On the Air: Broadcasting and Reception of Volatile Messages in Brood-Site Pollination Mutualisms

  • Renee M. BorgesEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM)


Brood-site pollination mutualisms are those in which plants offer sites to pollinators for the development of offspring or mimic the presence of these sites in exchange for pollination services. Floral scent is an important component of pollinator attraction in such mutualisms and is often composed of volatiles that are commonly emitted by plants in other contexts. Therefore, private channels that employ unusual scent compounds are not the norm. Pollinators must make sense of the volatile messages broadcast by plants against the ensuing background volatile noise using a combination of strategies at the peripheral olfactory system and at higher processing levels. Pollinator reproduction, parts of which occur on or within the host plant, imposes special restrictions on partner compatibility within brood-site pollination systems. A comprehensive understanding of constraints on volatile broadcasting and reception within ecological and evolutionary contexts in this cross-kingdom communication must inform and guide future research in this area.


Antennal Lobe Floral Scent Floral Volatile Butyric Acid Methyl Ester Brood Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I am grateful to Pratibha Yadav and Vignesh Venkateswaran for the help with the figures. Our work is supported by the Indian Ministry of Environment, Forests and Climate Change, the Department of Science and Technology and the Department of Biotechnology.


  1. Ahmed S, Compton SG, Butlin RK, Gilmartin PM (2009) Wind-borne insects mediate directional pollen transfer between desert fig trees 160 kilometers apart. Proc Natl Acad Sci USA 106:20342–20347PubMedPubMedCentralCrossRefGoogle Scholar
  2. Althoff DM, Segraves KA, Smith CI, Leebens-Mack J, Pellmyr O (2012) Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification. Mol Phylogenet Evol 62:898–906PubMedCrossRefGoogle Scholar
  3. Althoff DM, Fox KA, Frieden T (2014) The role of ecological availability and host plant characteristics in determining host use by the bogus yucca moth Prodoxus decipiens. Ecol Entomol 39:620–626CrossRefGoogle Scholar
  4. Andersson MN, Schlyter F, Hill SR, Dekker T (2012) What reaches the antenna? How to calibrate odor flux and ligand-receptor affinities. Chem Senses 37:403–420PubMedCrossRefGoogle Scholar
  5. Andersson MN, Löfstedt C, Newcomb RD (2015) Insect olfaction and the evolution of receptor tuning. Front Ecol Evol 3:53Google Scholar
  6. Appanah S, Chan HT (1981) Thrips: the pollinators of some dipterocarps. Malay For 44:234–252Google Scholar
  7. Askew RR (1968) Considerations on speciation in Chalcidoidea (Hymenoptera). Evolution 22:642–645CrossRefGoogle Scholar
  8. Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006PubMedCrossRefGoogle Scholar
  9. Beyaert I, Hilker M (2013) Plant odour plumes as mediators of plant–insect interactions. Biol Rev 89:68–81PubMedCrossRefGoogle Scholar
  10. Biere A, Honders SC (2006) Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia. New Phytol 169:719–727PubMedCrossRefGoogle Scholar
  11. Binyameen M, Jankuvová J, Blaženec M, Jakuš R, Song L, Schlyter F, Andersson MN (2014) Co-localization of insect olfactory sensory cells improves the discrimination of closely separated odour sources. Funct Ecol 28:1216–1223CrossRefGoogle Scholar
  12. Blande JD, Holopainen JK, Niinemets U (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bohbot JD, Pitts RJ (2015) The narrowing olfactory landscape of insect odorant receptors. Front Ecol Evol 3:39CrossRefGoogle Scholar
  14. Borges RM (2015) How to be a fig wasp parasite on the fig–fig wasp mutualism. Curr Opin Insect Sci 8:34–40CrossRefGoogle Scholar
  15. Borges RM, Bessière JM, Ranganathan Y (2013) Diel variation in fig volatiles across syconium development: making sense of scents. J Chem Ecol 39:630–642PubMedCrossRefGoogle Scholar
  16. Brodmann J, Twele R, Francke W, Hölzler G, Zhang Q-H, Ayasse M (2008) Orchid mimics green leaf volatiles to attract prey-hunting wasps for pollination. Curr Biol 18:740–744PubMedCrossRefGoogle Scholar
