Abstract
It would not surprise that two related termite species are similar in many traits, especially those related to reproduction such as similarity in sexual organs, spermathecae, gametes, glands in genital organs and micropyles of eggs. Because similarities of them are thought to be directly linked to increase their reproductive fitness. Moreover, the key data showing successful hybridization between the two termite species under laboratory conditions and in the field. The present study was conducted on the base of morphometric analyses and histological examinations of the sperm, testes, vas deferens, accessory glands, ejaculatory duct and spermathecae of Reticulitermes flaviceps and R. chinensis. The accessory glands of male alates were found without spermatozoa in both termites. The patterns of spermatogenesis in the alate testes of both species were quite similar and the gametes (spermatogonia, spermatocytes, spermatids, and sperm) produced in a sequence of essential developmental processes. The aflagellated sperm were transferred by male numerous times in a day after few copulations. They were stored alive in spermatheca by female and used for fertilization of oocytes. The nutrition was obtained by the sperm from the secretory cells, for a living and being functional during storage in the spermathecae. The spermathecae have finger shape and their thick walls divided into 4 type cells. Anatomically spermathecae of the two termite species consisted of lumens, ductules, and few glands, in thick wall structures. While the entire examinations revealed no more differences in the sexual organs of the two different species since R. flaviceps and R. chinensis can hybridize under experimental conditions as well as in wild to produce offspring. The similarity in the structure of sexual organs of both heterospecies provides possible evidence for the successful hybridization.
Similar content being viewed by others
Change history
16 February 2023
A Correction to this paper has been published: https://doi.org/10.1007/s42690-023-00956-1
References
Adam R, Mitchell J (2009) Energetics and development of incipient colonies of the harvester termite, Trinervitermes trinervoides (Sjöstedt)(Termitidae, Nasutitermitinae). Insect Soc 56:21–27
Afzelius BA (1970) Thoughts on comparative spermatology. Comparative spermatology 565–573
Baccetti B, Dallai R, Callaini G (1981) The spermatozoon of Arthropoda: Zootermopsis nevadensis and isopteran sperm phylogeny. Int J Invertebr Reprod 3:87–99. https://doi.org/10.1080/01651269.1981.10553385
Baccetti B (1979) Ultrastructure of sperm and its bearing on arthropod phylogeny. Arthropod phylogeny 609–644
Baccetti B, Dallai R (1978) The spermatozoon of arthropoda. XXX. The multiflagellate spermatozoon in the termite Mastotermes darwiniensis. J Cell Biol 76:569–576. https://doi.org/10.1083/jcb.76.3.569
Baccetti B, Afzelius BA (1976) Biology of the sperm cell. S. Karger
Baccetti B, Dallai R, Rosati F, Giusti F, Bernini F, Selmi G (1974) spermatozoon of Arthropoda. XXVI. The spermotozoon of Isoptera, Embioptera and Dermaptera. J Microsc Paris
Baccetti B, Dallai R, Fratello B (1973) The spermatozoon of Arthropoda. XXII. The ‘12+ 0’, ‘14+ 0’or aflagellate sperm of Protura. J Cell Sci 13:321–335
Baccetti B (1972) Insect sperm cells, Vol. 9: In Adv Insect Physiol (ed). Elsevier, pp. 315–397
Baccetti B (1970) Comparative spermatology. Academic Press
Baer B (2005) Sexual selection in Apis bees. Apidologie 36:187–200. https://doi.org/10.1051/apido:2005013
Ball M, Parker G (2003) Sperm competition games: sperm selection by females. J Theor Biol 224:27–42. https://doi.org/10.1016/S0022-5193(03)00118-8
