Neotenic reproductives influence worker caste differentiation in the termite Reticulitermes speratus (Isoptera; Rhinotermitidae)
DOI:
https://doi.org/10.13102/sociobiology.v60i4.446-452Keywords:
caste determination, parental effect, parthenogenesis, social organizationAbstract
Division of labor among castes in social insect colonies increases ergonomic efficiency and colony-level fitness, and has played a key role in the ecological success of social insects. Knowledge of the factors that regulate castes is important for understanding adaptive social organization. Our previous study on the termite Reticulitermes speratus demonstrated that the presence of a pair of nymphoid reproductives during development affected offspring caste ratios. In the present study, we investigated further the influence of individual neotenics on offspring caste ratios. Parthenogenetically-produced offspring were reared in worker-tended experimental colonies with the addition of different forms (nymphoid or ergatoid) and numbers of neotenics, and compared the caste ratios of the offspring between the different experimental treatments. We found that all offspring in worker-only tended colonies became nymphs, while a proportion of offspring in colonies with a single neotenic (with the exception of male ergatoids) differentiated into workers. These results show offspring caste ratios are influenced by the presence of single female ergatoids, single female and male nymphoids, while they remain unaffected by the presence of male ergatoids.
Downloads
References
Allison, P., Altman, M., Gill, J. & McDonald, M. P. (2004) Convergence Problems in Logistic Regression. In: Altman, M., Gill, J. & McDonald, M. P. (Eds.) Numerical Issues in Statistical Computing for the Social Scientist (pp. 238-252). Hoboken, NJ: John Wiley & Sons, Inc. DOI: https://doi.org/10.1002/0471475769.ch10
Buchli, H. (1958) L'Origine des castes et des potentialités ontogéniques des termites européens du genre Reticulitermes Holmgren. Ann. Sci. Nat. Zool., 20: 263-429.
Castle, G. B. (1934) An experimental investigation of caste differentiation in Zootermopsis angusticollis. In: Kofoid CA (Ed.) Termites and termite control, 2nd edn (pp. 292-310). Berkeley, CA: University of California Press.
Crozier, R. H. & Schluns, H. (2008) Genetic caste determination in termites: out of the shade but not from Mars. BioEssays, 30: 299-302. doi: 10.1002/bies.20732 DOI: https://doi.org/10.1002/bies.20732
Firth, D. (1993) Bias reduction of maximum likelihood estimates. Biometrika, 80: 27-38. doi: 10.1093/biomet/80.1.27 DOI: https://doi.org/10.1093/biomet/80.1.27
Fujita, A. & Watanabe, H. (2010) Inconspicuous matured males of worker form are produced in orphaned colonies of Reticulitermes speratus (Isoptera: Rhinotermitidae) and participate in reproduction. J. Insect. Physiol., 56: 1510-1515. doi: 10.1016/j.jinsphys.2010.04.020 DOI: https://doi.org/10.1016/j.jinsphys.2010.04.020
Hanus, R., Vrkoslav, V., Hrdy, I., Cvacka, J. & Sobotnik, J. (2010) Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. P. Roy. Soc. B-Biol. Sci., 277: 995-1002. doi: 10.1098/rspb.2009.1857 DOI: https://doi.org/10.1098/rspb.2009.1857
Hartke, T. R. & Baer, B. (2011) The mating biology of termites: a comparative review. Anim. Behav., 82: 927-936. doi:10.1016/j.anbehav.2011.07.022 DOI: https://doi.org/10.1016/j.anbehav.2011.07.022
Hayashi, Y., Lo, N., Miyata, H. & Kitade, O. (2007) Sex-linked genetic influence on caste determination in a termite. Science, 318: 985-987. doi: 10.1126/science.1146711 DOI: https://doi.org/10.1126/science.1146711
Helms Cahan, S., Daly, A. B., Schwander, T. & Woods, H. A. (2010) Genetic caste determination does not impose growth rate costs in Pogonomyrmex harvester ants. Funct. Ecol., 24: 301-309. doi: 10.1111/j.1365-2435.2009.01629.x DOI: https://doi.org/10.1111/j.1365-2435.2009.01629.x
Howard, R. W. & Haverty, M. I. (1980) Reproductives in mature colonies of Reticulitermes flavipes: abundance, sex ratio, and association with soldiers. Environ. Entomol., 9: 458-460. DOI: https://doi.org/10.1093/ee/9.4.458
Hu, J. & Forschler, B. T. (2012) Neotenic phenotype and sex ratios provide insight into developmental pathways in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Insects, 3: 538-552. doi:10.3390/insects3020538 DOI: https://doi.org/10.3390/insects3020538
Hughes, W. O. & Boomsma, J. J. (2008) Genetic royal cheats in leaf-cutting ant societies. Proc. Natl. Acad. Sci. U. S. A., 105: 5150-5153. doi: 10.1073/pnas.0710262105 DOI: https://doi.org/10.1073/pnas.0710262105
Kitade, O., Hoshi, M., Odaira, S., Asano, A., Shimizu, M., Hayashi, Y. & Lo, N. (2011) Evidence for genetically influenced caste determination in phylogenetically diverse species of the termite genus Reticulitermes. Biol. Lett., 7: 257-260. doi: 10.1098/rsbl.2010.0856 DOI: https://doi.org/10.1098/rsbl.2010.0856
Korb, J., Buschmann, M., Schafberg, S., Liebig, J. & Bagnères A.-G. (2012) Brood care and social evolution in termites. P. Roy. Soc. B-Biol. Sci., 279: 2662-2671. doi: 10.1098/rspb.2011.2639 DOI: https://doi.org/10.1098/rspb.2011.2639
Kosmidis, I. (2007) Bias reduction in exponential family nonlinear models. Ph. D. thesis, Department of Statistics, University of Warwick.
