Population Genetic Structure and Breeding Pattern of Higher Group Termite Globitermes sulphureus (Haviland) (Blattodea:Termitidae)

Nur Aizatul Nathasha Khizam, Abdul Hafiz Ab Majid


The subterranean termite Globitermes sulphureus (Blattodea: Termitidae) can be found in tropical regions. We chose seven novel species-specific microsatellite markers to infer the breeding pattern of G. sulphureus based on its colony and population genetic structure in eight selected populations (natural-n = 4 and metropolitan-n = 4) in Kedah and Penang, Malaysia. A strong correlation with their geographical location is shown by the acquired genetic gap for all studied populations from this study. The breeding pattern of family structure and comparisons of estimated F-statistics among G. sulphureus workers suggests 60% of all colonies are mixed families, whereas the remaining are simple families. Average relatedness values within simple and mixed family colonies are similar (r = 0.121). Positive fixation index FST values (FST = 0.086) indicate all eight populations (>500 m apart) have a significantly moderate genetic differentiation and low levels of inbreeding based on the low overall inbreeding coefficient FIT value of 0.391. Furthermore, four populations; Palapes USM (PU), Tmn Astana (TA), Kg Teluk (KT), and Penang National Park (NP), deviate from Hardy–Weinberg equilibrium (HWE, all p = 0.000) and five studied polymorphic loci (GS1, GS10, GS15, GS27 and GS29) are possibly under selection. The findings also reveal signs of a bottleneck effect in two populations: Tikam Batu (TB) and Penang National Park (NP), indicating genetic drift.


Globitermes sulphureus; higher group termite; population genetics; polymorphism; natural regions; metropolitan regions

Full Text:



Ab Majid, A.H. & Ahmad, A.H. (2011). Foraging population, territory and control of Globitermes sulphureus (Isoptera: Termitidae) with fipronil in Penang, Malaysia. Malaysian Applied Biology, 40: 61-65.

Ab Majid, A.H., Ahmad, A.H., Rashid, M.Z.A. & Rawi, C.S.M. (2007). Field efficacy of imidacloprid on Globitermes sulphureus (Isoptera; Termitidae) (Subterranean Termite) in Penang. Journal of Bioscience, 18: 107-112.

Ab Majid, A.H., Kamble, S. & Chen, H. (2018). Breeding Patterns and Population Genetics of Eastern Subterranean Termites Reticulitermes flavipes in Urban Environment of Nebraska, United States. Sociobiology, 65: 506-514. doi: 10.13 102/sociobiology.v65i3.2821

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

Aldrich, B.T. & Kambhampati, S. (2007). Population structure and colony composition of two Zootermopsis nevadensis subspecies. Heredity, 99: 443.

Allendorf, F.W. (2017). Genetics and the conservation of natural populations: allozymes to genomes. Molecular Ecology, 26: 420-430.

Aluko, G.A. & Husseneder, C. (2007). Colony dynamics of the Formosan subterranean termite in a frequently disturbed urban landscape. Journal of Economic Entomology, 100: 1037-1046.

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

Charlesworth, D. & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics, 18: 237-68. doi: 10.1146/annurev.es.18.110187.001321

Cheng, S., Lee, C.T., Wan, M.N. & Tan, S.G. (2013). Microsatellite markers uncover cryptic species of Odontotermes (Termitoidae: Termitidae) from Peninsular Malaysia. Gene, 518(2): 412-418.

Clément, J.L., Bagneres, A.G., Uva, P., Wilfert, L., Quintana, A., Reinhard, J. & Dronnet, S. (2001). Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insectes Sociaux, 48: 202-215.

DeHeer, C.J., and Vargo. E.L. (2004). Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Molecular Ecology, 13: 431-441.

DeHeer, C.J., Kutnik, M., Vargo, E.L. & Bagnères, A.G. (2005). The breeding system and population structure of the termite Reticulitermes grassei in southwestern France. Heredity, 95: 408-15.

Dronnet, S., Chapuisat, M., Vargo, E.L., Caroline, L., & Bagnères, A.G. (2005). Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Molecular Ecology, 14: 1311-1320. doi: 10.1111/j.1365-294X.2005.02508.x

Dronnet, S., Perdereau, E., Kutnik, M., Dupont, S. & Bagnères, A.G. (2015). Spatial structuring of the population genetics of a European subterranean termite species. Ecology and Evolution, 5: 3090-3102.

Fougeyrollas, R., Dolejšová, K., Křivánek, J., Sillam-Dussès, D., Roisin, Y., Hanus, R. & Roy, V. (2018). Dispersal and mating strategies in two neotropical soil-feeding termites, Embiratermes neotenicus and Silvestritermes minutus (Termitidae, Syntermitinae). Insectes Sociaux, 65: 251-262. doi: 10.1007/s00040-018-0606-y

Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126: 131-140. doi:10.1016/j.biocon.2005.05.002

Gathorne-Hardy, F.J., Jones, D.T. & Mawdsley, N.A. (2000). The recolonization of the Krakatau islands by termites (Isoptera), and their biogeographical origins. Biological Journal of the Linnaean Society, 71: 251-267. doi: 10.1111/j.1095-8312.2000.tb01257.x

Glass, D. (2017). The social structure of the hazel dormouse (Muscardinus avellanarius) (Doctoral dissertation, University of Brighton).

