Colony-dependent sex differences in protozoan communities of the lower termite Reticulitermes speratus (Isoptera: Rhinotermitidae)
In many animals, sex differences in hormones, behavior, and immunity lead to differences in their gut microbial communities. One of the best-known examples of mutualistic symbiosis is that between lower termites and their intestinal protozoa. Although differences in the protozoan communities of different castes have been studied in lower termites, nothing is known about the sex differences in protozoan communities in neuter castes. Here, we show that termite workers have different protozoan communities according to sex depending on the colony. We investigated the communities of symbiotic protozoa living in lower termites, Reticulitermes speratus, and how they are affected by sex and caste. Workers had the largest numbers of protozoa, followed by soldiers, whereas reproductives (primary kings and secondary queens) had no protozoa. Workers showed colony-dependent sex differences in the total abundance of protozoa, whereas soldiers showed no such sex differences. There were significant sex effect and/or interaction effect between colony and sex in abundances of five species of protozoa in workers. Workers also showed significant sex differences and/or colony-dependent sex differences in proportion of six species of protozoa. These may result in sex differences in the host–symbiont interaction due to physiological or behavioral sex differences in workers that have not been recognized previously. This study has an important implication: although workers are not engaged in reproduction, their potential sex difference may affect various aspects of social interactions.
KeywordsMutualistic symbiosis Sex differences Social insects Protozoa Isoptera
We thank S. Dobata and K. Kobayashi for helpful comments and T. Yashiro for termite photographs. This work was supported by Japan Society for the Promotion of Science (https://www.jsps.go.jp/english/index.html, No. 25221206 to KM).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Andrew BJ (1930) Method and rate of protozoan refaunation in the termite Termopsis angusticollus Hagen. Calif Univ Publ Zool 33:449–470Google Scholar
- Cook TJ, Gold RE (1998) Organization of the symbiotic flagellate community in three castes of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 31:25–39Google Scholar
- Cook TJ, Gold RE (1999) Symbiotic hindgut flagellate communities of the subterranean termites Reticulitermes virginicus and Reticulitermes flavipes in Texas (Isoptera: Rhinotermitidae). Sociobiology 34:533–544Google Scholar
- De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 107:14691–14696. doi: 10.1073/pnas.1005963107 CrossRefPubMedPubMedCentralGoogle Scholar
- De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ, Green W, Denou E, Silva MA, Santacruz A, Sanz Y, Surette MG, Verdu EF, Collins SM, Bercik P (2015) Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun 6:7735. doi: 10.1038/ncomms8735 CrossRefPubMedGoogle Scholar
- Honigberg BM (1970) Protozoa associated with termites and their role in digestion. In: Krishna K, Weesner FM (eds) Biology of termites, vol II., Academic PressNew York, London, pp 1–36Google Scholar
- Kirby H (1937) Host-parasite relations in the distribution of protozoa in termites. Univ Calif Publ Zool 41:189–211Google Scholar
- Kitade O (2007) Characteristics and host-symbiont relationships of termite gut flagellates. Jpn J Protozool 40:101–112Google Scholar
- Lewis JL, Forschler BT (2004) Protist communities from four castes and three species of Reticulitermes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 97:1242–1251. doi:10.1603/0013-8746(2004)097[1242:pcffca]2.0.co;2Google Scholar
- Markle JGM, Frank DN, Mortin-toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS (2013) Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339:1084–1088. doi: 10.1126/science.1233521 CrossRefPubMedGoogle Scholar
- Ohkuma M, Brune A (2011) Diversity, structure, and evolution of the termite gut microbial community. In: Bignel DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 413–438Google Scholar
- Roisin Y, Korb A (2011) Social organisation and the status of workers in termites. In: Bignel DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 133–164Google Scholar
- R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
- Yamaoka I, Sasabe K, Terada K (1986) A timely infection of intestinal protozoa in developing hindgut of the termite (Reticulitermes speratus). Zoolog Sci 3:175–180Google Scholar
- Zimet M, Stuart A (1982) Sexual dimorphism in the immature stages of the termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 7:1–7Google Scholar