  17. Brookes DR, Hereward JP, Terry LI, Walter GH (2015) Evolutionary dynamics of a cycad obligate pollination mutualism—pattern and process in extant Macrozamia cycads and their specialist thrips pollinators. Mol Phylogenet Evol 93:83–93PubMedCrossRefGoogle Scholar
  18. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72:1605–1611PubMedCrossRefGoogle Scholar
  19. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274PubMedCrossRefGoogle Scholar
  20. Burger H, Ayasse M, Dötterl S, Kreissl S, Galizia CG (2013) Perception of floral volatiles in host-plant finding behavior: comparison of a bee specialist and generalist. J Comp Physiol A 199:751–761CrossRefGoogle Scholar
  21. Byers KJRP, Bradshaw HD Jr, Riffell JA (2014a) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623PubMedPubMedCentralCrossRefGoogle Scholar
  22. Byers KJRP, Vela JP, Peng F, Riffell JA, Bradshaw HD Jr (2014b) Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkeyflowers (Mimulus). Plant J 80:1031–1042PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cande J, Prud’homme B, Gompel N (2013) Smells like evolution: the role of chemoreceptor evolution in behavioral change. Curr Opin Neurobiol 23:152–158PubMedCrossRefGoogle Scholar
  24. Cardé RT, Willis MA (2008) Navigational strategies used by insects to find distant, wind-borne sources of odor. J Chem Ecol 34:854–866PubMedCrossRefGoogle Scholar
  25. Chen S, Luetje CW (2013) Phenylthiophenecarboxamide antagonists of the olfactory receptor co-receptor subunit from a mosquito. PLoS ONE 8:e84575PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chen C, Song Q-S, Proffit M, Bessière J-M, Li Z-B, Hossaert-McKey M (2009) Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct Ecol 23:941–950CrossRefGoogle Scholar
  27. Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449PubMedPubMedCentralCrossRefGoogle Scholar
  28. Compton SG, Grehan K, van Noort S (2009) A fig crop pollinated by three or more species of agaonid fig wasps. Afr Entomol 17:215–222CrossRefGoogle Scholar
  29. Conchou L, Cabioch L, Rodriguez LJV, Kjellberg F (2014) Daily rhythm of mutualistic pollinator activity and scent emission in Ficus septica: ecological differentiation between co-occurring pollinators and potential consequences for chemical communication and facilitation of host speciation. PLoS ONE 9:e103581PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cook JM, Rasplus J-Y (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18:241–248CrossRefGoogle Scholar
  31. Cornille A, Underhill JG, Cruaud A, Hossaert-McKey M, Johnson SD, Tolley KA, Kjellberg F, van Noort S, Proffit M (2012) Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc R Soc Lond B 279:1731–1739CrossRefGoogle Scholar
  32. Cruaud A, Rønsted N, Chantarasuwan B, Chou LS, Clement WL, Couloux A, Cousins B, Genson G, Harrison RD, Hanson PE et al (2012) An extreme case of plant–insect codiversification: figs and fig-pollinating wasps. Syst Biol 61:1029–1047PubMedPubMedCentralCrossRefGoogle Scholar
  33. Cunningham JP (2012) Can mechanism help explain insect host choice? J Evol Biol 25:244–251PubMedCrossRefGoogle Scholar
  34. de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897PubMedCrossRefGoogle Scholar
  35. DeGennaro M (2015) The mysterious multi-modal repellency of DEET. Fly 9:45–51PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Curr Biol 16:101–109PubMedCrossRefGoogle Scholar
  37. Després L (2003) Sex and pollen: the role of males in stabilising a plant–seed eater pollinating mutualism. Oecologia 135:60–66PubMedCrossRefGoogle Scholar
  38. Després L, Jaeger N (1999) Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae). J Evol Biol 12:822–831CrossRefGoogle Scholar
  39. Dev SA, Kjellberg F, Hossaert-McKey M, Borges RM (2011) Fine-scale population genetic structure of two dioecious Indian keystone species, Ficus hispida and Ficus exasperata (Moraceae). Biotropica 43:309–316CrossRefGoogle Scholar
  40. Dickens JC, Bohbot JD (2013) Mini review: mode of action of mosquito repellents. Pest Biochem Physiol 106:149–155CrossRefGoogle Scholar
