Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Hunt, James H ^a,b   Wolschin, Florian ^c,d   Henshaw, Michael T ^e   Newman, Thomas C ^f   Toth, Amy L ^f,g   Amdam, Gro V ^c,d  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NATIONAL EVOLUTIONARY SYNTHESIS CENTER   (United States)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^d ARIZONA STATE UNIVERSITY   (United States)

^e GRAND VALLEY STATE UNIVERSITY   (United States)

^f UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^g PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT PROTEIN; MESSENGER RNA; PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAPAUSE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EXPRESSED SEQUENCE TAG; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; INSECT CASTE; LARVAL DEVELOPMENT; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PEPTIDE ANALYSIS; PHENOTYPE; POLISTES METRICUS; PROTEIN FUNCTION; PROTEOMICS; SEX DETERMINATION; SIGNAL TRANSDUCTION; WASP; ANIMAL; DISCRIMINANT ANALYSIS; EPIDEMIOLOGY; GENDER AND SEX; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LARVA; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; SOCIAL DOMINANCE;

APIS MELLIFERA; APOIDEA; HEXAPODA; HYMENOPTERA; POLISTES; POLISTES METRICUS; POLISTINAE;

ANIMALS; BIAS (EPIDEMIOLOGY); CHROMATOGRAPHY, LIQUID; DISCRIMINANT ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, INSECT; INSECT PROTEINS; LARVA; MASS SPECTROMETRY; PEPTIDES; RNA, MESSENGER; SEX DETERMINATION (GENETICS); SOCIAL DOMINANCE; WASPS;

EID: 77956277107     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010674     Document Type: Article

References (85)

