Colony-dependent sex differences in protozoan communities of the lower termite Reticulitermes speratus (Isoptera: Rhinotermitidae)
Tóm tắt
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.
Tài liệu tham khảo
Andrew BJ (1930) Method and rate of protozoan refaunation in the termite Termopsis angusticollus Hagen. Calif Univ Publ Zool 33:449–470
Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, Lusis AJ, Knight R, Caporaso JG, Svanbäck R (2014) Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun. doi:10.1038/ncomms5500
Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci 9:424–428. doi:10.1073/pnas.9.12.424
Cleveland LR (1925) The feeding habit of termite castes and its relation to their intestinal flagellates. Biol Bull 48:295–308. doi:10.1017/CBO9781107415324.004
Cleveland LR (1949) Hormone-induced sexual cycles of flagellates. J Morphol 85:197–295
Cook TJ, Gold RE (1998) Organization of the symbiotic flagellate community in three castes of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 31:25–39
Cook TJ, Gold RE (1999) Symbiotic hindgut flagellate communities of the subterranean termites Reticulitermes virginicus and Reticulitermes flavipes in Texas (Isoptera: Rhinotermitidae). Sociobiology 34:533–544
Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712. doi:10.1038/nrn3346
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
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
Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735. doi:10.1111/1574-6976.12025
Feldman M, Barnett C (1991) Fasting gastric pH and its relationship to true hypochlorhydria in humans. Dig Dis Sci 36:866–869. doi:10.1007/BF01297133
Freire AC, Basit AW, Choudhary R, Piong CW, Merchant HA (2011) Does sex matter? The influence of gender on gastrointestinal physiology and drug delivery. Int J Pharm 415:15–28. doi:10.1016/j.ijpharm.2011.04.069
Gomez A, Luckey D, Taneja V (2015) The gut microbiome in autoimmunity: sex matters. Clin Immunol 159:154–162. doi:10.1016/j.clim.2015.04.016
Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci 108:3047–3052. doi:10.1073/pnas.1010529108
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 1–36
Hu XP, Song D, Gao X (2011) Biological changes in the Eastern subterranean termite, Reticulitermes flavipes (Isoptera, Rhinotermitidae) and its protozoa profile following starvation. Insectes Soc 58:39–45. doi:10.1007/s00040-010-0114-1
Kirby H (1937) Host-parasite relations in the distribution of protozoa in termites. Univ Calif Publ Zool 41:189–211
Kirchner WH, Minkley N (2003) Nestmate discrimination in the harvester termite Hodotermes mossambicus. Insectes Soc 50:222–225. doi:10.1007/s00040-003-0667-3
Kitade O (2007) Characteristics and host-symbiont relationships of termite gut flagellates. Jpn J Protozool 40:101–112
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;2
Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788. doi:10.1038/nrmicro1978
Lo Pinto M, Varrica G, Agrò A (2016) Temporal variations in symbiotic hindgut protist community of the subterranean termite Reticulitermes lucifugus Rossi in Sicily. Insectes Soc 63:1–12. doi:10.1007/s00040-015-0449-8
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
Matsuura K (2001) Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92:20–26
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. doi:10.1007/s10682-006-9117-9
Menasria T, Moussa F, El-Hamza S, Tine S, Megri R, Chenchouni H (2014) Bacterial load of German cockroach (Blattella germanica) found in hospital environment. Pathog Glob Health 108:141–147. doi:10.1179/2047773214Y.0000000136
Minkley N, Fujita A, Brune A, Kirchner WH (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insectes Soc 53:339–344. doi:10.1007/s00040-006-0878-5
Mitaka Y, Kobayashi K, Mikheyev A, Tin MMY, Watanabe Y, Matsuura K (2016) Caste-specific and sex-specific expression of chemoreceptor genes in a termite. PLoS One 11:e0146125. doi:10.1371/journal.pone.0146125
Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Luigi F, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974. doi:10.1126/science.1198719
Nutting WL (1956) Reciprocal protozoan transfaunations between the roach, Cryptocercus, and the termite, Zootermopsis. Biol Bull 110:83–90
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 413–438
Prewett EJ, Smith JTL, Nwokolo AM, Sawyerr AM, Pounder RE (1991) Twenty-four hour intragastric acidity and plasma gastrin concentration profiles in female and male subjects. Clin Sci 80:619–624
Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R (2012) Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE 7:1–10. doi:10.1371/journal.pone.0030768
Restif O, Amos W (2010) The evolution of sex-specific immune defences. Proc R Soc Lond B 277:2247–2255. doi:10.1098/rspb.2010.0188
Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–1355. doi:10.1126/science.1190689
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 133–164
Schomburg L, Stoedter M, Renko K, Hög A, Schomburg L (2010) Selenium controls the sex-specific immune response and selenoprotein expression during the acute-phase response in mice. Biochem J 429:43–51. doi:10.1042/BJ20091868
Shastri P, McCarville J, Kalmokoff M, Brooks SPJ, Green-Johnson JM (2015) Sex differences in gut fermentation and immune parameters in rats fed an oligofructose-supplemented diet. Biol Sex Differ 6:13. doi:10.1186/s13293-015-0031-0
Shimada K, Lo N, Kitade O, Wakui A, Maekawa K (2013) Cellulolytic protist numbers rise and fall dramatically in termite queens and kings during colony foundation. Eukaryot Cell 12:545–550. doi:10.1128/EC.00286-12
Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674. doi:10.1126/science.1212782
Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414. doi:10.1016/j.cmet.2011.07.012
Su NY, La Fage JP (1987) Initiation of worker-soldier trophallaxis by the Formosan subterranean termite (Isoptera: Rhinotermitidae). Insectes Soc 34:229–235. doi:10.1007/BF02224355
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Toga K, Hanmoto S, Suzuki R, Watanabe D, Miura T, Maekawa K (2016) Sexual difference in juvenile-hormone titer in workers leads to sex-biased soldier differentiation in termites. J Insect Physiol 87:63–70. doi:10.1016/j.jinsphys.2016.02.005
Yamaoka I, Sasabe K, Terada K (1986) A timely infection of intestinal protozoa in developing hindgut of the termite (Reticulitermes speratus). Zoolog Sci 3:175–180
Zimet M, Stuart A (1982) Sexual dimorphism in the immature stages of the termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 7:1–7