  41. Dodd RJ, Linhart YB (1994) Reproductive consequences of interactions between Yucca glauca (Agavaceae) and Tegeticula yuccasella (Lepidoptera) in Colorado. Am J Bot 81:815–825CrossRefGoogle Scholar
  42. Dufaÿ M, Anstett MC (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14CrossRefGoogle Scholar
  43. Erasmus JC, van Noort S, Jousselin E, Greeff JM (2007) Molecular phylogeny of fig wasp pollinators (Agaonidae, Hymenoptera) of Ficus section Galoglychia. Zool Scr 36:61–78CrossRefGoogle Scholar
  44. Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2013) Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspect Plant Ecol Evol Syst 15:56–67CrossRefGoogle Scholar
  45. Fatouros NE, Lucas-Barbosa D, Weldegergis BT, Pashalidou FG, van Loon JJA, Dicke M, Harvey JA, Gols R, Huigens ME (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7:e43607PubMedPubMedCentralCrossRefGoogle Scholar
  46. Friberg M, Schwind C, Raguso RA, Thompson JN (2013) Extreme divergence in floral scent among woodland star species (Lithophragma spp.) pollinated by floral parasites. Ann Bot 111:539–550PubMedPubMedCentralCrossRefGoogle Scholar
  47. Friberg M, Schwind C, Roark LC, Raguso RA, Thompson JN (2014) Floral scent contributes to interaction specificity in coevolving plants and their pollinators. J Chem Ecol 40:955–965PubMedCrossRefGoogle Scholar
  48. Galizia CG (2014) Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci 39:1784–1975PubMedPubMedCentralCrossRefGoogle Scholar
  49. Ghana S, Suleman N, Compton SG (2015) Ability to gall: the ultimate basis of host specificity in fig wasps? Ecol Entomol 40:280–291CrossRefGoogle Scholar
  50. Ghara M, Borges RM (2010) Comparative life-history traits in a fig wasp community: implications for community structure. Ecol Entomol 35:139–148CrossRefGoogle Scholar
  51. Girling RD, Higbee BS, Cardé RT (2013) The plume also rises: trajectories of pheromone plumes issuing from point sources in an orchard canopy at night. J Chem Ecol 39:1150–1160PubMedCrossRefGoogle Scholar
  52. Goldman-Huertas B, Mitchell RF, Lapoint RT, Faucher CP, Hildebrand JG, Whiteman NK (2015) Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors and ancestral diet. Proc Natl Acad Sci USA 112:3026–3031PubMedPubMedCentralCrossRefGoogle Scholar
  53. Grafen A, Godfray HCJ (1991) Vicarious selection explains some paradoxes in dioecious fig pollinator systems. Proc R Soc Lond B 245:73–76CrossRefGoogle Scholar
  54. Grison-Pigé L, Bessière J-M, Hossaert-McKey M (2002) Specific attraction of fig-pollinating wasps: role of volatile compounds released by tropical figs. J Chem Ecol 28:283–295PubMedCrossRefGoogle Scholar
  55. Gu D, Compton SG, Peng Y-Q, Yang DR (2012) ‘Push’ and ‘pull’ responses by fig wasps to volatiles released by their host figs. Chemoecology 22:217–227CrossRefGoogle Scholar
  56. Gu HF, Xiao JH, Dunn DW, Niu LM, Wang B, Jia LY, Huang DW (2014) Evidence for the circadian gene period as a proximate mechanism of protandry in a pollinating fig wasp. Biol Lett 10:20130914Google Scholar
  57. Hackett S, Schaefer HM, Ruxton GD (2014) Linking signal fidelity and the efficiency costs of communication. J Evol Biol 27:1797–1810PubMedCrossRefGoogle Scholar
  58. Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711PubMedCrossRefGoogle Scholar
  59. Harrison RD (2003) Fig wasp dispersal and the stability of a keystone plant resource in Borneo. Proc R Soc Lond B 270:S76–S79CrossRefGoogle Scholar
  60. Harrison RD, Rasplus J-Y (2006) Dispersal of fig pollinators in Asian tropical rain forests. J Trop Ecol 22:631–639CrossRefGoogle Scholar
  61. Heiduk A, Kong H, Brake I, von Tschirnhaus M, Tolasch T, Tröger AG, Wittenberg E, Francke W, Meve U, Dötterl S (2015) Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent. Front Ecol Evol 3:66CrossRefGoogle Scholar
  62. Herre EA, Jandér KC, Machado CA (2008) Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu Rev Ecol Syst 39:439–458CrossRefGoogle Scholar
  63. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002) G protein-coupled receptors in Anopheles gambiae. Science 298:176–178PubMedCrossRefGoogle Scholar
  64. Hossaert-McKey M, Soler C, Schatz B, Proffit M (2010) Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20:75–88CrossRefGoogle Scholar
