Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-03T03:45:30.796Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative reproductive biology of pre-, imaginal, and neotenic castes of the Asian termite Coptotermes gestroi (Blattaria, Isoptera, Rhinotermitidae)

Published online by Cambridge University Press:  20 May 2022

Ana Maria Costa-Leonardo Open the ORCID record for Ana Maria Costa-Leonardo [Opens in a new window] ,
Vanelize Janei Open the ORCID record for Vanelize Janei [Opens in a new window]  and
Iago Bueno da Silva Open the ORCID record for Iago Bueno da Silva [Opens in a new window]
Ana Maria Costa-Leonardo*
Affiliation:
Laboratório de Cupins, Departamento de Biologia Geral e Aplicada, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900, Rio Claro, SP, Brazil
Vanelize Janei
Affiliation:
Laboratório de Cupins, Departamento de Biologia Geral e Aplicada, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900, Rio Claro, SP, Brazil
Iago Bueno da Silva
Affiliation:
Laboratório de Cupins, Departamento de Biologia Geral e Aplicada, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900, Rio Claro, SP, Brazil
*
Author for correspondence: Ana Maria Costa-Leonardo, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The Asian subterranean termite Coptotermes gestroi is a worldwide structural pest, although its reproductive biology has been poorly investigated due to a cryptic habit and occurrence of polycalic nests. In this study, we investigated ovarian development and oogenesis in different-aged females of C. gestroi: fourth-instar nymphs, non-functional neotenics, alates, and functional queens. We show that the ovaries develop gradually according to their age and functionality, as younger individuals possess immature oocytes, whereas alates and functional queens always undergo vitellogenesis. Oocytes were classified into previtellogenic (stages I, II, and III) or vitellogenic (stages IV, V, and VI). Ovary development varied among non-functional neotenics, and a rapid differentiation and/or the presence of primary reproductives are believed to influence such a maturation. Immature oocyte stages were shared between fourth-instar nymphs and neotenics. These characteristics, together with other neotenic features (wing buds, body pigmentation, and eye color), should be evaluated in detail aiming to clarify which nymphal instars differentiate into secondary reproductives. Oogenesis was not uniform among alate females, and cross-sectional area of terminal oocytes was significantly smaller in alates when compared to functional queens, suggesting different degrees of maturation in swarming individuals. Functional queens always had mature terminal oocytes (stage VI). Ovariole number and oocyte maturation in C. gestroi relies on several factors and may therefore differ among individuals of the same caste. Future studies should take into account these reproductive features to evaluate how they impact colony development.

Keywords

Oogenesisovary developmentpest speciesreproduction
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 6 , December 2022 , pp. 827 - 836
Check for updates
Copyright
Copyright © The Author(s), 2022. 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

