One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the “winner”) in pleometrotic associations survives and takes the lead of the young colony while the others (the “losers”) are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.
Vyšlo v časopise: Sociogenomics of Cooperation and Conflict during Colony Founding in the Fire Ant. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003633 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003633
1. HofmannHA (2003) Functional genomics of neural and behavioral plasticity. Journal of Neurobiology 54 : 272–282.
2. RossKG, KellerL (1995) Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annual Review of Ecology and Systematics 631–656.
3. RobinsonGE (2004) Beyond Nature and Nurture. Science 304 : 397–399.
4. RobinsonGE, FernaldRD, ClaytonDF (2008) Genes and Social Behavior. Science 322 : 896–900.
5. ZayedA, RobinsonGE (2012) Understanding the Relationship Between Brain Gene Expression and Social Behavior: Lessons from the Honey Bee. Annual Review of Genetics 46 : 591–615.
6. Duarte A, Weissing FJ, Pen I, Keller L (2011) An Evolutionary Perspective on Self-Organized Division of Labor in Social Insects. In: Futuyma DJ, Shaffer HB, Simberloff D, editors. Annual Review of Ecology, Evolution, and Systematics. Volume 42. Palo Alto: Annual Reviews. pp. 91–110.
7. DolezalAG, BrentCS, HolldoblerB, AmdamGV (2012) Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus. Journal of Experimental Biology 215 : 454–460.
8. SmithCR, TothAL, SuarezAV, RobinsonGE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nature Reviews Genetics 9 : 735–748.
9. Hölldobler B, Wilson EO (1990) The ants. Cambridge, MA: Belknap Press. 732 pp.
10. BernasconiG, StrassmannJE (1999) Cooperation among unrelated individuals: the ant foundress case. Trends in Ecology & Evolution 14 : 477–482.
11. KukukP, SageG (1994) Reproductivity and relatedness in a communal halictine bee Lasioglossum (Chilalictus) hemichalceum. Insectes Sociaux 41 : 443–455.
12. RoisinY (1993) Selective pressures on pleometrosis and secondary polygyny: a comparison of termites and ants. Queen number and sociality in insects 402–421.
13. ZanetteLRS, FieldJ (2011) Founders versus joiners: group formation in the paper wasp Polistes dominulus. Animal Behaviour 82 : 699–705.
14. QuellerDC, ZacchiF, CervoR, TurillazziS, HenshawMT, et al. (2000) Unrelated helpers in a social insect. Nature 405 : 784–787.
15. LiebertA, HuiJ, NonacsP, StarksP (2008) Extreme Polygyny: Multi-seasonal “Hypergynous” Nesting in the Introduced Paper Wasp Polistes dominulus. Journal of Insect Behavior 21 : 72–81.
16. RissingSW, PollockGB, HigginsMR, HagenRH, SmithDR (1989) Foraging specialization without relatedness or dominance among co-founding ant queens. Nature 338 : 420–422.
17. JeansonR, FewellJH (2008) Influence of the social context on division of labor in ant foundress associations. Behavioral Ecology 19 : 567–574.
18. TschinkelW, HowardD (1983) Colony founding by pleometrosis in the fire ant, Solenopsis invicta. Behavioral Ecology and Sociobiology 12 : 103–113.
19. BalasMT, AdamsES (1996) The dissolution of cooperative groups: mechanisms of queen mortality in incipient fire ant colonies. Behavioral Ecology and Sociobiology 38 : 391–399.
20. BernasconiG, KellerL (1998) Phenotype and individual investment in cooperative foundress associations of the fire ant, Solenopsis invicta. Behavioral Ecology 9 : 478–485.
21. BernasconiG, KriegerMJB, KellerL (1997) Unequal partitioning of reproduction and investment between cooperating queens in the fire ant, Solenopsis invicta, as revealed by microsatellites. Proceedings of the Royal Society B-Biological Sciences 264 : 1331–1336.