  65. Hossaert-McKey M, Proffit M, Soler CCL, Chen C, Bessière J-M, Schatz B, Borges RM (2016) How to be a dioecious fig: chemical mimicry between sexes matters only when both sexes flower synchronously. Sci Rep 6:21236PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hughes DT, Pelletier J, Luetje CW, Leal WS (2010) Odorant receptor from the southern house mosquito narrowly tuned to the oviposition attractant skatole. J Chem Ecol 36:797–800PubMedPubMedCentralCrossRefGoogle Scholar
  67. Ibanez S, Dujardin G, Després L (2009a) Stability of floral specialization in Trollius europaeus in contrasting ecological environments. J Evol Biol 22:1183–1192PubMedCrossRefGoogle Scholar
  68. Ibanez S, Gallet C, Dommanget F, Després L (2009b) Plant chemical defence: a partner control mechanism stabilising plant–seed-eating pollinator mutualisms. BMC Evol Biol 9:261PubMedPubMedCentralCrossRefGoogle Scholar
  69. Ibanez I, Dötterl S, Anstett M-C, Baudino S, Caissard J-C, Gallet C, Després L (2010) The role of volatile organic compounds, morphology and pigments of globeflowers in the attraction of their specific pollinating flies. New Phytol 188:451–463PubMedCrossRefGoogle Scholar
  70. Jardine AB, Jardine KJ, Fuentes JD, Martin ST, Martins G, Durgante F, Carneiro V, Higuchi N, Manzi AO, Chambers JQ (2015) Highly reactive light-dependent monoterpenes in the Amazon. Geophys Res Lett 42:1576–1583CrossRefGoogle Scholar
  71. Junker RR, Parachnowitsch AL (2015) Working towards a holistic view on flower traits—how floral scents mediate plant–animal interactions in concert with other floral characters. J Indian Inst Sci 95:43–68Google Scholar
  72. Jürgens A, Shuttleworth A (2015) Carrion and dung mimicry in plants. In: Benbow ME, Tomberlin JK, Tarone AM (eds) Carrion ecology, evolution, and their applications. CRC Press, Boca Raton, FL, pp 361–386CrossRefGoogle Scholar
  73. Kawakita A, Kato M (2006) Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees. Mol Ecol 15:3567–3581PubMedCrossRefGoogle Scholar
  74. Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytol 169:667–680PubMedCrossRefGoogle Scholar
  75. Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT (2013) Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol Lett 16:299–306PubMedCrossRefGoogle Scholar
  76. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  77. Kobmoo N, Hossaert-McKey M, Rasplus J-Y, Kjellberg F (2010) Ficus racemosa is pollinated by a single population of a single agaonid wasp species in continental South-east Asia. Mol Ecol 19:2700–2712PubMedCrossRefGoogle Scholar
  78. Krishnan A, Borges RM (2014) Parasites exert conflicting selection pressures to affect reproductive asynchrony of their host plant in an obligate pollination mutualism. J Ecol 102:1329–1340CrossRefGoogle Scholar
  79. Krishnan A, Joshi KA, Abraham A, Ayyub S, Lahiry M, Mukherjee R, Javadekar SM, Narayan V, Borges RM (2014) Finding hidden females in a crowd: mate recognition in fig wasps. Acta Oecol 57:80–87CrossRefGoogle Scholar
  80. Kromann SH, Saveer AM, Binyameen M, Bengtsson M, Birgersson G, Hansson BS, Schlyter F, Witzgall P, Ignell R, Becher PG (2014) Concurrent modulation of neuronal and behavioural olfactory response to sex and host plant cues in a male moth. Proc R Soc Lond B 282:20141884CrossRefGoogle Scholar
  81. Laothawornkitkul J, Taylor JE, Paul ND, Hewitt CN (2009) Biogenic volatile organic compounds in the Earth system. New Phytol 183:27–51PubMedCrossRefGoogle Scholar
  82. Linz J, Baschwitz A, Strutz A, Dweck HK, Sachse S, Hansson BS, Stensmyr MC (2013) Host plant-driven sensory specialization in Drosophila erecta. Proc R Soc Lond B 280:20130626CrossRefGoogle Scholar
  83. Liu C, Liu Y, Guo M, Cao D, Dong S, Wang G (2014) Narrow tuning of an odorant receptor to plant volatiles in Spodoptera exigua (Hübner). Insect Mol Biol 23:487–496PubMedCrossRefGoogle Scholar
  84. Liu G-X, Yang D-R, Peng Y-Q, Compton SG (2015) Complementary fruiting phenologies facilitate sharing of one pollinator fig wasp by two fig trees. J Plant Ecol 8:197–206CrossRefGoogle Scholar
