Hostname: page-component-6bf8c574d5-gr6zb Total loading time: 0 Render date: 2025-02-25T12:41:26.075Z Has data issue: false hasContentIssue false
  • English
  • Français

Asexual queen succession in the subterranean termite Reticulitermes aculabialis Tsai et Hwang (Blattodea: Heterotermitidae)

Published online by Cambridge University Press:  25 February 2025

Zahid Khan Open the ORCID record for Zahid Khan [Opens in a new window] ,
Haroon ,
Zhao Sha  and
Lian-Xi Xing Open the ORCID record for Lian-Xi Xing [Opens in a new window]
Zahid Khan
Affiliation:
College of Life Sciences, Northwest University, Xi’an, 710069, China Zoology Department, University of Swabi, Khyber Pakhtunkhwa, Pakistan
Haroon
Affiliation:
College of Life Sciences, Northwest University, Xi’an, 710069, China College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, 510642, China
Zhao Sha
Affiliation:
College of Life Sciences, Northwest University, Xi’an, 710069, China School of Medicine, Xi’an Peihua University, Xi’an 710125, China
Lian-Xi Xing*
Affiliation:
College of Life Sciences, Northwest University, Xi’an, 710069, China Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi’an, 710069, China Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), Ministry of Education, Xi’an, 710069, China
*
Corresponding author: Lian-Xi Xing; Email: lxxing@nwu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Asexual queen succession (AQS) species produce queens via thelytokous parthenogenesis, which significantly impacts their social life history. For the first time, we discovered that Reticulitermes aculabialis exhibits the phenomenon of parthenogenesis under experimental conditions, and we also investigated the genetic structure of wild colonies of this species using polymorphic microsatellite loci. Our genetic analysis revealed that 93.2% of the secondary queens in the wild colonies were homozygous at all loci, indicating parthenogenesis in these secondary queens, while workers (2.5%), soldiers (0%), nymphs (0%), and alates (6.7%) had low rates. Genetic analysis revealed that the mean number of alleles per group (Na) ranged from 2.000 ± 0.000 to 2.500 ± 0.428, with 83.3% polymorphic loci (PPL). The observed heterozygosity (Ho) varied from 0.467 ± 0.141 to 0.583 ± 0.098, indicating significant genetic diversity among workers and soldiers. In contrast, soldiers and nymph develop predominantly through sexual reproduction than alates and workers. The occurrence of AQS in R. aculabialis suggests a different mechanism of ploidy restoration, highlighting the diversity of reproductive mechanisms across various lineages of the Termitidae and non-Termitidae termites.

Keywords

AQSmicrosatellite lociReticulitermes aculabialisthelytokous parthenogenesisNeotenic queen worker
Type
Research Paper
Information
Bulletin of Entomological Research , First View , pp. 1 - 11
Check for updates
Copyright
© The Author(s), 2025. Published by Cambridge University Press.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aldrich, B and Kambhampati, S (2007) Population structure and colony composition of two Zootermopsis nevadensis subspecies. Heredity 99, 443–451.CrossRefGoogle ScholarPubMed
Bagnères, A-G and Hanus, R (2015) Communication and social regulation in termites. Social Recognition in Invertebrates: The Knowns and the Unknowns 193–248.CrossRefGoogle Scholar
Bai, Z, Liu, Y, Sillam-Dussès, D and Wang, R-W (2022) Behavioral differentiation among workers may reduce reproductive conflicts during colony inheritance in the termite Reticulitermes labralis. Insectes Sociaux 69, 229–236.CrossRefGoogle Scholar
