Abstract
Termites differ from hymenopteran social insects in several important respects, perhaps most significantly in their sex and caste determination systems: while hymenopteran colonies are female dominated (and sex determination is haplo-diploid), termite colonies are usually split evenly between males and females (and sex determination is through sex chromosomes). Not all termite species have an equal sex ratio—in the termite genus Schedorhinotermes, almost all workers and soldiers are females. The mechanism maintaining this sex ratio skew is unknown, but a possible mechanism (known in other termites as a mechanism for producing reproductives) is parthenogenesis. Under this scenario, soldiers and workers would be offspring of the queen only. In this study, we performed microsatellite analysis on 11 colonies of Schedorhinotermes intermedius (Isoptera: Rhinotermitidae) to investigate the parentage of workers, soldiers and alates within colonies, and to determine whether parthenogenesis is responsible for the production of female workers and soldiers. We also conducted a preliminary analysis of population and colony genetic structure. We found that females from a single colony had in some instances more than two alleles among them at a single microsatellite locus. This indicates that a single female cannot be producing these offspring, as she has a maximum of two different alleles at any locus, ruling out the possibility that the high proportion of females in this species comes about through parthenogenesis.
Similar content being viewed by others
References
Bourguignon T, Roisin Y (2011) Revision of the termite family Rhinotermitidae (Isoptera) in New Guinea. ZooKeys 148:55–103. doi:10.3897/zookeys.148.1826
Bourguignon T, Šobotník J, Hanus R, Roisin Y (2009) Developmental pathways of Glossotermes oculatus (Isoptera, Serritermitidae): at the cross-road of worker caste evolution in termites. Evol Dev 11:659–668
Bourguignon T, Hayashi Y, Miura T (2012) Skewed soldier sex ratio in termites: testing the size-threshold hypothesis. Insectes Soc 59:557–563
Churbanov A, Ryan R, Hasan N, Bailey D, Chen H, Milligan B, Houde P (2012) HighSSR: high-throughput SSR characterization and locus development from next-gen sequencing data. Bioinformatics 28:2797–2803. doi:10.1093/bioinformatics/bts524
Evans TA (2011) Invasive termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht
Foucaud J, Fournier D, Orivel J, Delabie JHC, Loiseau A, Le Breton J, Kergoat GJ, Estoup A (2007) Sex and clonality in the little fire ant. Mol Biol Evol 24:2465–2473
Fougeyrollas R, Dolejšová K, Sillam-Dussès D, Roy V, Poteaux C, Hanus R, Roisin Y (2015) Asexual queen succesion in the higher termite Embiratermes neotenicus. Proc R Soc B. doi:10.1098/rspb.2015.0260
Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234. doi:10.1038/nature03705
Gay FJ, Calaby JH (1970) Termites of the Australian region. In: Krishna K, Weesner FM (eds) Biology of termites, vol II., Academic PressNew York, USA, pp 393–448
Gene Codes Corporation (2011) Sequencher® version 5.0.1 sequence analysis software. http://www.genecodes.com. Accessed 15 Aug 2015
Hadlington P, Staunton I (2008) Australian termites. UNSW Press, Sydney
Himler AG, Caldera EJ, Baer BC, Fernández-Marín H, Mueller UG (2009) No sex in fungus-farming ants or their crops. Proc R Soc B 276:2611–2616. doi:10.1098/rspb.2009.0313
Husseneder C, Brandl R, Epplen C, Epplen JT, Kaib M (1998) Variation between and within colonies in the termite: morphology, genomic DNA, and behaviour. Mol Ecol 7:983–990. doi:10.1046/j.1365-294x.1998.00416.x
Krishna K, Grimaldi DA, Krishna V, Engel MS (2013) Treatise on the Isoptera of the world. Bull Am Mus Nat Hist 377:623–973. doi:10.1206/377.3
Lo N, Hayashi Y, Kitade O (2009) Should environmental caste determination be assumed for termites? Am Nat 173:848–853. doi:10.1086/598498
Matsuura K (2006) A novel hypothesis for the origin of the sexual division of labor in termites: which sex should be soldiers? Evol Ecol 20:565–574
Matsuura K (2011) Sexual and asexual reproduction in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht
Matsuura K, Vargo EL, Kawatsu K, Labadie PE, Nakano H, Yashiro T, Tsuji K (2009) Queen succession through asexual reproduction in termites. Science 323:1687. doi:10.1126/science.1169702
Meglecz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin J-F (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26:403–404. doi:10.1093/bioinformatics/btp670
Muller H, Korb J (2008) Male or female soldiers? An evaluation of several factors which may influence soldier sex ratio in lower termites. Insect Soc 55:213–219. doi:10.1007/s00040-008-0996-3
Noirot C (1955) Recherche sur le polymorphisme des termites supérieurs (Termitidae). Ann Sci Nat Zool 17:399–595
Noirot C, Darlington JPEC (2000) Termite nests: architecture, regulation and defence. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer academic publishing, Dordrecht, pp 121–139
Renoux J (1976) Le polymorphisme de Schedorhinotermes lamanianus (Sjöstedt) (Isoptera-Rhinotermitidae). Essai d’interpétation. Insect Soc 23:279–494
Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht
Roisin Y (2001) Caste sex ratios, sex linkage, and reproductive strategies in termites. Insect Soc 48:224–230
Roonwal ML (1970) Termites of the Oriental region. In: Krishna K, Weesner FM (eds) Biology of Termites, vol II. Academic Press, New York
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234. doi:10.1038/72708
Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275–282. doi:10.1016/j.tree.2009.12.001
Thompson GJ, Lenz M, Crozier RH, Crespi BJ (2007) Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system. Aust J Zool 55:219–227
Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant, Cerapachys biroi. Insect Soc. 42:333–336. doi:10.1007/bf01240430
Vargo EL (2003) Hierarchical analysis of colony and population genetic structure of the Eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57:2805–2818. doi:10.1111/j.0014-3820.2003.tb01522.x
Vargo EL, Husseneder C, Grace JK (2003) Colony and population genetic structure of the Formosan subterranean termite, Coptotermes formosanus, in Japan. Mol Ecol 12:2599–2608
Vargo EL, Husseneder C, Woodson D, Waldvogel MG, 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. Environ Entomol 35:151–166
Vargo EL, Labadie PE, Matsuura K (2012) Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc R Soc B 279:813–819
Watson JAL, Abbey HM (1993) Atlas of Australian termites. CSIRO Division of Entomology, Canberra
Weir BS (1996) Genetic Data Analysis, 2nd edn. Sinauer Associates, Massachusetts
Zablotny JE (2003) Sociality. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic Press, San Diego
Acknowledgements
We thank Julie Lim, Gabrielle Bachmann, Roz Gloag, Grace Heng Wei and Beata Ujivari for assistance with microsatellite analysis, and Nick Cooper for assistance with specimen collection. TRCL was supported by an Australian Postgraduate Award, and an Australian Biological Resources Survey (ABRS) APA top-up grant (Grant No. CT212-11). NL was supported by the Australian Research Council (Grant No. DP1097265). TB was supported by a University of Sydney Postdoctoral Fellowship.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lee, T.R.C., Bourguignon, T. & Lo, N. Female-only workers and soldiers in Schedorhinotermes intermedius are not produced by parthenogenesis. Insect. Soc. 64, 133–139 (2017). https://doi.org/10.1007/s00040-016-0523-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-016-0523-x