Abstract

Termites are known as social insects worldwide. Presently in China 473 species, 44 genera and 4 families of termites have been reported. Of them, 111 Reticulitermes species are widely spread in different zones of China. The dispersion flight season of these Chinese Reticulitermes species are usually started from February to June, but in some regions different species are distributed, sharing their boundaries and having overlapping flight seasons. These reasons become important sources of hybridization between two different heterospecific populations of termites. It was confirmed that the fertilized eggs and unfertilized eggs of some Reticulitermes termites have the capacity of cleavage. While the unfertilized eggs of R. aculabialis, R. chinensis and R. labralis cleaved normally and the only R. aculabialis unfertilized eggs develop in embryos. While, the R. flaviceps and R. chinensis were observed with their abnormal embryonic development, and not hatching of eggs parthenogenetically. They were reported more threatening to Chinese resources as they propagate with parthenogenesis, hybridization and sexual reproduction. Eggshell and macrophiles of eggs play important roles in species identification and control. Although, they are severe pests and cause a wide range of damages to wooden structures and products in homes, buildings, building materials, trees, crops, and forests in China’s Mainland.

Keywords:
Reticulitermes species; hybridization; embryonic development; parthenogenesis

Resumo

Os cupins são conhecidos como insetos sociais em todo o mundo. Atualmente na China foram relatadas 473 espécies, 44 gêneros e 4 famílias de cupins. Destas, 111 espécies de Reticulitermes estão amplamente distribuídas em diferentes zonas da China. A temporada de voo de dispersão dessas espécies chinesas de Reticulitermes geralmente começa de fevereiro a junho, mas em algumas regiões diferentes espécies são distribuídas, compartilhando seus limites e tendo temporadas de voo sobrepostas. Essas razões tornam-se importantes fontes de hibridização entre duas populações heteroespecíficas de cupins. Foi confirmado que os ovos fertilizados e não fertilizados de alguns cupins Reticulitermes possuem capacidade de clivagem. Já os ovos não fertilizados de R. aculabialis, R. chinensis e R. labralis clivaram normalmente, e os únicos ovos não fertilizados de R. aculabialis se desenvolvem em embriões. R. flaviceps e R. chinensis foram observados com desenvolvimento embrionário anormal, e não eclosão de ovos por partenogênese. Eles foram relatados como mais ameaçadores para os recursos chineses à medida que se propagam com partenogênese, hibridização e reprodução sexual. Casca de ovo e macrófilos de ovos desempenham papéis importantes na identificação e controle de espécies, embora sejam pragas graves e causem uma ampla gama de danos a estruturas e produtos de madeira em residências, edifícios, materiais de construção, árvores, plantações e florestas na China continental.

Palavras-chave:
espécies de Reticulitermes; hibridização; desenvolvimento embrionário; partenogênese

1. Introduction

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Therefore, termite species have a wide diversity of feeding behaviours, especially they consume cellulose of woods, tree farmings, structural timbers, decompose organic animal matters in different degrees and cause severe losses in the billions of dollars per year due to direct damage and chemical control costs worldwide (Su et al., 2004SU, N-Y., SCHEFFRAHN, R. H. & CABRERA, B., 2004. Native subterranean termites: Reticulitermes flavipes (Kollar), Reticulitermes virginicus (Banks), Reticulitermes hageni Banks (Insecta: Isoptera: Rhinotermitidae). Florida: EDIS.; Cameron and Whiting, 2007CAMERON, S.L. and WHITING, M.F., 2007. Mitochondrial genomic comparisons of the subterranean termites from the Genus Reticulitermes (Insecta: Isoptera: Rhinotermitidae). Genome, vol. 50, no. 2, pp. 188-202. http://dx.doi.org/10.1139/g06-148. PMid:17546084.
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A total of 3106 species of termites were reported globally, while 371 of them were counted the most destructive and caused severe damages to human properties (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the Isoptera of the World: Termitidae (Part One). Bulletin of the American Museum of Natural History, vol. 2013, no. 7, pp. 973-1495. http://dx.doi.org/10.1206/377.4.
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http://dx.doi.org/10.3390/insects1001003... ). They are abundant and responsible for approximately 2 billion RMB annually equivalent to $217 million US (Tonini et al., 2013TONINI, F., HOCHMAIR, H.H., SCHEFFRAHN, R.H. and DEANGELIS, D.L., 2013. Simulating the spread of an invasive termite in an urban environment using a stochastic individual-based model. Environmental Entomology, vol. 42, no. 3, pp. 412-423. http://dx.doi.org/10.1603/EN12325. PMid:23726049.
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http://dx.doi.org/10.3390/insects1001003... ).

About 150 termite species belonged to 4 families and 28 genera that were reported to damage plants in hilly Southern land (Li et al., 2010aLI, H.-F., YANG, R.-L. and SU, N.-Y., 2010a. Interspecific competition and territory defense mechanisms of Coptotermes formosanus and Coptotermes gestroi (Isoptera: rhinotermitidae). Environmental Entomology, vol. 39, no. 5, pp. 1601-1607. http://dx.doi.org/10.1603/EN09262. PMid:22546458.
http://dx.doi.org/10.1603/EN09262... ; Paul et al., 2018PAUL, B., KHAN, M. A., PAUL, S., SHANKARGANESH, K. & CHAKRAVORTY, S., 2018. Termites and Indian agriculture. In: M. A. KHAN and W. AHMAD, eds. Termites and sustainable management. Cham: Springer, pp. 51-96. http://dx.doi.org/10.1007/978-3-319-68726-1_3.
http://dx.doi.org/10.1007/978-3-319-6872... ). They have more active and dynamic breeding activities, which are sped up by their well-developed reproductive abilities (Tonini et al., 2013TONINI, F., HOCHMAIR, H.H., SCHEFFRAHN, R.H. and DEANGELIS, D.L., 2013. Simulating the spread of an invasive termite in an urban environment using a stochastic individual-based model. Environmental Entomology, vol. 42, no. 3, pp. 412-423. http://dx.doi.org/10.1603/EN12325. PMid:23726049.
http://dx.doi.org/10.1603/EN12325... ; Perdereau et al., 2019PERDEREAU, E., BAUDOUIN, G., BANKHEAD-DRONNET, S., CHEVALIER, Z., ZIMMERMANN, M., DUPONT, S., DEDEINE, F. and BAGNÈRES, A.-G., 2019. Invasion dynamics of a termite, Reticulitermes flavipes, at different spatial scales in France. Insects, vol. 10, no. 1, pp. 30. http://dx.doi.org/10.3390/insects10010030. PMid:30650655.
http://dx.doi.org/10.3390/insects1001003... ). The following study was arranged on the Reticulitermes termites of China, to know their embryonic development in parthenogenetic and sexual eggs, their related developmental stages, hybridization, and morphology of gonads.

The insect parthenogenesis consists of three mechanisms, first like in honeybee haploid parthenogenesis, the second is the fusion of unfertilized eggs in diploid offspring, including end fusion and nuclear fusion (Verma and Ruttner, 1983VERMA, S. and RUTTNER, F., 1983. Cytological analysis of the thelytokous parthenogenesis in the Cape honeybee (Apis mellifera capensis Escholtz). Apidologie, vol. 14, no. 1, pp. 41-57. http://dx.doi.org/10.1051/apido:19830104.
http://dx.doi.org/10.1051/apido:19830104... ). In the third case, parthenogenesis is generally (sporadic parthenogenesis) responsible for the growth of unfertilized eggs directly into embryos such as silkworms (Liu et al., 2015LIU, P., WANG, Y., DU, X., YAO, L., LI, F. and MENG, Z., 2015. Transcriptome analysis of thermal parthenogenesis of the domesticated silkworm. PLoS One, vol. 10, no. 8, pp. e0135215. http://dx.doi.org/10.1371/journal.pone.0135215. PMid:26274803.
http://dx.doi.org/10.1371/journal.pone.0... ). While, periodic parthenogenesis alternates between parthenogenesis and sexual reproduction in aphids (Dedryver et al., 2013DEDRYVER, C.-A., LE GALLIC, J.F., MAHEO, F., SIMON, J.-C. and DEDRYVER, F., 2013. The genetics of obligate parthenogenesis in an aphid species and its consequences for the maintenance of alternative reproductive modes. Heredity, vol. 110, no. 1, pp. 39-45. http://dx.doi.org/10.1038/hdy.2012.57. PMid:22990313.
http://dx.doi.org/10.1038/hdy.2012.57... ). Additionally, Origin of transmission: males of wasps reproducing two sexual categories of both sexes and parthenogenesis after mating with their sexual females (Ma et al., 2015MA, W.-J., PANNEBAKKER, B.A., VAN DE ZANDE, L., SCHWANDER, T., WERTHEIM, B. and BEUKEBOOM, L.W., 2015. Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp. BMC Evolutionary Biology, vol. 15, no. 1, pp. 84. http://dx.doi.org/10.1186/s12862-015-0370-9. PMid:25963738.
http://dx.doi.org/10.1186/s12862-015-037... ). Moreover, artificial induction: the warm soup is used to treat silkworms eggs with it, they grow and adapt parthenogenesis for conforming female lines (Long et al., 2015LONG, D., LU, W., ZHANG, Y., BI, L., XIANG, Z. and ZHAO, A., 2015. An efficient strategy for producing a stable, replaceable, highly efficient transgene expression system in silkworm, Bombyx mori. Scientific Reports, vol. 5, no. 1, pp. 8802. http://dx.doi.org/10.1038/srep08802. PMid:25739894.
http://dx.doi.org/10.1038/srep08802... ; Rhainds, 2019RHAINDS, M., 2019. Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids. Entomologia Experimentalis et Applicata, vol. 167, no. 1, pp. 73-84. http://dx.doi.org/10.1111/eea.12759.
http://dx.doi.org/10.1111/eea.12759... ). Except for finding males, the females produce their offspring with facultative parthenogenesis. It is common in the Isoptera to reproduce with facultative parthenogenesis (Kobayashi and Miyaguni, 2016KOBAYASHI, K. and MIYAGUNI, Y., 2016. Facultative parthenogenesis in the Ryukyu drywood termite Neotermes koshunensis. Scientific Reports, vol. 6, no. 1, pp. 30712. http://dx.doi.org/10.1038/srep30712. PMid:27464523.
http://dx.doi.org/10.1038/srep30712... ).

Hybridization is an important corridor for organisms to obtain variation, allowing the gene introgression of an organism to penetrate in the next generation and different populations for their successful adaptation (Harrison and Larson, 2014HARRISON, R.G. and LARSON, E.L., 2014. Hybridization, introgression, and the nature of species boundaries. The Journal of Heredity, vol. 105, suppl. 1, pp. 795-809. http://dx.doi.org/10.1093/jhered/esu033. PMid:25149255.
http://dx.doi.org/10.1093/jhered/esu033... ). Speciation of insects through hybridization is recognized based on chromosomal and isozymal studies in which combination of genes and chromosome sets is due to diploid or polyploid of two species. Recently, reviewed examples in numerous species of insects like planthopper Muellerianella fairmairei-brevipennis, grasshopper Warramaba virgo; Otiorrhynchus, black flies of the genera Gymnopais and Prosimulium (Bullini and Nascetti, 1990BULLINI, L. and NASCETTI, G., 1990. Speciation by hybridization in phasmids and other insects. Canadian Journal of Zoology, vol. 68, no. 8, pp. 1747-1760. http://dx.doi.org/10.1139/z90-256.
http://dx.doi.org/10.1139/z90-256... ; Taylor and Larson, 2019TAYLOR, S.A. and LARSON, E.L., 2019. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nature Ecology & Evolution, vol. 3, no. 2, pp. 170-177. http://dx.doi.org/10.1038/s41559-018-0777-y. PMid:30697003.
http://dx.doi.org/10.1038/s41559-018-077... ; Pierce et al., 2014PIERCE, A.A., ZALUCKI, M.P., BANGURA, M., UDAWATTA, M., KRONFORST, M.R., ALTIZER, S., HAEGER, J.F. and ROODE, J.D., 2014. Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proceedings. Biological Sciences, vol. 281, no. 1797, pp. 20142230-20142230. http://dx.doi.org/10.1098/rspb.2014.2230. PMid:25377462.
http://dx.doi.org/10.1098/rspb.2014.2230... ).

This study was arranged with the following aims and objectives.

To know the importance of micropyles and gas exchange through termite eggshell in parthenogenetic, hybrid and sexual eggs.

To know about the damages of the parthenogenetic, sexual and hybrid progeny of Reticulitermes species.

To know the comparative reproductive competencies of Reticulitermes species.

To know the effect of the hybrid progeny of Reticulitermes termites on the local population.

2. Results and Discussion

2.1. Distribution of termites in China

Recently, in China the four most dangerous species, the subterranean termites Reticulitermes aculabialis Tsai et Hwang, R. chinensis Snyder (1923), R. labralis and R. flaviceps Oshima (2011) (Rhinotermitidae, Blattodea) reported that they caused losses in different regions of administrative level and also most widely distributed (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the Isoptera of the World: Termitidae (Part One). Bulletin of the American Museum of Natural History, vol. 2013, no. 7, pp. 973-1495. http://dx.doi.org/10.1206/377.4.
http://dx.doi.org/10.1206/377.4... ; Li et al., 2010bLI, H., XU, Z., DENG, T., CHEN, L., LI, J., WEI, J. and MO, J., 2010b. Species of termites (Isoptera) attacking trees in China. Sociobiology, vol. 56, pp. 109-120., 2018LI, J., ZHU, J.L., LOU, S.D., WANG, P., ZHANG, Y.S., WANG, L., YIN, R.C. and ZHANG, P.P., 2018. The complete mitochondrial genome of Coptotermes’ suzhouensis' (syn. Coptotermes formosanus) (Isoptera: Rhinotermitidae) and molecular phylogeny analysis. Journal of Insect Science, vol. 18, no. 2, pp. 26. http://dx.doi.org/10.1093/jisesa/iey018. PMid:29718488.
http://dx.doi.org/10.1093/jisesa/iey018... ). Compared to termites of the Northern part with the South part, the distribution of four termite species is more common in 20 provinces and autonomous regions of China, which mostly cause severe damage to trees, crops, and human constructions. In future, it is more predictable that these termite species more frequently reproduce, expanding and they will damage the North part of China (Gui-Xiang et al., 1994GUI-XIANG, L., ZI-RONG, D. and BIAO, Y., 1994. Introduction to termite research in China. Journal of Applied Entomology, vol. 117, no. 1-5, pp. 360-369. http://dx.doi.org/10.1111/j.1439-0418.1994.tb00747.x.
http://dx.doi.org/10.1111/j.1439-0418.19... ; Mo et al., 2004MO, J., YANG, T., SONG, X. and CHENG, J., 2004. Cellulase activity in five species of important termites in China. Applied Entomology and Zoology, vol. 39, no. 4, pp. 635-641. http://dx.doi.org/10.1303/aez.2004.635.
http://dx.doi.org/10.1303/aez.2004.635... ; Appel et al., 2012APPEL, A.G., HU, X.P., ZHOU, J., QIN, Z., ZHU, H., CHANG, X., WANG, Z., LIU, X. and LIU, M., 2012. Observations of the biology and ecology of the black-winged termite, Odontotermes formosanus Shiraki (Termitidae: Isoptera), in camphor, Cinnamomum camphora (L.) (Lauraceae). Psyche: a Journal of Entomology, vol. 2012, pp. 123102. http://dx.doi.org/10.1155/2012/123102.
http://dx.doi.org/10.1155/2012/123102... ).

