Breeding Patterns and Population Genetics of Eastern Subterranean Termites Reticulitermes flavipes in Urban Environment of Nebraska, United States

Abdul Hafiz Ab Majid, Shripat Kamble, Hong Chen


Reticulitermes flavipes (Kollar) has become the most destructive subterranean termite pest, on urban structures in Nebraska. In this study, we used seven microsatellite loci to infer the colony breeding system and population genetic structure among 20 infested urban structures in Nebraska. Our data revealed that 17 structures were infested by simple family colonies of R. flavipes, while, the remaining three were infested with mixed family colonies. The measure of population differentiation, FCT value (0.459) indicated that all the 20 urban colonies (10 - 410 km apart) represented pronounced levels of genetic differentiation. The Mantel test disclosed a weak and significantly-positive correlation between genetic and geographic distance (slope = 0.0009, P = 0.001). The urban populations of R. flavipes in Nebraska possessed a breeding system characterized by monogamous pairs of outbred reproductives with excessive heterozygosity.


Subterranean termites; Reticulitermes flavipes; urban environment; colony breeding; genetic structure

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Ab Majid A.H., Kamble S.T., Miller N.J. (2013). Colony genetic structure of Reticulitermes flavipes (Kollar) from Natural Populations in Nebraska. Journal of Entomological Science, 48: 222–233.

Booth, W., Brent, C.S., Calleri, D.V., Rosengaus, R. B., J. F. A. Trainello, J. F. A., &. Vargo, E.L. (2012). Population genetic structure and colony breeding system in dampwood termites (Zootermopsis angusticollis and Z. nevadensisnutinggi). Insectes Soc. 59: 127-137.

Bulmer, M. S., Adams, E. S., & J. F. A. Traniello, J. F. A. (2001). Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav. Ecol. Sociobiol. 49: 236-243.

Bulmer, M. S., & Traniello. J. F. A. (2002). Foraging range expansion and colony genetic organization in the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae).

Environ. Entomol. 31: 293-298.

Chapman, R. E., & Bourke, A. F. G. (2001). The influence of sociality on the conservation biology of social insects. Ecol. Lett. 4: 650-662.

Chapius, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24: 621-631.

Clement, J. L. (1981). Enzymatic polymorphism in the European populations of various Reticulitermes species (Isoptera). pp. 49–61. In P. E.Howse, and J. L. Clement [eds.],

Biosytematics Social Insects. Academic Press, London.

Copren, K. A. (2007). Characterization of microsatellite loci in the western subterranean térmite Reticulitermes hesperus and cross-amplification in closely related cryptic species. J. Insect. Sci. 7: 17.

Cornuet, J. M., & G. Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.

Crissman J. R, Booth, W., Santangelo, R. G., Mukha, D. V., Vargo, E. L. & Schal, C. ( 2010). Population genetic structure of the German cockroach (Blattodea: Blatellidae) in apartment

buildings. J. Med. Entomol. 74; 553-564.

Crozier, R. H., & Pamilo, P. (1996). Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford

Crozier, R. H., Smith, B. H., & Crozier, Y. C. (1987). Relatedness and population structure of the primitively eusocial bee Lasioglossum zephyrum (Hymenoptera: Halictidae) in Kansas. Evol. 41: 902-910.

Curl, G. (2008). A strategic analysis of the U.S. structural pest control industry, Specialty Products Consultants, LLC, Mendham, NJ.

DeHeer, C. J., & Kamble, S.T. (2008). Colony genetic organization, fusion and inbreeding in Reticulitermes flavipes from the Midwestern U.S. Sociobiology, 51: 307-325.

DeHeer, C. J., & Vargo, E.L. (2004). Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as evealed by foraging patterns over time and space. Mol. Ecol.

: 431-441.

DeHeer, C. J., & Vargo, E.L. (2006). An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav. Ecol. Sociobiol. 59: 753-761.

DeHeer, C. J., & Vargo, E.L. (2008). Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the térmite Reticulitermes flavipes. Insectes Soc. 55: 190-199.

DeHeer, C. J., Kutnik, M., Vargo, E. L., & Bagneres, A.G. (2005). The breeding system and population structure of the termite Reticulitermes grassei in southern France. Heridity 95: 408-415.

Fraser, R. N. (1998). Multispectral remote sensing of turbidity among Nebraska Sand Hills lakes. International Journal of Remote Sensing.19: 3011-3016.

Goodisman, M. A. D., & Crozier, R. H. (2002). Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evol. 56: 70-83.

Google Inc. (2013). Google Earth 7,

Goudet, J. (2001).FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). (

Goudet, J., Raymond, M., DeMeeus, T., & Rousset, F. (1996). Testing differentiation in diploid populations. Genetics. 144: 1933-140.

Huang, Q., Li, G., Husseneder, C., & Lei, C. (2013). Genetic analysis of population structure and reproductive mode of the termite Reticulitermes chinensis Snyder. PLoS ONE 8:1– 12.

Husen, T. J., Kamble, S. T., & Stone, J.M. (2006). A characterization of subterranean termites in Nebraska using micro-morphological and molecular techniques. Sociobiology, 48: 247-266.

Husseneder, C., Vargo, E. L. & Grace, J (2003). Molecular genetic methods: New approaches to termite biology. Pp. 358-370. In: B. Goodell, D. D. Nicholas and T. P. Schultz (eds.), Wood deterioration and preservation: advances in our changing world. Oxford University Press.

Jenkins, T. M., Basten, C. J. & Dean, R. (1999). Matriarchal genetic structure of Reticulitermes (Isoptera: Rhinotermitidae) populations. Sociobiology, 33: 239 – 263.