Albino, E and Costa-Leonardo, AM (2011) Nymphs in foraging populations of Coptotermes gestroi (Isoptera: Rhinotermitidae). Animal Biology 61, 427–439.10.1163/157075511X596909CrossRefGoogle Scholar
Barsotti, RC and Costa-Leonardo, AM (2005) The caste system of Coptotermes gestroi (Isoptera: Rhinotermitidae). Sociobiology 46, 87–103.Google Scholar
Brent, CS and Traniello, JF (2001 a) Influence of sex-specific stimuli on ovarian maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis. Physiological Entomology 26, 239–247.10.1046/j.0307-6962.2001.00243.xCrossRefGoogle Scholar
Brent, CS and Traniello, JF (2001 b) Social influence of larvae on ovarian maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis. Physiological Entomology 26, 78–85.Google Scholar
Brent, CS and Traniello, JF (2002) Effect of enhanced dietary nitrogen on reproductive maturation of the termite Zootermopsis angusticollis (Isoptera: Termopsidae). Environmental Entomology 31, 313–318.10.1603/0046-225X-31.2.313CrossRefGoogle Scholar
Büning, J (1994) The ovary of Ectognatha, the Insecta s.str. In Büning, J (ed.), The Insect Ovary: Ultrastructure, Previtellogenic Growth and Evolution. London: Chapman & Hall, pp. 281–299.CrossRefGoogle Scholar
Chouvenc, T (2019) The relative importance of queen and king initial weights in termite colony foundation success. Insectes Sociaux 66, 177–184.CrossRefGoogle Scholar
Chouvenc, T and Su, N-Y (2014) Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insectes Sociaux 61, 171–182.10.1007/s00040-014-0343-9CrossRefGoogle Scholar
Chouvenc, T, Mullins, AJ and Su, N-Y (2015 a) Rare production of nymphs in an Asian subterranean termite (Isoptera: Rhinotermitidae) incipient colony. Florida Entomologist 98, 972–973.10.1653/024.098.0327CrossRefGoogle Scholar
Chouvenc, T, Basille, M and Su, N-Y (2015 b) The production of soldiers and the maintenance of caste proportions delay the growth of termite incipient colonies. Insectes Sociaux 62, 23–29.10.1007/s00040-014-0369-zCrossRefGoogle Scholar
Costa-Leonardo, AM (ed.) (2002) Cupins-Praga: Morfologia, Biologia e Controle. Rio Claro: Divisa Editora, p. 128.Google Scholar
Costa-Leonardo, AM and Barsotti, RC (1998) Swarming and incipient colonies of Coptotermes havilandi (Isoptera, Rhinotermitidae). Sociobiology 31, 131–142.Google Scholar
Costa-Leonardo, AM and Barsotti, RC (2001) Growth patterns of incipient colonies of Coptotermes havilandi (Isoptera, Rhinotermitidae) initiated in the laboratory from swarming alates. Sociobiology 37, 551–561.Google Scholar
Costa-Leonardo, AM and Arab, A (2004) Reproductive strategy of Coptotermes gestroi (Isoptera: Rhinotermitidae). Sociobiology 44, 123–125.Google Scholar
Costa-Leonardo, AM, Arab, A and Casarin, FE (2004) Neotenic formation in laboratory colonies of the termite Coptotermes gestroi after orphaning. Journal of Insect Science 4, 10.CrossRefGoogle ScholarPubMed
Dean, SR and Gold, RE (2004) Sex ratios and development of the reproductive system in castes of Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America 97, 147–152.CrossRefGoogle Scholar
Dossi, FCA and Cônsoli, FL (2014) Gross morphology and ultrastructure of the female reproductive system of Diaphorina citri (Hemiptera: Liviidae). Zoologia 31, 162–169.CrossRefGoogle Scholar
Ghesini, S, Puglia, G and Marini, M (2011) First report of Coptotermes gestroi in Italy and Europe. Bulletin of Insectology 64, 53–54.Google Scholar
Grandi, G (1988) Oogenesis in Kalotermes flavicollis (Fabr.) (Isoptera: Kalotermitidae). II-prefollicular and follicular cell ultrastructure during oogenesis in female supplementary reproductives. Bollettino di zoologia 55, 279–292.10.1080/11250008809386625CrossRefGoogle Scholar
Grandi, G (1990) Oogenesis in Kalotermes flavicollis (Fabr.) (Isoptera, Kalotermitidae) III. Choriogenesis and corpus luteum formation in female supplementary reproductive. Bollettino di zoologia 57, 97–107.CrossRefGoogle Scholar
Grandi, G (1991) Oogenesis in immature stages and sterile castes of Kalotermes flavicollis (Fabr.) (Isoptera Kalotermitidae). Ethology Ecology & Evolution 3, 29–32.CrossRefGoogle Scholar
Grandi, G and Chicca, M (1999) Oogenesis in supplementary reproductives of Reticulitermes lucifugus Rossi (Isoptera Rhinotermitidae): an ultrastructural study. Invertebrate Reproduction & Development 35, 65–79.CrossRefGoogle Scholar