  85. Lloyd LL (1920) The habits of the glasshouse tomato moth, Hadena (Folia) oleracea, and its control. Ann Appl Biol 7:66–102CrossRefGoogle Scholar
  86. Lu B, Wang N, Xiao J, Xu Y, Murphy RW, Huang D (2009) Expression and evolutionary divergence of the non-conventional olfactory receptor in four species of fig wasp associated with one species of fig. BMC Evol Biol 9:43PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lusebrink I, Girling RD, Farthing E, Newman TA, Jackson CW, Poppy GM (2015) The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. J Chem Ecol 41:904–912PubMedCrossRefGoogle Scholar
  88. Machado CA, Robbins N, Gilbert MTP, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci USA 102:6558–6565PubMedPubMedCentralCrossRefGoogle Scholar
  89. Mainland JD, Keller A, Li YR, Zhou T, Trimmer C, Snyder LL, Moberly AH, Adipietro KA, Liu WLL, Zhuang H et al (2014) The missense of smell: functional variability in the human odorant receptor repertoire. Nat Neurosci 17:114–120PubMedCrossRefGoogle Scholar
  90. Majetic CJ, Raguso RA, Ashman T-L (2009) Sources of floral scent variation: can environment define floral scent phenotype? Plant Signal Behav 4:129–131PubMedPubMedCentralCrossRefGoogle Scholar
  91. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723PubMedCrossRefGoogle Scholar
  92. Mansourian S, Stensmyr MC (2015) The chemical ecology of the fly. Curr Opin Neurobiol 34:95–102PubMedCrossRefGoogle Scholar
  93. Martos F, Cariou M-L, Pailler T, Fournel J, Bytebier B, Johnson SD (2015) Chemical and morphological filters in a specialized floral mimicry system. New Phytol 207:225–234PubMedCrossRefGoogle Scholar
  94. McBride C (2007) Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc Natl Acad Sci USA 104:4996–5001PubMedPubMedCentralCrossRefGoogle Scholar
  95. McBride CS, Arguello JR (2007) Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416PubMedPubMedCentralCrossRefGoogle Scholar
  96. McFrederick QS, Kathilankal JC, Fuentes JD (2008) Air pollution modifies floral scent trails. Atmos Environ 42:2336–2348CrossRefGoogle Scholar
  97. Moe AM, Weiblen GD (2012) Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae). Evolution 66:3710–3721PubMedCrossRefGoogle Scholar
  98. Moe AM, Rossi DR, Weiblen GD (2011) Pollinator sharing in dioecious figs (Ficus: Moraceae). Biol J Linn Soc 103:546–558CrossRefGoogle Scholar
  99. Moré M, Cocucci AA, Raguso RA (2013) The importance of oligosulphides in the attraction of fly pollinators to the brood-site deceptive species Jaborosa rotacea (Solanaceae). Int J Plant Sci 174:863–876CrossRefGoogle Scholar
  100. Murlis J, Willis MA, Cardé RT (1992) Odor plumes and how insects use them. Annu Rev Entomol 37:505–532CrossRefGoogle Scholar
  101. Nazareno AG, Alzate-Marin AL, Pereira RAS (2013) Dioecy, more than monoecy, affects plant spatial genetic structure: the case study of Ficus. Ecol Evol 3:3495–3508PubMedPubMedCentralGoogle Scholar
  102. Nehring V, Wyatt TD, d’Ettorre P (2013) Noise in chemical communication. In: Brumm H (ed) Animal communication and noise. Springer, Berlin, Heidelberg, pp 373–405CrossRefGoogle Scholar
  103. Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963PubMedCrossRefGoogle Scholar
  104. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804PubMedCrossRefGoogle Scholar
  105. Nottingham SF, Hardie J, Dawson GW, Hick AJ, Pickett JA, Wadhams LJ, Woodcock CM (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. J Chem Ecol 17:1231–1242PubMedCrossRefGoogle Scholar
  106. Oelschlägel B, Nuss M, von Tschirnhaus M, Pätzold C, Neinhuis C, Dötterl S, Wanke S (2015) The betrayed thief—the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytol 206:342–351PubMedCrossRefGoogle Scholar
  107. Okamoto T, Kawakita A, Kato M (2007) Interspecific variation of floral scent composition in Glochidion and its association with host-specific pollinating seed parasite (Epicephala). J Chem Ecol 33:1065–1081PubMedCrossRefGoogle Scholar
  108. Olsson SB, Linn CE Jr, Roelofs WL (2006a) The chemosensory basis for behavioral divergence involved in sympatric host shifts. I. Characterizing olfactory receptor neuron classes responding to key host volatiles. J Comp Physiol A 192:279–288CrossRefGoogle Scholar