1. Hölldobler B, Wilson EO (1990) The ants. Cambridge: Belknap Press of Harvard University Press. xii732 p.
2. Michener CD (1974) The social behavior of the bees: A comparative study. Cambridge: Belknap Press of Harvard University Press. xii 404 p.
3. Wilson EO (1971) The insect societies. Cambridge: Belknap Press of Harvard University Press. x 548 p.
4. Greene A (1991) Dolichovespula and Vespula. In: Ross KG, Matthews RW, eds. The social biology of wasps. Ithaca: Comstock Publishing Associates, Cornell University Press. pp 263-305.
5. Matsuura M (1991) Vespa and Provespa. In: Ross KG, Matthews RW, eds. The social biology of wasps. Ithaca: Comstock Publishing Associates, Cornell University Press. pp 232-262.
6. Noll FB, Wenzel JW, Zucchi R (2004) Evolution of caste in Neotropical swarmfounding wasps (Hymenoptera: Vespidae; Epiponini). American Museum Novitates 3467: 1-24.
7. Batra SWT (1966) Nests and social behavior of halictine bees of India. Indian Journal of Entomology 28: 375-393.
8. Sullivan JD, Strassmann JE (1984) Physical variability among nest foundresses in the polygynous social wasp, Polistes annularis. Behavioral Ecology and Sociobiology 15: 249-256.
9. Hunt JH (2007) The evolution of social wasps. New York: Oxford University Press. xxi 259 p.
10. O'Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annual Review of Entomology 43: 323-346.
11. Reeve HK (2001) In search of unified theories in sociobiology: Help from social wasps. In: Dugatkin LA, ed. Model Systems in Behavioral Ecology. Princeton: Princeton University Press. pp 57-71.
12. Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. The American Naturalist 128: 13-34.
13. Sumner S, Kelstrup H, Fanelli D (2010) Reproductive constraints, direct fitness and indirect fitness benefits explain helping behaviour in the primitively eusocial wasp, Polistes canadensis. Proceedings of the Royal Society of London B 277: 1721-1728.
14. Marchal P (1897) La castration nutriciale chez les Hyme ́nopteres sociaux. Comptes rendus des se ́ances de la Socie ́te ́ de Biologie (Paris) 1897: 556-557.
15. Pardi L (1948) Dominance order in Polistes wasps. Physiological Zoology 21: 1-13.
16. West Eberhard MJ (1969) The social biology of polistine wasps. Miscellaneous Publications, Museum of Zoology, University of Michigan 140: 1-101.
17. Reeve HK (1991) Polistes. In: Ross KG, Matthews RW, eds. The social biology of wasps. Ithaca: Comstock Publishing Associates, Cornell University Press. pp 99-148.
18. Reeve HK, Peters JM, Nonacs P, Starks PT (1998) Dispersal of first ''workers'' in social wasps: casuses and implications of an alternative reproductive strategy. Proceedings of the National Academy of Sciences USA 95: 13737-13742.
19. Cini A, Dapporto L (2009) Atumnal helpers of Polistes dominulus represent a distinct behavioural phenotype. Annales Zoologici Fennici 46: 423-430.
20. Dapporto L, Palagi E, Turillazzi S (2005) Sociality outside the nest: helpers inpre-hibernating clusters of Polistes dominulus. Annales Zoologici Fennici 42: 135-139.
21. Hunt JH, Amdam GV (2005) Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308: 264-267.
22. Alam SM (1958) Some interesting revelations about the nest of Polistes hebroeus Fabr. (Vespidae, Hymenoptera) - the common yellow wasp of India. Proceedings of the Zoological Society of Calcutta 11: 113-122.
23. Kundu HL (1967) Observations on Polistes hebraeus (Hymenoptera). Birla Institute of Technological Science, Journal (Pilani) 1: 152-161.
24. Keeping MG (2002) Reproductive and worker castes in the primitively eusocial wasp Belonogaster petiolata (DeGeer) (Hymenoptera: Vespidae): evidence for reimaginal differentiation. Journal of Insect Physiology 48: 867-879.
25. Wenzel JW (1992) Extreme queen-worker dimorphism in Ropalidia ignobilis, a small-colony wasp (Hymenoptera: Vespidae). Insectes Sociaux 39: 31-43.
26. Gadagkar R, Bhagavan S, Chandrashekara K, Vinutha C (1991) The role of larval nutrition in pre-imaginal biasing of caste in the primitively eusocial wasp Ropalidia marginata (Hymenoptera: Vespidae). Ecological Entomology 16: 435-440.
27. Gadagkar R, Bhagavan S, Malpe R, Vinutha C (1990) On reconfirming the evidence for pre-imaginal caste bias in a primitively eusocial wasp. Proceedings of the Indian Academy of Sciences (Animal Science) 99: 141-150.
28. Gadagkar R, Vinutha C A S, Gore AP (1988) Pre-imaginal biasing of caste in a primitively eusocial insect. Proceedings of the Royal Society of London B 233: 175-189.
29. Eickwort K (1969) Separation of the castes of Polistes exclamans and notes on its biology (Hym.: Vespidae). Insectes Sociaux 16: 67-72.
