Ovarian development and insulin-signaling pathways during reproductive differentiation in the queenless ponerine ant Diacamma sp.

Journal of Insect Physiology

Volumn 56, Issue 3, 2010, Pages 288-295

  Okada, Yasukazu ^a   Miyazaki, Satoshi ^a   Miyakawa, Hitoshi ^a   Ishikawa, Asano ^a   Tsuji, Kazuki ^b   Miura, Toru ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

Insulin signaling; Ovary; Ponerine ant; Reproductive division of labor

Indexed keywords

INSECT PROTEIN; INSULIN; INSULIN RECEPTOR;

ANT; BEHAVIORAL RESPONSE; DEVELOPMENTAL BIOLOGY; ENZYME ACTIVITY; FUNCTIONAL MORPHOLOGY; GENE EXPRESSION; GENETIC DIFFERENTIATION; GROWTH RATE; HISTOLOGY; HORMONE; HYBRIDIZATION; INSULATION; LABOR DIVISION; POLYMERASE CHAIN REACTION; QUEEN; REPRODUCTIVE BEHAVIOR; WORKER CASTE;

ANIMAL; ANT; ARTICLE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OOCYTE; OOCYTE DEVELOPMENT; OVARY; PHYSIOLOGY; REPRODUCTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; INSULIN; OOCYTES; OOGENESIS; OVARY; RECEPTOR, INSULIN; REPRODUCTION; SIGNAL TRANSDUCTION;

DIACAMMA; HEXAPODA;

EID: 75749148305     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2009.10.013     Document Type: Article

References (61)