Carrijo, TF, Engel, MS, Chouvenc, T, Gile, GH, Mikaelyan, A, Dedeine, F, Ware, JL, Haifig, I, Arab, A, Constantini, JP, Souza, JP, Lee, SB, Buček, A, Roisin, Y, Cancello, EM and Santos, CMD (2023) A call to termitologists: It is time to abandon the use of “lower” and “higher” termites. Insectes Sociaux 70, 295–299.CrossRefGoogle Scholar
Chhotani, OB (1962) Further observations on biology and parthenogenesis in the termite Kalotermes beesoni (Kalotermitidae). In Zoological Survey of India, termites in the humid tropics. Proceedings of the New Delhi Symposium: UNESCO, 73–75.Google Scholar
Chouvenc, T (2022) Eusociality and the transition from biparental to alloparental care in termites. Functional Ecology 36, 3049–3059.CrossRefGoogle Scholar
Dang, Y-L, Zhang, H-G, Meng, Y-F, Zhang, M, Zhao, S, You, P, Su, X-H and Xing, L-X (2017) Isolation and Characterization of Polymorphic Microsatellite Markers for Two Subterranean Termites. Sociobiology 64, 352–355.CrossRefGoogle Scholar
da Silva, IB and Haifig, I (2020) Ergatoid reproductives in the Neotropical termite Nasutitermes aquilinus (Holmgren) (Blattaria: Isoptera: Termitidae): Developmental origin, fecundity, and genetics. Insect Science 27, 1322–1333.CrossRefGoogle ScholarPubMed
Dedeine, F, Dupont, S, Guyot, S, Matsuura, K, Wang, C, Habibpour, B, Bagnères, A-G, Mantovani, B and Luchetti, A (2016) Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mitochondrial and nuclear loci. Molecular Phylogenetics & Evolution 94, 778–790.CrossRefGoogle ScholarPubMed
Dolejšová, K, Křivánek, J, Štáfková, J, Horáček, N, Havlíčková, J, Roy, V, Kalinová, B, Roy, A, Kyjaková, P and Hanus, R (2022) Identification of a queen primer pheromone in higher termites. Communication Biology, 5, 1165.CrossRefGoogle ScholarPubMed
Dronnet, S, Chapuisat, M, Vargo, EL, Lohou, C and Bagnères, AG (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Molecular Ecology 14, 1311–1320.CrossRefGoogle Scholar
Eyer, P-A, Moran, MN, Richardson, S, Shults, PT, Liu, K-L, Blumenfeld, AJ, Davis, R and Vargo, EL (2023) Comparative genetic study of the colony structure and colony spatial distribution between the higher termite Amitermes parvulus and the lower, subterranean termite Reticulitermes flavipes in an urban environment. Insectes Sociaux 70, 301–316.CrossRefGoogle Scholar
Felsenstein, J (1974) The evolutionary advantage of recombination. Genetics 78, 737–756.CrossRefGoogle ScholarPubMed
Fougeyrollas, R, Dolejšová, K, Sillam-Dussès, D, Roy, V, Poteaux, C, Hanus, R and Roisin, Y (2015) Asexual queen succession in the higher termite Embiratermes neotenicus. Proceedings of the Royal Society B: Biological Sciences 282, 20150260.CrossRefGoogle ScholarPubMed
Fougeyrollas, R, Křivánek, J, Roy, V, Dolejšová, K, Frechault, S, Roisin, Y, Hanus, R and Sillam‐Dussès, D (2017) Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus. Molecular Ecology 26, 3295–3308.CrossRefGoogle ScholarPubMed
Fournier, D, Hellemans, S, Hanus, R and Roisin, Y (2016) Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proceedings of the Royal Society B: Biological Sciences 283, 20160196.CrossRefGoogle ScholarPubMed
Grassé, PP (1949) Ordre des Isoptères ou termites. In: Grassé, P-P (ed) Traité de zoologie, Masson, Paris, 9, 408–544.Google Scholar
Han, S, Ding, H, Peng, H, Dai, C, Zhang, S, Yang, J, Gao, J and Kan, X (2024) Sturnidae sensu lato mitogenomics: Novel insights into codon aversion, selection, and phylogeny. Animals 14, 2777.CrossRefGoogle ScholarPubMed
Haroon, C-XY, Li, Y-X, Zhang, H-X, Liu, Q, Su, X-H and Xing, L-X (2021) Breeding Biology of Reticulitermes aculabialis (Isoptera: Rhinotermitidae). Pakistan Journal of Zoology 54, 2127–2136.Google Scholar