Termites are generally dispersed in tropical rain forests near the equator, North and South latitudes worldwide (Matsumoto, 1976MATSUMOTO, T., 1976. The role of termites in an equatorial rain forest ecosystem of West Malaysia. I. Population density, biomass, carbon, nitrogen and calorific content and respiration rate. Oecologia, vol. 22, pp. 153-178. http://dx.doi.org/10.1007/BF00344714. PMid:28308653.
http://dx.doi.org/10.1007/BF00344714... ; Eggleton, 2000EGGLETON, P. (2000). Global patterns of termite diversity. In: T. ABE, D.E. BIGNELL and M. HIGASHI, eds. Termites: evolution, sociality, symbioses, ecology. Dordrecht: Springer, pp. 25-51. http://dx.doi.org/10.1007/978-94-017-3223-9_2.
http://dx.doi.org/10.1007/978-94-017-322... ; Veera Singham et al., 2017VEERA SINGHAM, G., OTHMAN, A.S. and LEE, C.-Y., 2017. Phylogeography of the termite Macrotermes gilvus and insight into ancient dispersal corridors in Pleistocene Southeast Asia. PLoS One, vol. 12, no. 11, pp. e0186690. http://dx.doi.org/10.1371/journal.pone.0186690. PMid:29186140.
http://dx.doi.org/10.1371/journal.pone.0... ). The distribution of termite species in the Eastern Hemisphere is more than in Northern latitudes. Similarly, in the Eastern Hemisphere, the dispersion is exceeded than in the Western Hemisphere, moreover, the biodiversity of termites in the Northern Hemisphere increased comparative the Southern Hemisphere, and some termite species distributed in the mountains at an elevation of 2000 m (Suiter et al., 2009SUITER, D.R., JONES, S.C. and FORSCHLER, B.T., 2009. Biology of subterranean termites in the Eastern United States. Bulletin, vol. 1209, pp. 1-16.; Hu et al., 2010HU, J., ZHONG, J.-H. and XIAO, W.-L., 2010. New Flight distances record for alates of Odontotermes formosanus (Isoptera: termitidae). Journal of Entomological Science, vol. 45, no. 4, pp. 385-387. http://dx.doi.org/10.18474/0749-8004-45.4.385.
http://dx.doi.org/10.18474/0749-8004-45.... ; Guo et al., 2013GUO, Q., KELT, D.A., SUN, Z., LIU, H., HU, L., REN, H. and WEN, J., 2013. Global variation in elevational diversity patterns. Scientific Reports, vol. 3, no. 1, pp. 3007. http://dx.doi.org/10.1038/srep03007. PMid:24157658.
http://dx.doi.org/10.1038/srep03007... ).

In the Northern part of China, the distribution of termites initiates in Gongzhuling of Liaoning province (latitude 43°11'40′′- 44°9'20′′), through Jiexiu of Shanxi (latitude 37° North), Hancheng of Shaanxi (latitude 35.5° North), Gansu Wenxian county (33° North latitude), Westward to Tibet Medog (29.5° North latitude) (Li et al., 2009LI, H.-F., YE, W., SU, N.-Y. and KANZAKI, N., 2009. Phylogeography of Coptotermes gestroi and Coptotermes formosanus (Isoptera: Rhinotermitidae) in Taiwan. Annals of the Entomological Society of America, vol. 102, no. 4, pp. 684-693. http://dx.doi.org/10.1603/008.102.0413.
http://dx.doi.org/10.1603/008.102.0413... ; Husseneder et al., 2012bHUSSENEDER, C., SIMMS, D.M., DELATTE, J.R., WANG, C., GRACE, J.K. and VARGO, E.L., 2012b. Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus. Biological Invasions, vol. 14, no. 2, pp. 419-437. http://dx.doi.org/10.1007/s10530-011-0087-7.
http://dx.doi.org/10.1007/s10530-011-008... ; Li et al., 2013bLI, H.-F., FUJISAKI, I. and SU, N.-Y., 2013b. Predicting habitat suitability of Coptotermes gestroi (Isoptera: Rhinotermitidae) with species distribution models. Journal of Economic Entomology, vol. 106, no. 1, pp. 311-321. http://dx.doi.org/10.1603/EC12309. PMid:23448046.
http://dx.doi.org/10.1603/EC12309... ; Tong et al., 2017TONG, R.L., GRACE, J.K., MASON, M., KRUSHELNYCKY, P.D., SPAFFORD, H. and AIHARA-SASAKI, M., 2017. Termite species distribution and flight periods on Oahu, Hawaii. Insects, vol. 8, no. 2, pp. 58. http://dx.doi.org/10.3390/insects8020058. PMid:28587241.
http://dx.doi.org/10.3390/insects8020058... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ), which connects a line formed by each point from Northeast to Southwest and termites distributed in the Southeast of the boundary line. Termite species in two provinces such as Yunnan and Hainan distributed, which also have the soil termite genus, that spread up to the parts of China, they cause severe damages than other termite groups (Li et al., 2011aLI, H.-F., LAN, Y.-C. and SU, N.-Y., 2011a. Redescription of Prorhinotermes japonicus (Isoptera: Rhinotermitidae) from Taiwan. Annals of the Entomological Society of America, vol. 104, no. 5, pp. 878-885. http://dx.doi.org/10.1603/AN11064.
http://dx.doi.org/10.1603/AN11064... ; Hu and Song, 2014HU, X.P. and SONG, D., 2014. Behavioral responses of two subterranean termite species (Isoptera: Rhinotermitidae) to instant freezing or chilling temperatures. Environmental Entomology, vol. 36, no. 6, pp. 1450-1456. http://dx.doi.org/10.1603/0046-225X(2007)36[1450:BROTST]2.0.CO;2. PMid:18284773.
http://dx.doi.org/10.1603/0046-225X(2007... ; Cao and Jiang, 2014CAO, J. and JIANG, X., 2014. Preservation of wood and other sustainable biomaterials in China. In: T. P. SCHULTZ, B. GOODELL and D. D. NICHOLAS, eds. Deterioration and protection of sustainable biomaterials. New York: Oxford University Press.; Soleymaninejadian et al., 2014SOLEYMANINEJADIAN, E., JI, B.-Z., LIU, S.-W., YANG, J.-J., ZHANG, X., WANG, H. and DING, F., 2014. morphological characteristics of different casts in Odontotermes formosanus Shiraki. International Journal of Agriculture Innovation and Research, vol. 2, pp. 1114-1121.; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ).

R. flaviceps was collected and identified for the first time from Taipei, Taiwan (Oshima, 1911OSHIMA, M., 1911. On the difference between Leucotermes flaviceps, n. sp. and Leucotermes speratus (Kolbe) and the specific name of the termites found in Japan proper. Insect World, vol. 15, pp. 355-363.), and examined as the amplest species based on its abundance, lifestyle and colony size (Li et al., 2011bLI, H.-F., LIN, J.-S., LAN, Y.-C., PEI, K.J.-C. and SU, N.-Y., 2011b. Survey of the termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) in a Formosan pangolin habitat. The Florida Entomologist, vol. 94, no. 3, pp. 534-538. http://dx.doi.org/10.1653/024.094.0318.
http://dx.doi.org/10.1653/024.094.0318... ). Although R. flaviceps is distributed in the South part of China especially Fujian, Guangdong, Guangxi, Hunan, Jiangxi, Jiangsu, Zhejiang, Anhui, Hubei, Sichuan, Yunnan, Guizhou and Shaanxi provinces (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the Isoptera of the World: Termitidae (Part One). Bulletin of the American Museum of Natural History, vol. 2013, no. 7, pp. 973-1495. http://dx.doi.org/10.1206/377.4.
http://dx.doi.org/10.1206/377.4... ; Su et al., 2016SU, L., YANG, L., HUANG, S., SU, X., LI, Y., WANG, F., WANG, E., KANG, N., XU, J. and SONG, A., 2016. Comparative gut microbiomes of four species representing the higher and the lower termites. Journal of Insect Science, vol. 16, no. 1, pp. 97. http://dx.doi.org/10.1093/jisesa/iew081. PMid:27638955.
http://dx.doi.org/10.1093/jisesa/iew081... ). This invasive species crossed the Qinling Mountain range during the last decade, attacked about 100 km North from the Changjiang river basin to Huanghe river basin, and became an urban insect pest in the Northern areas of China (Xing unpublished data).

R. flaviceps is endemic to China and distributed in many tropical, subtropical and temperate regions of China (Veeresh et al., 1990VEERESH, G., MALLIK, B. and VIRAKTAMATH, C., 1990. Social insects and the environment. In: Proceedings of the 11th International Congress of IUSSI, 1990, Bangalore, India. Delhi: Oxford & IBH Publishing Co., 765 p.; Mo et al., 2005MO, J., HE, H., SONG, X., CHEN, C. and CHENG, J.A., 2005. Toxicity of ivermectin to Reticulitermes flaviceps (Isoptera: rhinotermitidae). Sociobiology, vol. 46, pp. 603-613.; Li et al., 2009LI, H.-F., YE, W., SU, N.-Y. and KANZAKI, N., 2009. Phylogeography of Coptotermes gestroi and Coptotermes formosanus (Isoptera: Rhinotermitidae) in Taiwan. Annals of the Entomological Society of America, vol. 102, no. 4, pp. 684-693. http://dx.doi.org/10.1603/008.102.0413.
http://dx.doi.org/10.1603/008.102.0413... , 2011aLI, H.-F., LAN, Y.-C. and SU, N.-Y., 2011a. Redescription of Prorhinotermes japonicus (Isoptera: Rhinotermitidae) from Taiwan. Annals of the Entomological Society of America, vol. 104, no. 5, pp. 878-885. http://dx.doi.org/10.1603/AN11064.
http://dx.doi.org/10.1603/AN11064... ). It is now found the most destructive and notorious subterranean termite pest in Reticulitermes throughout China and responsible for structural damage (Li et al., 2011bLI, H.-F., LIN, J.-S., LAN, Y.-C., PEI, K.J.-C. and SU, N.-Y., 2011b. Survey of the termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) in a Formosan pangolin habitat. The Florida Entomologist, vol. 94, no. 3, pp. 534-538. http://dx.doi.org/10.1653/024.094.0318.
http://dx.doi.org/10.1653/024.094.0318... , 2016cLI, H.-F., YEH, H.-T., CHIU, C.-I., KUO, C.-Y. and TSAI, M.-J., 2016c. Vertical distribution of termites on trees in two forest landscapes in Taiwan. Environmental Entomology, vol. 45, no. 3, pp. 577-581. http://dx.doi.org/10.1093/ee/nvw019. PMid:27016004.
http://dx.doi.org/10.1093/ee/nvw019... ; Rust and Su, 2012RUST, M.K. and SU, N.-Y., 2012. Managing social insects of urban importance. Annual Review of Entomology, vol. 57, no. 1, pp. 355-375. http://dx.doi.org/10.1146/annurev-ento-120710-100634. PMid:21942844.
http://dx.doi.org/10.1146/annurev-ento-1... ; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Veera-Singham et al., 2017; Khan et al., 2019KHAN, Z., ZHANG, M., MENG, Y., ZHAO, J., KONG, X., SU, X. and XING, L., 2019. Alates of the termite Reticulitermes flaviceps feed independently during their 5-month residency in the natal colony. Insectes Sociaux, vol. 66, no. 3, pp. 425-433. http://dx.doi.org/10.1007/s00040-019-00698-9.
http://dx.doi.org/10.1007/s00040-019-006... ). The subterranean termite R. chinensis is an important termite species that is distributed in Beijing, Tianjin, Shaanxi, Shanxi, Huanggang, Chongqing, Changsha and the drainage range of the Yangtse River in China (Wei et al., 2007WEI, J., MO, J., WANG, X. and MAO, W., 2007. Biology and ecology of Reticulitermes chinensis (Isoptera: Rhinotermitidae) in China. Sociobiology, vol. 50, pp. 553-559.; Huang et al., 2013HUANG, Q., LI, G., HUSSENEDER, C. and LEI, C., 2013. Genetic analysis of population structure and reproductive mode of the termite Reticulitermes chinensis Snyder. PLoS One, vol. 8, no. 7, e69070. http://dx.doi.org/10.1371/journal.pone.0069070.
http://dx.doi.org/10.1371/journal.pone.0... ). That potential pest damage the trees, wood products of buildings and the xylem of plants (Wu et al., 2019WU, C.-C., TSAI, C.-L., LIANG, W.-R., TAKEMATSU, Y. and LI, H.-F., 2019. Identification of Subterranean Termite Genus, Reticulitermes (Blattodea: Rhinotermitidae) in Taiwan. Journal of Economic Entomology, vol. 112, no. 6, pp. 2872-2881. http://dx.doi.org/10.1093/jee/toz183. PMid:31265067.
http://dx.doi.org/10.1093/jee/toz183... ). Another subterranean termite R. aculabialis is the main Isopteran species that is a harmful pest to the environment of China. The population distribution of this species was investigated in Xi'an, Shaanxi, Nanjing and Jiangsu (Zhao et al., 2019ZHAO, S., WANG, Y., BIE, B., XU, L. and BAI, H. 2019. Study on the Genetic Diversity of Reticulitermes aculabialis. In: The Second International Conference on Materials Chemistry and Environmental Protection, 2018, Sanya, China. Setúbal: SciTePress, pp. 255-259. http://dx.doi.org/10.5220/0008188402550259.
http://dx.doi.org/10.5220/00081884025502... ). R. aculabialis is dispersed in 18 provinces and autonomous regions in China (Xing et al., 1998XING, L., HU, C. and CHENG, J., 1998. Foraging populations and territories of Reticulitermes aculabialis Tsai et Hwang (Isoptera: Rhinotermitidae) in urban environment. Acta Agriculturae Universitatis Chekianensis, vol. 24, pp. 167-170.; Kai et al., 2016KAI, W., XIAO-HUI, G., CHUN-HUA, D., LIAN-XI, X., JIANG-LI, T. and XIAO-HONG, S., 2016. Complete mitochondrial genome of a parthenogenetic subterranean termite, Reticulitermes aculabialis Tsai et Hwang (Isoptera: rhinotermitidae). Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis, vol. 27, no. 5, pp. 3133-3134. http://dx.doi.org/10.3109/19401736.2015.1007299. PMid:25703853.
http://dx.doi.org/10.3109/19401736.2015.... ). According to the Gui-Xiang et al. (1994)GUI-XIANG, L., ZI-RONG, D. and BIAO, Y., 1994. Introduction to termite research in China. Journal of Applied Entomology, vol. 117, no. 1-5, pp. 360-369. http://dx.doi.org/10.1111/j.1439-0418.1994.tb00747.x.
http://dx.doi.org/10.1111/j.1439-0418.19... and Li et al. (2010a)LI, H.-F., YANG, R.-L. and SU, N.-Y., 2010a. Interspecific competition and territory defense mechanisms of Coptotermes formosanus and Coptotermes gestroi (Isoptera: rhinotermitidae). Environmental Entomology, vol. 39, no. 5, pp. 1601-1607. http://dx.doi.org/10.1603/EN09262. PMid:22546458.
http://dx.doi.org/10.1603/EN09262... report, this termite has become a serious pest, causing damage in the Northwest part increasingly and in some zones closed to the South Bank of the Yangtze River. Reticulitermes termite populations have been recorded in East Asia, Southern China, Taiwan, Korea and Japan. Hence, these species have diverse ecological requirements (Hochmair and Scheffrahn, 2010HOCHMAIR, H.H. and SCHEFFRAHN, R.H., 2010. Spatial association of marine dockage with land-borne infestations of invasive termites (Isoptera: Rhinotermitidae: Coptotermes) in urban South Florida. Journal of Economic Entomology, vol. 103, no. 4, pp. 1338-1346. http://dx.doi.org/10.1603/EC09428. PMid:20857745.
http://dx.doi.org/10.1603/EC09428... , Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ), but they have established populations in many native areas include Northern and Southern parts and expanded in invasive areas due to human transportation, floods and wind (Su, 2013SU, N.-Y., 2013. How to become a successful invader. The Florida Entomologist, vol. 96, no. 3, pp. 765-769. http://dx.doi.org/10.1653/024.096.0309.
http://dx.doi.org/10.1653/024.096.0309... ; Corn and Johnson, 2013CORN, M.L. and JOHNSON, R., 2013. Invasive species: major laws and the role of selected federal agencies. Washington: Congressional Research Service, 58 p.; Chunco, 2014CHUNCO, A.J., 2014. Hybridization in a warmer world. Ecology and Evolution, vol. 4, no. 10, pp. 2019-2031. http://dx.doi.org/10.1002/ece3.1052. PMid:24963394.
http://dx.doi.org/10.1002/ece3.1052... ; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Li et al., 2016cLI, H.-F., YEH, H.-T., CHIU, C.-I., KUO, C.-Y. and TSAI, M.-J., 2016c. Vertical distribution of termites on trees in two forest landscapes in Taiwan. Environmental Entomology, vol. 45, no. 3, pp. 577-581. http://dx.doi.org/10.1093/ee/nvw019. PMid:27016004.
http://dx.doi.org/10.1093/ee/nvw019... ). This observation is currently reviewed in many ecosystems of the world that are responsible for the replacement of this non-native species in native regions of China (Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ; Wu et al., 2020WU, J., XU, H., HASSAN, A. and HUANG, Q., 2020. Interspecific hybridization between the two sympatric termite Reticulitermes species under laboratory conditions. Insects, vol. 11, no. 1, pp. 14. http://dx.doi.org/10.3390/insects11010014. PMid:31877914.
http://dx.doi.org/10.3390/insects1101001... ; Fournier and Aron, 2021FOURNIER, D. and ARON, S., 2021. Hybridization and invasiveness in social insects: the good, the bad and the hybrid. Current Opinion in Insect Science, vol. 46, pp. 1-9. http://dx.doi.org/10.1016/j.cois.2020.12.004. PMid:33484875.
http://dx.doi.org/10.1016/j.cois.2020.12... ).

