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Insectes Sociaux

, Volume 59, Issue 1, pp 55–59 | Cite as

Paternally inherited alleles in male body parts of an ant (Diacamma sp.) sex mosaic: implication for androgenetic male production in the Hymenoptera

  • S. DobataEmail author
  • H. ShimojiEmail author
  • H. Ohnishi
  • E. Hasegawa
  • K. Tsuji
Research Article

Abstract

Sex mosaicism, also called gynandromorphism, refers to an accidental phenomenon in dioecious organisms (mainly animals) in which an individual phenotype includes both female and male characteristics. Despite the rarity of this phenomenon, elucidating the mechanisms of naturally occurring sex mosaicism should deepen our understanding of diverse sex determination and differentiation systems in nature. We report the results of a genetic study of a sex mosaic individual of the ant Diacamma sp. from Japan’s Okinawa Island. Parentage analysis using microsatellite markers revealed that the female and male parts of the sex mosaic showed different inheritance patterns: female parts had alleles consistent with their biparental inheritance, whereas most of the male parts had alleles consistent with their paternal inheritance (i.e., androgenesis). We discuss plausible cytogenetic mechanisms that gave rise to the male parts of this individual: polyspermy and the subsequent independent cleavage by a surplus sperm pronucleus, and maternal genome elimination after fertilization of an ovule. Moreover, we hypothesize that the androgenetically produced males found in some Hymenoptera might share the same underlying cytogenetic mechanism with hymenopteran sex mosaicism.

Keywords

Gynandromorph Androgenesis Haplodiploid Male clonality Polyspermy 

Notes

Acknowledgments

We thank T. Akino and R. Yasudai for assistance in the field survey and M. Okamoto and A. Mikheyev for discussions. We also thank the editor and two anonymous referees for their constructive comments. SD was supported by Research Fellowship from the Japan Society for the Promotion of Science for Young Scientists (22-9877).

Supplementary material

Supplementary material 1 (MPG 1743 kb)

40_2011_187_MOESM2_ESM.pdf (78 kb)
Supplementary material 2 (PDF 77 kb)
40_2011_187_MOESM3_ESM.xls (34 kb)
Supplementary material 3 (XLS 34 kb)