Banerjee B (1961) Chromosome morphology during the spermatogenesis of Odontotermes redemanni (Wasmann). Caryologia 14:155–158. https://doi.org/10.1080/00087114.1961.10796021
Bawa S (1964) Electron microscope study of spermiogenesis in a fire-brat insect, Thermobia domestica pack: I. Mature Spermatozoon J Cell Biol 23:431–446. https://doi.org/10.1083/jcb.23.3.431
Boomsma JJ (2009) Strict life-time monogamy as universal condition for transitions towards eusociality: 12th congress of the European Society for Evolutionary Biology (ESEB) (ed)
Boomsma JJ, Baer B, Heinze J (2005) The evolution of male traits in social insects. Annu Rev Entomol 50:395–420. https://doi.org/10.1146/annurev.ento.50.071803.130416
Bourke AF (2011) Principles of social evolution. Oxford University Press
Chouvenc T, Helmick EE, Su N-Y (2015) Hybridization of two major termite invaders as a consequence of human activity. PLoS ONE 10:e0120745. https://doi.org/10.1007/s00040-014-0343-9
Chouvenc T, Su N-Y (2014) Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insect Soc 61:171–182. https://doi.org/10.1007/s00040-014-0343-9
Chunco AJ (2014) Hybridization in a warmer world. Ecol Evol 4:2019–2031. https://doi.org/10.1002/ece3.1052
Cohen J (1971) The comparative physiology of gamete populations, Vol. 4: Advances in comparative physiology and biochemistry (ed). Elsevier, pp. 267–380.
Connetable S, Robert A, Bordereau CJ (2012) Dispersal flight and colony development in the fungus-growing termites Pseudacanthotermes spiniger and P. militaris. Insect Soc 59:269–277. https://doi.org/10.1007/s00040-011-0216-4
Costa-Leonardo AM, Patricio GB (2005) Structure of the spermatheca in five families of Isoptera. Sociobiology 659–670
Dallai R, Gottardo M, Beutel RG (2016) Structure and evolution of insect sperm: new interpretations in the age of phylogenomics. Annu Rev Entomol 61:1–23. https://doi.org/10.1146/annurev-ento-010715-023555
Dallai R, Fanciulli PP, Frati F (2004) New data on the aberrant spermatogenesis of Collembola. Pedobiologia 48:487–492. https://doi.org/10.1016/j.pedobi.2004.05.006
Dávila F, Botteaux A, Bauman D, Chérasse S, Aron S (2018) Antibacterial activity of male and female sperm-storage organs in ants. J Exp Biol: jeb. 175158.https://doi.org/10.1242/jeb.175158. Published26
Dean SR, Gold RE (2014) Sex ratios and development of the reproductive system in castes of Reticulitermes flavipes (Kollar)(Isoptera: Rhinotermitidae). Ann Entomol Soc Am 97:147–152. https://doi.org/10.1603/0013-8746(2004)097[0147:SRADOT]2.0.CO;2
den Boer SP, Baer B, Boomsma JJ (2010) Seminal fluid mediates ejaculate competition in social insects. Science 327:1506–1509. https://doi.org/10.1126/science.1184709
Franck P, Solignac M, Vautrin D, Cornuet J-M, Koeniger G, Koeniger N (2002) Sperm competition and last-male precedence in the honeybee. Anim Behav 64:503–509. https://doi.org/10.1006/anbe.2002.3078
Gärtner SM, Rathke C, Renkawitz-Pohl R, Awe S (2014) Ex vivo culture of Drosophila pupal testis and single male germ-line cysts: dissection, imaging, and pharmacological treatment. JoVE. https://doi.org/10.3791/51868
Gomendio M, Roldan ER (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243:181–185. https://doi.org/10.1098/rspb.1991.0029
Gotoh A, Billen J, Hashim R, Ito F (2016) Degeneration patterns of the worker spermatheca during morphogenesis in ants (Hymenoptera: Formicidae). Evol Dev 18:96–104. https://doi.org/10.1111/ede.12182
Gotoh A, Billen J, Hashim R, Ito F (2008) Comparison of spermatheca morphology between reproductive and non-reproductive females in social wasps. Arthropod Struct Dev 37:199–209. https://doi.org/10.1016/j.asd.2007.11.001
Grace JK (2014) Invasive termites revisited: Coptotermes gestroi meets Coptotermes formosanus, Vol. 1: Proc. 10th Pacific-rim termite research group conference (ed) pp. 1–7.