Goodisman, M.A., & Crozier, R.H. (2002). Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution, 56: 70-83. doi: 10.1111/j.0014-3820. 2002.tb00850.x

Goudet, J. (2001). FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices Version 2.9.3.

Guichoux, E., Lagache, L., Wagner, S., Chaumeil, P., Léger, P., Lepais, O., & Petit, R.J. (2011). Current trends in microsatellite genotyping. Molecular Ecology Resources, 11: 591-611. doi: 10.1111/j.1755-0998.2011.03014.x

Hamilton, M. (2011). Population genetics. John Wiley & Sons.

Hardy, O.J., Charbonnel, N., Fréville, H. & Heuertz, M. (2003). Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics, 163: 1467-1482.

Harrison, M. C., Jongepier, E., Robertson, H. M., Arning, N., Bitard-feildel, T., Chao, H. & Bornberg-bauer, E. (2018). Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution, 2. doi: 10.1038/s41559-017-0459-1

Howard, K.J., Johns, P.M., Breisch, N.L. & Thorne, B.L. (2013). Frequent colony fusions provide opportunities for helpers to become reproductives in the termite Zootermopsis nevadensis. Behavioral Ecology and Sociobiology, 67: 1575-1585.

Hussin, N.A. & Ab Majid, A.H. (2017). Inter and intra termites colonies comparisons of gut microbial diversity from worker and soldier caste of Globitermes sulphureus (Blattodea: Termitidae) using 16S rRNA gene. Malaysian Journal of Microbiology, 13: 228-234.

Hussin, N.A., Zarkasi, K.Z. & Ab Majid, A.H. (2018). Characterization of gut bacterial community associated with worker and soldier castes of Globitermes sulphureus Haviland (Blattodea: Termitidae) using 16S rRNA metagenomic. Journal of Asia-Pacific Entomology, 21: 1268-1274. doi: 10.10 16/j.aspen.2018.10.002

Ioannidis, J.P., Ntzani, E.E., Trikalinos, T.A. & Contopoulos-Ioannidis, D.G. (2001). Replication validity of genetic association studies. Nature Genetics, 29: 306. doi :10.1038/ng749

Julio, G., Kiyoto, M., Toru, M. & Tadao, M. (2002). Population structure and genetic diversity in insular populations of nasutitermes takasagoensis (Isoptera: Termitidae) analyzed by AFLP markers. Zoological Science, 19: 1141-1146. doi: 10.2108/zsj.19.1141

Kawecki, T.J., Barton, N.H. & Fry, J.D. (1997). Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation. Journal of Evolutionary Biology, 10: 407-429.

Kaeuffer, R., Réale, D., Coltman, D.W. & Pontier, D. (2007). Detecting population structure using STRUCTURE software: Effect of background linkage disequilibrium. Heredity, 99: 374. doi: 10.1038/sj.hdy.6801010

Keller, L.F., & Waller, D.M. (2002). Inbreeding effects in wild populations. Trends in Ecology and Evolution, 17: 230-241.

Khizam, N.A.N. & Ab Majid, A.H. (2019). Development and annotation of species-specific microsatellite markers from transcriptome sequencing for a higher group termite, Globitermes sulphureus Haviland (Blattodea: Termitidae). Meta Gene, 20: 100568. doi: 10.1016/j.mgene.2019.100568

Lande, R. (2015). Evolution of phenotypic plasticity in colonizing species. Molecular Ecology, 24: 2038-2045. doi: 10.1111/mec.13037

Lenormand, T. (2002). Gene flow and the limits to natural selection. Trends in Ecology and Evolution, 17: 183-189. doi: 10.1016/S0169-5347(02)02497-7

Luchetti, A., Dedeine, F., Velonà, A. & Mantovani, B. (2013). Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera, Kalotermitidae). Molecular Ecology, 22: 3391-3402. doi: 10.1111/mec.12302

Meirmans, P.G. (2012). AMOVA-Based clustering of population genetic data. Journal of Heredity, 103: 744-750. doi: 10.1093/jhered/ess047

Miller, K.M., Kaukinen, K.H., Beacham, T.D. & Withler, R.E. (2001). Geographic heterogeneity in natural selection on an mhc locus in sockeye salmon. Genetica, 111: 237-257. doi: 10.1023/A:1013716020351

Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press, New-York.

Pamilo, P., Seppä, P. & Helanterä, H. (2016). Population genetics of wood ants. Wood Ant Ecology and Conservation, 7: 51. doi: 10.1017/CBO9781107261402.004

Painter, J.N., Crozier, R.H., Poiani, A., Robertson, R.J. & Clarke, M.F. (2000). Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Molecular Ecology, 9: 1339-1347.