22. AdamsES, TschinkelWR (1995) Effects of foundress number on brood raids and queen survival in the fire ant Solenopsis invicta. Behavioral Ecology and Sociobiology 37 : 233–242.
23. BalasMT, AdamsES (1996) Nestmate discrimination and competition in incipient colonies of fire ants. Animal Behaviour 51 : 49–59.
24. MarkinGP, DillierJH, CollinsHL (1972) Colony founding by queens of red imported fire ant, Solenopsis invicta - Hymenoptera - Formicidae. Annals of the Entomological Society of America 65 : 1053–1058.
25. TschinkelWR (1995) Stimulation of fire ant queen fecundity by a highly specific brood stage. Annals of the Entomological Society of America 88 : 876–882.
26. BernasconiG, KellerL (1996) Reproductive conflicts in cooperative associations of fire ant queens (Solenopsis invicta). Proceedings of the Royal Society B-Biological Sciences 263 : 509–513.
27. WurmY, WangJ, Riba-GrognuzO, CoronaM, NygaardS, et al. (2011) The genome of the fire ant Solenopsis invicta. Proceedings of the National Academy of Sciences of the United States of America 108 : 5679–5684.
28. HuangDW, ShermanBT, LempickiRA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37 : 1–13.
29. HuangDW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4 : 44–57.
30. KanehisaM, GotoS, SatoY, FurumichiM, TanabeM (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40: D109–D114.
31. HuZL, BaoJ, ReecyJM (2008) CateGOrizer: A Web-Based Program to Batch Analyze Gene Ontology Classification Categories. Online Journal of Bioinformatics 9 : 108–112.
32. SturnA, QuackenbushJ, TrajanoskiZ (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18 : 207–208.
33. ValanneS, MyllymäkiH, KallioJ, SchmidMR, KleinoA, et al. (2010) Genome-Wide RNA Interference in Drosophila Cells Identifies G Protein-Coupled Receptor Kinase 2 as a Conserved Regulator of NF-kB Signaling. The Journal of Immunology 184 : 6188–6198.
34. Drummond-BarbosaD, SpradlingAC (2004) alpha-Endosulfine, a potential regulator of insulin secretion, is required for adult tissue growth control in Drosophila. Developmental Biology 266 : 310–321.
35. VieiraFG, RozasJ (2011) Comparative Genomics of the Odorant-Binding and Chemosensory Protein Gene Families across the Arthropoda: Origin and Evolutionary History of the Chemosensory System. Genome Biology and Evolution 3 : 476–490.
36. MinK-T, BenzerS (1999) Preventing Neurodegeneration in the Drosophila Mutant bubblegum. Science 284 : 1985–1988.
37. WangPY, NerettiN, WhitakerR, HosierS, ChangCY, et al. (2009) Long-lived Indy and calorie restriction interact to extend life span. Proceedings of the National Academy of Sciences of the United States of America 106 : 9262–9267.
38. PearsonJC, JuarezMT, KimM, DrivenesØ, McGinnisW (2009) Multiple transcription factor codes activate epidermal wound-response genes in Drosophila. Proceedings of the National Academy of Sciences 106 : 2224–2229.
39. RiemenspergerT, IsabelG, CoulomH, NeuserK, SeugnetL, et al. (2011) Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proceedings of the National Academy of Sciences of the United States of America 108 : 834–839.
40. HouotB, BousquetFo, FerveurJ-Fo (2010) The Consequences of Regulation of desat1 Expression for Pheromone Emission and Detection in Drosophila melanogaster. Genetics 185 : 1297–1309.
41. ShinodaT, ItoyamaK (2003) Juvenile hormone acid methyltransferase: a key regulatory enzyme for insect metamorphosis. Proceedings of the National Academy of Sciences of the United States of America 100 : 11986–11991.
42. AmdamGV (2011) Social context, stress, and plasticity of aging. Aging Cell 10 : 18–27.
43. WheelerDE, BuckN, EvansJD (2006) Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Molecular Biology 15 : 597–602.
44. AmentSA, ChanQW, WheelerMM, NixonSE, JohnsonSP, et al. (2011) Mechanisms of stable lipid loss in a social insect. J Exp Biol 214 : 3808–3821.