Grandi, G, Barbieri, R and Colombo, G (1988) Oogenesis in Kalotermes flavicollis (Fabr.) (Isoptera: Kalotermitidae). I. Differentiation and maturation of oocytes in female supplementary reproductives. Bolletino di Zoologia 55, 103–122.CrossRefGoogle Scholar
Grassé, PP (1982) Termitologia. Vol. 1, Paris: Masson, p. 676.Google Scholar
Greenberg, SLW and Stuart, AM (1979) The influence of group size on ovarian development in adult and neotenic reproductives of the termite Zootermopsis angusticollis (Hagen)(Hodotermitidae). International Journal of Invertebrate Reproduction 1, 99–108.CrossRefGoogle Scholar
Husseneder, C, McGregor, C, Lang, RP, Collier, R and Delatte, J (2012) Transcriptome profiling of female alates and egg-laying queens of the Formosan subterranean termite. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 7, 14–27.Google ScholarPubMed
Jenkins, TM, Jones, SC, Lee, C-Y, Forschler, BT, Chen, Z, Lopez-Martinez, G, Gallagher, NT, Brown, G, Neal, M, Thistleton, B and Kleinschmidt, S (2007) Phylogeography illuminates maternal origins of exotic Coptotermes gestroi (Isoptera: Rhinotermitidae). Molecular Phylogenetics and Evolution 42, 612–621.10.1016/j.ympev.2006.11.024CrossRefGoogle ScholarPubMed
Korb, J (2007) Workers of a drywood termite do not work. Frontiers in Zoology 4, 1–7.CrossRefGoogle Scholar
Laranjo, LT, Haifig, I and Costa-Leonardo, AM (2019) A glycoproteinaceous secretion in the seminal vesicles of the termite Coptotermes gestroi (Isoptera: Rhinotermitidae). Insects 10, 428.10.3390/insects10120428CrossRefGoogle ScholarPubMed
Lelis, AT (1999) Primeiro registro no Brasil de rainha de substituição de Coptotermes havilandi e sua implicação no controle desse cupim. Vetores Pragas 4, 19–23.Google Scholar
Li, H-F, Fujisaki, I and Su, N-Y (2013) Predicting habitat suitability of Coptotermes gestroi (Isoptera: Rhinotermitidae) with species distribution models. Journal of Economic Entomology 106, 311–321.CrossRefGoogle ScholarPubMed
Maekawa, 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 35, 52–58.CrossRefGoogle Scholar
Martins, C, Fontes, LR, Bueno, OC and Martins, VG (2010) Coptotermes gestroi (Isoptera: Rhinotermitidae) in Brazil: possible origins inferred by mitochondrial cytochrome oxidase II gene sequences. Genome 53, 651–657.CrossRefGoogle ScholarPubMed
Morini, MSC and Costa-Leonardo, AM (1992) The functional ovarioles in female imagoes of Cornitermes cumulans (Isoptera, Termitidae) at the swarming time. Revista Brasileira de Entomologia 36, 709–715.Google 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, 1–43.Google Scholar
Noirot, C (1969) Formation of castes in the higher termites. In Krishna, K and Weesner, FM (eds), Biology of Termites, Vol. 1. New York, NY, USA: Academic Press, pp. 311–350.CrossRefGoogle Scholar
Noirot, C (1990) Sexual castes and reproductive strategies in termites. In Engels, W (ed.), Social Insects - an Evolutionary Approach to Caste and Reproduction. Heidelberg: Springer Verlag, pp. 5–35.Google Scholar
Oguchi, K, Shimoji, H, Hayashi, Y and Miura, T (2016) Reproductive organ development along the caste differentiation pathways in the dampwood termite Hodotermopsis sjostedti. Insectes Sociaux 63, 519–529.CrossRefGoogle Scholar
Raina, A, Park, YI and Florane, C (2003) Behavior and reproductive biology of the primary reproductives of the Formosan subterranean termite (Isoptera: Rhinotermitidae). Sociobiology 41, 37.Google Scholar
Robinet, C and Roques, A (2010) Direct impacts of recent climate warming on insect populations. Integrative Zoology 5, 132–142.10.1111/j.1749-4877.2010.00196.xCrossRefGoogle ScholarPubMed
Santos, CG, Humann, FC and Hartfelder, K (2019) Juvenile hormone signaling in insect oogenesis. Current Opinion in Insect Science 31, 43–48.CrossRefGoogle ScholarPubMed
Thorne, BL (1997) Evolution of eusociality in termites. Annual Review of Ecology and Systematics 28, 27–54.CrossRefGoogle Scholar
Van Antwerpen, R and Law, JH (1993) Lipophorin lipase from the yolk of Manduca sexta eggs: identification and partial characterization. Archives of Insect Biochemistry and Physiology 20, 1–12.CrossRefGoogle Scholar
Wheeler, D (1996) The role of nourishment in oogenesis. Annual Review of Entomology 41, 407–431.CrossRefGoogle ScholarPubMed
Wilson, EO (1985) The sociogenesis of insect colonies. Science (New York, N.Y.) 228, 1489–1495.CrossRefGoogle ScholarPubMed