1. Allard D., Ito F., Gobin B., Tsuji K., and Billen J. Differentiation of the reproductive tract between dominant and subordinate workers in the Japanese queenless ant Diacamma sp. Acta Zoologica (Stockholm, Sweden) 86 (2005) 159-166
2. Billen J. Ultrastructure of the worker ovarioles in Formica ants (Hymenoptera: Formicidae). International Journal of Insect Morphology and Embryology 14 (1985) 21-32
3. Bloch G., Borst D.W., Huang Z.Y., Robinson G.E., Cnaani J., and Hefetz A. Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. Journal of Insect Physiology 46 (2000) 47-57
4. Bloch G., Borst D.W., Robinson G.E., Huang Z.Y., and Hefetz A. Effects of social conditions on juvenile hormone mediated reproductive development in Bombus terrestris workers. Physiological Entomology 21 (1996) 257-267
5. Boleli I.C., Paulino-Simões Z.L., and Gentile-Bitondi M.M. Cell death in ovarioles cause permanent sterility in Frieseomelitta varia worker bees. Journal of Morphology 242 (1999) 271-282
6. Bourke A.F.G. Worker reproduction in the higher eusocial hymenoptera. The Quarterly Review of Biology 63 (1988) 291-311
7. Brent C., Peeters C., Dietmann V., Crewe R., and Vargo E. Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi. Journal of Comparative Physiology A 192 (2006) 315-320
8. Brent C.S., and Vargo E.L. Changes in juvenile hormone in biosynthetic rate and whole body content maturing virgin queens of Solenopsis invicta. Journal of Insect Physiology 49 (2003) 967-974
9. Brown M.R., Clark K.D., Gulia M., Zhao Z., Garczynski S.F., Crim J.W., Suderman R.J., and Strand M.R. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proceedings of National Academy of Sciences of the United States of America 105 (2008) 5716-5721
10. Büning J. The Insect Ovary (1994), Chapman & Hall, London
11. Choe J.C. Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager J.C. (Ed). Advances in Myrmecology (1988), E.J. Brill, Leiden 163-187
12. Cooley L., and Theurkauf W.E. Cytoskeletal functions during Drosophila oogenesis. Science 266 (1994) 590-596
13. de Azevedo S.V., and Hartfelder K. The insulin signaling pathway in honey bee (Apis mellifera) caste development-differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. Journal of Insect Physiology 54 (2008) 1064-1071
14. Fernandez R., Tabarini D., Azpiazu N., Frasch M., and Schlessinger J. The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. The EMBO Journal 14 (1995) 3373-3384
15. Fukumoto Y., Abe T., and Taki A. A novel form of colony organization in the "queenless" ant Diacamma rugosum. Physiology and Ecology Japan 26 (1989) 55-61
16. Gadagkar R. Origin and evolution of eusociality: a perspective from studying primitively eusocial wasps. Journal of Genetics 70 (1990) 1-31
17. Garofalo R.S., and Rosen O.M. Tissue localization of Drosophila melanogaster insulin receptor transcripts during development. Molecular and Cellular Biology 8 (1988) 1638-1647
18. Gavis E.R., Lunsford L., Bergsten S.E., and Lehmann R. A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122 (1996) 2791-2800
19. Gotoh A., Sameshima S., Tsuji K., Matsumoto T., and Miura T. Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae). Development Genes and Evolution 215 (2005) 69-77
20. Gutzeit H.O., Zissler D., and Fleig R. Oogenesis in the honeybee Apis mellifera: cytological observations on the formation and differentiation of previtellogenic ovarian follicles. Roux's Archives of Developmental Biology 202 (1993) 181-191
21. Helbling P., and Graf R. Localization of the mosquito insulin receptor homolog (MIR) in reproducing yellow fever mosquitoes (Aedes aegypti). Journal of Insect Physiology 44 (1998) 1127-1135
22. Heming B.S. Insect Development and Evolution (2003), Cornell University Press, New York
23. Higashi S., Ito F., Sugiura N., and Ohkawara K. Worker's age regulates the linear dominance hierarchy in the queenless ponerine ant, Pachycondyla sublaevis (Hymenoptera: Formicidae). Animal Behaviour 47 (1994) 179-184
24. Hölldobler B., and Wilson E.O. The Ants (1990), Harvard University Press, Cambridge, MA, USA
25. Jeanne R.L. Social biology of the neotropical wasp Mischocyttarus drewseni. Bulletin of the Museum of Comparative Zoology 144 (1972) 63-150
26. Khila A., and Abouheif E. Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Proceedings of the National Academy of Sciences of the United States of America 105 (2008) 17884-17889
27. Kikuchi T., Nakagawa T., and Tsuji K. Changes in relative importance of multiple social regulatory forces with colony size in the ant Diacamma sp. from Japan. Animal Behaviour 76 (2008) 2069-2077
28. King R.C. Ovarian Development in Drosophila melanogaster (1970), Academic Press, New York
29. Mirth C.K., and Riddiford L.M. Size assessment and growth control: how adult size is determined in insects. Bioessays 29 (2007) 344-355
30. Monnin T., and Peeters C. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behavioral Ecology 10 (1999) 323-332
31. Nakata K., and Tsuji K. The effect of colony size on conflict over male-production between gamergate and dominant workers in the ponerine ant Diacamma sp. Ethology, Ecology and Evolution 8 (1996) 147-156