However, the studies of spreading are concerned with interaction and overlap in small localities of the world including the South part of China (Hartke and Baer, 2011HARTKE, T.R. and BAER, B., 2011. The mating biology of termites: a comparative review. Animal Behaviour, vol. 82, no. 5, pp. 927-936. http://dx.doi.org/10.1016/j.anbehav.2011.07.022.
http://dx.doi.org/10.1016/j.anbehav.2011... ; Grace, 2014GRACE, J.K., 2014. Invasive termites revisited: Coptotermes gestroi meets Coptotermes formosanus. In: Proceedings of the 10th Pacific-Rim Termite Research Group Conference, 2014, Kuala Lumpur, Malaysia. Singapore: Pacific Rim Termite Research Group, 7 p.; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ). The Formosan subterranean termite (Coptotermes formosanus) and the Asian subterranean termite (C. gestroi) are the two most destructive structural pests in the world and are responsible for most of the economic loss annually (Messenger et al., 2002MESSENGER, M.T., SU, N.Y. and SCHEFFRAHN, R.H., 2002. Current distribution of the formosan subterranean termite and other termite species (Isoptera: Rhinotermitidae, Kalotermitidae) in Louisiana. The Florida Entomologist, vol. 85, no. 4, pp. 580-587. http://dx.doi.org/10.1653/0015-4040(2002)085[0580:CDOTFS]2.0.CO;2.
http://dx.doi.org/10.1653/0015-4040(2002... ; Rust and Su, 2012RUST, M.K. and SU, N.-Y., 2012. Managing social insects of urban importance. Annual Review of Entomology, vol. 57, no. 1, pp. 355-375. http://dx.doi.org/10.1146/annurev-ento-120710-100634. PMid:21942844.
http://dx.doi.org/10.1146/annurev-ento-1... ; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ).

2.2. Termite morphology

According to external morphology, termites can be classified into first and metamorphic categories from the viewpoint of phylogeny (Eggleton, 2010EGGLETON, P. (2010) An introduction to termites: biology, taxonomy and functional morphology. In: D. BIGNELL, Y. ROISIN and N. LO, eds. Biology of termites: a modern synthesis. Dordrecht: Springer, pp. 1-26. http://dx.doi.org/10.1007/978-90-481-3977-4_1.
http://dx.doi.org/10.1007/978-90-481-397... ; Dedeine et al., 2016DEDEINE, F., DUPONT, S., GUYOT, S., MATSUURA, K., WANG, C., HABIBPOUR, B., BAGNÈRES, A., MANTOVANI, B. and LUCHETTI, A., 2016. Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mitochondrial and nuclear loci. Molecular Phylogenetics and Evolution, vol. 94, no. Pt B, pp. 778-790. http://dx.doi.org/10.1016/j.ympev.2015.10.020. PMid:26541239.
http://dx.doi.org/10.1016/j.ympev.2015.1... ). There have been no extraordinary variations in their original status and wings, such as the head and thorax (reproductive and workers) species, while they have changes in their external shape of the soldiers like scorpion variability. Such modifications are only found in the soldiers' thorax and head; those are used as significant sources of classification and identification (Ye et al., 2009YE, Y., JONES, S.C. and AMMAR, E., 2009. Reproductive characteristics of imagos of Reticulitermes flavipes (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 102, no. 5, pp. 889-894. http://dx.doi.org/10.1603/008.102.0515.
http://dx.doi.org/10.1603/008.102.0515... ; Booth et al., 2012BOOTH, W., BRENT, C.S., CALLERI, D.V., ROSENGAUS, R.B., TRANIELLO, J. and VARGO, E.L., 2012. Population genetic structure and colony breeding system in dampwood termites (Zootermopsis angusticollis and Z. nevadensis nuttingi). Insectes Sociaux, vol. 59, no. 1, pp. 127-137. http://dx.doi.org/10.1007/s00040-011-0198-2.
http://dx.doi.org/10.1007/s00040-011-019... ; Perdereau et al., 2013PERDEREAU, E., BAGNERES, A.G., BANKHEAD‐DRONNET, S., DUPONT, S., ZIMMERMANN, M., VARGO, E. and DEDEINE, F., 2013. Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Molecular Ecology, vol. 22, no. 4, pp. 1105-1119. http://dx.doi.org/10.1111/mec.12140. PMid:23205642.
http://dx.doi.org/10.1111/mec.12140... ; Perdereau et al., 2019PERDEREAU, E., BAUDOUIN, G., BANKHEAD-DRONNET, S., CHEVALIER, Z., ZIMMERMANN, M., DUPONT, S., DEDEINE, F. and BAGNÈRES, A.-G., 2019. Invasion dynamics of a termite, Reticulitermes flavipes, at different spatial scales in France. Insects, vol. 10, no. 1, pp. 30. http://dx.doi.org/10.3390/insects10010030. PMid:30650655.
http://dx.doi.org/10.3390/insects1001003... ). For example, R. chinensis has a sharply pointed lip on the upper lip, and the transparent part of the lip looks like a needle. The R. flaviceps has an upper lip narrow like a snail. The alates of R. flaviceps have a plate of grey-yellow colour on the anterior side of the thorax. While, the head peak of a soldier is slightly longer, and the forehead is approximately flat.

Termites are divided into two types based on reproductive ability, reproductives (king and queen) and non-reproductives (soldiers and workers). Reproductives are mainly divided based on their forms and sources. Primary reproductives are actual adults in the nest, have visible compound eyes, well-developed wings, and a more pigmented body. They are founders of first nests after dispersion flight and making tandem pairings. In contrast to primary reproductive, the secondary reproductive (workers) from the nest of older individuals. They have the ability of mating and egg-laying after ecdysis and play a significant character in the growth of the colony (Ye et al., 2009YE, Y., JONES, S.C. and AMMAR, E., 2009. Reproductive characteristics of imagos of Reticulitermes flavipes (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 102, no. 5, pp. 889-894. http://dx.doi.org/10.1603/008.102.0515.
http://dx.doi.org/10.1603/008.102.0515... ; Vidyashree et al., 2018VIDYASHREE, A.S., KALLESHWARASWAMY, C.M., SWAMY, H.M., ASOKAN, R. and ADARSHA, S.K., 2018. Morphological, molecular identification and phylogenetic analysis of termites from western Ghats of Karnataka, India. Journal of Asia-Pacific Entomology, vol. 21, no. 1, pp. 140-149. http://dx.doi.org/10.1016/j.aspen.2017.11.006.
http://dx.doi.org/10.1016/j.aspen.2017.1... ). They are differentiated according to shape, age and divided into various types such as long wing bud types, wing scale types, micro wing bud types and short wing bud types. It can be discriminated into workers and secondary reproductive according to diverse sources. Most of the workers, except the reproduction, are responsible for sustaining the healthy life of the colony and care. The numbers of individuals in the colony of Reticulitermes termites are the highest, while the soldiers are only responsible for defence and have no feeding ability (Soleymaninejadian et al., 2014SOLEYMANINEJADIAN, E., JI, B.-Z., LIU, S.-W., YANG, J.-J., ZHANG, X., WANG, H. and DING, F., 2014. morphological characteristics of different casts in Odontotermes formosanus Shiraki. International Journal of Agriculture Innovation and Research, vol. 2, pp. 1114-1121.; Lillico-Ouachour et al., 2018LILLICO-OUACHOUR, M.A., METSCHER, B., KAJI, T. and ABOUHEIF, E., 2018. Internal head morphology of minor workers and soldiers in the hyperdiv. Revue Canadienne De Zoologie, vol. 96, no. 5, pp. 383-392. http://dx.doi.org/10.1139/cjz-2017-0209.
http://dx.doi.org/10.1139/cjz-2017-0209... ; Khan et al., 2021aKHAN, Z., KHAN, M.S., SULEMAN, MUHAMMAD, N., HAROON, SU, X.-H., XING, L.-X., 2021a. Morphology of testis, sperm, and spermatheca in two capable hybridized termite species indicates no interspecific reproductive isolation. International Journal of Tropical Insect Science. In press.).

2.3. Classification of termites

According to traditional classification, termites were classified into the order of eusocial insect Isoptera (Donovan et al., 2000DONOVAN, S.E., JONES, D.T., SANDS, W.A. and EGGLETON, P., 2000. Morphological phylogenetics of termites (Isoptera). Biological Journal of the Linnean Society. Linnean Society of London, vol. 70, no. 3, pp. 467-513. http://dx.doi.org/10.1111/j.1095-8312.2000.tb01235.x.
http://dx.doi.org/10.1111/j.1095-8312.20... ). Most of the researchers accept the truth that they are related to Blattodea and even they knew that the termites belong to the net-winged parents. There are arguments about their relationship. Termites are social insects like Hymenoptera while their molecular tree also indicates that their lineages lead to Cryptocercus roaches and assemblage in a monophyletic group.

Taxonomists classified the termite species into 7 families in early 2009. Moreover, the termites were re-identified and divided into 9 families by American scholars Engel, Grimaldi and Krishna after 2009. They are Hodotermitidae, Archatermopsidae, Kalotermitidae, Mastotermitidae, Rhinotermitidae, Serritermitidae, Stolotermitidae, Termiteidae and Stylotermitidae (Krishna et al., 2013KRISHNA, K., GRIMALDI, D.A., KRISHNA, V. and ENGEL, M.S., 2013. Treatise on the Isoptera of the World: Termitidae (Part One). Bulletin of the American Museum of Natural History, vol. 2013, no. 7, pp. 973-1495. http://dx.doi.org/10.1206/377.4.
http://dx.doi.org/10.1206/377.4... ). A total of 473 species belonged to 44 genera and 4 families of Isoptera that were divided into the lower and higher termites mainly consisted of seriously destructive agents. Among them, 5 species were found significantly in Southern parts of China (Li et al., 2011aLI, H.-F., LAN, Y.-C. and SU, N.-Y., 2011a. Redescription of Prorhinotermes japonicus (Isoptera: Rhinotermitidae) from Taiwan. Annals of the Entomological Society of America, vol. 104, no. 5, pp. 878-885. http://dx.doi.org/10.1603/AN11064.
http://dx.doi.org/10.1603/AN11064... , bLI, H.-F., LIN, J.-S., LAN, Y.-C., PEI, K.J.-C. and SU, N.-Y., 2011b. Survey of the termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) in a Formosan pangolin habitat. The Florida Entomologist, vol. 94, no. 3, pp. 534-538. http://dx.doi.org/10.1653/024.094.0318.
http://dx.doi.org/10.1653/024.094.0318... ; Kuswanto et al., 2015KUSWANTO, E., AHMAD, I. and DUNGANI, R., 2015. Threat of subterranean termites attack in the Asian Countries and their control: a review. Asian Journal of Applied Sciences, vol. 8, no. 4, pp. 227-239. http://dx.doi.org/10.3923/ajaps.2015.227.239.
http://dx.doi.org/10.3923/ajaps.2015.227... ).

