Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding

English version České info

Ants are a highly successful family of insects that thrive in a variety of habitats across the world. Perhaps their best-known features are complex social organization and strict division of labor, separating reproduction from the day-to-day maintenance and care of the colony, as well as strict discrimination against foreign individuals. Since these social characteristics in ants are thought to be mediated by semiochemicals, a thorough analysis of these signals, and the receptors that detect them, is critical in revealing mechanisms that lead to stereotypic behaviors. To address these questions, we have defined and characterized the major chemoreceptor families in a pair of behaviorally and evolutionarily distinct ant species, Camponotus floridanus and Harpegnathos saltator. Through comprehensive re-annotation, we show that these ant species harbor some of the largest yet known repertoires of odorant receptors (Ors) among insects, as well as a more modest number of gustatory receptors (Grs) and variant ionotropic glutamate receptors (Irs). Our phylogenetic analyses further demonstrate remarkably rapid gains and losses of ant Ors, while Grs and Irs have also experienced birth-and-death evolution to different degrees. In addition, comparisons of antennal transcriptomes between sexes identify many chemoreceptors that are differentially expressed between males and females and between species. We have also revealed an agonist for a worker-enriched OR from C. floridanus, representing the first case of a heterologously characterized ant tuning Or. Collectively, our analysis reveals a large number of ant chemoreceptors exhibiting patterns of differential expression and evolution consistent with sex/species-specific functions. These differentially expressed genes are likely associated with sex-based differences, as well as the radically different social lifestyles observed between C. floridanus and H. saltator, and thus are targets for further functional characterization. Our findings represent an important advance toward understanding the molecular basis of social interactions and the differential chemical ecologies among ant species.

Vyšlo v časopise: Phylogenetic and Transcriptomic Analysis of Chemosensory Receptors in a Pair of Divergent Ant Species Reveals Sex-Specific Signatures of Odor Coding. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002930
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002930

Souhrn

Zdroje

1. MoreauCS, BellCD, VilaR, ArchibaldSB, PierceNE (2006) Phylogeny of the ants: diversification in the age of angiosperms. Science 312: 101–104.

2. Hölldobler B, Wilson EO (1990) The ants. Cambridge, Mass.: Belknap Press of Harvard University Press. xii, 732 p., 724 p. of plates p.

3. DavidsonDW, CookSC, SnellingRR, ChuaTH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300: 969–972.

4. DavidsonDW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61: 153–181.

5. BoltonB (2003) Synopsis and Classification of Formicidae. Mem Am Entomol Inst 71: 1–370.

6. WilsonEO (1976) Which are the most prevalent ant genera? Stud Entomol 19: 187–200.

7. MooreD, LiebigJ (2010) Mechanisms of social regulation change across colony development in an ant. BMC Evol Biol 10: 328.

8. EndlerA, LiebigJ, HölldoblerB (2006) Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav Ecol Sociobiol 59: 490–499.

9. EndlerA, LiebigJ, SchmittT, ParkerJE, JonesGR, et al. (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci U S A 101: 2945–2950.

10. EndlerA, HölldoblerB, LiebigJ (2007) Lack of physical policing and fertility cues in egg-laying workers of the ant Camponotus floridanus. Anim Behav 74: 1171–1180.

11. PeetersC, LiebigJ, HölldoblerB (2000) Sexual reproduction by both queens and workers in the ponerine ant Harpegnathos saltator. Insect Soc 47: 325–332.

12. PeetersC, HölldoblerB (1995) Reproductive cooperation between queens and their mated workers: the complex life history of an ant with a valuable nest. Proc Natl Acad Sci U S A 92: 10977–10979.

13. LiebigJ, PeetersC, HölldoblerB (1999) Worker policing limits the number of reproductives in a ponerine ant. Proc R Soc B 266: 1865–1870.

14. LiangZS, NguyenT, MattilaHR, Rodriguez-ZasSL, SeeleyTD, et al. (2012) Molecular determinants of scouting behavior in honey bees. Science 335: 1225–1228.

15. RobertsonHM, WarrCG, CarlsonJR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100 Suppl 2: 14537–14542.

16. GaoQ, ChessA (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60: 31–39.

17. ClynePJ, WarrCG, FreemanMR, LessingD, KimJ, et al. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22: 327–338.

18. VosshallLB, AmreinH, MorozovPS, RzhetskyA, AxelR (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96: 725–736.

19. FoxAN, PittsRJ, RobertsonHM, CarlsonJR, ZwiebelLJ (2001) Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc Natl Acad Sci U S A 98: 14693–14697.

20. ScottK, BradyRJr, CravchikA, MorozovP, RzhetskyA, et al. (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104: 661–673.

21. DunipaceL, MeisterS, McNealyC, AmreinH (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11: 822–835.

22. ClynePJ, WarrCG, CarlsonJR (2000) Candidate taste receptors in Drosophila. Science 287: 1830–1834.

23. WangL, HanX, MehrenJ, HiroiM, BilleterJ-C, et al. (2011) Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14: 757–U392.