Hayashi, Y, Kitade, O and Kojima, JI (2002) Microsatellite loci in the Japanese subterranean termite, Reticulitermes speratus. Molecular Ecology Notes 2, 518–520.CrossRefGoogle Scholar
Hellemans, S, Dolejšová, K, Křivánek, J, Fournier, D, Hanus, R and Roisin, Y (2019) Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae). BMC Evolutionary Biology 19, 1–14.CrossRefGoogle ScholarPubMed
Hellemans, S, Rocha, MM, Wang, M, Romero Arias, J, Aanen, DK, Bagnères, A-G, Buček, A, Carrijo, TF, Chouvenc, T, Cuezzo, C, Constantini, JP, Constantino, R, Dedeine, F, Deligne, J, Eggleton, P, Evans, TA, Hanus, R, Harrison, MC, Harry, M, Josens, G, Jouault, C, Kalleshwaraswamy, CM, Kaymak, E, Korb, J, Lee, C-Y, Legendre, F, Li, H-F, Lo, N, Lu, T, Matsuura, K, Maekawa, K, McMahon, DP, Mizumoto, N, Oliveira, DE, Poulsen, M, Sillam-Dussès, D, Su, N-Y, Tokuda, G, Vargo, EL, Ware, JL, Šobotník, J, Scheffrahn, RH, Cancello, E, Roisin, Y, Engel, MS and Bourguignon, T (2024) Genomic data provide insights into the classification of extant termites. Nature Communications 15, 6724.CrossRefGoogle ScholarPubMed
Hellemans, S and Roisin, Y (2020) Asexual queen succession in termites. ELS 2, 13–20.Google Scholar
Hoffmann, KA (2011) Conflict and Conflict-resolution in Lower Termite Societies.), PhD Thesis. University of Osnabrück: Osnabrück, Germany.Google Scholar
Huang, F, Zhu, S, Ping, Z, He, X, Li, G and Gao, D (2000) Fauna Sinica: Insecta, Vol. 17: Isoptera. Beijing: Science Press, 961.Google Scholar
Husseneder, C, Simms, DM, Delatte, JR, Wang, C, Grace, JK and Vargo, EL (2012) Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus. Biological Invasions 14, 419–437.CrossRefGoogle Scholar
Javanrouh, A and Khodamoradi, S (2022) Study of the genetic structure of the Shin Bash sheep population by molecular markers. Animal Production Research 11, 27–40.Google Scholar
Keller, L and Chapuisat, M (1999) Cooperation among selfish individuals in insect societies. Bioscience 49, 899–909.CrossRefGoogle Scholar
Khan, Z, Khan, MS, Suleman, MN, Haroon, , Su, X-H and Xing, L-X (2022) Morphology of testis, sperm, and spermatheca in two capable hybridized termite species indicates no interspecific reproductive isolation. International Journal of Tropical Insect Science 42, 2909–2926.CrossRefGoogle Scholar
Khan, Z, Li, Y-X, Liu, Q, Su, X-H and Xing, L-X (2021) The first description of alate and supplementary description of soldier of Reticulitermes aculabialis Tsai et Hwang (Isoptera, Rhinotermitidae). International Journal of Tropical Insect Science 41, 2643–2648.CrossRefGoogle Scholar
Khan, 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 66, 425–433.CrossRefGoogle Scholar
Kobayashi, K and Miyaguni, Y (2016) Facultative parthenogenesis in the Ryukyu drywood termite Neotermes koshunensis. Scientific Reports 6, 30712.CrossRefGoogle ScholarPubMed
Korb, J and Hartfelder, K (2008) Life history and development‐a framework for understanding developmental plasticity in lower termites. Biological Reviews 83, 295–313.CrossRefGoogle ScholarPubMed
Light, SF (1944) Parthenogenesis in termites of the genus Zootermopsis. University of California Publications in Zoölogy, 43, 405–412.Google Scholar
Luchetti, A, Scicchitano, V and Mantovani, B (2013) Origin and evolution of the Italian subterranean termite Reticulitermes lucifugus (Blattodea, Termitoidae, Rhinotermitidae). Bulletin of Entomological Research, 103, 734–741.CrossRefGoogle ScholarPubMed
Matsuura, K (2011) Sexual and asexual reproduction in termites. Biology of Termites: A Modern Synthesis 255–277.Google Scholar