Peakall, R. & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research - an update. Bioinformatics, 28: 2537-2539. doi :10.1111/j.1471-8286.2005.01155.x

Perdereau, E., Bagnères, A.G., Dupont, S. & Dedeine, F. (2010). High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insectes Sociaux, 57: 393-402.

Pironon, S., Villellas, J., Morris, W.F., Doak, D.F. & García, M.B. (2015). Do geographic, climatic or historical ranges differentiate the performance of central versus peripheral populations. Global Ecology and Biogeography, 24: 611-620. doi: 10.1111/geb.12263

Piry, S., Luikart, G. & Cornuet, J. M. (1999). BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90: 502-503.

Powell, J.E., Visscher, P.M. & Goddard, M.E. (2010). Reconciling the analysis of IBD and IBS in complex trait studies. Nature Reviews Genetics, 11, 800-805.

Reddy, P.C. (2017). Unit-3 population genetics. Essentials of physical anthropology. Belmont California; Wadsworth.

Ross, K.G. & Carpenter, J.M. (1991). Phylogenetic analysis and the evolution of queen number in eusocial hymenoptera. Journal of Evolutionary Biology, 4: 117-130. doi: 10.1046/j. 1420-9101.1991.4010117.x

Ross, K.G. (2001). Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Molecular Ecology, 10: 265-284. doi: 10.1046/j.1365-294X.2001.01191.x

Roussel, V., Koenig, J., Beckert, M. & Balfourier, F. (2004). Molecular diversity in french bread wheat accessions related to temporal trends and breeding programmes. Theoretical and Applied Genetics, 108: 920-930. doi: 10.1007/s00122-003-1502-y

Rousset, F. (2008). Genepop’007: A complete re-implementation of the genepop software for windows and linux. Molecular Ecology Resources, 8: 103-106.

Salanti, G., Sanderson, S. & Higgins, J.P. (2005). Obstacles and opportunities in meta-analysis of genetic association studies. Genetics in Medicine, 7: 13. doi: 10.1097/01.GIM. 0000 151839.12032.1A

Schwalm, D., Epps, C.W., Rodhouse, T.J., Monahan, W.B., Castillo, J.A., Ray, C. & Jeffress, M.R. (2016). Habitat availability and gene flow influence diverging local population trajectories under scenarios of climate change: a place-based approach. Global Change Biology, 22: 1572-1584. doi: 10.11 11/gcb.13189

Seri Masran, S.N.A. & Ab Majid, A.H. (2018). Isolation and characterization of novel polymorphic microsatellite markers for Cimex hemipterus F. (Hemiptera: Cimicidae). Journal of Medical Entomology, 55: 760-765. doi: 10.1093/jme/tjy008

Taylor, M.S. & Hellberg, M.E. (2003). Genetic evidence for local retention of pelagic larvae in a caribbean reef fish. Science, 299: 107-109. doi: 10.1126/science.1079365

Thompson, G.J., Lenz, M., Crozier, R.H. & Crespi, B.J. (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. Australian Journal of Zoology, 55: 219-227. doi: 10.10 71/ZO07023

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 the evidence from behavioral, ecological, and genetic studies. Ethology, Ecology and Evolution, 11: 149-169. doi: 10.1080/08927014.1999.9522833

Tong, R.L., Grace, J.K., Mason, M., Krushelnycky, P.D., Spafford, H. & Aihara-Sasaki, M. (2017). Termite species distribution and flight periods on oahu, hawaii. Insects, 8: 58. doi: 10.3390/insects8020058

Vargo, E.L. & Carlson, J.R. (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. Environmental Entomology, 35: 173-187. doi: 10.1603/0046-225X-35.1.173

Vargo, E.L. & Husseneder, C. (2009). Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annual Review of Entomology, 54: 379-403. doi: 10.1146/annurev.ento.54.110807.090443

Williams, G.C. (2018). Adaptation and natural selection: A critique of some current evolutionary thought. Princeton University Press.

Wlasiuk, G., Garza, J.C. & Lessa, E.P. (2003). Genetic and geographic differentiation in the Rio Negro Tuco-Tuco (Ctenomys rionegrensis): inferring the roles of migration and drift from multiple genetic markers. Evolution, 57: 913-926. doi: 10.1111/j.0014-3820.2003.tb00302.x

Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution, 19: 395-420.

DOI: http://dx.doi.org/10.13102/sociobiology.v68i1.5772


  • There are currently no refbacks.



JCR Impact Factor (2019): 0.690

JCR 5-year Impact Factor (2019): 0.846

Google Scholar h5-index (Insects and Arthropods journals): 12 

Scimago h-index (whole journal circulation period): 37         

Scopus CiteScore (2016-2019): 0.90

Mean time for editorial decision (2020): 78 days

Mean time for article publication (2020): 171 days


Sociobiology is indexed in the following databases: