva P, Clément J-L, Austin JW et al (2004b) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Mol Phylogenet Evol 30:344–353PubMedCrossRefGoogle Scholar
  136. Uva P, Clément J-L, Bagnères A-G (2004a) Colonial and geographic variations in agonistic behaviour, cuticular hydrocarbons and mtDNA of Italian populations of Reticulitermes lucifugus (Isoptera, Rhinotermitidae). Insectes Soc 51:163–170CrossRefGoogle Scholar
  137. Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–820PubMedCrossRefGoogle Scholar
  138. Vargo EL (2003a) Genetic structure of Reticulitermes flavipes and R. virginicus (Isoptera: Rhinotermitidae) colonies in an urban habitat and tracking of colonies following treatment with hexaflumuron bait. Environ Entomol 32:1271–1282CrossRefGoogle Scholar
  139. Vargo EL (2003b) Hierarchical analysis of colony and population genetic structure in the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57:2805–2818PubMedGoogle Scholar
  140. Vargo EL, Carlson JC (2006) Comparative study of breeding systems of sympatric subterranean termites (Reticulitermes flavipes and R. hageni) in central North Carolina using two classes of molecular genetic markers. Environ Entomol 35:173–187CrossRefGoogle Scholar
  141. Vargo EL, Henderson G (2000) Identification of polymorphic microsatellite loci in the Formosan subterranean termite Coptotermes formosanus Shiraki. Mol Ecol 9:1935–1938PubMedCrossRefGoogle Scholar
  142. Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403PubMedCrossRefGoogle Scholar
  143. Vargo EL, Husseneder C, Grace JK (2003) Colony and population genetic structure of the Formosan subterranean termite, Coptotermes formosanus, in Japan. Mol Ecol 12:2599–2608PubMedCrossRefGoogle Scholar
  144. Vargo EL, Husseneder C, Woodson D et al (2006a) Genetic analysis of colony and population genetic structure of three introduced populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the Continental United States. Environ Entomol 35:151–166CrossRefGoogle Scholar
  145. Vargo EL, Juba TR, DeHeer CJ (2006b) Relative abundance and comparative breeding structure of subterranean termite colonies (Reticulitermes flavipes, R. hageni, R. virginicus, and Coptotermes formosanus) in a South Carolina lowcountry site as revealed by molecular markers. Ann Entomol Soc Am 99:1101–1109CrossRefGoogle Scholar
  146. Wang JS, Grace JK (2000) Genetic relationship of Coptotermes formosanus (Isoptera: Rhinotermitidae) populations from the United States and China. Sociobiology 36:7–19Google Scholar
  147. Zhang DX, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584PubMedCrossRefGoogle Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA
  2. 2.Department of EntomologyLSU Agricultural CenterBaton RougeUSA

Personalised recommendations