Kosmidis, I. (2008) brglm: Bias reduction in binomial-response GLMs. http://cran.r-project.org/web/packages/brglm/
Lüscher, M. (1961) Social control of polymorphism in termites. In: Kennedy, J. S. (Ed.), Insect Polymorphism (pp. 57-67). London: Royal Entomological Society of London.
Lecoutey, E., Chaline, N. & Jaisson, P. (2011) Clonal ant societies exhibit fertility-dependent shifts in caste ratios. Behav. Ecol., 22: 108-113. doi: 10.1093/beheco/arq182 DOI: https://doi.org/10.1093/beheco/arq182
Leniaud, L., Darrouzet, E., Dedeine, F., Ahn, K., Huang, Z. & Bagnères, A. G. (2011) Ontogenic potentialities of the worker caste in two sympatric subterranean termites in France. Evol. Dev., 13: 138-148. doi: 10.1111/j.1525-142X.2011.00464.x DOI: https://doi.org/10.1111/j.1525-142X.2011.00464.x
Matsuura, K., Himuro, C., Yokoi, T., Yamamoto, Y., Vargo, E. L. & Keller, L. (2010) Identification of a pheromone regulating caste differentiation in termites. Proc. Natl. Acad. Sci. U. S. A., 107: 12963-12968. doi: 10.1073/pnas.1004675107 DOI: https://doi.org/10.1073/pnas.1004675107
Matsuura, K., Tamura, T., Kobayashi, N., Yashiro, T., Tatsumi, S. (2007) The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLoS One, 2: e813. doi: 10.1371/journal.pone.0000813 DOI: https://doi.org/10.1371/journal.pone.0000813
Matsuura, K., Vargo, E. L., Kawatsu, K., Labadie, P. E., Nakano, H., Yashiro, T. & Tsuji, K. (2009) Queen succession through asexual reproduction in termites. Science, 323: 1687-1687. doi: 10.1126/science.1169702 DOI: https://doi.org/10.1126/science.1169702
Matsuura, K., Yamamoto, Y. (2011) Workers do not mediate the inhibitory power of queens in a termite, Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Soc., 58: 513-518. doi: 10.1007/s00040-011-0170-1 DOI: https://doi.org/10.1007/s00040-011-0170-1
Miura, T. (2001) Morphogenesis and gene expression in the soldier-caste differentiation of termites. Insectes Soc., 48: 216-223. doi: 10.1007/PL00001769 DOI: https://doi.org/10.1007/PL00001769
Miura, T., Koshikawa, S. & Matsumoto, T. (2003) Winged presoldiers induced by a juvenile hormone analog in Zootermopsis nevadensis: implications for plasticity and evolution of caste differentiation in termites. J. Morphol. 257: 22-32. doi: 10.1002/jmor.10100 DOI: https://doi.org/10.1002/jmor.10100
Miyata, H., Furuichi, H. & Kitade, O. (2004) Patterns of neotenic differentiation in a subterranean termite, Reticulitermes speratus (Isoptera: Rhinotermitidae). Entomol. Sci. 7: 309-314. doi: 10.1111/j.1479-8298.2004.00078.x DOI: https://doi.org/10.1111/j.1479-8298.2004.00078.x
Myles, T. (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology, 33: 1-91.