References

  1. Berndt K.P. and Kremer G. 1982. Heat shock-induced gynandromorphism in the pharaoh’s ant, Monomorium pharaonis (L.). Cell. Mol. Life Sci. 38: 798-799Google Scholar
  2. Birkhead T.R., Hosken D.J. and Pitnick S. 2009. Sperm Biology: An Evolutionary Perspective. Academic Press, LondonGoogle Scholar
  3. Clark A.M., Gould A.B. and Potts M.F. 1968. Mosaicism in Habrobracon juglandis associated with the ebony locus. Genetics 58: 415-422Google Scholar
  4. Doums C. 1999. Characterization of microsatellite loci in the queenless Ponerine ant Diacamma cyaneiventre. Mol. Ecol. 8: 1957-1959Google Scholar
  5. Foucaud J., Fournier D., Orivel J. et al. 2007. Sex and clonality in the little fire ant. Mol. Biol. Evol. 24: 2465-2473Google Scholar
  6. Foucaud J., Estoup A., Loiseau A. et al. 2010. Thelytokous parthenogenesis, male clonality and genetic caste determination in the little fire ant: new evidence and insights from the lab. Heredity 105: 205-212Google Scholar
  7. Fournier D., Estoup A., Orivel J. et al. 2005. Clonal reproduction by males and females in the little fire ant. Nature 435: 1230-1234Google Scholar
  8. Fukumoto Y., Abe T. and Taki A. 1989. A novel form of colony organization in the “queenless” ant Diacamma rugosum. Physiol. Ecol. Jpn 26: 55-61Google Scholar
  9. Kinomura K. and Yamauchi K. 1994. Frequent occurrence of gynandromorphs in the natural population of the ant Vollenhovia emeryi (Hymenoptera: Formicidae). Insect. Soc. 41: 273-278Google Scholar
  10. Koeniger N., Hemmling C. and Yoshida T. 1989. Drones as sons of drones in Apis mellifera. Apidologie 20: 391-394Google Scholar
  11. Moilanen A., Sundström L. and Pedersen J.S. 2004. MATESOFT: a program for deducing parental genotypes and estimating mating system statistics in haplodiploid species. Mol. Ecol. Notes 4: 795-797Google Scholar
  12. Morgan T.H. 1905. An alternative interpretation of the origin of gynandromorphous insects. Science 21: 632-634Google Scholar
  13. Nachtsheim H. 1913. Cytologische Studien über die Geschlechtsbestimmung bei der Honigbiene (Apis mellifera L.). Arch. Zellforsch. 11: 169-239Google Scholar
  14. Nakata K., Tsuji K., Hölldobler B. and Taki A. 1998. Sexual calling by workers using the metatibial glands in the ant, Diacamma sp. J. Insect Behav. 11: 869-877Google Scholar
  15. Nilsson G.E. 1987. A gynandromorphic specimen of Evylaeus albipes (Fabricius) (Hymenoptera, Halictidae) and a discussion of possible causes of gynandromorphism in haplo-diploid insects. Not. Ent. 67: 157-162Google Scholar
  16. Ohkawara K., Nakayama M., Satoh A. et al. 2006. Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol. Lett. 2: 359-363Google Scholar
  17. Okada Y., Miyazaki S., Koshikawa S. et al. 2010. Identification of a reproductive-specific, putative lipid transport protein gene in a queenless ponerine ant. Naturwissenschaften 97: 971-979Google Scholar
  18. Pearcy M., Goodisman M.A.D. and Keller L. 2011. Sib mating without inbreeding in the longhorn crazy ant. Proc. R. Soc. Lond. B. doi: 10.1098/rspb.2010.2562
  19. Queller D. 2005. Evolutionary biology: Males from Mars. Nature 435: 1167-1168Google Scholar
  20. Raymond M. and Rousset F. 1995. GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249Google Scholar
  21. Rothenbuhler W.C., Gowen J.W.and Park O.W. 1952. Androgenesis with zygogenesis in gynandromorphic honeybees (Apis mellifera L.). Science 115: 637-638Google Scholar
  22. Speitcher B.R. 1936. Oogenesis, fertilization and early cleavage in Habrobracon. J. Morphol. 59: 401-421Google Scholar
  23. Takahashi J., Kikuchi T., Ohnishi H. and Tsuji K. 2005. Isolation and characterization of 10 microsatellite loci in the Ponerinae ant Pachycondyla luteipes (Hymenoptera; Formicidae). Mol. Ecol. Notes 5: 749-751Google Scholar
  24. Viginier B., Peeters C., Brazier L. and Doums C. 2004. Very low genetic variability in the Indian queenless ant Diacamma indicum. Mol. Ecol. 13: 2095-2100Google Scholar
  25. Walsh P.S., Metzger D.A. and Higuchi R. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10: 506-513Google Scholar
  26. Yang A.S. and Abouheif E. 2011. Gynandromorphs as indicators of modularity and evolvability in ants. J. Exp. Zool. B Mol. Dev. Evol. 316B: 313-318Google Scholar
  27. Yoshizawa J., Mimori K., Yamauchi K. and Tsuchida K. 2009. Sex mosaics in a male dimorphic ant Cardiocondyla kagutsuchi. Naturwissenschaften 96: 49-55Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2011

Authors and Affiliations

  1. 1.Department of Agro-Environmental Sciences, Faculty of AgricultureUniversity of the RyukyusNishiharaJapan
  2. 2.Resource and Environmental Science of Agriculture, Forestry and Fisheries, United Graduate School of Agricultural SciencesKagoshima UniversityKagoshimaJapan
  3. 3.Laboratory of Animal Ecology, Department of Ecology and Systematics, Graduate School of AgricultureHokkaido UniversitySapporoJapan

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