Liu Y.Z., Tan S.J., Wei H.J., Sun J.N., Tang G.Q. & Chen S. (2002). The developmental length for flight and inhibition from reproductives on individual differentiation of colony of Reticulitermes chinensis Snyder. Acta Entomol. Sin. 45: 346–351.

Luikart, G, & Cornuet, J.M. (1998). Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12: 228-237.

Ma Y. 1989. Study on the biological characteristics of Reticulitermes labralis in Bengbu. Sci. Tech. Termites. 6: 29–31.

Matsuura, K., & Nishida, T. (2001). Colony fusion in a termite: what makes a society ‘open’? Insectes Soc. 48: 378-383.

Miller, M. P. (1997). Tools for population genetic analyses (TFPGA) 2.3: A window’s program for analysis of allozyme and molecular population genetics data. Computer software distributed by the author.

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 89: 583-590.

Nobre, T., Nunes, L., & Bignell, D. E. (2008). Colony interactions in a termite population assessed bybehavioral and molecular genetic methods. Insectes Soc. 55: 66-73.

Parman, V., & Vargo, E.L. (2008). Population density, species abundance, and breeding structure of subterranean térmite colonies in and around infested houses in central North

Carolina. J. Econ. Entomol. 101: 1349-1359.

Peakall, R., & Smouse, P.E. (2005). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes. 6: 288-295.

Perdereau, E., Bagneres, A.G. & Dupont, S. (2010). High occurrence of colony fusion in an European population of the America termite Reticulitermes flavipes. Insectes Soc. 57: 393-402.

Perdereau, E., Bagneres, A.G., Vargo, E.L., Baudouin, G., Xu, Y., Labadie, P., Dupont, S., Dedeine, F. (2015). Relationship between invasion success and colony breeding structure in a subterranean termite. Mol. Ecol. 24, 2125–2142.

Porter, J., Deere, D., Hardman, M., Edwards, C., & Pickup, R. (1997). Go with the flow: use of flow cytometry in environmental targeted oligonucleotide probe for fluorescent labelling of microbiology. FEMS Microbiol. Ecol. 24: 93–101.

Pusadee, T., Jamjod, S., Chiang, Y. C., Rerkasem, B. & Schaal, B. A. (2009). Genetic structure and isolation by distance of Thai rice. P.N.A.S. 106: 13880-1385.

Raymond, M., & Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.

Ross, K. G. (2001). Molecular ecology of social behavior: analyses of breeding systems and genetic structure. Mol. Ecol. 10: 265-284.

Ross, K. G., Vargo, E. L., Keller, L. & Trager, J. C. (1993). Effect of a founder event on variation in the genetic sexdetermining system of the fire ants Solenopsis invicta. Genetics. 135: 843-854.

Thorne, B. L. (1997). Evolution of eusociality in termites. Annu. Rev. Ecol. Evol. Syst. 28: 27-54.

Thorne, B. L., Traniello, J. F. A., Adams, E. S. & Bulmer, M. (1999). Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera: Rhinotermitidae): a review of evidence from behavioral, ecological, and genetic studies.Ethol. Ecol. Evol. 11: 149-169.

Tsutsui, N. D, Suarez, A. V., & Grosberg, R. K. (2003). Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. P.N.A.S, U.S.A.100: 1078–1083.

Vargo, E. L. (2000). Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol. Ecol. 9: 817-820.

Vargo, E. L. (2003a). Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evol. 57: 2805-2818.

Vargo, E. L. (2003b). 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: 1271-1282.

Vargo, E. L., & Carlson, J. R. (2006). Comparative study of breeding systems of sympatric subterranean térmites (Reticulitermes flavipes and R. hageni) in Central North Carolina using two classes of molecular genetic markers. Environ. Entomol. 35: 173-187.

Vargo, E. L., & Husseneder, C. (2009). The biology of subterranean termites: Insight from molecular studies on Reticulitermes and Coptotermes. Annu. Rev. Entomol. 54: 379-403.

Vargo, E. L., & Husseneder, C. (2011). Genetic structure of termite colonies and populations. pp. 321-348. In D. E. Bignell, Y. Roisin, and N. Lo. (eds.). Biology of Termites: A Modern Synthesis. Springer.

Vargo, E. L., Hussender, C., Woodson, D., Waldvogel, M. G. & Grace, J. K. (2006a). Genetic analysis of colony and population structure of three introduce populations of the Formoson Subterranean Termite (Isoptera: Rhinotermitidae) in continental United States. Environ. Entomol. 35: 151-166.

Vargo, E. L., Juba, T. R. & DeHeer, C.J. (2006b). Relative abundance and comparative breeding structure of subterranean termite colonies (Reticulitermes flavipes, Reticulitermes hageni, Reticulitermes virginicus, and Coptotermes formosanus) in a South Carolina low country site as revealed by molecular markers. Ann. Entomol. Soc. Am. 99: 1101- 1109.

Vargo, E.L., Leniaud, L., Swoboda, L.E., Diamond, S.E.,Michael M.D., Miller, D.M., & Bagners A.G. (2013). Clinal variation in colony breeding structure and level of inbreeding in the subterranean termites R. flavipes and R. grassei. Mol. Ecol. 22:1447-1462

Wade, M. J., & Kalisz, S (1990). The causes of natural selection. Evol. 44: 1947-1955.

Xing, L. X., Wu, J., Wang, K., Kong, X.H., Liu, M.H., & Su, X.H. (2015). The ‘floppy-wing’ morph of the subterranean termite Reticulitermes labralis has a secondary reproductive function. Insectes Sociaux. 62: 183–191.



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