45. AmentSA, CoronaM, PollockHS, RobinsonGE (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. PNAS 105 : 4226–4231.
46. BakerN, WolschinF, AmdamGV (2012) Age-related learning deficits can be reversible in honeybees Apis mellifera. Experimental Gerontology 47 : 764–772.
47. ZhanM, YamazaH, SunY, SinclairJ, LiH, et al. (2007) Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster. Genome Research 17 : 1236–1243.
48. EvansJD, AronsteinK, ChenYP, HetruC, ImlerJL, et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology 15 : 645–656.
49. KunteAS, MatthewsKA, RawsonRB (2006) Fatty acid auxotrophy in Drosophila larvae lacking SREBP. Cell Metabolism 3 : 439–448.
50. ShafqatN, MarschallHU, FillingC, NordlingE, WuXQ, et al. (2003) Expanded substrate screenings of human and Drosophila type 10 17-hydroxysteroid dehydrogenases (HSDs) reveal multiple specificities in bile acid and steroid hormone metabolism: characterization of multifunctional 3/7/7/17/20/21-HSD. The Biochemical Journal 376 : 49–60.
51. ChengW, SongC, AnjumKM, ChenM, LiD, et al. (2011) Coenzyme Q plays opposing roles on bacteria/fungi and viruses in Drosophila innate immunity. International journal of immunogenetics 38 : 331–337.
52. LiuJ, WuQ, HeD, MaT, DuL, et al. (2011) Drosophila sbo regulates lifespan through its function in the synthesis of coenzyme Q in vivo. Journal of Genetics and Genomics [Yi chuan xue bao] 38 : 225–234.
53. LeePT, LinHW, ChangYH, FuTF, DubnauJ, et al. (2011) Serotonin-mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 108 : 13794–13799.
54. CostaA, JanE, SarnowP, SchneiderD (2009) The Imd pathway is involved in antiviral immune responses in Drosophila. Plos One 4: e7436.
55. HowellL, SampsonCJ, XavierMJ, BolukbasiE, HeckMM, et al. (2012) A directed miniscreen for genes involved in the Drosophila anti-parasitoid immune response. Immunogenetics 64 : 155–161.
56. ScherferC, KarlssonC, LosevaO, BidlaG, GotoA, et al. (2004) Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Current Biology 14 : 625–629.
57. WangXH, AliyariR, LiWX, LiHW, KimK, et al. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312 : 452–454.
58. KimM, LeeJH, LeeSY, KimE, ChungJ (2006) Caspar, a suppressor of antibacterial immunity in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 103 : 16358–16363.
59. FerreiraPG, PatalanoS, ChauhanR, Ffrench-ConstantR, GabaldonT, et al. (2013) Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biology 14: R20.
60. JohnsonBR, TsutsuiND (2011) Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. Bmc Genomics 12 : 164.
61. JohnsonBR, LinksvayerTA (2010) Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. The Quarterly Review of Biology 85 : 57–79.
62. TschinkelWR (1993) Resource allocation, brood production and cannibalism during colony founding in the fire ant, Solenopsis invicta. Behavioral Ecology and Sociobiology 33 : 209–223.
63. WurmY, WangJ, KellerL (2010) Changes in reproductive roles are associated with changes in gene expression in fire ant queens. Molecular Ecology 19 : 1200–1211.
64. CoronaM, HughesKA, WeaverDB, RobinsonGE (2005) Gene expression patterns associated with queen honey bee longevity. Mechanisms of ageing and development 126 : 1230–1238.
65. PaabyAB, SchmidtPS (2009) Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3 : 29–38.
66. WangD, QianL, XiongH, LiuJ, NeckameyerWS, et al. (2006) Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 103 : 13520–13525.
67. VermeulenCJ, LoeschckeV (2007) Longevity and the stress response in Drosophila. Experimental Gerontology 42 : 153–159.