Matsuura, K (2017) Evolution of the asexual queen succession system and its underlying mechanisms in termites. Journal of Experimental Biology 220, 63–72.CrossRefGoogle ScholarPubMed
Matsuura, 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 51, 325–332.CrossRefGoogle Scholar
Matsuura, K, Himuro, C, Yokoi, T, Yamamoto, Y, Vargo, EL and Keller, L (2010) Identification of a pheromone regulating caste differentiation in termites. Proceedings of the National Academy of Sciences 107, 12963–12968.CrossRefGoogle ScholarPubMed
Matsuura, K, Vargo, EL, Kawatsu, K, Labadie, PE, Nakano, H, Yashiro, T and Tsuji, K (2009) Queen succession through asexual reproduction in termites. Science 323, 1687–1687.CrossRefGoogle ScholarPubMed
Muller, HJ (1964) The relation of recombination to mutational advance. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 1, 2–9.CrossRefGoogle Scholar
Myles, TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33, 16.Google Scholar
Nozaki, T, Yashiro, T and Matsuura, K (2018) Preadaptation for asexual queen succession: Queen tychoparthenogenesis produces neotenic queens in the termite Reticulitermes okinawanus. Insectes Sociaux 65, 225–231.CrossRefGoogle Scholar
Pamilo, P and Seppä, P (1994) Reproductive competition and conflicts in colonies of the ant Formica sanguinea. Animal Behaviour 48, 1201–1206.CrossRefGoogle Scholar
Peakall, R and Smouse, PE (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.CrossRefGoogle Scholar
Pearcy, M, Aron, S, Doums, C and Keller, L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306, 1780–1783.CrossRefGoogle ScholarPubMed
Peng, X, Khan, Z, Liu, X-M, Deng, S-L, Fang, Y-G, Zhang, M, Su, X-H, Xing, L-X and Yan, X-R (2023) Embryonic development of parthenogenetic and sexual eggs in lower termites. Insects 14, 640.CrossRefGoogle ScholarPubMed
Ross, KG (2001) Molecular ecology of social behaviour: Analyses of breeding systems and genetic structure. Molecular Ecology 10, 265–284.CrossRefGoogle ScholarPubMed
Scicchitano, V, Dedeine, F, Bagnères, A-G, Luchetti, A and Mantovani, B (2018) Genetic diversity and invasion history of the European subterranean termite Reticulitermes urbis (Blattodea, Termitoidae, Rhinotermitidae). Biological Invasions 20, 33–44.CrossRefGoogle Scholar
Shigenobu, S, Hayashi, Y, Watanabe, D, Tokuda, G, Hojo, MY, Toga, K, Saiki, R, Yaguchi, H, Masuoka, Y and Suzuki, R (2022) Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: Gene duplication facilitates social evolution. Proceedings of the National Academy of Sciences 119, e2110361119.CrossRefGoogle ScholarPubMed
Stansly, PA (1987) Parthénogenèse chez Velocitermes spp. (Isoptera: Nasutiterminae). (Parthenogenesis by Velocitermes spp.) C. R. Acad. Sc. Paris, 304, 457–460.Google Scholar
Stansly, PA and Korman, AK (1993) Parthenogenic development in Velocitermes spp. (Isoptera: Nasutiterminae). Sociobiology, 23, 13–24.Google Scholar
Su, X-H, Xue, W, Liu, H, Chen, J-L, Zhang, X-J, Xing, L-X and Liu, M-H (2015) The development of adultoid reproductives and brachypterous neotenic reproductives from the last instar nymphs in Reticulitermes labralis (Isoptera: Rhinotermitidae): A comparative study. Journal of Insect Science 15, 147.CrossRefGoogle ScholarPubMed
Templeton, AR (1982) The prophecies of parthenogenesis. Proceedings in Life Sciences Evolution and Genetics of Life Histories 75–101.Google Scholar
Thorne, B, Traniello, J, Adams, E and Bulmer, M (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): A review of the evidence from behavioral, ecological, and genetic studies. Ethology Ecology & Evolution 11, 149–169.CrossRefGoogle Scholar
Vargo, E (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Molecular Ecology 9, 817–820.CrossRefGoogle ScholarPubMed
