Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus

PLoS Genetics

Volumn 9, Issue 8, 2013, Pages

  Corona, Miguel ^a,b   Libbrecht, Romain ^a,c   Wurm, Yannick ^a,d   Riba Grognuz, Oksana ^a   Studer, Romain A ^e   Keller, Laurent ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; VITELLOGENIN;

ANIMAL BEHAVIOR; ANT; ARTICLE; CONTROLLED STUDY; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENETIC SELECTION; INSECT GENETICS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PHYLOGENETIC TREE; POGONOMYRMEX BARBATUS; QUANTITATIVE ANALYSIS; QUEEN (INSECT); REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VG1 GENE; VITELLOGENIN GENE; WORKER (INSECT);

ANIMALS; ANTS; BEES; BEHAVIOR, ANIMAL; EVOLUTION, MOLECULAR; GENOME, INSECT; PHYLOGENY; REPRODUCTION; VITELLOGENINS;

EID: 84884626538     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003730     Document Type: Article

References (79)

1. Wilson EO (1971) The insects societies. Cambridge: Harvard University Press.
2. Hölldobler B, Wilson EO (1990) The Ants. Cambridge, Mass: Harvard University Press.
3. Robinson GE, (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37: 637-665.
4. Gordon D, Chu J, Lillie A, Tissot M, Pinter N, (2005) Variation in the transition from inside to outside work in the red harvester ant Pogonomyrmex barbatus. Insectes Sociaux 52: 212-217.
5. Andersson M, (1984) The Evolution of Eusociality. Annu Rev Ecol Syst 15: 165-189.
6. Cardinal S, Danforth BN, (2011) The antiquity and evolutionary history of social behavior in bees. PLoS One 6: e21086.
7. Bourke AFG, Franks NR (1995) Social Evolution in Ants. Princeton, NJ.: Princeton University Press.
8. Ingram K, Kleeman L, Peteru S, (2011) Differential regulation of the foraging gene associated with task behaviors in harvester ants. BMC Ecol 11: 19.
9. Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE, (2002) Influence of gene action across different time scales on behavior. Science 296: 741-744.
10. Lucas C, Sokolowski MB, (2009) Molecular basis for changes in behavioral state in ant social behaviors. Proc Natl Acad Sci U S A 106: 6351-6356.
11. Ingram K, Krummey S, LeRoux M, (2009) Expression patterns of a circadian clock gene are associated with age-related polyethism in harvester ants, Pogonomyrmex occidentalis. BMC Ecol 9: 7.
12. Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang YC, et al. (2013) A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493: 664-668.
13. West-Eberhard MJ (1987) Flexible strategy and social evolution. In: Ito Y, Brown, J. L., Kikkawa, J., editor. Animal Societies: Theories and Facts. Tokyo: Japan Sci. Soc. Press. pp. 35-51.
14. West-Eberhard M (1996) Wasp societies as microcosms for the study of development and evolution. In: West-Eberhard STaMJ, editor. Natural History and Evolution of Paper- Wasps. New York, USA: Oxford Unviersity Press.
15. 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. Proc Natl Acad Sci U S A 101: 11350-11355.
16. Amdam GV, Csondes A, Fondrk MK, Page RE Jr, (2006) Complex social behaviour derived from maternal reproductive traits. Nature 439: 76-78.
17. Siegel A (2011) Ovarian Regulation of Honey Bee (Apis mellifera) Foraging Division of Labor [Doctoral Dissertation]: Arisona State University. 122 p.
18. Lin H, Winston ML, Haunerland NH, Slessor KN, (1999) Influence of age and population size on ovarian development, and of trophallaxis on ovarian development and vitellogenin titers of queenless worker honey bee (Hymenoptera: Apidae). Can Entomol 13: 695-706.
19. Engels W, (1974) Occurrence and significance of vitellogenin in female castes of social Hymenoptera. Am Zool 14: 1229-1237.
20. Page R, Fondrk MK, (1995) The effects of colony level selection on the social organization of honey bee (Apis mellifera L.) colonies-colony level components of pollen hoarding. Behav Ecol Sociobiol 36: 135-144.
21. Snodgrass RE (1956) Anatomy of the Honey Bee. Ithaca, NY: Cornell Univ Press.
22. Jackson JT, Tarpy DR, Fahrbach SE, (2011) Histological estimates of ovariole number in honey bee queens, Apis mellifera, reveal lack of correlation with other queen quality measures. J Insect Sci 11: 82.