68. WangH-D, Kazemi-EsfarjaniP, BenzerS (2004) Multiple-stress analysis for isolation of Drosophila longevity genes. Proceedings of the National Academy of Sciences of the United States of America 101 : 12610–12615.
69. OrrW, SohalR (1993) Effects of Cu-Zn Superoxide Dismutase Overexpression on Life Span and Resistance to Oxidative Stress in Transgenic Drosophila melanogaster. Archives of biochemistry and biophysics 301 : 34–40.
70. ParkerJD, ParkerKM, SohalBH, SohalRS, KellerL (2004) Decreased expression of Cu-Zn superoxide dismutase 1 in ants with extreme lifespan. Proceedings of the National Academy of Sciences of the United States of America 101 : 3486–3489.
71. SpencerCC, HowellCE, WrightAR, PromislowDEL (2003) Testing an “aging gene” in long-lived Drosophila strains: increased longevity depends on sex and genetic background. Aging Cell 2 : 123–130.
72. RuanHY, WuCF (2008) Social interaction-mediated lifespan extension of Drosophila Cu/Zn superoxide dismutase mutants. Proceedings of the National Academy of Sciences of the United States of America 105 : 7506–7510.
73. CareyJR, HarshmanLG, LiedoP, MüllerH-G, WangJ-L, et al. (2008) Longevity–fertility trade-offs in the tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell 7 : 470–477.
74. WuQ, BrownMR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51 : 1–24.
75. HartfelderK (2000) Insect juvenile hormone: from “status quo” to high society. Brazilian Journal of Medical and Biological Research 33 : 157–177.
76. CoronaM, VelardeRA, RemolinaS, Moran-LauterA, WangY, et al. (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences 104 : 7128–7133.
77. BrennanCA, AndersonKV (2004) Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 22 : 457–483.
78. RämetM, LanotR, ZacharyD, ManfruelliP (2002) JNK Signaling Pathway Is Required for Efficient Wound Healing in Drosophila. Developmental Biology 241 : 145–156.
79. WilliamsMJ (2007) Drosophila hemopoiesis and cellular immunity. The Journal of Immunology 178 : 4711–4716.
80. Schmid-HempelP (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B: Biological Sciences 270 : 357–366.
81. GrozingerCM, FanYL, HooverSER, WinstonML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Molecular Ecology 16 : 4837–4848.
82. NiñoEL, TarpyDR, GrozingerC (2013) Differential effects of insemination volume and substance on reproductive changes in honey bee queens (Apis mellifera L.). Insect Molecular Biology 22(3): 233–44.
83. Blomquist GJ, Bagnères AG (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press. 504 p.
84. RichardFJ, HoltH, GrozingerC (2012) Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). Bmc Genomics 13 : 558.
85. KöhlerK, BrunnerE, GuanXL, BouckeK, GreberUF, et al. (2009) A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvation-induced autophagy in Drosophila. Autophagy 5 : 980–990.
86. SelvaN, Cortés-AvizandaA, LemusJA, BlancoG, MuellerT, et al. (2011) Stress associated with group living in a long-lived bird. Biology Letters 7 : 608–610.
87. TannerCJ, SalaliGD, JacksonAL (2011) The ghost of social environments past: dominance relationships include current interactions and experience carried over from previous groups. Biology Letters 7 : 818–821.
88. CristollDA (1995) Costs of switching social groups for dominant and subordinate dark-eyed juncos (Junco hyemalis). Behavioral Ecology and Sociobiology 37 : 93–101.
89. MonninT (2006) Chemical recognition of reproductive status in social insects. Helsinki: Suomen Biologian Seura Vanamo, 1964-. Ann Zool Fennici 43 : 515–530.
90. VallesSM, PorterSD (2003) Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Insectes Sociaux 50 : 199–200.
91. OliverosJ (2009) VENNY. An interactive tool for comparing lists with Venn Diagrams 2007.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