  109. Olsson SB, Linn CE Jr, Roelofs WL (2006b) The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles. J Comp Physiol A 192:289–300CrossRefGoogle Scholar
  110. Peakall R, Whitehead MR (2014) Floral odour chemistry defines species boundaries and underpins strong reproductive isolation in sexually deceptive orchids. Ann Bot 113:341–355PubMedCrossRefGoogle Scholar
  111. Pellegrino M, Steinbach N, Stensmyr MC, Hansson BS, Vosshall LB (2011) A natural polymorphism alters odour and DEET sensitivity in an insect odorant receptor. Nature 478:511–516PubMedPubMedCentralCrossRefGoogle Scholar
  112. Pellmyr O (1997) Pollinating seed eaters: why is active pollination so rare? Ecology 78:1655–1660CrossRefGoogle Scholar
  113. Pellmyr O, Krenn HW (2002) Origin of a complex key innovation in an obligate insect–plant mutualism. Proc Natl Acad Sci USA 99:5498–5502PubMedPubMedCentralCrossRefGoogle Scholar
  114. Peñuelas J, Llusià J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404PubMedCrossRefGoogle Scholar
  115. Proffit M, Johnson SD (2009) Specificity of the signal emitted by figs to attract their pollinating wasps: comparison of volatile organic compounds emitted by receptive syconia of Ficus sur and F. sycomorus in Southern Africa. South Afr J Bot 75:771–777CrossRefGoogle Scholar
  116. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569CrossRefGoogle Scholar
  117. Raguso RA (2009) Floral scent in a whole-plant context: moving beyond pollinator attraction. Funct Ecol 23:837–840CrossRefGoogle Scholar
  118. Rakosy D, Streinzer M, Paulus HF, Spaethe J (2012) Floral visual signal increases reproductive success in a sexually deceptive orchid. Arthropod Plant Interact 6:671–681PubMedPubMedCentralCrossRefGoogle Scholar
  119. Ramdya P, Benton R (2010) Evolving olfactory systems on the fly. Trends Genet 26:307–316PubMedCrossRefGoogle Scholar
  120. Riffell JA (2011) The neuroecology of a pollinator’s buffet: olfactory preferences and learning in insect pollinators. Integr Comp Biol 51:781–793PubMedCrossRefGoogle Scholar
  121. Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19:335–340PubMedPubMedCentralCrossRefGoogle Scholar
  122. Riffell JA, Lei H, Abrell L, Hildebrand JG (2013) Neural basis of a pollinator’s buffet: olfactory specialization and learning in Manduca sexta. Science 339:200–204PubMedCrossRefGoogle Scholar
  123. Robertson HM, Wanner KW (2006) The chemosensory superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403PubMedPubMedCentralCrossRefGoogle Scholar
  124. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100:14537–14542PubMedPubMedCentralCrossRefGoogle Scholar
  125. Sakai S (2002) A review of brood-site pollination mutualism: plants providing breeding sites for their pollinators. J Plant Res 115:161–168PubMedCrossRefGoogle Scholar
  126. Salzmann CC, Nardella AM, Cozzolino S, Schiestl FP (2007) Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection? Ann Bot 100:757–765PubMedPubMedCentralCrossRefGoogle Scholar
  127. Sane SP, Jacobson NP (2006) Induced airflow in flying insects II. Measurement of induced flow. J Exp Biol 209:43–56PubMedCrossRefGoogle Scholar
  128. Saveer AM, Kromann SH, Birgersson G, Bengtsson M, Lindblom T, Balkenius A, Hansson BS, Witzgall P, Becher PG, Ignell R (2012) Floral to green: mating switches moth olfactory coding and preference. Proc R Soc Lond B 279:2314–2322CrossRefGoogle Scholar
  129. Schaefer HM, Ruxton GD (2009) Deception in plants: mimicry or perceptual exploitation? Trends Ecol Evol 24:676–685PubMedCrossRefGoogle Scholar
  130. Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656PubMedCrossRefGoogle Scholar
  131. Schiestl FP (2015) Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytol 206:571–577PubMedCrossRefGoogle Scholar
  132. Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximizing reproductive success? Oecologia 126:531–534CrossRefGoogle Scholar
  133. Schiestl FP, Cozzolino S (2008) Evolution of sexual mimicry in the orchid subtribe Orchidinae: the role of preadaptations in the attraction of male bees as pollinators. BMC Evol Biol 8:27PubMedPubMedCentralCrossRefGoogle Scholar