Greeff M & Schmid-Hempel P (2008) Sperm viability in the male accessory testes and female spermathecae of the bumblebee Bombus terrestris (Hymenoptera: Apidae). Eur J Entomol 105(5):849–854. https://doi.org/10.14411/eje.2008.112
Haberl M, Tautz D (1998) Sperm usage in honey bees. Behav Ecol Sociobiol 42:247–255. https://doi.org/10.1007/s002650050436
Haifig I, Vargo EL, Labadie P, Costa-Leonardo AM (2016) Unrelated secondary reproductives in the neotropical termite Silvestritermes euamignathus (Isoptera: Termitidae). Sci Nat 103:9. https://doi.org/10.1016/j.zool.2016.12.001
Harbo JR (1990) Artificial mixing of spermatozoa from honeybees and evidence for sperm competition. J Apic Res 29:151–158. https://doi.org/10.1080/00218839.1990.11101212
Hartke T, Baer B (2011) The mating biology of termites: a comparative review. Anim Behav 82:927–936. https://doi.org/10.1016/j.anbehav.2011.07.022
Hartke TR, Rosengaus RB (2011) Heterospecific pairing and hybridization between Nasutitermes corniger and N. ephratae. Naturwissenschaften 98:745. https://doi.org/10.1126/science.1184709
Hartke TR (2010) Breeding strategies and the reproductive ecology of Nasutitermes corniger: Northeastern University
Heinze J (2016) The male has done his work—the male may go. Curr Opin Insect Sci 16:22–27. https://doi.org/10.1016/j.cois.2016.05.005
Higa SY, Bess HA (1974) The internal anatomy of the reproductive systems of young primary reproductives of the formosan subterranean termite, Coptotermes formosanus Shiraki (Rhinotermitidae: Isoptera). Proceedings: Proc Hawaii Entomol Soc 21:377–395
Husseneder C, Simms DM (2008) Size and heterozygosity influence partner selection in the Formosan subterranean termite. Behav Ecol 19:764–773. https://doi.org/10.1093/beheco/arn041
Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152
Jaffe K (2008) The need for sperm selection may explain why termite colonies have kings and queens, whereas those of ants, wasps and bees have only queens. Theory Biosci 127:359–363. https://doi.org/10.1007/s12064-008-0050-z
Jaffe K (2004) Sex promotes gamete selection: A quantitative comparative study of features favoring the evolution of sex. Complexity 9:43–51. https://doi.org/10.1002/cplx.20042
Jamieson BG (1987) The ultrastructure and phylogeny of insect spermatozoa. CUP Archive
Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:958. https://doi.org/10.1038/40130
Khan Z, Li YX, Liu Q, Su XH, Xing LX (2021) The first description of alate and supplementary description of soldier of Reticulitermes aculabialis Tsai et Hwang (Isoptera, Rhinotermitidae). Int J Trop Insect Sci 41(4):2643–2648. https://doi.org/10.1007/s42690-021-00445-3
Khan Z, Zhang M, Meng Y, Zhao J, Kong X, Su X, Xing L (2019) Alates of the termite Reticulitermes flaviceps feed independently during their 5-month residency in the natal colony. Insect Soc 66:425–433. https://doi.org/10.1007/s00040-019-00698-9
Khan Z, Khan MS, Bawazeer S, Bawazeer N, Irfan M, Rauf A, Su XH, Xing LX (2022) A comprehensive review on the documented characteristics of four Reticulitermes termites (Rhinotermitidae, Blattodea) of China. Braz J Biol 84. https://doi.org/10.1590/1519-6984.256354
Koshikawa S, Matsumoto T, Miura T (2004) Soldier-like intercastes in the rotten-wood termite Hodotermopsis sjostedti (Isoptera: Termopsidae). Zool Sci 21:583–588. https://doi.org/10.2108/zsj.21.583