2.4. Mating behaviour of termites

Termite adults fly in groups for their reproduction from the parental colony, then they dispersed in different directions distant to the parental colony to build new colonies for egg-laying and hatching more offspring (Hartke and Rosengaus, 2011HARTKE, T.R. and ROSENGAUS, R.B., 2011. Heterospecific pairing and hybridization between Nasutitermes corniger and N. ephratae. Naturwissenschaften, vol. 98, no. 9, pp. 745-753. http://dx.doi.org/10.1007/s00114-011-0823-y. PMid:21761130.
http://dx.doi.org/10.1007/s00114-011-082... ; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ). Their dispersion is dependent on the humidity, temperature, pressure and seasons (Krishna, 2013KRISHNA, B., 2013. Role of substrate moisture, relative humidity and temperature on survival and foraging behavior of formosan subterranean termites. Baton Rouge: Louisiana State University. Doctoral Dissertation in Philosophy, 134 p.). After dispersion flight, the alates fall off their wings and the males start to follow the females primarily. The kings and queens paired up with each other and form tandem pairings, which is the most important genetic behaviour of termites during building new colonies. The queen leads the king to select the accurate nest site to start the new nest (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Raina et al., 2003RAINA, A., PARK, Y.I. and FLORANE, C., 2003. Behavior and reproductive biology of the primary reproductives of the Formosan subterranean termite (Isoptera: rhinotermitidae). Sociobiology, vol. 41, pp. 37-48.; Hartke, 2010HARTKE, T. R., 2010. Breeding strategies and the reproductive ecology of Nasutitermes corniger. Dissertations & Theses Gradworks, 258 p.; Pervez, 2018PERVEZ, A., 2018. Termite biology and social behaviour. In: M. KHAN and W. AHMAD, eds. Termites and sustainable management. Cham: Springer, pp. 119-143. http://dx.doi.org/10.1007/978-3-319-72110-1_6.
http://dx.doi.org/10.1007/978-3-319-7211... ).

Imagoes mate after the foundation of the initial colony and start egg laying in time about one week (Hu et al., 2010HU, J., ZHONG, J.-H. and XIAO, W.-L., 2010. New Flight distances record for alates of Odontotermes formosanus (Isoptera: termitidae). Journal of Entomological Science, vol. 45, no. 4, pp. 385-387. http://dx.doi.org/10.18474/0749-8004-45.4.385.
http://dx.doi.org/10.18474/0749-8004-45.... ). Similarly, in swarming flights of R. flaviceps, thousands of individuals release and fly from matured colonies annually. After the dispersal flight, the alates drop their wings, find females, pair up, and involve in tandem behaviour for mating, eggs laying and hatching after colony set up. While the male initiates tandem behaviour by maintaining contact with the tip of the female’s abdomen. The female then leads the way in search of a favourable nesting site, in which both individuals seclude themselves and establish the early colony. It takes up unknown time for maturation and initiates dispersal flights (Xing et al., unpublished data; Li et al., 2011bLI, H.-F., LIN, J.-S., LAN, Y.-C., PEI, K.J.-C. and SU, N.-Y., 2011b. Survey of the termites (Isoptera: Kalotermitidae, Rhinotermitidae, Termitidae) in a Formosan pangolin habitat. The Florida Entomologist, vol. 94, no. 3, pp. 534-538. http://dx.doi.org/10.1653/024.094.0318.
http://dx.doi.org/10.1653/024.094.0318... ; Chen et al., 2016CHEN, Q., WANG, K., TAN, Y.L. and XING, L.X., 2016. The complete mitochondrial genome of the subterranean termite, Reticulitermes chinensis Snyder (Isoptera: rhinotermitidae). Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis, vol. 27, no. 2, pp. 1428-1429. http://dx.doi.org/10.3109/19401736.2014.953077. PMid:25162155.
http://dx.doi.org/10.3109/19401736.2014.... ).

2.5. Gonads of termites

The termite gonads are positioned in the last segments of the abdomen in females and males. All castes of termite have male and female individuals, but only the fully mature, morphological and physiological functional sexual organs were dissected out from the main reproductive castes such as primary reproductive and secondary reproductive (Su et al., 2015SU, X.H., CHEN, J.L., ZHANG, X.J., XUE, W., LIU, H. and XING, L.X., 2015. Testicular development and modes of apoptosis during spermatogenesis in various castes of the termite Reticulitermes labralis (Isoptera:Rhinotermitidae). Arthropod Structure & Development, vol. 44, no. 6 Pt B, pp. 630-638. http://dx.doi.org/10.1016/j.asd.2015.08.009. PMid:26344723.
http://dx.doi.org/10.1016/j.asd.2015.08.... ; Brent et al., 2016BRENT, C.S., PENICK, C.A., TROBAUGH, B., MOORE, D. and LIEBIG, J., 2016. Induction of a reproductive-specific cuticular hydrocarbon profile by a juvenile hormone analog in the termite Zootermopsis nevadensis. Chemoecology, vol. 26, no. 5, pp. 195-203. http://dx.doi.org/10.1007/s00049-016-0219-8.
http://dx.doi.org/10.1007/s00049-016-021... ). The queen reproductive system comprises the genital cavity, accessory gland, spermatheca, oviducts, and branched ovary (Raina et al., 2007RAINA, A., MURPHY, C., FLORANE, C., WILLIAMS, K., PARK, Y.I. and INGBER, B., 2007. Structure of spermatheca, sperm dynamics, and associated bacteria in Formosan subterranean termite (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 100, no. 3, pp. 418-424. http://dx.doi.org/10.1603/0013-8746(2007)100[418:SOSSDA]2.0.CO;2.
http://dx.doi.org/10.1603/0013-8746(2007... ) while in king it consists of the accessory gland, ejaculatory duct, seminal vesicle, vas deferens and testis (Laranjo et al., 2018LARANJO, L.T., HAIFIG, I. and COSTA-LEONARDO, A.M., 2018. Morphology of the male reproductive system during post-embryonic development of the termite Silvestritermes euamignathus (Isoptera: termitidae). Zoologischer Anzeiger, vol. 272, pp. 20-28. http://dx.doi.org/10.1016/j.jcz.2017.11.015.
http://dx.doi.org/10.1016/j.jcz.2017.11.... ; Vargo, 2019VARGO, E.L., 2019. Diversity of termite breeding systems. Insects, vol. 10, no. 2, pp. 52. http://dx.doi.org/10.3390/insects10020052. PMid:30759735.
http://dx.doi.org/10.3390/insects1002005... ). The ovary is composed of multiple branched oocytes that are arranged in turn inside the ovarian tubes (Husseneder et al., 2012aHUSSENEDER, C., MCGREGOR, C., LANG, R.P., COLLIER, R. and DELATTE, J., 2012a. Transcriptome profiling of female alates and egg-laying queens of the Formosan subterranean termite. Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics, vol. 7, no. 1, pp. 14-27. http://dx.doi.org/10.1016/j.cbd.2011.10.002. PMid:22079412.
http://dx.doi.org/10.1016/j.cbd.2011.10.... ). The swollen belly of the termite queens is the sign of the matured ovaries, which felled of a large number of eggs in tubes (Aanen, 2018AANEN, D.K., 2018. The disposable male-the ultimate emancipation of females? BMC Biology, vol. 16, no. 1, pp. 106. http://dx.doi.org/10.1186/s12915-018-0574-8. PMid:30249271.
http://dx.doi.org/10.1186/s12915-018-057... ). The female of secondary reproductive in the matured colonies also has notably expanded abdomen as alates due to matured ovaries (Maekawa et al., 2010MAEKAWA, K., ISHITANI, K., GOTOH, H., CORNETTE, R. and MIURA, T., 2010. Juvenile Hormone titre and vitellogenin gene expression related to ovarian development in primary reproductives compared with nymphs and nymphoid reproductives of the termite Reticulitermes speratus. Physiological Entomology, vol. 35, no. 1, pp. 52-58. http://dx.doi.org/10.1111/j.1365-3032.2009.00711.x.
http://dx.doi.org/10.1111/j.1365-3032.20... ).

The adult female mate with a male, the sperm are transferred and stored in the spermatheca of the female (Raina et al., 2007RAINA, A., MURPHY, C., FLORANE, C., WILLIAMS, K., PARK, Y.I. and INGBER, B., 2007. Structure of spermatheca, sperm dynamics, and associated bacteria in Formosan subterranean termite (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 100, no. 3, pp. 418-424. http://dx.doi.org/10.1603/0013-8746(2007)100[418:SOSSDA]2.0.CO;2.
http://dx.doi.org/10.1603/0013-8746(2007... ; Saran et al., 2007SARAN, R.K., MILLAR, J.G. and RUST, M.K., 2007. Role of (3Z,6Z,8E)-dodecatrien-1-ol in trail following, feeding, and mating behavior of Reticulitermes hesperus. Journal of Chemical Ecology, vol. 33, no. 2, pp. 369-389. http://dx.doi.org/10.1007/s10886-006-9229-2. PMid:17200889.
http://dx.doi.org/10.1007/s10886-006-922... ; Husseneder et al., 2012aHUSSENEDER, C., MCGREGOR, C., LANG, R.P., COLLIER, R. and DELATTE, J., 2012a. Transcriptome profiling of female alates and egg-laying queens of the Formosan subterranean termite. Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics, vol. 7, no. 1, pp. 14-27. http://dx.doi.org/10.1016/j.cbd.2011.10.002. PMid:22079412.
http://dx.doi.org/10.1016/j.cbd.2011.10.... ; Yashiro and Lo, 2019YASHIRO, T. and LO, N., 2019. Comparative screening of endosymbiotic bacteria associated with the asexual and sexual lineages of the termite Glyptotermes nakajimai. Communicative & Integrative Biology, vol. 12, no. 1, pp. 55-58. http://dx.doi.org/10.1080/19420889.2019.1592418. PMid:31143363.
http://dx.doi.org/10.1080/19420889.2019.... ). The sperm is released from the spermatheca, to fertilize the ovum in the genital cavity and then expelled through the gonopore (Raina et al., 2003RAINA, A., PARK, Y.I. and FLORANE, C., 2003. Behavior and reproductive biology of the primary reproductives of the Formosan subterranean termite (Isoptera: rhinotermitidae). Sociobiology, vol. 41, pp. 37-48.; Raina et al., 2007RAINA, A., MURPHY, C., FLORANE, C., WILLIAMS, K., PARK, Y.I. and INGBER, B., 2007. Structure of spermatheca, sperm dynamics, and associated bacteria in Formosan subterranean termite (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 100, no. 3, pp. 418-424. http://dx.doi.org/10.1603/0013-8746(2007)100[418:SOSSDA]2.0.CO;2.
http://dx.doi.org/10.1603/0013-8746(2007... ). Dispersion flight, site selection and foundation of the colony, tandem pair, mating and fertilization, egg-laying, egg hatching, feeding, and brood care are the life potential processes (Matsuura et al., 2002aMATSUURA, K., FUJIMOTO, M., GOKA, K. and NISHIDA, T., 2002a. Cooperative colony foundation by termite female pairs: altruism for survivorship in incipient colonies. Animal Behaviour, vol. 64, no. 2, pp. 167-173. http://dx.doi.org/10.1006/anbe.2002.3062.
http://dx.doi.org/10.1006/anbe.2002.3062... ; Kusaka and Matsuura, 2018KUSAKA, A. and MATSUURA, K., 2018. Allee effect in termite colony formation: influence of alate density and flight timing on pairing success and survivorship. Insectes Sociaux, vol. 65, no. 1, pp. 17-24. http://dx.doi.org/10.1007/s00040-017-0580-9.
http://dx.doi.org/10.1007/s00040-017-058... ). If the laid eggs are unfertilized (parthenogenetic) in some termites like R. flaviceps, they will not be capable to develop usually and hatching offspring (Xing unpublished data; Yashiro and Matsuura, 2014YASHIRO, T. and MATSUURA, K., 2014. Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction. Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 48, pp. 17212-17217. http://dx.doi.org/10.1073/pnas.1412481111. PMid:25404335.
http://dx.doi.org/10.1073/pnas.141248111... ). The mated females reserve sperm in spermatheca with a functional capacity for a long time and use them for fertilization of the ova in the body (Raina et al., 2003RAINA, A., PARK, Y.I. and FLORANE, C., 2003. Behavior and reproductive biology of the primary reproductives of the Formosan subterranean termite (Isoptera: rhinotermitidae). Sociobiology, vol. 41, pp. 37-48.; Raina et al., 2007RAINA, A., MURPHY, C., FLORANE, C., WILLIAMS, K., PARK, Y.I. and INGBER, B., 2007. Structure of spermatheca, sperm dynamics, and associated bacteria in Formosan subterranean termite (Isoptera: rhinotermitidae). Annals of the Entomological Society of America, vol. 100, no. 3, pp. 418-424. http://dx.doi.org/10.1603/0013-8746(2007)100[418:SOSSDA]2.0.CO;2.
http://dx.doi.org/10.1603/0013-8746(2007... ).

2.6. Egg laying of termites

Macrotermes anandalei termite has laid 2949 eggs and the M. subhyalinus has 3,600 eggs in 24 hours (Krishna, 2020KRISHNA, K., 2020 [viewed 10 March 2022]. Termite [online]. Encyclopedia Britannica. Available from: https://www.britannica.com/animal/termite.
https://www.britannica.com/animal/termit... ); while the G. haviandi has been laid 8 eggs that were less in number. Similarly, an average record of queens is 25 eggs laying per min, 36,000 eggs daily and 13,140,000 eggs per year (Wako, 2015WAKO, S.E., 2015. Behaviour and ecological impacts of termites: fecundity investigations in mounds. Ekológia, vol. 34, no. 1, pp. 72-81.). Matsuura and Kobayashi (2007)MATSUURA, K. and KOBAYASHI, N., 2007. Size, hatching rate, and hatching period of sexually and asexually produced eggs in the facultatively parthenogenetic termite Reticulitermes speratus (Isoptera: rhinotermitidae). Applied Entomology and Zoology, vol. 42, no. 2, pp. 241-246. http://dx.doi.org/10.1303/aez.2007.241.
http://dx.doi.org/10.1303/aez.2007.241... also reported that the termites in the North part of Japan begin egg laying in April with a comparative less in number than the eggs laid in July and in October. Alates of R. speratus mostly the female paired up with another female partner cooperatively and started to build a new nest, while a single female can also build and start a colony without mating with male adults (Matsuura et al., 2004MATSUURA, K., FUJIMOTO, M. and GOKA, K., 2004. Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Sociaux, vol. 51, no. 4, pp. 325-332. http://dx.doi.org/10.1007/s00040-004-0746-0.
http://dx.doi.org/10.1007/s00040-004-074... ). Queens R. speratus established colonies by parthenogenesis in the Northern parts of Japan (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Li et al., 2016cLI, H.-F., YEH, H.-T., CHIU, C.-I., KUO, C.-Y. and TSAI, M.-J., 2016c. Vertical distribution of termites on trees in two forest landscapes in Taiwan. Environmental Entomology, vol. 45, no. 3, pp. 577-581. http://dx.doi.org/10.1093/ee/nvw019. PMid:27016004.
http://dx.doi.org/10.1093/ee/nvw019... ). Moreover, the queen of R. speratus in a mature colony laid a total of 24.7 eggs each day, so the rate of egg production was found greater than 0.3 eggs per day. Hence termite fecundity is also related to the season, temperature and humidity. R. aculabialis and R. flaviceps female-female (RaFF and RfFF) alates firstly laid eggs 35.12±2.59 and 26.64±3.78 days after colony foundation, and the monthly average number of one colony collected eggs respectively were 18.24±3.18 and 11.53±4.51 in August, 11.16±4.26 and 3.67±1.24 in September. The result suggested that R. aculabialis parthenogenetically laid more eggs than R. flaviceps in two months. While the R. flaviceps laid more eggs in August rather than September. There was no difference in the number of eggs produced parthenogenetically and the eggs sexually in R. chinensis, R. labralis and R. speratus. There was a significant difference in the number of eggs in the two females without the parthenogenetic ability (Xing unpublished data (Li et al., 2016aLI, G., LIU, L., SUN, P., WU, Y., LEI, C., CHEN, X. & HUANG, Q. 2016a. Physiological profiles associated with ceasing growth of unfertilized eggs produced by unmated queens in the subterranean termite Reticulitermes chinensis. Biology Open, vol. 5, bio.017319.).