23. Haydak MH, (1970) Honey bee nutrition. Annu Rev Entomol 15: 143-156.
24. Cremonez T, De Jong D, Bitondi MM, (1998) Quantification of Hemolymph Proteins as a Fast Method for Testing Protein Diets for Honey Bees (Hymenoptera: Apidae). J Econ Entomol 91: 1284-1289.
25. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, et al. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A 104: 7128-7133.
26. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV, (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5: e62.
27. Marco Antonio DS, Guidugli-Lazzarini KR, do Nascimento AM, Simões ZL, Hartfelder K, (2008) RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. Naturwissenschaften 95: 953-961.
28. Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE, (2006) Phylogeny of the ants: diversification in the age of angiosperms. Science 312: 101-104.
29. Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, et al. (2010) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci U S A 108: 5679-5684.
30. Khila A, Abouheif E, (2010) Evaluating the role of reproductive constraints in ant social evolution. Philos Trans R Soc Lond B Biol Sci 365: 617-630.
31. Bourke AFG, (1988) Worker Reproduction in the Higher Eusocial Hymenoptera. The Quarterly Review of Biology 63: 291-311.
32. Smith C, Schoenick C, Anderson KE, Gadau J, Suarez AV, (2007) Potential and realized reproduction by different worker castes in queen-less and queen-right colonies of Pogonomyrmex badius. Insect Soc 54: 260-267.
33. Smith C, Smith CD, Robertson HM, Helmkampf M, Zimin A, et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci U S A 108: 5667-5672.
34. Hancock J, (2005) Gene factories, microfunctionalization and the evolution of gene families. Trends Genet 21: 591-595.
35. Babin P, Bogerd J, Kooiman FP, Van Marrewijk WJ, Van der Horst DJ, (1999) Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor. J Mol Evol 49: 150-160.
36. Khalil S, Donohue KV, Thompson DM, Jeffers LA, Ananthapadmanaban U, et al. (2011) Full-length sequence, regulation and developmental studies of a second vitellogenin gene from the American dog tick, Dermacentor variabilis. J Insect Physiol 57: 400-408.
37. Suen G, Teiling C, Li L, Holt C, Abouheif E, et al. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet 7: e1002007.
38. Nygaard S, Zhang G, Schiøtt M, Li C, Wurm Y, et al. (2011) The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res 21: 1339-1348.
39. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, et al. (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1071.
40. Smith C, Zimin A, Holt C, Abouheif E, Benton R, et al. (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci U S A 108: 5673-5678.
41. Li A, Sadasivam M, Ding JL, (2003) Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E. The first three ligand-binding repeats of VtgR interact with the amino-terminal region of Vtg. J Biol Chem 278: 2799-2806.
42. Wilson EO, Hölldobler B, (2005) The rise of the ants: a phylogenetic and ecological explanation. Proc Natl Acad Sci U S A 102: 7411-7414.
43. West-Eberhard M (1996) Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S W-EM, editor. Natural History and Evolution of Paper-Wasps. Oxford: Oxford University Press. pp. 290-317.
44. Gadagkar R, (1997) The evolution of caste polymorphism in social insects: Genetic release followed by diversifying evolution. J Genet 76: 167-179.
45. Acher R, (1980) Molecular evolution of biologically active polypeptides. Proc R Soc Lond B Biol Sci 210: 21-43.
46. Hawkins M, Godwin J, Crews D, Thomas P, (2005) The distributions of the duplicate oestrogen receptors ER-beta a and ER-beta b in the forebrain of the Atlantic croaker (Micropogonias undulatus): evidence for subfunctionalization after gene duplication. Proc Biol Sci 272: 633-641.
47. Kent C, Issa A, Bunting AC, Zayed A, (2011) Adaptive evolution of a key gene affecting queen and worker traits in the honey bee, Apis mellifera. Mol Ecol 20: 5226-5235.
48. Havukainen H, Halskau Ø, Amdam GV, (2011) Social pleiotropy and the molecular evolution of honey bee vitellogenin. Mol Ecol 20: 5111-5113.