Kraus F, Neumann P, Van Praagh J, Moritz R (2004) Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 55:494–501
Kronauer DJ (2009) Recent advances in army ant biology (Hymenoptera: Formicidae). Myrmecological News 12:51–65. https://doi.org/10.1111/j.1365-294X.2004.02262.x
Laranjo LT, Haifig I, Costa-Leonardo AM (2018) Morphology of the male reproductive system during post-embryonic development of the termite Silvestritermes euamignathus (Isoptera: Termitidae). Zoologischer Anzeiger-A J Comparative Zool 272:20–28. https://doi.org/10.1016/j.jcz.2017.11.015
Lefebvre T, Vargo EL, Zimmermann M, Dupont S, Kutnik M, Bagnères AG (2016) Subterranean termite phylogeography reveals multiple postglacial colonization events in southwestern Europe. Ecol Evol 6:5987–6004. https://doi.org/10.1002/ece3.2333
Li K, Yang Y, Mao L, Zhang J, Geng J, Yin H (2017) Morphology and fine organization of the spermatheca of Haplotropis brunneriana (Orthoptera: Pamphagidae). Rev Bras Entomol 61:323–329. https://doi.org/10.1016/j.asd.2007.11.001
Li G, Gao Y, Sun P, Lei C, Huang QJ (2013) Factors affecting mate choice in the subterranean termite Reticulitermes chinensis (Isoptera: Rhinotermitidae). J Ethol 31:159–164. https://doi.org/10.1007/s10164-013-0363-3
Li Z-Q, Liu B-R, Li Q-J, Xiao W-L, Zhong J-H (2011) Two new synonyms of Coptotermes gestroi (Wasmann)(Isoptera: Rhinotermitidae) in China. Sociobiology 58:449
Li H-F, Yang R-L, Su N-Y (2010) Interspecific competition and territory defense mechanisms of Coptotermes formosanus and Coptotermes gestroi (Isoptera: Rhinotermitidae). Environ Entomol 39:1601–1607. https://doi.org/10.1603/EN09262
Li H-F, Ye W, Su N-Y, Kanzaki NJ (2009) Phylogeography of Coptotermes gestroi and Coptotermes formosanus (Isoptera: Rhinotermitidae) in Taiwan. Ann Entomol 102:684–693. https://doi.org/10.1603/008.102.0413
Martins GF, SerrãO JE (2002) A comparative study of the spermatheca in bees (Hymenoptera; Apoidea). Sociobiology 40:711
Mattei AL, Riccio ML, Avila FW, Wolfner MF (2015) Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning. Proc Natl Acad Sci 112:8475–8480. https://doi.org/10.1073/pnas.1505797112
Miura T, Roisin Y, Matsumoto T (2000) Molecular phylogeny and biogeography of the nasute termite genus Nasutitermes (Isoptera: Termitidae) in the Pacific tropics. Mol Phylogenet Evol 17:1–10. https://doi.org/10.1006/mpev.2000.0790
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci 98:5446–5451. https://doi.org/10.1073/pnas.091093398
Morrow EH (2004) How the sperm lost its tail: the evolution of aflagellate sperm. Biol Rev 79:795–814. https://doi.org/10.1017/S1464793104006451
Mulugeta E, Marion-Poll L, Gentien D, Ganswindt SB, Ganswindt A, Bennett NC, Blackburn EH, Faulkes CG, Heard E (2017) Molecular insights into the pathways underlying naked mole-rat eusociality. bioRxiv:209932. https://doi.org/10.1101/209932
Negroni MA, Jongepier E, Feldmeyer B, Kramer BH, Foitzik S (2016) Life history evolution in social insects: a female perspective. Curr Opin Insect Sci 16:51–57. https://doi.org/10.1016/j.cois.2016.05.008
Oguchi K, Shimoji H, Hayashi Y, Miura T (2016) Reproductive organ development along the caste differentiation pathways in the dampwood termite Hodotermopsis sjostedti. Insect Soc 63:519–529. https://doi.org/10.1007/s00040-016-0495-x
Oshima M (1911) Discrimination between Termes flaviceps Oshima and Termes speratus Kolbe, and several remarks on the scientific names of Japanese termites. Insect World 15:355–363