Vargo, EL (2019) Diversity of termite breeding systems. Insects 10, 52.CrossRefGoogle ScholarPubMed
Vargo, EL and Carlson, JR (2006) Comparative study of breeding systems of sympatric subterranean termites (Reticulitermes flavipes and R. hageni) in central North Carolina using two classes of molecular genetic markers. Environmental Entomology 35, 173–187.CrossRefGoogle Scholar
Vargo, EL, Husseneder, C, Woodson, D, Waldvogel, MG and Grace, JK (2006) Genetic analysis of colony and population structure of three introduced populations of the formosan subterranean termite (Isoptera: Rhinotermitidae) in the Continental United States. Environmental Entomology 35, 151–166.CrossRefGoogle Scholar
Vargo, EL, Labadie, PE and Matsuura, K (2012) Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proceedings of the Royal Society B: Biological Sciences, Cham, Springer 279, 813–819.CrossRefGoogle ScholarPubMed
Wenseleers, T, Princen, S, Caliari Oliveira, R and Oi, CA (2021) Conflicts of interest within colonies. Encyclopedia of Social Insects 279–293.CrossRefGoogle Scholar
Wu, J, Xu, H, Hassan, A and Huang, Q (2019) Interspecific hybridization between the two sympatric termite Reticulitermes species under laboratory conditions. Insects 11, 14.CrossRefGoogle ScholarPubMed
Wu, W, Huang, Z, Zhang, S, Li, Z, Liu, B, Zeng, W and Xia, C (2024) Types and fecundity of neotenic reproductives produced in 5-year-old orphaned colonies of the drywood termite, Cryptotermes domesticus (Blattodea: Kalotermitidae). Diversity 16, 250. 10.3390/d16040250.CrossRefGoogle Scholar
Xing, L-X, Liu, M-H, Kong, X-H, Liu, X, Su, X-H, Yin, L-F and Tan, J-L (2013) Parthenogenetic reproductive behavior and initial colony foundation in the termite, Reticulitermes aculabialis. Chinese Bulletin of Entomology 1671–1678.Google Scholar
Yamamoto, Y and Matsuura, K (2012) Genetic influence on caste determination underlying the asexual queen succession system in a termite. Behavioral Ecology and Sociobiology 66, 39–46.CrossRefGoogle Scholar
Yashiro, T (2024) Evolution of obligate asexuality in termites with mixed‐sex societies. Population Ecology, 66, 219–231.CrossRefGoogle Scholar
Yashiro, T, Lo, N, Kobayashi, K, Nozaki, T, Fuchikawa, T, Mizumoto, N, Namba, Y and Matsuura, K (2018) Loss of males from mixed-sex societies in termites. BMC Biology 16, 96.CrossRefGoogle ScholarPubMed
Yashiro, T, Tea, Y-K, Van Der Wal, C, Nozaki, T, Mizumoto, N, Hellemans, S, Matsuura, K and Lo, N (2021) Enhanced heterozygosity from male meiotic chromosome chains is superseded by hybrid female asexuality in termites. Proceedings of the National Academy of Sciences of the United States of America, 118, e2009533118CrossRefGoogle Scholar
Ye, C, Rasheed, H, Ran, Y, Yang, X, Xing, L and Su, X (2019) Transcriptome changes reveal the genetic mechanisms of the reproductive plasticity of workers in lower termites. BMC Genomics 20, 1–13.CrossRefGoogle ScholarPubMed
Yüzer, Ö, Doğaç, E, Tonguç, A and Günenç, E (2023) ISSR-based population genetic structure of some Turkish honeybee (Apis mellifera L., 1758) populations. Turkish Journal of Bioscience and Collections 7, 83–90.CrossRefGoogle Scholar
Zeb, U, Aziz, T, Azizullah, A, Zan, XY, Khan, AA, Bacha, SAS and Cui, FJ (2024) Complete mitochondrial genomes of edible mushrooms: Features, evolution, and phylogeny. Physiologia Plantarum 176, e14363. doi:10.1111/ppl.14363CrossRefGoogle ScholarPubMed
Zeb, U, Wang, R, Dong, P, Wang, N, Zhang, T, Lin, C and Wang, X (2019) Characterization of the complete chloroplast genome sequence of Pinus pumila (Pinaceae). Mitochondrial Dna Part B 4, 290–291.CrossRefGoogle Scholar