24. BentonR, VanniceKS, Gomez-DiazC, VosshallLB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136: 149–162.

25. AbuinL, BargetonB, UlbrichMH, IsacoffEY, KellenbergerS, et al. (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69: 44–60.

26. CrosetV, RytzR, CumminsSF, BuddA, BrawandD, et al. (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6: e1001064 doi:10.1371/journal.pgen.1001064.

27. HillCA, FoxAN, PittsRJ, KentLB, TanPL, et al. (2002) G protein-coupled receptors in Anopheles gambiae. Science 298: 176–178.

28. RobertsonHM, GadauJ, WannerKW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol 19 Suppl 1: 121–136.

29. LarssonMC, DomingosAI, JonesWD, ChiappeME, AmreinH, et al. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43: 703–714.

30. BentonR, SachseS, MichnickSW, VosshallLB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4: e20 doi:10.1371/journal.pbio.0040020.

31. KriegerJ, KlinkO, MohlC, RamingK, BreerH (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189: 519–526.

32. SatoK, PellegrinoM, NakagawaT, NakagawaT, VosshallLB, et al. (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452: 1002–1006.

33. WicherD, SchaferR, BauernfeindR, StensmyrMC, HellerR, et al. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452: 1007–1011.

34. SmartR, KielyA, BealeM, VargasE, CarraherC, et al. (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38: 770–780.

35. JonesPL, PaskGM, RinkerDC, ZwiebelLJ (2011) Functional agonism of insect odorant receptor ion channels. Proc Natl Acad Sci U S A 108: 8821–8825.

36. PaskGM, JonesPL, RutzlerM, RinkerDC, ZwiebelLJ (2011) Heteromeric anopheline odorant receptors exhibit distinct channel properties. PLoS ONE 6: e28774 doi:10.1371/journal.pone.0028774.

37. DahanukarA, FosterK, van der Goes van NatersWM, CarlsonJR (2001) A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4: 1182–1186.

38. UenoK, OhtaM, MoritaH, MikuniY, NakajimaS, et al. (2001) Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol 11: 1451–1455.

39. MoonSJ, KottgenM, JiaoY, XuH, MontellC (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16: 1812–1817.

40. BrayS, AmreinH (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019–1029.

41. WangL, HanX, MehrenJ, HiroiM, BilleterJC, et al. (2011) Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14: 757–762.

42. MiyamotoT, AmreinH (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11: 874–876.

43. JonesWD, CayirliogluP, KadowIG, VosshallLB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445: 86–90.

44. LuT, QiuYT, WangG, KwonJY, RutzlerM, et al. (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol 17: 1533–1544.

45. ThorneN, AmreinH (2008) Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J Comp Neurol 506: 548–568.

46. BonasioR, ZhangG, YeC, MuttiNS, FangX, et al. (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068–1071.

47. SmithCD, ZiminA, HoltC, AbouheifE, BentonR, 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.

48. SmithCR, SmithCD, RobertsonHM, HelmkampfM, ZiminA, et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci U S A 108: 5667–5672.

49. PittsRJ, RinkerDC, JonesPL, RokasA, ZwiebelLJ (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 12: 271.

50. RobertsonHM, WannerKW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16: 1395–1403.

51. EngsontiaP, SandersonAP, CobbM, WaldenKK, RobertsonHM, et al. (2008) The red flour beetle's large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38: 387–397.

52. NozawaM, NeiM (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci U S A 104: 7122–7127.

53. Penalva-AranaDC, LynchM, RobertsonHM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evol Biol 9: 79.

54. SmadjaC, ShiP, ButlinRK, RobertsonHM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26: 2073–2086.

55. KentLB, RobertsonHM (2009) Evolution of the sugar receptors in insects. BMC Evol Biol 9: 41.

56. SloneJ, DanielsJ, AmreinH (2007) Sugar receptors in Drosophila. Curr Biol 17: 1809–1816.

57. DahanukarA, LeiYT, KwonJY, CarlsonJR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56: 503–516.

58. JiaoY, MoonSJ, MontellC (2007) A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A 104: 14110–14115.

59. KwonJY, DahanukarA, WeissLA, CarlsonJR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci U S A 104: 3574–3578.

60. RobertsonHM, KentLB (2009) Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J Insect Sci 9: 19.

61. KleineidamC, TautzJ (1996) Perception of carbon dioxide and other “air-condition” parameters in the leaf cutting ant Atta cephalotes. Naturwissenschaften 83: 566–568.

62. De BieT, CristianiniN, DemuthJP, HahnMW (2006) CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22: 1269–1271.

63. ChenK, DurandD, Farach-ColtonM (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7: 429–447.

64. HahnMW, De BieT, StajichJE, NguyenC, CristianiniN (2005) Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome Res 15: 1153–1160.