Page RE Jr, Metcalf RA (1982) Multiple mating, sperm utilization, and social evolution. Am Nat 119:263–281. https://doi.org/10.1086/283907
Pascini TV, Martins GF (2017) The Insect Spermatheca: an Overview 121:56–71
Premoli M, Sella G (1995) Sex economy in benthic polychaetes. Ethol Ecol Evol 7:27–48. https://doi.org/10.1080/08927014.1995.9522968
Raina A, Murphy C, Florane C, Williams K, Park YI, Ingber B (2014) Structure of spermatheca, sperm dynamics, and associated bacteria in Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 100:418–424. https://doi.org/10.1603/0013-8746(2007)100[418:SOSSDA]2.0.CO;2
Raina A, Park Y, Florane C (2003) Behavior and reproductive biology of the primary reproductives of the Formosan subterranean termite. Sociobiology 37–48
Rayl R, Wratten S (2017) A comparison of anesthesia techniques for entomological experimentation: Longevity of the leaf-mining fly pest Scaptomyza flava Fallén (Drosophilidae): PeerJ Preprints. 2167–9843. https://doi.org/10.7287/peerj.preprints.2571v1
Reinhardt K, Ribou A-C (2013) Females become infertile as the stored sperm’s oxygen radicals increase. Sci Rep 3:2888. https://doi.org/10.1038/srep02888
Riparbelli MG, Callaini G, Mercati D, Hertel H, Dallai R (2009) Centrioles to basal bodies in the spermiogenesis of Mastotermes darwiniensis (Insecta, Isoptera). Cell Motil Cytoskelet 66:248–259. https://doi.org/10.1002/cm.20352
Román-Ruiz AK, Michel B, Dufour BP, Rojas JC, Cruz-López L, Barrera JF (2017) Description of the sperm and spermatheca of Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) for the differentiation of mated and unmated females. Ann Entomol Soc Am 110(4):353–359. https://doi.org/10.1093/aesa/sax033
Rubenstein DR, Abbot P (2017) Comparative social evolution. Cambridge University Press
Rust MK, Su N-Y (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375. https://doi.org/10.1146/annurev-ento-120710-100634
Santos HP, Zama U, Dolder H, Lino-Neto J (2013) Sperm morphology of Trichospilus diatraeae and Palmistichus elaeisis (Hymenoptera: Chalcidoidea: Eulophidae). Micron 51:36–40. https://doi.org/10.1016/j.micron.2013.06.006
Scheffrahn RHJFE (2013) Overview And Current Status of Non-Native Termites (Isoptera) in Florida §. Florida Entomologist 96:781–789. https://doi.org/10.1653/024.096.0311
Sella G, Ramella L (1999) Sexual conflict and mating systems in the dorvilleid genus Ophryotrocha and the dinophilid genus Dinophilus. Hydrobiologia 402:203–213. https://doi.org/10.1023/A:1003748710921
Sieber R, Leuthold R (1982) Repeated copulation and testes enlargement in Macrotermes michaelseni. Physio Entomol 7:457–465. https://doi.org/10.1111/j.1365-3032.1982.tb00322.x
Snyder TE (1923) A new Reticulitermes (Reticulitermes chinensis) from the Orient., U. S. Bureau of Entomology. J Wash Acad Sci 13(6):107–109
Su N-Y, Chouvenc T, Li H-F (2017a) Potential hybridization between two invasive termite species, Coptotermes formosanus and C. gestroi (Isoptera: Rhinotermitidae), and its biological and economic implications. Insects 8:14. https://doi.org/10.3390/insects8010014
Su XH, Chen JL, Zhang XJ, Xue W, Liu H, Xing LX (2015) Testicular development and modes of apoptosis during spermatogenesis in various castes of the termite Reticulitermes labralis (Isoptera: Rhinotermitidae). Arthropod Struct Dev 44:630–638. https://doi.org/10.1016/j.asd.2015.08.009