30. Strassmann JE, Lee RE, Rojas RR, Baust JG (1984) Caste and sex differences in cold-hardiness in the social wasps, Polistes annularis and Polistes exclamans (Hymenoptera, Vespidae). Insectes Sociaux 31: 291-301.
31. Karsai I, Hunt JH (2002) Food quantity affects traits of offspring in the paper wasp Polistes metricus (Hymenoptera: Vespidae). Environmental Entomology 31: 99-106.
32. Toth AL, Bilof KBJ, Henshaw MT, Hunt JH, Robinson GE (2009) Lipid stores, ovary development, and brain gene expression in Polistes females. Insectes Sociaux 56: 77-84.
33. Toth AL, Varala K, Newman TC, Miguez FE, Hutchison S, et al. (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318: 441-444.
34. Toth AL, Varala K, Henshaw MT, Rodriguez-Zas S, Hudson ME, et al. (2010) Brain transcriptomic analysis in paper wasps identifies genes associated with behavior across social insect lineages. Proceedings of the Royal Society of London B. doi:10.1098/rspb.2010.0090 published online March 17, 2010.
35. Bohm MK (1972) Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus. Journal of Insect Physiology 18: 1875-1883.
36. Wolschin F, Amdam GV (2007) Comparative proteomics reveal characteristics of life-history transitions in a social insect. Proteome Science 5: Article #10.
37. Hunt JH, Kensinger BA, Kossuth J, Henshaw MT, Norberg K, et al. (2007) From casteless to castes - a diapause pathway underlies the gyne phenotype in Polistes paper wasps. Proceedings of the National Academy of Sciences USA 104: 14020-14025.
38. Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annual Review of Entomology 53: 209-230.
39. Liebert AE, Johnson RN, Switz GT, Starks PT (2004) Triploid females and diploid males: underreported phenomena in Polistes wasps? Insectes Sociaux 51: 205-211.
40. Toth AL, Varala K, Henshaw MT, Rodriguez-Zas SL, Hudson ME, et al. (2010) Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proceedings of the Royal Society of London B. doi:10.1098/rspb.2010.0090 published online March 17, 2010.
41. Hunt JH, Buck NA, Wheeler DE (2003) Storage proteins in vespid wasps: characterization, developmental pattern, and occurrence in adults. Journal of Insect Physiology 49: 785-794.
42. Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE (2003) CGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. Journal of Experimental Biology 206: 2507-2515.
43. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, et al. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences USA 104: 7128-7133.
44. Ament SA, Corona M, Pollock HS, Robinson GE (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proceedings of the National Academy of Sciences USA 105: 4226-4231.
45. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302: 296-299.
46. Evans JD, Wheeler DE (1999) Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proceedings of the National Academy of Sciences USA 96: 5575-5580.
47. Corona M, Estrada E, Zurita M (1999) Differential expression of mitochondrial genes between queens and workers during caste determination in the honeybee Apis mellifera. The Journal of Experimental Biology 202.
48. Wheeler DE, Buck N, Evans JD (2006) Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Molecular Biology 15: 597-602.
49. Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, et al. (2007) The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2(6): e509.
50. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic logical alignment search tool. Journal of Molecular Biology 215: 403-410.
51. Wessel D, Flugge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Analytical Biochemistry 138: 141-143.
52. Wolschin F, Amdam GV (2007) Plasticity and robustness of protein patterns during reversible development in the honey bee (Apis mellifera). Analytical and Bioanalitical Chemistry 389: 1095-1100.
53. Geer LY, Markey SP, Kowalak JA, Wagner L, Xu M, et al. (2004) Open mass spectrometry search algorithm. Journal of Proteome Research 3: 958-964.
54. Wolschin F, Gadau J (2009) Deciphering proteomic signatures of early diapause in Nasonia. PLoS ONE 4: e6394.
55. Wolschin F, Munch D, Amdam GV (2009) Structural and proteomic analyses reveal regional brain differences during honeybee aging. Journal of Experimental Biology 212: 4027-4032.
56. Hunt JH, Dove MA (2002) Nourishment affects colony demographics in the paper wasp Polistes metricus. Ecological Entomology 27: 467-474.
57. Rossi AM, Hunt JH (1988) Honey supplementation and its developmental consequences: evidence for food limitation in a paper wasp, Polistes metricus. Ecological Entomology 13: 437-442.
58. Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Molecular Cell Biology 19: 1720-1730.
59. Amdam GV, Norberg K, Hagen A, Omholt SW (2003) Social exploitation of vitellogenin. Proceedings of the National Academy of Sciences USA 100: 1799-1802.
60. Amdam GV, Norberg K, Fondrk MK, Page RE, Jr. (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proceedings of the National Academy of Sciences USA 101: 11350-11355.
61. Page RE, Amdam GV (2007) The making of a social insect: developmental architectures of social design. BioEssays 29: 334-343.
62. Flannagan RD, Tammariello SP, Joplin KH, Cikra-Ireland RA, Yocum GD, et al. (1998) Diapause-specific gene expression in pupae of the flesh fly Sarcophaga crassipalpis. Proceedings of the National Academy of Sciences USA 95: 5616-5620.
63. Rinehart JP, Denlinger DL (2000) Heat-shock protein 90 is down-regulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress. Insect Molecular Biology 9: 641-645.
64. Yocum GD, Joplin KH, Denlinger DL (1998) Upregulation of a 23 kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 28: 677-682.
65. Yocum GD (2001) Differential expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. Journal of Insect Physiology 47: 1139-1145.
66. Rinehart JP, Yocum GD, Denlinger DL (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 30: 515-521.
67. Lewis DK, Spurgeon D, Sappington TW, Keeley LL (2002) A hexamerin protein, AgSP-1, is associated with diapause in the boll weevil. Journal of Insect Physiology 48: 887-901.
68. Denlinger DL (2002) Regulation of diapause. Annual Review of Entomology 47: 3-122.
69. Williams KD, Busto M, Suster ML, So AK-C, Ben-Shahar Y, et al. (2006) Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proceedings of the National Academy of Sciences USA 103: 15911-15915.
70. Sim C, Denlinger DL (2009) A shut-down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens. Insect Molecular Biology 18: 325-332.
71. Sim C, Denlinger DL (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proceedings of the National Academy of Sciences USA 105: 6777-6781.
72. Pereboom JJM, Jordan WC, Sumner S, Hammond RL, Bourke AFG (2005) Differential gene expression in queen-worker caste determination in bumblebees. Proceedings of the Royal Society of London B 272: 1145-11562.
73. Sumner S, Pereboom JJM, Jordan WC (2006) Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proceedings of the Royal Society of London B 273: 19-26.
74. Kawamura K, Shibata T, Saget O, Peel D, Bryant PJ (1999) A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development 126: 211-219.
75. Sweeney NT, Brenman JE, Jan YN, Gao FB (2006) The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Current Biology 16: 1006-1011.
76. Van der Horst DJ, Roosendaal SD, Rodenburg KW (2009) Circulatory lipid transport: lipoprotein assembly and function from an evolutionary perspective. Molecular and Cellular Biochemistry 326: 105-119.
77. Hunt JH, Brodie RJ, Carithers TP, Goldstein PZ, Janzen DH (1999) Dry season migration by Costa Rican lowland paper wasps to high elevation cold dormancy sites. Biotropica 31: 192-196.
78. Gobbi N, Noll FB, Penna MAH (2006) ''Winter'' aggregations, colony cycle, and seasonal phenotypic change in the paper wasp Polistes versicolor in Brazil. Naturwissenschaften 93: 487-494.
79. Hoffman EA, Goodisman MAD (2007) Gene expression and the evolution of phenotypic diversity in social wasps. BMC Biology 5: 23.
80. Judd TM, Magnus RM, Fasnacht MP (2010) A nutritional profile of the social wasp Polistes metricus: Differences in nutrient levels between castes and changes within castes during the annual life cycle. Journal of Insect Physiology 56: 42-56.
81. Mead F, Pratte M (2002) Prey supplementation increases productivity in the social wasp Polistes dominulus Christ (Hymenoptera Vespidae). Ethology Ecology & Evolution 14: 111-128.
82. Winston ML (1987) The biology of the honey bee. Cambridge: Harvard University Press. xiii 281 p.
83. Judice CC, Carazzole MF, Festa F, Sogayar MC, Hartfelder K, et al. (2006) Gene expression profiles underlying alternative caste phenotypes in a highly eusocial bee, Melipona quadrifasciata. Insect Molecular Biology 15: 33-44.
84. Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simões ZLP, et al. (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology 2007 7: 70. doi:10.1186/1471-1213X-1187-1170.
85. Hayward SAL, Pavlides SC, Tammariello SP, Rinehart JP, Denlinger DL (2005) Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. Journal of Insect Physiology 51: 631-640.