An interaction of termites and fungi (Fibulorhizoctonia sp.) are considered as a mutualistic association between them. However, lower termite R. chinensis and R. labralis use fungi sclerotia within their egg piles in nests. The fungi sclerotia don't germinate in the egg piles under worker observation; whereas R. aculabialis have no such a phenomenon to collect sclerotia in their nests; while R. okinawanus has no natural association with the fungi that tended termite balls along with its eggs. To date, it has been found egg-mimicking fungus in four Reticulitermes termites (R. miyatakei, R. amamianus, R. kanmonensis and R. speratus) in Japan.

2.7. Termite eggs and embryo development

The insect eggshell is principally made of a high concentration of lipoprotein (Velentzas et al., 2018VELENTZAS, A.D., VELENTZAS, P.D., KATARACHIA, S.A., ANAGNOSTOPOULOS, A.K., SAGIOGLOU, N.E., THANOU, E.V., TSIOKA, M., MPAKOU, V.E., KOLLIA, Z., GAVRIIL, V.E., PAPASSIDERI, I.S., TSANGARIS, G.T., CEFALAS, A.-C., SARANTOPOULOU, E. and STRAVOPODIS, D.J., 2018. The indispensable contribution of s38 protein to ovarian-eggshell morphogenesis in Drosophila melanogaster. Scientific Reports, vol. 8, no. 1, pp. 1610331. http://dx.doi.org/10.1038/s41598-018-34532-2.
http://dx.doi.org/10.1038/s41598-018-345... ). The thickness of an insect eggshell is ranged between l-70 μm (Church et al., 2019CHURCH, S., DONOUGHE, S., MEDEIROS, B. and EXTAVOUR, C.G., 2019. A database of egg size and shape from more than 6,700 insect 2 species. Scientific Data, vol. 6, no. 1, pp. 104. http://dx.doi.org/10.1038/s41597-019-0049-y. PMid:31270334.
http://dx.doi.org/10.1038/s41597-019-004... ; Isoe et al., 2019ISOE, J., KOCH, L.E., ISOE, Y.E., RASCÓN JUNIOR, A., BROWN, H.E., MASSANI, B.B. and MIESFELD, R.L., 2019. Identification and characterization of a mosquito-specific eggshell organizing factor in Aedes aegypti mosquitoes. PLoS Biology, vol. 17, no. 1, e3000068. http://dx.doi.org/10.1371/journal.pbio.3000068. PMid:30620728.
http://dx.doi.org/10.1371/journal.pbio.3... ). For example, the thickness of the eggshell of Apis mellifera is about 0.35-0.43 mm (Wegener et al., 2009WEGENER, J., AL-KAHTANI, S. and BIENEFELD, K., 2009. Collection of viable honey bee (Apis mellifera) larvae after hatching in vitro. Journal of Apicultural Research, vol. 48, no. 2, pp. 115-120. http://dx.doi.org/10.3896/IBRA.1.48.2.05.
http://dx.doi.org/10.3896/IBRA.1.48.2.05... ). The micropyles on the external surface of the eggshell were observed, which mostly allow the passage of sperm into the eggs and regulate the exchange of gases during the development of embryos (Yanagimachi et al., 2013YANAGIMACHI, R., CHERR, G., MATSUBARA, T., ANDOH, T., HARUMI, T., VINES, C., PILLAI, M., GRIFFIN, F., MATSUBARA, H., WEATHERBY, T. and KANESHIRO, K., 2013. Sperm attractant in the micropyle region of fish and insect eggs. Biology of Reproduction, vol. 88, no. 2, pp. 47. http://dx.doi.org/10.1095/biolreprod.112.105072. PMid:23303675.
http://dx.doi.org/10.1095/biolreprod.112... ; Matsuura, 2017MATSUURA, K., 2017. Evolution of the asexual queen succession system and its underlying mechanisms in termites. The Journal of Experimental Biology, vol. 220, no. 1, pp. 63-72. http://dx.doi.org/10.1242/jeb.142547. PMid:28057829.
http://dx.doi.org/10.1242/jeb.142547... ). In insect eggshells, there many micropyles were counted between 1-10 (Pijnacker and Godeke, 1984PIJNACKER, L.P. and GODEKE, J., 1984. Structure of the Micropyle in the eggs of the parthenogenetic stick insect Carausius Morosus Br. (Phasmatodea, Phasmatidea). Netherlands Journal of Zoology, vol. 34, pp. 407-413.; Iossa et al., 2016IOSSA, G., GAGE, M. and EADY, P.E., 2016. Micropyle number is associated with elevated female promiscuity in Lepidoptera. Biology Letters, vol. 12, no. 12, pp. 20160782. http://dx.doi.org/10.1098/rsbl.2016.0782. PMid:28003521.
http://dx.doi.org/10.1098/rsbl.2016.0782... ). The termite egg has a significant structure on the surface, such as micropyle, which is the passageway of the air into the egg (Gautam et al., 2014GAUTAM, S.G., OPIT, G.P., MARGOSAN, D., TEBBETS, J.S. and WALSE, S., 2014. Egg Morphology of Key Stored-Product Insect Pests of the United States. Annals of the Entomological Society of America, vol. 107, no. 1, pp. 1-10. http://dx.doi.org/10.1603/AN13103.
http://dx.doi.org/10.1603/AN13103... ; Bowers et al., 2015BOWERS, E.K., WHITE, A., LANG, A., PODGORSKI, L., THOMPSON, C.F., SAKALUK, S.K., JAECKLE, W.B. and HARPER, R.G., 2015. Eggshell porosity Covaries with egg size among female House Wrens (Troglodytes aedon) but is unrelated to incubation onset and egg-laying order within clutches. Canadian Journal of Zoology, vol. 93, no. 6, pp. 421-425. http://dx.doi.org/10.1139/cjz-2014-0279. PMid:26146408.
http://dx.doi.org/10.1139/cjz-2014-0279... ). The eggs of different termites have different numbers and shapes of micropyles (Church et al., 2019CHURCH, S., DONOUGHE, S., MEDEIROS, B. and EXTAVOUR, C.G., 2019. A database of egg size and shape from more than 6,700 insect 2 species. Scientific Data, vol. 6, no. 1, pp. 104. http://dx.doi.org/10.1038/s41597-019-0049-y. PMid:31270334.
http://dx.doi.org/10.1038/s41597-019-004... ). The structure and distribution features of micropyles on eggshells can be used for insect identification and classification (Ubero-Pascal and Puig, 2007UBERO-PASCAL, N. and PUIG, M., 2007. Microscopy and egg morphology of mayflies. In: A. MÉNDEZ-VILAS and J. DÍAZ, eds. Modern research and educational topics in microscopy. Badajoz: Formatex, pp. 326-335.; Hilker and Meiners, 2011HILKER, M. and MEINERS, T., 2011. Plants and insect eggs: how do they affect each other? Phytochemistry, vol. 72, no. 13, pp. 1612-1623. http://dx.doi.org/10.1016/j.phytochem.2011.02.018. PMid:21439598.
http://dx.doi.org/10.1016/j.phytochem.20... ).

The termite eggs are oval cylindrical shaped, and micropyles are situated at one end of the egg. The micropyles of R. speratus were found in the funnels shape channels, with an average diameter of 3.23 μm and a total number of 9 egg holes. In the nest, the queen produced eggs asexually in the absence or presence of kings who have no holes in the shell to stop fertilization (Pervez, 2018PERVEZ, A., 2018. Termite biology and social behaviour. In: M. KHAN and W. AHMAD, eds. Termites and sustainable management. Cham: Springer, pp. 119-143. http://dx.doi.org/10.1007/978-3-319-72110-1_6.
http://dx.doi.org/10.1007/978-3-319-7211... ). The eggs produced through sexual reproduction have holes in eggshells. Moreover, the new queens are more preferred to lay non-porous eggs. Such several micropyles in R. aculabialis female-female (RaFF), R. aculabialis female-male (RaFM), R. flaviceps female-female (RfFF), R. flaviceps (RfFM) eggs were 6.31±1.89, 8.18±3.22, 8.15±2.67 and 8.43±3.05 respectively. The number of micropyles in RaFF was significantly more than in RfFF, but there was no significant difference among the other group (Xing unpublished data).

Most of the insect males and females are mating through sexual reproduction, the sperm and egg fused to form a zygote. Furthermore, the zygote is divided commonly through cleavage (Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.; Vargo et al., 2012VARGO, E.L., LABADIE, P.E. and MATSUURA, K., 2012. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proceedings of the Royal Society Biology, vol. 279, no. 1729, pp. 813-819. http://dx.doi.org/10.1098/rspb.2011.1030. PMid:21831899.
http://dx.doi.org/10.1098/rspb.2011.1030... ; Rhainds, 2019RHAINDS, M., 2019. Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids. Entomologia Experimentalis et Applicata, vol. 167, no. 1, pp. 73-84. http://dx.doi.org/10.1111/eea.12759.
http://dx.doi.org/10.1111/eea.12759... ). At the start of cleavage, the zygote produces a great mass of daughter nuclei, which in turn forms the blastoderms (Kawanishi, 1975KAWANISHI, C.Y., 1975. Embryonic development of the drywood termite, Cryptotermes brevis. Hawaii: Hawaii Agricultural Experiment Station, University of Hawaii, vol. 95, 38 p.; Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.). At the beginning of the cleavage, the nucleus is mostly located in the centre of the egg and then migrates to the surface of the yolk (Hinton, 1981HINTON, H.E., 1981. Biology of insect eggs. Oxford: Pergamon, vols. 1-3, pp. 779-999.; Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.). Some species are distributed to the periplasm at 64 subnuclei, while some species reach the periplasm at 1024 nuclei (Perondini et al., 1986PERONDINI, A., GUTZEIT, H.O. and MORI, L., 1986. Nuclear division and migration during early embryogenesis of Bradysia tritici coquillet (syn. Sciara ocellaris) (diptera: sciaridae). International Journal of Insect Morphology & Embryology, vol. 15, no. 3, pp. 155-163. http://dx.doi.org/10.1016/0020-7322(86)90054-1.
http://dx.doi.org/10.1016/0020-7322(86)9... ). The nucleus of a mature egg on cleavage is divided into two daughter nuclei, this is a type of surface cleavage and complete cleavage, while in most insects it belongs to the surface cleavage (Counce and Ruddle, 1969COUNCE, S.J. and RUDDLE, N.H., 1969. Strain differences in egg structure in Drosophila hydei. Genetica, vol. 40, no. 1, pp. 324-338. http://dx.doi.org/10.1007/BF01787360. PMid:5392211.
http://dx.doi.org/10.1007/BF01787360... ; Illmensee, 1972ILLMENSEE, K., 1972. Developmental potencies of nuclei from cleavage, preblastoderm, and syncytial blastoderm transplanted into unfertilized eggs of Drosophila melanogaster. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen, vol. 170, no. 4, pp. 267-298. http://dx.doi.org/10.1007/BF01380620. PMid:28304727.
http://dx.doi.org/10.1007/BF01380620... ; Counce, 1973COUNCE, S.J., 1973. The analysis of insect embryogenesis. Annual Review of Entomology, vol. 6, no. 1, pp. 295-312. http://dx.doi.org/10.1146/annurev.en.06.010161.001455.
http://dx.doi.org/10.1146/annurev.en.06.... ; Kawamura, 2001KAWAMURA, N., 2001. Fertilization and the first cleavage mitosis in insects. Development, Growth & Differentiation, vol. 43, no. 4, pp. 343-349. http://dx.doi.org/10.1046/j.1440-169x.2001.00584.x. PMid:11473541.
http://dx.doi.org/10.1046/j.1440-169x.20... ).