49. Blank S, Seismann H, McIntyre M, Ollert M, Wolf S, et al. (2013) Vitellogenins Are New High Molecular Weight Components and Allergens (Api m 12 and Ves v 6) of Apis mellifera and Vespula vulgaris Venom. PLoS One 8: e62009.
50. Toth A, Varala K, Newman TC, Miguez FE, Hutchison SK, et al. (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318: 441-444.
51. Scharf M, Wu-Scharf D, Zhou X, Pittendrigh BR, Bennett GW, (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol Biol 14: 31-44.
52. Piulachs M, Guidugli KR, Barchuk AR, Cruz J, Simões ZL, et al. (2003) The vitellogenin of the honey bee, Apis mellifera: structural analysis of the cDNA and expression studies. Insect Biochem Mol Biol 33: 459-465.
53. Dolezal A, Johnson J, Hölldobler B, Amdam GV, (2013) Division of labor is associated with age-independent changes in ovarian activity in Pogonomyrmex californicus harvester ants. J Insect Physiol 59: 519-524.
54. Camazine S, Crailsheim K, Hrassnigg N, Robinson GE, Leonhard B, et al. (1998) Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.). Apidologie 29: 113-126.
55. Crailsheim K, (1998) Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie 29: 97-112.
56. Fujita T, Kozuka-Hata H, Ao-Kondo H, Kunieda T, Oyama M, Kubo T, (2013) Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee. J Proteome Res 12: 404-411.
57. Rutz W, Luscher M, (1974) The occurrence of vitellogenin in workers and queens of Apis mellifera and the possibility of its transmission to the queen. J Insect Physiol 20: 897-909.
58. Trenczek T, Engels W, (1986) Occurrence of vitellogenin in drone honey bees (Apis mellifera). Int J Invert Reprod and Dev 10: 307-311.
59. Amdam GV, Omholt SW, (2002) The regulatory anatomy of honeybee lifespan. J Theor Biol 216: 209-228.
60. Cardoen D, Wenseleers T, Ernst UR, Danneels EL, Laget D, et al. (2011) Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. Mol Ecol 20: 4070-4084.
61. Franks N, Scovell E, (1983) Dominance and reproductive success among slave-making worker ants. Nature 304: 724-725.
62. Bourke A, (1988) Worker reproduction in the higher Eusocial hymenoptera. Quarterly Review of Biology 63: 291-311.
63. Wurm Y, Uva P, Ricci F, Wang J, Jemielity S, et al. (2009) Fourmidable: a database for ant genomics. BMC Genomics 10: 5.
64. Goto N, Prins P, Nakao M, Bonnal R, Aerts J, et al. (2010) BioRuby: bioinformatics software for the Ruby programming language. Bioinformatics 26: 2617-2619.
65. Holt C, Yandell M, (2011) Maker2: an annotation pipeline and genome- database management tool for second-generation genome projects. BMC Bioinformatics 12: 491.
66. Lewis S, Searle SM, Harris N, Gibson M, Lyer V, et al. (2002) Apollo: a sequence annotation editor. Genome Biol 3: RESEARCH0082.
67. Tóth A, Hausknecht A, Krisai-Greilhuber I, Papp T, Vágvölgyi C, et al. (2013) Iteratively refined guide trees help improving alignment and phylogenetic inference in the mushroom family Bolbitiaceae. PLoS One 8: e56143.
68. Capella-Gutiérrez S, Gabaldón T, (2013) Measuring guide-tree dependency of inferred gaps in progressive aligners. Bioinformatics 29: 1011-1017.
69. Katoh K, Toh H, (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
70. Capella-Gutiérrez S, Silla-Martìnez JM, Gabaldón T, (2009) Trimal: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
71. Stamatakis A, (2006) Raxml-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
72. Junier T, Zdobnov EM, (2010) The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 26: 1669-1670.
73. Löytynoja A, Goldman N, (2008) Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science 320: 1632-1635.
74. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
75. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
76. Rychlik W (2007) OLIGO 7 Primer Analysis Software. Methods in Molecular Biology. Totowa, NJ: Humana Press Inc. pp. 35-59.
77. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
78. Bates D, (2005) Fitting linear mixed models in R. R News 5: 27-30.
79. Baayen R (2008) Analyzing linguistic data: a practical introduction to statistics using R. Cambridge: Cambridge University Press.