  134. Schröder R, Hilker M (2008) The relevance of background odor in resource location by insects: a behavioral approach. Bioscience 58:308–316CrossRefGoogle Scholar
  135. Schuman MC, Baldwin IT (2012) Asking the ecosystem if herbivory-inducible plant volatiles (HIPVs) have defensive functions. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: genes to global processes. Cambridge University Press, Cambridge, pp 287–307CrossRefGoogle Scholar
  136. Shenoy M, Borges RM (2008) A novel mutualism between an ant-plant and its resident pollinator. Naturwissenschaften 95:61–65PubMedCrossRefGoogle Scholar
  137. Soler C, Proffit M, Chen C, Hossaert-McKey M (2010) Private channels in plant–pollinator mutualisms. Plant Signal Behav 5:893–895PubMedPubMedCentralCrossRefGoogle Scholar
  138. Soler C, Hossaert-McKey M, Buatois B, Bessière J-M, Schatz B, Proffit M (2011) Geographic variation of floral scent in a highly specialized pollination mutualism. Phytochemistry 72:74–81PubMedCrossRefGoogle Scholar
  139. Soler CC, Proffit M, Bessière J-M, Hossaert-McKey M, Schatz B (2012) Evidence for intersexual chemical mimicry in a dioecious plant. Ecol Lett 15:978–985PubMedCrossRefGoogle Scholar
  140. Song B, Chen G, Stöcklin J, Peng D-L, Niu Y, Li Z-M, Sun H (2014) A new pollinating seed-consuming mutualism between Rheum nobile and a fly fungus gnat, Bradysia sp., involving attraction by a specific floral compound. New Phytol 203:1109–1118PubMedCrossRefGoogle Scholar
  141. Souza CD, Pereira RAS, Marinho CR, Kjellberg F, Teixeira SP (2015) Diversity of fig glands is associated with nursery mutualism in fig trees. Am J Bot 102:1564–1577PubMedCrossRefGoogle Scholar
  142. Steiger S, Schmitt T, Schaefer HM (2010) The origin and dynamic evolution of chemical information transfer. Proc R Soc Lond B. doi: 10.1098/rspb.2010.2285 Google Scholar
  143. Stensmyr MC, Dekker T, Hansson BS (2003) Evolution of the olfactory code in the Drosophila melanogaster subgroup. Proc R Soc Lond B 270:2333–2340CrossRefGoogle Scholar
  144. Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S et al (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357PubMedCrossRefGoogle Scholar
  145. Stökl J, Strutz A, Dafni A, Svatos A, Doubsky J, Knaden M, Sachse S, Hansson BS, Stensmyr MC (2010) A deceptive pollination system targeting Drosophilids through olfactory mimicry of yeast. Curr Biol 20:1846–1852PubMedCrossRefGoogle Scholar
  146. Stökl J, Brodmann J, Dafni A, Ayasse M, Hansson BS (2011) Smells like aphids: orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination. Proc R Soc Lond B 278:1216–1222CrossRefGoogle Scholar
  147. Suh GSB, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854–859PubMedCrossRefGoogle Scholar
  148. Suinyuy TN, Donaldson JS, Johnson SD (2013) Patterns of odour emission, thermogenesis and pollinator activity in cones of an African cycad: what mechanisms apply? Ann Bot 112:891–902PubMedPubMedCentralCrossRefGoogle Scholar
  149. Svensson GP, Pellmyr O, Raguso RA (2006) Strong conservation of floral scent composition in two allopatric yuccas. J Chem Ecol 32:2657–2665PubMedCrossRefGoogle Scholar
  150. Svensson GP, Okamoto T, Kawakita A, Goto R, Kato M (2010) Chemical ecology of obligate pollination mutualisms: testing the ‘private channel’ hypothesis in the Breynia–Epicephala association. New Phytol 186:995–1004PubMedCrossRefGoogle Scholar
  151. Svensson GP, Pellmyr O, Raguso RA (2011) Pollinator attraction to volatiles from virgin and pollinated host flowers in a yucca/moth obligate mutualism. Oikos 120:1577–1583CrossRefGoogle Scholar
  152. Szyszka P, Stierle JS, Biergans S, Galizia CG (2012) The speed of smell: odor-object segregation within milliseconds. PLoS ONE 7:e36096PubMedPubMedCentralCrossRefGoogle Scholar
  153. Szyszka P, Gerkin RC, Galizia CG, Smith BH (2014) High-speed odor transduction and pulse tracking by insect olfactory receptor neurons. Proc Natl Acad Sci USA 111:16925–16930PubMedPubMedCentralCrossRefGoogle Scholar
  154. Szyszka P, Galizia CG (2015) Olfaction in insects. In: Doty RL (ed) Handbook of olfaction and gustation, 3rd edn. Wiley, New York, NY, pp 531–545CrossRefGoogle Scholar