Complete cleavage occurs in insects with a small amount of yolk, such as the D. melanogaster, Hymenoptera (Panfilio, 2008PANFILIO, K.A., 2008. Extraembryonic development in insects and the acrobatics of blastokinesis. Developmental Biology, vol. 313, no. 2, pp. 471-491. http://dx.doi.org/10.1016/j.ydbio.2007.11.004. PMid:18082679.
http://dx.doi.org/10.1016/j.ydbio.2007.1... ). After the formation of the blastoderm, the cells thicken and become more significant to form an embryonic band (Fernandez-Nicolas and Belles, 2017FERNANDEZ-NICOLAS, A. and BELLES, X., 2017. Juvenile hormone signaling in short germ-band hemimetabolan embryos. Development, vol. 144, no. 24, pp. 4637-4644. http://dx.doi.org/10.1242/dev.152827. PMid:29122840.
http://dx.doi.org/10.1242/dev.152827... ; Benton et al., 2019BENTON, M.A., FREY, N., NUNES DA FONSECA, R., VON LEVETZOW, C., STAPPERT, D., HAKEEMI, M.S., CONRADS, K.H., PECHMANN, M., PANFILIO, K.A., LYNCH, J.A. and ROTH, S., 2019. Fog signaling has diverse roles in epithelial morphogenesis in insects. Life Sciences, vol. 8, e47346. http://dx.doi.org/10.7554/eLife.47346.
http://dx.doi.org/10.7554/eLife.47346... ). There are three types of insect embryos: long embryos in Drosophila (Markova et al., 2019MARKOVA, O., SENATORE, S. and LENNE, P.F., 2019. Spatiotemporal dynamics of calcium transients during embryogenesis of Drosophila melanogaster. bioRxiv. In press. http://dx.doi.org/10.1101/540070.
http://dx.doi.org/10.1101/540070... ), little embryos in termites (Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.) and intermediate embryos in bean weevil (Teixeira et al., 2008TEIXEIRA, I., BARCHUK, A.R. and ZUCOLOTO, F.S., 2008. Host preference of the bean weevil Zabrotes subfasciatus. Insect Science, vol. 15, no. 4, pp. 335-341. http://dx.doi.org/10.1111/j.1744-7917.2008.00218.x.
http://dx.doi.org/10.1111/j.1744-7917.20... ). Embryos are mainly classified into invaginate and superficial types depending on where the embryonic primordia occur (Tojo and Machida, 1997TOJO, K. and MACHIDA, R., 1997. Embryogenesis of the mayfly Ephemera japonica McLachlan (Insecta: Ephemeroptera, Ephemeridae), with special reference to abdominal formation. Journal of Morphology, vol. 234, no. 1, pp. 97-107. http://dx.doi.org/10.1002/(SICI)1097-4687(199710)234:1<97::AID-JMOR9>3.0.CO;2-K. PMid:29852673.
http://dx.doi.org/10.1002/(SICI)1097-468... , Panfilio, 2008PANFILIO, K.A., 2008. Extraembryonic development in insects and the acrobatics of blastokinesis. Developmental Biology, vol. 313, no. 2, pp. 471-491. http://dx.doi.org/10.1016/j.ydbio.2007.11.004. PMid:18082679.
http://dx.doi.org/10.1016/j.ydbio.2007.1... ). The invagination type is that the embryo develops in the yolk, while the surface type embryo develops on the peripheral surface of the yolk (Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.; Corley and Lavine, 2006CORLEY, L.S. and LAVINE, M., 2006. A review of insect stem cell types. Seminars in Cell & Developmental Biology, vol. 17, no. 4, pp. 510-517. http://dx.doi.org/10.1016/j.semcdb.2006.07.002. PMid:16920369.
http://dx.doi.org/10.1016/j.semcdb.2006.... ). The embryonic band forms different germ layers by invagination and expansion, and the segmentation begins when the germinal layer differentiates (Dearden, 2006DEARDEN, P.K., 2006. Germ cell development in the Honeybee (Apis mellifera); Vasa and Nanosexpression. BMC Developmental Biology, vol. 6, no. 1, pp. 6. http://dx.doi.org/10.1186/1471-213X-6-6. PMid:16503992.
http://dx.doi.org/10.1186/1471-213X-6-6... ; Fang et al., 2014FANG, Y., FENG, M., HAN, B., LU, X., RAMADAN, H. and LI, J., 2014. In-depth Proteomics Characterization of Embryogenesis of the Honey Bee Worker (Apis mellifera ligustica). Molecular & Cellular Proteomics, vol. 13, no. 9, pp. 2306-2320. http://dx.doi.org/10.1074/mcp.M114.037846. PMid:24895377.
http://dx.doi.org/10.1074/mcp.M114.03784... ; Korb, 2015KORB, J., 2015. Juvenile Hormone. Advances in Insect Physiology, vol. 48, pp. 131-161. http://dx.doi.org/10.1016/bs.aiip.2014.12.004.
http://dx.doi.org/10.1016/bs.aiip.2014.1... ). The full front end of the embryo develops into the head region (Korb, 2015KORB, J., 2015. Juvenile Hormone. Advances in Insect Physiology, vol. 48, pp. 131-161. http://dx.doi.org/10.1016/bs.aiip.2014.12.004.
http://dx.doi.org/10.1016/bs.aiip.2014.1... ). A pair of appendage primordia appear on each part of the embryo and develops into an appendage (Maekawa et al., 2008MAEKAWA, K., MIZUNO, S., KOSHIKAWA, S. and MIURA, T., 2008. Compound eye development during caste differentiation in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Zoological Science, vol. 25, no. 7, pp. 699-705. http://dx.doi.org/10.2108/zsj.25.699. PMid:18828656.
http://dx.doi.org/10.2108/zsj.25.699... ). Both sides of the embryonic band are sealed at the midline of the back. At this point, the various organ systems inside the insect are fully developed, and the embryo is finally developed (Kishimoto and Ando, 1985KISHIMOTO, T. and ANDO, H., 1985. External features of the developing embryo of the stonefly, Kamimuria tibialis (pictet) (Plecoptera, Perlidae). Journal of Morphology, vol. 183, no. 3, pp. 311-326. http://dx.doi.org/10.1002/jmor.1051830308. PMid:29969870.
http://dx.doi.org/10.1002/jmor.105183030... ; Maekawa et al., 2008MAEKAWA, K., MIZUNO, S., KOSHIKAWA, S. and MIURA, T., 2008. Compound eye development during caste differentiation in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Zoological Science, vol. 25, no. 7, pp. 699-705. http://dx.doi.org/10.2108/zsj.25.699. PMid:18828656.
http://dx.doi.org/10.2108/zsj.25.699... ; Panfilio, 2008PANFILIO, K.A., 2008. Extraembryonic development in insects and the acrobatics of blastokinesis. Developmental Biology, vol. 313, no. 2, pp. 471-491. http://dx.doi.org/10.1016/j.ydbio.2007.11.004. PMid:18082679.
http://dx.doi.org/10.1016/j.ydbio.2007.1... ). There are characteristic differences in the development of different types of insect embryos. Termites evolved from the order of the Cryptocercus roaches (Bourguignon et al., 2015BOURGUIGNON, T., LO, N., CAMERON, S.L., ŠOBOTNÍK, J., HAYASHI, Y., SHIGENOBU, S., WATANABE, D., ROISIN, Y., MIURA, T. and EVANS, T.A., 2015. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Molecular Biology and Evolution, vol. 32, no. 2, pp. 406-421. http://dx.doi.org/10.1093/molbev/msu308. PMid:25389205.
http://dx.doi.org/10.1093/molbev/msu308... ; Legendre and Grandcolas, 2018LEGENDRE, F. and GRANDCOLAS, P., 2018. The evolution of sociality in termites from cockroaches: a taxonomic and phylogenetic perspective. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, vol. 330, no. 5, pp. 279-287. http://dx.doi.org/10.1002/jez.b.22812. PMid:29989317.
http://dx.doi.org/10.1002/jez.b.22812... ), and the cleavage mode of the sexual reproductive embryos is surface cleavage (Kawanishi, 1975KAWANISHI, C.Y., 1975. Embryonic development of the drywood termite, Cryptotermes brevis. Hawaii: Hawaii Agricultural Experiment Station, University of Hawaii, vol. 95, 38 p.). Embryonic development is divided into six stages: cleavage and blastocyst formation, the formation of the blastoderm, embryonic bands, elongation and segmentation, the formation of a tail bend, rotation, closure, and hatching (Hu and Xu, 2005HU, X.P. and XU, Y.Y., 2005. Morphological embryonic development of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: rhinotermitidae). Sociobiology, vol. 45, pp. 573-586.; Maekawa et al., 2008MAEKAWA, K., MIZUNO, S., KOSHIKAWA, S. and MIURA, T., 2008. Compound eye development during caste differentiation in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Zoological Science, vol. 25, no. 7, pp. 699-705. http://dx.doi.org/10.2108/zsj.25.699. PMid:18828656.
http://dx.doi.org/10.2108/zsj.25.699... ).

2.8. Parthenogenesis of termites

In sexual reproduction, the eggs of insects are activated by the fusion of the sperm and ovum nuclei after completing meiosis (Maekawa et al., 2008MAEKAWA, K., MIZUNO, S., KOSHIKAWA, S. and MIURA, T., 2008. Compound eye development during caste differentiation in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Zoological Science, vol. 25, no. 7, pp. 699-705. http://dx.doi.org/10.2108/zsj.25.699. PMid:18828656.
http://dx.doi.org/10.2108/zsj.25.699... ), while the eggs develop in some insect individuals without fertilization through parthenogenesis (Rhainds, 2019RHAINDS, M., 2019. Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids. Entomologia Experimentalis et Applicata, vol. 167, no. 1, pp. 73-84. http://dx.doi.org/10.1111/eea.12759.
http://dx.doi.org/10.1111/eea.12759... ). Constant parthenogenetic reproduction was found in a few insect species such as stick insects and bees (Morgan‐Richards et al., 2010MORGAN‐RICHARDS, M., TREWICK, S.A. and STRINGER, I.A., 2010. Geographic parthenogenesis and the common tea‐tree stick insect of New Zealand. Molecular Ecology, vol. 19, no. 6, pp. 1227-1238. http://dx.doi.org/10.1111/j.1365-294X.2010.04542.x. PMid:20163549.
http://dx.doi.org/10.1111/j.1365-294X.20... ). In insects, the evolution of parthenogenesis includes viz. self-initiating sources, in some moths, aphids, and stick insects (Wei et al., 2000WEI, Y.Q., LIU, Y.C., ZHANG, S.X., MA, S.Q., GONG, Y.J., LI, H.X., YANG, R.X., WANG, C.Z. and LI, G., 2000. Parthenogenesis induced by chemicals in spring wheat and its application in wheat breeding. Ningxia Journal of Agricultural & Forestry Science & Technology, vol. 3, pp. 1-3.; Balázs and Burg, 1963BALÁZS, A. and BURG, M., 1963. Influence of Copulation on the Longevity of the Great Wax Moth (Galleria mellonella). Gerontology, vol. 7, no. 4, pp. 233-244. http://dx.doi.org/10.1159/000211199.
http://dx.doi.org/10.1159/000211199... ; Dedryver et al., 2017DEDRYVER, C.A., BONHOMME, J., GALLIC, J. and SIMON, J.C., 2017. Differences in egg hatching time between cyclical and obligate parthenogenetic lineages of aphids. Insect Science, vol. 26, no. 1, pp. 135-141. http://dx.doi.org/10.1111/1744-7917.12493. PMid:28608995.
http://dx.doi.org/10.1111/1744-7917.1249... ) and evolution of hybrid in polyploid animals such as moths, sexual reproduction and parthenogenesis play roles in hybridization (Wei et al., 2000WEI, Y.Q., LIU, Y.C., ZHANG, S.X., MA, S.Q., GONG, Y.J., LI, H.X., YANG, R.X., WANG, C.Z. and LI, G., 2000. Parthenogenesis induced by chemicals in spring wheat and its application in wheat breeding. Ningxia Journal of Agricultural & Forestry Science & Technology, vol. 3, pp. 1-3.).

Facultative parthenogenesis is very important for the maintenance of sex, evolution and is beneficial in a few aspects of sexual and asexual reproduction (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Yashiro and Matsuura, 2014YASHIRO, T. and MATSUURA, K., 2014. Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction. Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 48, pp. 17212-17217. http://dx.doi.org/10.1073/pnas.1412481111. PMid:25404335.
http://dx.doi.org/10.1073/pnas.141248111... ; Stelzer, 2015STELZER, C.-P., 2015. Does the avoidance of sexual costs increase fitness in asexual invaders? Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 29, pp. 8851-8858. http://dx.doi.org/10.1073/pnas.1501726112. PMid:26195736.
http://dx.doi.org/10.1073/pnas.150172611... ). For a prosperous colony of termite parthenogenesis play, an essential role in the case of females getting a failure to mate with males (Matsuura and Kobayashi, 2007MATSUURA, K. and KOBAYASHI, N., 2007. Size, hatching rate, and hatching period of sexually and asexually produced eggs in the facultatively parthenogenetic termite Reticulitermes speratus (Isoptera: rhinotermitidae). Applied Entomology and Zoology, vol. 42, no. 2, pp. 241-246. http://dx.doi.org/10.1303/aez.2007.241.
http://dx.doi.org/10.1303/aez.2007.241... ). If the adult female feels the deficiency of males after dispersion flight, it builds a colony with the cooperation of another female partner and achieves parthenogenesis for continuity of the colony. If a single female builds a nest, it must be responsible for the entire work related to the colony (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Matsuura et al., 2002aMATSUURA, K., FUJIMOTO, M., GOKA, K. and NISHIDA, T., 2002a. Cooperative colony foundation by termite female pairs: altruism for survivorship in incipient colonies. Animal Behaviour, vol. 64, no. 2, pp. 167-173. http://dx.doi.org/10.1006/anbe.2002.3062.
http://dx.doi.org/10.1006/anbe.2002.3062... ). The rate of survival of female pairing is closely related to the survival rate of male-female pairing due to cooperation between the coupled females that ensure their normal lives and activities in the colony (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Matsuura et al., 2002bMATSUURA, K., KUNO, E. and NISHIDA, T., 2002b. Homosexual tandem running as selfish herd in Reticulitermes speratus: novel antipredatory behavior in termites. Journal of Theoretical Biology, vol. 214, no. 1, pp. 63-70. http://dx.doi.org/10.1006/jtbi.2001.2447. PMid:11786032.
http://dx.doi.org/10.1006/jtbi.2001.2447... ). Although twice beneficial adaptations are provided by parthenogenetic reproduction comparative sex reproduction. Both genetic and developmental conditions limit parthenogenesis, and the survival rate of its offspring is usually lower than that of sexual reproduction (Corley et al., 1999CORLEY, L.S., BLANKENSHIP, J.R., MOORE, A.J. and MOORE, P.J., 1999. Developmental constraints on the mode of reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea. Evolution & Development, vol. 1, no. 2, pp. 90-99. http://dx.doi.org/10.1046/j.1525-142x.1999.99001.x. PMid:11324032.
http://dx.doi.org/10.1046/j.1525-142x.19... ).