65. VosshallLB, WongAM, AxelR (2000) An olfactory sensory map in the fly brain. Cell 102: 147–159.

66. WangG, CareyAF, CarlsonJR, ZwiebelLJ (2010) Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 107: 4418–4423.

67. Burdock GA (1997) Encyclopedia of food and color additives. Boca Raton: CRC Press.

68. Khan IA, Abourashed EA (2010) Leung's encyclopedia of common natural ingredients: used in food, drugs, and cosmetics. Hoboken, N.J.: John Wiley & Sons, Inc. xxix, 810 p. p.

69. Sánchez-Gracia A, Vieira FG, Almeida FC, Rozas J (2011) Comparative Genomics of the Major Chemosensory Gene Families in Arthropods. eLS. Chichester: John Wiley & Sons Ltd.

70. GadauJ, HelmkampfM, NygaardS, RouxJ, SimolaDF, et al. (2012) The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 28: 14–21.

71. NeiM, NiimuraY, NozawaM (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9: 951–963.

72. XuG, MaH, NeiM, KongH (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci U S A 106: 835–840.

73. UrbaniCB, BoyanGS, BlarerA, BillenJ, AliTMM (1994) A Novel Mechanism for Jumping in the Indian Ant Harpegnathos Saltator (Jerdon) (Formicidae, Ponerinae). Experientia 50: 63–71.

74. LiebigJ, HeinzeJ, HölldoblerB (1997) Trophallaxis and aggression in the ponerine ant, Ponera coarctata: Implications for the evolution of liquid food exchange in the Hymenoptera. Ethology 103: 707–722.

75. SatoK, TanakaK, TouharaK (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci U S A 108: 11680–11685.

76. ZubeC, RosslerW (2008) Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. Arthropod Struct Dev 37: 469–479.

77. HoyerSC, LiebigJ, RösslerW (2005) Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain. Arthropod Struct Dev 34: 429–440.

78. NakanishiA, NishinoH, WatanabeH, YokohariF, NishikawaM (2010) Sex-specific antennal sensory system in the ant Camponotus japonicus: glomerular organizations of antennal lobes. J Comp Neurol 518: 2186–2201.

79. OzakiM, Wada-KatsumataA, FujikawaK, IwasakiM, YokohariF, et al. (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309: 311–314.

80. NakanishiA, NishinoH, WatanabeH, YokohariF, NishikawaM (2009) Sex-specific antennal sensory system in the ant Camponotus japonicus: structure and distribution of sensilla on the flagellum. Cell Tissue Res 338: 79–97.

81. DobritsaAA, van der Goes van NatersW, WarrCG, SteinbrechtRA, CarlsonJR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37: 827–841.

82. GoldmanAL, Van der Goes van NatersW, LessingD, WarrCG, CarlsonJR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45: 661–666.

83. FishilevichE, VosshallLB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15: 1548–1553.

84. CoutoA, AleniusM, DicksonBJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535–1547.

85. WannerKW, NicholsAS, WaldenKK, BrockmannA, LuetjeCW, et al. (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci U S A 104: 14383–14388.

86. HölldoblerB (1966) Futterverteilung durch Männchen im Ameisenstaat. Z Vergl Physiol 52: 430–455.

87. ErlerF, UlugI, YalcinkayaB (2006) Repellent activity of five essential oils against Culex pipiens. Fitoterapia 77: 491–494.

88. PrajapatiV, TripathiAK, AggarwalKK, KhanujaSP (2005) Insecticidal, repellent and oviposition-deterrent activity of selected essential oils against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Bioresour Technol 96: 1749–1757.

89. Munoz-TorresMC, ReeseJT, ChildersCP, BennettAK, SundaramJP, et al. (2011) Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39: D658–662.

90. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

91. BirneyE, ClampM, DurbinR (2004) GeneWise and Genomewise. Genome Res 14: 988–995.

92. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

93. ZdobnovEM, ApweilerR (2001) InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847–848.

94. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

95. RoshanU, LivesayDR (2006) Probalign: multiple sequence alignment using partition function posterior probabilities. Bioinformatics 22: 2715–2721.

96. NicholasKB, NicholasHB, DeerfieldDW (1997) GeneDoc: analysis and visualization of genetic variation. EMBNETnews 4: 1–4.

97. Capella-GutierrezS, Silla-MartinezJM, GabaldonT (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972–1973.

98. LeSQ, GascuelO (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307–1320.

99. NamJ, NeiM (2005) Evolutionary change of the numbers of homeobox genes in bilateral animals. Mol Biol Evol 22: 2386–2394.

100. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

101. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.

102. BradySG, SchultzTR, FisherBL, WardPS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci U S A 103: 18172–18177.

103. BohbotJD, JonesPL, WangG, PittsRJ, PaskGM, et al. (2011) Conservation of indole responsive odorant receptors in mosquitoes reveals an ancient olfactory trait. Chem Senses 36: 149–160.