32. Oldham S., and Hafen E. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends in Cell Biology 13 (2003) 79-85
33. Osborn P., and Dearden P.K. Non-radioactive in-situ hybridisation to honeybee embryos and ovaries. Apidologie 36 (2005) 113-118
34. Peeters C. The occurrence of sexual reproduction among ant workers. Biological Journal of the Linnean Society 44 (1991) 141-152
35. Peeters C. Monogamy and polygyny in ponerine ants with or without queens. In: Keller L. (Ed). Queen Number and Sociality in Insects (1993), Oxford University Press, Oxford 234-261
36. Peeters C., and Crewe R. Worker reproduction in the ponerine ant Ophthalmopone berthoudi: an alternative form of eusocial organization. Behavioural Ecology and Sociobiology 18 (1985) 29-37
37. Peeters C., and Higashi S. Reproductive dominance controlled by mutilation in the queenless ant Diacamma australe. Naturwissenschaften 76 (1989) 177-180
38. Peeters C., and Tsuji K. Reproductive conflict among ant workers in Diacamma sp. from Japan: dominance and oviposition in the absence of the gamergate. Insectes Sociaux 40 (1993) 119-136
39. Riehle M.A., and Brown M.R. Insulin stimulates ecdysteroid production through a conserved signaling cascade in the mosquito Aedes aegypti. Insect Biochemistry and Molecular Biology 29 (1999) 855-860
40. Riehle M.A., and Brown M.R. Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti. Cell and Tissue Research 308 (2002) 409-420
41. Robinson G.E., Strambi C., Strambi A., and Huang Z.Y. Reproduction in worker honey bees is associated with low juvenile hormone titers and rates of biosynthesis. General and Comparative Endocrinology 87 (1992) 471-480
42. Robinson G.E., and Vargo E.L. Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Archives of Insect Biochemistry and Physiology 35 (1997) 559-583
43. Röseler P.F., Röseler I., and Strambi A. Role of ovaries and ecdysteroids in dominance hierarchy establishment among foundresses of the primitively social wasp, Polistes gallicus. Behavioral Ecology and Sociobiology 18 (1985) 9-13
44. Röseler P.F., Röseler I., Strambi A., and Augier R. Influence of insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp, Polistes gallicus. Behavioral Ecology and Sociobiology 15 (1984) 133-142
45. Roy S.G., Hansen I.A., and Raikhel A.S. Effect of insulin and 20-hydroxyecdysone in the fat body of the yellow fever mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 37 (2007) 1317-1326
46. Ruan Y., Chen C., Cao Y., and Garofalo R.S. The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction. Journal of Biological Chemistry 270 (1995) 4236-4243
47. Schmidt-Capella I.C., and Hartfelder K. Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. Journal of Insect Physiology 44 (1998) 385-391
48. Schmidt-Capella I.C., and Hartfelder K. Juvenile-hormone-dependent interaction of actin and spectrin is crucial for polymorphic differentiation of the larval honey bee ovary. Cell and Tissue Research 307 (2002) 265-272
49. Sommer K., Hölldobler B., and Rembold H. Behavioral and physiological aspects of reproductive control in a Diacamma species from Malaysia (Formicidae, Ponerinae). Ethology 94 (1993) 162-170
50. Tanaka E.D., and Hartfelder K. The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Structure and Development 33 (2004) 431-442
51. Tanaka E.D., and Hartfelder K. Sequence and expression pattern of the germ line marker vasa in honey bees and stingless bees. Genetics and Molecular Biology 32 (2009) 582-593
52. Tsuji K., Egashira K., and Hölldobler B. Regulation of worker reproduction by direct physical contact in the ant Diacamma sp. from Japan. Animal Behaviour 58 (1999) 337-343
53. Turillazzi S., and West-Eberhard M.J. Natural History and Evolution of Paper-Wasps (1996), Oxford University Press, Oxford
54. West-Eberhard M.J. Temporary queens in Metapolybia wasps: non-reproductive helpers without altruism?. Science 200 (1978) 441-443
55. West-Eberhard M.J. Sexual selection, social competition and evolution. Proceedings of the American Philosophical Society 123 (1979) 222-234
56. West-Eberhard M.J. Intragroup selection and the evolution of insect societies. In: Alexander R.D., and Tinkle D.W. (Eds). Natural Selection and Social Behavior: Recent Research and New Theory (1981), Chiron Press, New York 3-17
57. West-Eberhard M.J. Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S., and West-Eberhard M.J. (Eds). Natural History and Evolution of Paper-Wasps (1996), Oxford University Press, New York 290-317
58. Wheeler D. The role of nourishment in oogenesis. Annual Review of Entomology 41 (1996) 407-431
59. Wheeler D.E., Buck N., and Evans J.D. Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Molecular Biology 15 (2006) 597-602
60. Wu Q., and Brown M.R. Signaling and function of insulin-like peptides in insects. Annual Review of Entomology 51 (2006) 1-24
61. Yamane S.O. The colony life cycle of the Sumatran paper wasp Ropalidia (Icariola) variegata jacobsoni (Buysson). With reference to the possible occurrence of serial polygyny. (Hymenoptera Vespidae). Monitore Zoologico Italiano 20 (1986) 135-161