Currently, few Isopteran species have been found with the ability of parthenogenesis (Matsuura and Nishida, 2001MATSUURA, K. and NISHIDA, T., 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: rhinotermitidae). Population Ecology, vol. 43, no. 2, pp. 119-124. http://dx.doi.org/10.1007/PL00012022.
http://dx.doi.org/10.1007/PL00012022... ; Matsuura, 2017MATSUURA, K., 2017. Evolution of the asexual queen succession system and its underlying mechanisms in termites. The Journal of Experimental Biology, vol. 220, no. 1, pp. 63-72. http://dx.doi.org/10.1242/jeb.142547. PMid:28057829.
http://dx.doi.org/10.1242/jeb.142547... ) and asexual reproduction is also used by some propagative termites (Hayashi et al., 2003HAYASHI, Y., KITADE, O. and KOJIMA, J.C., 2003. Parthenogenetic reproduction in neotenics of the subterranean termite Reticulitermes speratus (Isoptera: rhinotermitidae). Entomological Science, vol. 6, no. 4, pp. 253-257. http://dx.doi.org/10.1046/j.1343-8786.2003.00030.x.
http://dx.doi.org/10.1046/j.1343-8786.20... ). Asexual queen succession (AQS) is an exceptional system of termite parthenogenesis (Matsuura et al., 2009MATSUURA, K., VARGO, E.L., KAWATSU, K., LABADIE, P.E., NAKANO, H., YASHIRO, T. and TSUJI, K., 2009. Queen succession through asexual reproduction in termites. Science, vol. 323, no. 5922, pp. 1687. http://dx.doi.org/10.1126/science.1169702. PMid:19325106.
http://dx.doi.org/10.1126/science.116970... ). The AQS system has been recognized already all over the world in the termites such as R. verginicus and R. lucifugus (Vargo et al., 2012VARGO, E.L., LABADIE, P.E. and MATSUURA, K., 2012. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proceedings of the Royal Society Biology, vol. 279, no. 1729, pp. 813-819. http://dx.doi.org/10.1098/rspb.2011.1030. PMid:21831899.
http://dx.doi.org/10.1098/rspb.2011.1030... ; Luchetti et al., 2013LUCHETTI, A., VELONÀ, A., MUELLER, M. and MANTOVANI, B., 2013. Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: rhinotermitidae). Insectes Sociaux, vol. 60, no. 2, pp. 203-211. http://dx.doi.org/10.1007/s00040-013-0284-8.
http://dx.doi.org/10.1007/s00040-013-028... ), and two higher termites Cavitermes tuberosus and Embiratermes neotenicus (Fougeyrollas et al., 2015FOUGEYROLLAS, R., DOLEJŠOVÁ, K., SILLAM-DUSSÈS, D., ROY, V. and ROISIN, Y., 2015. Asexual queen succession in the higher termite Embiratermes neotenicus. Proceedings. Biological Sciences, vol. 282, no. 1809, pp. 1-7. http://dx.doi.org/10.1098/rspb.2015.0260. PMid:26019158.
http://dx.doi.org/10.1098/rspb.2015.0260... ; Fournier et al., 2016FOURNIER, D., HELLEMANS, S., HANUS, R. and ROISIN, Y., 2016. Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proceedings. Biological sciences The Royal Society, vol. 283, no. 1832, pp. 20160196. http://dx.doi.org/10.1098/rspb.2016.0196. PMid:27252019.
http://dx.doi.org/10.1098/rspb.2016.0196... ). The process of parthenogenesis in lower termites is considered the “end fusion” (Matsuura et al., 2004MATSUURA, K., FUJIMOTO, M. and GOKA, K., 2004. Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Sociaux, vol. 51, no. 4, pp. 325-332. http://dx.doi.org/10.1007/s00040-004-0746-0.
http://dx.doi.org/10.1007/s00040-004-074... ; Vargo et al., 2012VARGO, E.L., LABADIE, P.E. and MATSUURA, K., 2012. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proceedings of the Royal Society Biology, vol. 279, no. 1729, pp. 813-819. http://dx.doi.org/10.1098/rspb.2011.1030. PMid:21831899.
http://dx.doi.org/10.1098/rspb.2011.1030... ; Matsuura and Kobayashi, 2010MATSUURA, K. and KOBAYASHI, N., 2010. Termite queens adjust egg size according to colony development. Behavioral Ecology, vol. 21, no. 5, pp. 1018-1023. http://dx.doi.org/10.1093/beheco/arq101.
http://dx.doi.org/10.1093/beheco/arq101... ), while in higher termites “central fusion” (Fournier et al., 2016FOURNIER, D., HELLEMANS, S., HANUS, R. and ROISIN, Y., 2016. Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proceedings. Biological sciences The Royal Society, vol. 283, no. 1832, pp. 20160196. http://dx.doi.org/10.1098/rspb.2016.0196. PMid:27252019.
http://dx.doi.org/10.1098/rspb.2016.0196... ).

R. chinensis with asexual queen succession, produced unfertilized eggs can be but have no phenomenon of egg incubation (Li et al., 2016bLI, G., LIU, L., SUN, P., WU, Y., LEI, C., CHEN, X. and HUANG, Q., 2016b. Physiological reason for ceasing growth of unfertilized eggs produced by unmated queens in the subterranean termite Reticulitermes chinensis. bioRxiv. In press.). Embryonic development between fertilized and unfertilized eggs in two termite species, R. chinensis and R. aculabialis for external morphology of eggs, cleavage and embryo were observed by using laser scanning and digital microscope. Both types of egg development were compared in two termite species based on size, width, volume, number of nuclei and cleavage in 24 and 48 hrs that had a significant difference in the FF eggs. In contrast on the 15^th day, there are no significant changes occurred in the volume of FF egg, whereas the FM egg significantly increased. The FF eggs died on the 15^th-20^th day, while the FM eggs were in normal development. Similarly, there was no variance in nuclei number between the fertilized and unfertilized eggs of R. aculabialis. While the increase of length, width, volume and nuclei number higher in fertilized than unfertilized eggs 10^th to 15^th day in R. aculabialis. Unfertilized eggs of R. chinensis can be cleaved with abnormal development and cannot be hatched in the end. The cleavage features of the unfertilized egg of R. chinensis may be an adaptive stage from bisexual reproduction to facultative parthenogenesis in termite reproductive evolution (Tan et al., 2016TAN, Y.L., DANG, Y.L., ZHANG, H.G., GUO, X.H., YAN, X.R., HONG, S.X. and XING, L.X., 2016. A comparative study of embryonic development between gamogenesis and parthenogenesis in two Reticulitermes termites (Isoptera: Rhinotermitidae) (in Chinese with English abstract). Acta Entomologica Sinica, vol. 59, pp. 438-445.). R. aculabialis have the ability of parthenogenesis while R. flaviceps which have no parthenogenesis in both morphological and genetic level (Xing unpublished data). Termite colonies are initiated by a couple of sexual reproducers, sometimes that are replaced by some asexual queens of Reticulitermes and Embiratermes. Asexual queen succession (Cavitermes tuberosus) is also replaced by neotenic daughters, as they were produced by parthenogenesis, which is finally ready to mate with the primary king. Here, to cast light on the evolution of AQS, we investigated another candidate species (Fournier et al., 2016FOURNIER, D., HELLEMANS, S., HANUS, R. and ROISIN, Y., 2016. Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proceedings. Biological sciences The Royal Society, vol. 283, no. 1832, pp. 20160196. http://dx.doi.org/10.1098/rspb.2016.0196. PMid:27252019.
http://dx.doi.org/10.1098/rspb.2016.0196... ).

2.9. Termite hybridization

Hybridization is a reproductive behavioural phenomenon that commonly occurs between the two species of termites that genetically came from distinct populations (Kuswanto et al., 2015KUSWANTO, E., AHMAD, I. and DUNGANI, R., 2015. Threat of subterranean termites attack in the Asian Countries and their control: a review. Asian Journal of Applied Sciences, vol. 8, no. 4, pp. 227-239. http://dx.doi.org/10.3923/ajaps.2015.227.239.
http://dx.doi.org/10.3923/ajaps.2015.227... ; Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ). They cause genetically interactions of offspring inherited from two parents possibly from different species genetically (Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ; Buczkowski and Bertelsmeier, 2017BUCZKOWSKI, G. and BERTELSMEIER, C., 2017. Invasive termites in a changing climate: a global perspective. Ecology and Evolution, vol. 7, no. 3, pp. 974-985. http://dx.doi.org/10.1002/ece3.2674. PMid:28168033.
http://dx.doi.org/10.1002/ece3.2674... ). This variation contains some moderate distinction, accumulates in different ways and is compatible and successful ecologically, overlapped with a new economic influence on the world, some of which are produced by connections between hybrids (Patel et al., 2019PATEL, J.S., TONG, R.L., CHOUVENC, T. and SU, N.Y., 2019. Comparison of temperature-dependent survivorship and wood-consumption rate among two invasive subterranean termite species (Blattodea: Rhinotermitidae: Coptotermes) and their hybrids. Journal of Economic Entomology, vol. 112, no. 1, pp. 300-304. http://dx.doi.org/10.1093/jee/toy347. PMid:30462223.
http://dx.doi.org/10.1093/jee/toy347... ).

Heterozygous domains resulting from hybridization have favourable ecological and evolutionary consequences than the parental populations (Roberts et al., 2009ROBERTS, D.G., GRAY, C.A., WEST, R.J. and AYRE, D.J., 2009. Evolutionary impacts of hybridization and interspecific gene flow on an obligately estuarine fish. Journal of Evolutionary Biology, vol. 22, no. 1, pp. 27-35. http://dx.doi.org/10.1111/j.1420-9101.2008.01620.x. PMid:18800995.
http://dx.doi.org/10.1111/j.1420-9101.20... ; Patel et al., 2019PATEL, J.S., TONG, R.L., CHOUVENC, T. and SU, N.Y., 2019. Comparison of temperature-dependent survivorship and wood-consumption rate among two invasive subterranean termite species (Blattodea: Rhinotermitidae: Coptotermes) and their hybrids. Journal of Economic Entomology, vol. 112, no. 1, pp. 300-304. http://dx.doi.org/10.1093/jee/toy347. PMid:30462223.
http://dx.doi.org/10.1093/jee/toy347... ). The resultant progeny from hybridization have dominant effects and promote species dispersion in a wide range in few regions, such an example came from the two invasive fire ant species (Solenopsis richteri×S. invicta) in the Southern United States where they established a fully hybrid zone now (Gibbons and Simberloff, 2005GIBBONS, L. and SIMBERLOFF, D., 2005. Interaction of hybrid imported fire ants (Solenopsis invicta × S. richteri) with native ants at baits in Southeastern Tennessee. Southeastern Naturalist, vol. 4, no. 2, pp. 303-320. http://dx.doi.org/10.1656/1528-7092(2005)004[0303:IOHIFA]2.0.CO;2.
http://dx.doi.org/10.1656/1528-7092(2005... ; Chen et al., 2015CHEN, J., RASHID, T. and FENG, G., 2015. Esterase in Imported Fire Ants, Solenopsis invicta and S. richteri (Hymenoptera: Formicidae): Activity, Kinetics and Variation. Scientific Reports, vol. 4, no. 1, pp. 7112-7112. http://dx.doi.org/10.1038/srep07112. PMid:25408118.
http://dx.doi.org/10.1038/srep07112... ) and another one from the subspecies of A. mellifera (European honey bee × Africanized honey bee) became trouble for human population in South and North part of America (Schneider et al., 2004SCHNEIDER, S.S., DEGRANDIHOFFMAN, G. and SMITH, D.R., 2004. The African honey bee: factors contributing to a successful biological invasion. Annual Review of Entomology, vol. 49, no. 1, pp. 351-376. http://dx.doi.org/10.1146/annurev.ento.49.061802.123359. PMid:14651468.
http://dx.doi.org/10.1146/annurev.ento.4... ; Jensen et al., 2005JENSEN, A.B., PALMER, K.A., BOOMSMA, J.J. and PEDERSEN, B., 2005. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, vol. 14, no. 1, pp. 93-106. http://dx.doi.org/10.1111/j.1365-294X.2004.02399.x. PMid:15643954.
http://dx.doi.org/10.1111/j.1365-294X.20... ; Vanengelsdorp and Meixner, 2010VANENGELSDORP, D. and MEIXNER, M., 2010. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, vol. 103, suppl. 1, pp. S80-S95. http://dx.doi.org/10.1016/j.jip.2009.06.011. PMid:19909973.
http://dx.doi.org/10.1016/j.jip.2009.06.... ).

While the hybridization hinders species formation due to the flow of genes between species with diverse ploidy levels is understood to be improbable, such species are expected to be reproductively isolated from one another due to strong reproductive barriers (Todesco et al., 2016TODESCO, M., PASCUAL, M.A., OWENS, G.L., OSTEVIK, K.L., MOYERS, B.T., HÜBNER, S., HEREDIA, S.M., HAHN, M.A., CASEYS, C., BOCK, D.G. and RIESEBERG, L.H., 2016. Hybridization and extinction. Evolutionary Applications, vol. 9, no. 7, pp. 892-908. http://dx.doi.org/10.1111/eva.12367. PMid:27468307.
http://dx.doi.org/10.1111/eva.12367... ).

Hybridization of organisms enhances the chances of species adaptability and living under severe environmental factors (Pfennig, 2007PFENNIG, K.S., 2007. Facultative mate choice drives adaptive hybridization. Science, vol. 318, no. 5852, pp. 965-967. http://dx.doi.org/10.1126/science.1146035. PMid:17991861.
http://dx.doi.org/10.1126/science.114603... ; Pfennig et al., 2016PFENNIG, K.S., KELLY, A.L. and PIERCE, A.A., 2016. Hybridization as a facilitator of species range expansion. Proceedings. Biological Sciences, vol. 283, no. 1839, pp. 20161329. http://dx.doi.org/10.1098/rspb.2016.1329. PMid:27683368.
http://dx.doi.org/10.1098/rspb.2016.1329... ) and produce variation in offspring that have more advantages over the parents in terms of adaptability, viability, growth potential and stress resistance, especially in the plant kingdom (Mesgaran et al., 2016MESGARAN, M.B., LEWIS, M.A., ADES, P.K., DONOHUE, K., OHADI, S., LI, C. and COUSENS, R.D., 2016. Hybridization can facilitate species invasions, even without enhancing local adaptation. Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 36, pp. 10210-10214. http://dx.doi.org/10.1073/pnas.1605626113. PMid:27601582.
http://dx.doi.org/10.1073/pnas.160562611... ). Hybridization occurs in various ecological and environmental zones between the nearby population's boundaries that allow the dispersion flight in common period and transmission of the hybrid genome (Harrison and Harrison, 1993HARRISON, R.G. and HARRISON, R.G., 1993. Hybrid zones and the evolutionary process, Oxford University Press on Demand. Journal of Evolutionary Biology, vol. 7, pp. 623-637. http://dx.doi.org/10.1046/j.1420-9101.1994.7050631.x.
http://dx.doi.org/10.1046/j.1420-9101.19... ; Chunco, 2014CHUNCO, A.J., 2014. Hybridization in a warmer world. Ecology and Evolution, vol. 4, no. 10, pp. 2019-2031. http://dx.doi.org/10.1002/ece3.1052. PMid:24963394.
http://dx.doi.org/10.1002/ece3.1052... ). Many crosses occur in regions where territories are closed and intermixed, and these new phenotypes are adapted to the native environment (Chunco, 2014CHUNCO, A.J., 2014. Hybridization in a warmer world. Ecology and Evolution, vol. 4, no. 10, pp. 2019-2031. http://dx.doi.org/10.1002/ece3.1052. PMid:24963394.
http://dx.doi.org/10.1002/ece3.1052... ).