Su N-Y, Scheffrahn RH (1988) Foraging population and territory of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in an urban environment. Sociobiology 14:353–360
Tschinkel WR (1987) Relationship between ovariole number and spermathecal sperm count in ant queens: a new allometry. Ann Entomol Soc Am 80:208–211. https://doi.org/10.1093/aesa/80.2.208
Vargo EL (2019) Diversity of Termite Breeding Systems Insects 10:52. https://doi.org/10.3390/insects10020052
Vargo EL, Husseneder C (2010) Genetic structure of termite colonies and populations: Biology of termites: a modern synthesis (ed. Springer, pp. 321–347. https://doi.org/10.1007/978-90-481-3977-4_12
Volny VP, Gordon DM (2002) Genetic basis for queen–worker dimorphism in a social insect. Proc Natl Acad Sci 99:6108–6111. https://doi.org/10.1073/pnas.092066699
Weesner FM (1969) External Anatomy Biology of Termites 1:19–47
Wu J, Xu H, Hassan A, Huang Q (2020) Interspecific Hybridization between the Two Sympatric Termite Reticulitermes Species under Laboratory Conditions. Insects 11(1):14. https://doi.org/10.3390/insects11010014
Wu J, Su X, Kong X, Liu M, Xing L (2013) Multiple male and female reproductive strategies and the presence of a polyandric mating system in the termite Reticulitermes labralis (Isoptera: Rhinotermitidae). Sociobiology 60:459–465
Yanagimachi R, Cherr G, Matsubara T, Andoh T, Harumi T, Vines C, Pillai M, Griffin F, Matsubara H, Weatherby T (2013) Sperm attractant in the micropyle region of fish and insect eggs. Biol Reprod 88(2013):88. https://doi.org/10.1095/biolreprod.112.105072
Yashiro T, Lo N, Kobayashi K, Nozaki T, Fuchikawa T, Mizumoto N, Namba Y, Matsuura K (2018) Loss of males from mixed-sex societies in termites. BMC Biol 16:96. https://doi.org/10.1186/s12915-018-0563-y
Yashiro T, Matsuura K (2014) Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction. Pro Nat Acad Sci 111:17212–17217
Ye Y, Jones SC, Ammar E-D (2009) Reproductive characteristics of imagos of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 102:889–894. https://doi.org/10.1603/008.102.0515
Acknowledgements
Thanks to the Chinese Gov’t Scholarship Council and Northwest University, China for supporting my Ph.D studies. Similar golden wishes to Prof. Yan Xing Rong for his valuable guidance and Zhang Hong Guo for his company during experiments. This work was supported by grants (31870389) from the National Natural Science Foundation of China.
Author information
Authors and Affiliations
Contributions
Xing Lian-Xi and Zahid Khan conceived and designed the study, and wrote the main manuscript text. Su Xiao-Hong, and Haroon performed the study and help in photography through Micro CT Scan and SEM. While Mian Sayed Khan, Suleman and Nehaz Muhammad collected termites and help in the statistical analysis. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The author contributing equally and declare that they have no conflict of interest interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised to remove a duplicate reference from the reference list.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Khan, Z., Khan, M.S., Suleman et al. Morphology of testis, sperm, and spermatheca in two capable hybridized termite species indicates no interspecific reproductive isolation. Int J Trop Insect Sci 42, 2909–2926 (2022). https://doi.org/10.1007/s42690-022-00817-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-022-00817-3