  155. Tasin M, Bäckman AC, Coracini M, Casado D, Ioriatti C, Witzgall P (2007) Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68:203–209PubMedCrossRefGoogle Scholar
  156. Terry I, Moore CJ, Walter GH, Forster PI, Roemer RB, Donaldson J, Machin P (2004) Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads. Plant Syst Evol 243:233–247CrossRefGoogle Scholar
  157. Terry I, Walter GH, Moore C, Roemer R, Hull C (2007) Odor-mediated push–pull pollination in cycads. Science 318:70PubMedCrossRefGoogle Scholar
  158. Thompson JN, Schwind C, Guimarães PR Jr, Friberg M (2013) Diversification through multitrait evolution in a coevolving interaction. Proc Natl Acad Sci USA 110:11487–11492PubMedPubMedCentralCrossRefGoogle Scholar
  159. Urru I, Stensmyr MC, Hansson BS (2011) Pollination by brood-site deception. Phytochemistry 72:1655–1666PubMedCrossRefGoogle Scholar
  160. Van Noort S, Ware AB, Compton SG (1989) Pollinator-specific volatile attractants released from the figs of Ficus burtt-davyi. South Afr J Sci 85:323–324Google Scholar
  161. Vereecken NJ, McNeil JN (2010) Cheaters and liars: chemical mimicry at its finest. Can J Zool 88:725–752CrossRefGoogle Scholar
  162. Vickers NJ (2000) Mechanisms of animal navigation in odor plumes. Biol Bull 198:203–212PubMedCrossRefGoogle Scholar
  163. Wang G, Compton SG, Chen J (2013) The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues. Ann Bot 111:173–181PubMedCrossRefGoogle Scholar
  164. Wang N, Wang NX, Niu LM, Bian SN, Xiao JH, Huang DW (2014) Odorant-binding protein (OBP) genes affect host specificity in a fig–pollinator mutualistic system. Insect Mol Biol 23:621–631PubMedCrossRefGoogle Scholar
  165. Webster B, Bruce T, Pickett J, Hardie J (2010) Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim Behav 79:451–457CrossRefGoogle Scholar
  166. Wei Z-D, Kobmoo N, Cruaud A, Kjellberg F (2014) Genetic structure and hybridization in the species group of Ficus auriculata: can closely related sympatric Ficus species retain their genetic identity while sharing pollinators? Mol Ecol 23:3538–3550PubMedCrossRefGoogle Scholar
  167. Weissburg MJ (2000) The fluid dynamical context of chemosensory behavior. Biol Bull 198:188–202PubMedCrossRefGoogle Scholar
  168. Wicher D (2015) Olfactory signaling in insects. In: Glatz R (ed) Progress in molecular biology and translational science, vol 130. Elsevier, New York, NY, pp 37–54Google Scholar
  169. Wilson JK, Kessler A, Woods HA (2015) Noisy communication via airborne infochemicals. Bioscience. doi: 10.1093/biosci/biv062 Google Scholar
  170. Xiao J-H, Yue Z, Jia L-Y, Yang X-H, Niu L-H, Wang Z, Zhang P, Sun B-F, He S-M, Li Z et al (2013) Obligate mutualism within a host drives the extreme specialization of a fig wasp genome. Genome Biol 14:R141PubMedPubMedCentralCrossRefGoogle Scholar
  171. Xu P, Choo Y-M, De La Rosa A, Leal WS (2014) Mosquito odorant receptor for DEET and methyl jasmonate. Proc Natl Acad Sci USA 111:16592–16597PubMedPubMedCentralCrossRefGoogle Scholar
  172. Yáñez-Serrano AM, Nölscher AC, Williams J, Wolff S, Alves E, Martins GA, Bourtsoukidis E, Brito J, Jardine K, Artaxo P, Kesselmeier J (2015) Diel and seasonal changes of biogenic volatile organic compounds within and above an Amazonian rainforest. Atmos Chem Phys 15:3359–3378CrossRefGoogle Scholar
  173. Yang L-Y, Machado CA, Dang X-D, Peng Y-Q, Yang D-R, Zhang D-Y, Liao W-J (2014) The incidence and pattern of copollinator diversification in dioecious and monoecious figs. Evolution 69:294–304CrossRefGoogle Scholar
  174. Zavodna M, Arens P, Van Dijk PJ, Partomihardjo T, Vosman B, Van Damme JM (2005) Pollinating fig wasps: genetic consequences of island recolonization. J Evol Biol 18:1234–1243PubMedCrossRefGoogle Scholar
  175. Zhou X, Rinker DC, Pitts RJ, Rokas A, Zwiebel LJ (2014) Divergent and conserved elements comprise the chemoreceptive repertoire of the nonblood-feeding mosquito Toxorhynchites amboinensis. Genome Biol Evol 6:2883–2896PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Centre for Ecological SciencesIndian Institute of ScienceBangaloreIndia

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