There are also gene interactions that occur among the native inhabitants, such as parasites interaction among the herbivorous arthropods (Šimková et al., 2013ŠIMKOVÁ, A., DÁVIDOVÁ, M., PAPOUŠEK, I. and VETEŠNÍK, L., 2013. Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? Parasites & Vectors, vol. 6, no. 1, pp. 95. http://dx.doi.org/10.1186/1756-3305-6-95. PMid:23587287.
http://dx.doi.org/10.1186/1756-3305-6-95... ). There is no standard spatial isolation scale for the measurement of hybridization, but it is dependent on interference from distribution or habitats (Waits et al., 2001WAITS, L.P., LUIKART, G. and TABERLET, P., 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology, vol. 10, no. 1, pp. 249-256. http://dx.doi.org/10.1046/j.1365-294X.2001.01185.x. PMid:11251803.
http://dx.doi.org/10.1046/j.1365-294X.20... ; Seifert et al., 2016SEIFERT, B., BUSCHINGER, A., ALDAWOOD, A., ANTONOVA, V., BHARTI, H., BOROWIEC, L., DEKONINCK, W., DUBOVIKOFF, D., ESPADALER, X., FLEGR, J., GEORGIADIS, C., HEINZE, J., NEUMEYER, R., ØDEGAARD, F., OETTLER, J., RADCHENKO, A., SCHULTZ, R., SHARAF, M., TRAGER, J., VESNIĆ, A., WIEZIK, M. and ZETTEL, H., 2016. Banning paraphylies and executing Linnaean taxonomy is discordant and reduces the evolutionary and semantic information content of biological nomenclature. Insectes Sociaux, vol. 63, no. 2, pp. 237-242. http://dx.doi.org/10.1007/s00040-016-0467-1.
http://dx.doi.org/10.1007/s00040-016-046... ). Hybridization related to the contacts of parental populations on the boundaries and their population growth may either two native species or invasive species, and the other is a native one, have been recognized in a wide range of organisms (Harbicht et al., 2014HARBICHT, A.B., ALSHAMLIH, M., WILSON, C.C. and FRASER, D.J., 2014. Anthropogenic and habitat correlates of hybridization between hatchery and wild brook trout. Canadian Journal of Fisheries and Aquatic Sciences, vol. 71, no. 5, pp. 688-697. http://dx.doi.org/10.1139/cjfas-2013-0460.
http://dx.doi.org/10.1139/cjfas-2013-046... ; Wielstra et al., 2016WIELSTRA, B., BURKE, T., BUTLIN, R., SCHAAP, O., SHAFFER, H., VRIELING, K. and ARNTZEN, J., 2016. Efficient screening for ‘genetic pollution’in an anthropogenic crested newt hybrid zone. Conservation Genetics Resources, vol. 8, no. 4, pp. 553-560. http://dx.doi.org/10.1007/s12686-016-0582-3.
http://dx.doi.org/10.1007/s12686-016-058... ). Hybridization increases the chances of adjustments and adaptability of parental populations by differentiation through genes combination and also produces new descendants that are mixed to a level of two ancestral populations but still divergent from the parental population (Abbott et al., 2010ABBOTT, R.J., HEGARTY, M.J., HISCOCK, S.J. and BRENNAN, A.C., 2010. Homoploid hybrid speciation in action. Taxon, vol. 59, no. 5, pp. 1375-1386. http://dx.doi.org/10.1002/tax.595005.
http://dx.doi.org/10.1002/tax.595005... ; Wielstra et al., 2016WIELSTRA, B., BURKE, T., BUTLIN, R., SCHAAP, O., SHAFFER, H., VRIELING, K. and ARNTZEN, J., 2016. Efficient screening for ‘genetic pollution’in an anthropogenic crested newt hybrid zone. Conservation Genetics Resources, vol. 8, no. 4, pp. 553-560. http://dx.doi.org/10.1007/s12686-016-0582-3.
http://dx.doi.org/10.1007/s12686-016-058... ).

In organisms, the nature and habits of species are highly restricted and conserved (Chunco, 2014CHUNCO, A.J., 2014. Hybridization in a warmer world. Ecology and Evolution, vol. 4, no. 10, pp. 2019-2031. http://dx.doi.org/10.1002/ece3.1052. PMid:24963394.
http://dx.doi.org/10.1002/ece3.1052... ; Matsuura, 2005MATSUURA, K., 2005. Distribution of termite egg-mimicking fungi (“termite balls”) in Reticulitermes spp. (Isoptera: Rhinotermitidae) nests in Japan and the United States. Applied Entomology and Zoology, vol. 40, no. 1, pp. 53-61. http://dx.doi.org/10.1303/aez.2005.53.
http://dx.doi.org/10.1303/aez.2005.53... ), and crosses between diverse species often result in reproductive barriers. Reproductive isolation includes pre-zygotic and post-zygotic barriers (Turissini et al., 2018TURISSINI, D.A., MCGIRR, J.A., PATEL, S.S., DAVID, J.R. and MATUTE, D.R., 2018. The rate of evolution of postmating-prezygotic reproductive isolation in Drosophila. Molecular Biology and Evolution, vol. 35, no. 2, pp. 312-334. http://dx.doi.org/10.1093/molbev/msx271. PMid:29048573.
http://dx.doi.org/10.1093/molbev/msx271... ). Pre-zygotic isolation is considered morphology, feeding, breeding season, geography and ecology (Ma et al., 2016MA, Y.-P., XIE, W.-J., SUN, W.-B. and MARCZEWSKI, T., 2016. Strong reproductive isolation despite occasional hybridization between a widely distributed and a narrow endemic Rhododendron species. Scientific Reports, vol. 6, no. 1, pp. 19146. http://dx.doi.org/10.1038/srep19146. PMid:26751844.
http://dx.doi.org/10.1038/srep19146... ). The parents may not become closed for mating and fertilization properly, to produce offspring due to a reasonable gap in a few important parameters (Lowry, 2012LOWRY, D.B., 2012. Ecotypes and the controversy over stages in the formation of new species. Biological Journal of the Linnean Society. Linnean Society of London, vol. 106, no. 2, pp. 241-257. http://dx.doi.org/10.1111/j.1095-8312.2012.01867.x.
http://dx.doi.org/10.1111/j.1095-8312.20... ).

There are also many ways to segregate post-zygotic barriers, such as gamete isolation, developmental isolation, early death of hybrid embryos, hybrid infertility and poor adaptability and adjustment of hybrids descendants (Palumbi, 1994PALUMBI, S.R., 1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics, vol. 25, no. 1, pp. 547-572. http://dx.doi.org/10.1146/annurev.es.25.110194.002555.
http://dx.doi.org/10.1146/annurev.es.25.... ; Presgraves, 2010PRESGRAVES, D.C., 2010. The molecular evolutionary basis of species formation. Nature Reviews. Genetics, vol. 11, no. 3, pp. 175-180. http://dx.doi.org/10.1038/nrg2718. PMid:20051985.
http://dx.doi.org/10.1038/nrg2718... ). The interactions were found restricted between soldiers and workers from matured colonies, where individuals showed interspecies competence and agonism for the resources access (Du et al., 2016DU, H., CHOUVENC, T., OSBRINK, W. and SU, N.-Y., 2016. Social interactions in the central nest of Coptotermes formosanus juvenile colonies. Insectes Sociaux, vol. 63, no. 2, pp. 279-290. http://dx.doi.org/10.1007/s00040-016-0464-4.
http://dx.doi.org/10.1007/s00040-016-046... ). While the interspecies competition of members from the alates has not yet been examined (Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ).

Hybridization is a characteristic consequence that happened among many species of organisms (Abbott et al., 2013ABBOTT, R., ALBACH, D., ANSELL, S., ARNTZEN, J.W., BAIRD, S., BIERNE, N., BOUGHMAN, J., BRELSFORD, A., BUERKLE, C.A., BUGGS, R., BUTLIN, R.K., DIECKMANN, U., EROUKHMANOFF, F., GRILL, A., CAHAN, S.H., HERMANSEN, J.S., HEWITT, G., HUDSON, A.G., JIGGINS, C., JONES, J., KELLER, B., MARCZEWSKI, T., MALLET, J., MARTINEZ-RODRIGUEZ, P., MÖST, M., MULLEN, S., NICHOLS, R., NOLTE, A.W., PARISOD, C., PFENNIG, K., RICE, A.M., RITCHIE, M.G., SEIFERT, B., SMADJA, C.M., STELKENS, R., SZYMURA, J.M., VÄINÖLÄ, R., WOLF, J.B. and ZINNER, D., 2013. Hybridization and speciation. Journal of Evolutionary Biology, vol. 26, no. 2, pp. 229-246. http://dx.doi.org/10.1111/j.1420-9101.2012.02599.x. PMid:23323997.
http://dx.doi.org/10.1111/j.1420-9101.20... ) and also found in a few cross-breeding studies on termites such as R. lucifugus and Z. nevadensis (Aldrich and Kambhampati, 2009ALDRICH, B. and KAMBHAMPATI, S., 2009. Preliminary analysis of a hybrid zone between two subspecies of Zootermopsis nevadensis. Insectes Sociaux, vol. 56, no. 4, pp. 439-450. http://dx.doi.org/10.1007/s00040-009-0041-1.
http://dx.doi.org/10.1007/s00040-009-004... ), N. corniger (Hartke and Rosengaus, 2011HARTKE, T.R. and ROSENGAUS, R.B., 2011. Heterospecific pairing and hybridization between Nasutitermes corniger and N. ephratae. Naturwissenschaften, vol. 98, no. 9, pp. 745-753. http://dx.doi.org/10.1007/s00114-011-0823-y. PMid:21761130.
http://dx.doi.org/10.1007/s00114-011-082... ). Chouvenc et al. (2015)CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... observed the C. formosanus and C. gestroi dispersal flight seasons overlapped of both species for the first time in 2013-2014, their hybridization in the wild at the Southern United States, and the number of offspring was double than the parental species of mating colonies after eighteen months. The vitality and number of offspring were advantageous in interspecific cross-breeding (Chouvenc et al., 2015CHOUVENC, T., HELMICK, E.E. and SU, N.-Y., 2015. Hybridization of two major termite invaders as a consequence of human activity. PLoS One, vol. 10, no. 3, pp. e0120745. http://dx.doi.org/10.1371/journal.pone.0120745. PMid:25806968.
http://dx.doi.org/10.1371/journal.pone.0... ; Su et al., 2017SU, N.-Y., CHOUVENC, T. and LI, H.-F., 2017. Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects, vol. 8, no. 1, pp. 14. http://dx.doi.org/10.3390/insects8010014. PMid:28125068.
http://dx.doi.org/10.3390/insects8010014... ). These results suggested that the wingless males are heterogeneous, healthy, heavy, and well-known with the environment in R. chinensis. They have noticeable advantages in the choice of mate. This principle of mate choice is supportive for termites to evade inbreeding and to continue the genetic change of offspring, which is very significant for the ecological adaptability and expansion of termite colonies (Li et al., 2013aLI, G., GAO, Y., SUN, P., LEI, C. and HUANG, Q., 2013a. Factors affecting mate choice in the subterranean termite Reticulitermes chinensis (Isoptera: rhinotermitidae). Journal of Ethology, vol. 31, no. 2, pp. 159-164. http://dx.doi.org/10.1007/s10164-013-0363-3.
http://dx.doi.org/10.1007/s10164-013-036... ; Farnesi et al., 2015FARNESI, L.C., MENNA-BARRETO, R.F.S., MARTINS, A.J., VALLE, D. and REZENDE, G.L., 2015. Physical features and chitin content of eggs from the mosquito vectors Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus: connection with distinct levels of resistance to desiccation. Journal of Insect Physiology, vol. 83, pp. 43-52. http://dx.doi.org/10.1016/j.jinsphys.2015.10.006. PMid:26514070.
http://dx.doi.org/10.1016/j.jinsphys.201... ). Whether hybridization was found between two termites viz. R. flaviceps and R. chinensis under laboratory conditions. The frequencies of acceptance were found significantly higher than that of agonism between interspecies partners. There were no important alterations in occurrences of tandem and mating manners between interspecific and intraspecific partners. However, the allogrooming frequencies of intraspecific partners were importantly lower than interspecific partners. There were no important changes in the time of tandem, mating behaviour, or allogrooming at each time between heterospecific partners and conspecific partners. Additionally, genotypic and morphological analyses exposed that interspecific and intraspecific mating was capable to produce offspring (Wu et al., 2019WU, C.-C., TSAI, C.-L., LIANG, W.-R., TAKEMATSU, Y. and LI, H.-F., 2019. Identification of Subterranean Termite Genus, Reticulitermes (Blattodea: Rhinotermitidae) in Taiwan. Journal of Economic Entomology, vol. 112, no. 6, pp. 2872-2881. http://dx.doi.org/10.1093/jee/toz183. PMid:31265067.
http://dx.doi.org/10.1093/jee/toz183... , Khan et al., 2021aKHAN, Z., KHAN, M.S., SULEMAN, MUHAMMAD, N., HAROON, SU, X.-H., XING, L.-X., 2021a. Morphology of testis, sperm, and spermatheca in two capable hybridized termite species indicates no interspecific reproductive isolation. International Journal of Tropical Insect Science. In press.). R. aculabialis and R. flaviceps can also be hybrid under laboratory experiments (Khan et al., 2021bKHAN, Z., LI, Y.-X., LIU, Q., SU, X.-H. and XING, L.-X., 2021b. The first description of alate and supplementary description of soldier of Reticulitermes aculabialis Tsai et Hwang (Isoptera, Rhinotermitidae). International Journal of Tropical Insect Science, vol. 41, no. 4, pp. 2643-2648. http://dx.doi.org/10.1007/s42690-021-00445-3.
http://dx.doi.org/10.1007/s42690-021-004... ).

3 Conclusion

Briefly, hybridization and parthenogenesis are the additional reproductive behaviours of termites to achieve more advantages for successful adaptation in a challenging environment. These reproductive advancements of Isoptera have threatened the economy of China. As spreading by sexual reproduction, hybridization and parthenogenesis they can invade new regions and cause more damages to buildings in urban areas, trees and crops. Sufficient importance is needed for effective control and prevention of termite invasion in new areas of economic importance. Hence, a large number of laid eggs, increase embryonic development, survival ship of parthenogenetic and hybridized offspring make them more competent to utilize Chinese resources. This study means to investigate the species, type of reproductive behaviour, egg numbers, micropyle numbers, eggshell, rate of embryonic development, progeny, the season of reproduction, and dispersion flight of Reticulitermes termites. They are abundant and responsible for approximately 2 billion RMB annually equivalent to the US $ 217 million.

Acknowledgements

This research project was funded by Grant Number 14-MED333-10 from National Science, Technology and Innovation Plan (MAARIFAH), King Abdul Aziz City for Science and Technology (KACST), Saudi Arabia.

References

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