Oster, G. F. & Wilson, E. O. (1978) Caste and ecology in the social insects. Princeton, NJ: Princeton University Press.
Pichon, A., Kutnik, M., Leniaud, L., Darrouzet, E., Chaline, N., Dupont, S. & Bagnères, A. G. (2007) Development of experimentally orphaned termite worker colonies of two Reticulitermes species (Isoptera: Rhinotermitidae). Sociobiology, 50: 1015-1034.
Scharf, M. E., Buckspan, C. E., Grzymala, T. L. & Zhou, X. (2007) Regulation of polyphenic caste differentiation in the termite Reticulitermes flavipes by interaction of intrinsic and extrinsic factors. J. Exp. Biol., 210: 4390-4398. doi: 10.1242/jeb.010876 DOI: https://doi.org/10.1242/jeb.010876
Scharf, M. E., Wu-Scharf, D., Pittendrigh, B. R. & Bennett, G. W. (2003) Caste- and development-associated gene expression in a lower termite. Genome Biol., 4: R62. doi: 10.1186/gb-2003-4-10-r62 DOI: https://doi.org/10.1186/gb-2003-4-10-r62
Scharf, M. E., Wu-Scharf, D., Zhou, X., Pittendrigh, B. R., Bennett, G. W. (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol. Biol., 14: 31-44. doi: 10.1111/j.1365-2583.2004.00527.x DOI: https://doi.org/10.1111/j.1365-2583.2004.00527.x
Schmid-Hempel, P. (1992) Worker castes and adaptive demography. J. Evol. Biol., 5: 1-12. doi: 10.1046/j.1420-9101.1992.5010001.x DOI: https://doi.org/10.1046/j.1420-9101.1992.5010001.x
Schwander, T., Lo, N., Beekman, M., Oldroyd, B. P. & 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 DOI: https://doi.org/10.1016/j.tree.2009.12.001
Shimizu, K. (1970) Studies on the caste differentiation of the supplementary reproductive of the Japanese termite, Reticulitermes speratus (Kolbe). Bulletin of the faculty of agriculture, Miyazaki University, 17: 1-46.
Smith, C. R., Anderson, K. E., Tillberg, C. V., Gadau, J. & Suarez, A. V. (2008a) Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am. Nat., 172: 497-507. doi: 10.1086/590961 DOI: https://doi.org/10.1086/590961
Smith, C. R., Toth, A. L., Suarez, A. V. & Robinson, G. E. (2008b) Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet., 9: 735-748. doi:10.1038/nrg2429 DOI: https://doi.org/10.1038/nrg2429
Takematsu, Y. (1992) Biometrical study on the development of the castes in Reticulitermes speratus (Isoptera, Rhinotermitidae). Jpn. J. Entomol., 60: 67-76.
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Thompson, C. B. & Snyder, T. E. (1920) The ‘third form,’ the wingless reproductive type of termites: Reticulitermes and Prorhinotermes. J. Morphol., 34: 590-633. doi: 10.1002/jmor.1050340304 DOI: https://doi.org/10.1002/jmor.1050340304
Thorne, B. L., Traniello, J. F. A., Adams, E. S. & Bulmer, M. (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera: Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol. Ecol. Evol., 11: 149-169. doi: 10.1080/08927014.1999.9522833 DOI: https://doi.org/10.1080/08927014.1999.9522833
Tsuchiya, M., Watanabe, D. & Maekawa, K. (2008) Effect on mandibular length of juvenile hormones and regulation of soldier differentiation in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). App. Entomol. Zool., 43: 307-314. doi: 10.1303/aez.2008.307 DOI: https://doi.org/10.1303/aez.2008.307
Watanabe, D. & Maekawa, K. (2008) Frontal-pore formation during soldier differentiation induced by juvenile hormone III in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Sociobiology, 52: 437-447.
Watanabe, H. & Noda, H. (1991) Small-scale rearing of a subterranean termite, Reticulitermes speratus (Isoptera, Rhinotermitidae). App. Entomol. Zool., 26: 418-420. DOI: https://doi.org/10.1303/aez.26.418
Wheeler, D. M. (2003) One hundred years of caste determination. In: Kikuchi T, Azuma N, Higashi S (Eds.) Genes, Behaviors and Evolution of Social Insects (pp. 35-53). Sapporo, Japan: Hokkaido University Press.
Wilson, E. O. (1971) The insect societies. Cambridge, MA: Belknap Press of Harvard University Press.
Downloads
Published
How to Cite
Issue
Section
License
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).