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Chemical communication and coevolution in an ant–plant mutualism

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Abstract

Protective ant–plant interactions provide valuable model systems to study mutualisms. Here, we summarise our recent research on chemical and physiological adaptations that contribute to the stabilisation of the mutualism between Mesoamerican Acacia host plants and their Pseudomyrmex ant inhabitants against exploiters, that is, species using host-derived rewards without rendering a service. Acacia hosts produce food bodies (FBs) and extrafloral nectar (EFN). Both types of reward are chemically adapted to their specific function as ant food and protected from different exploiters. FBs contained higher amounts of specific proteins than the leaves from which they originate. EFN possessed amino acids making it attractive for the mutualist ants and an invertase making its carbohydrate composition nutritionally suitable for the mutualists but unattractive for generalists. Moreover, pathogenesis-related proteins such as glucanases, chitinases and peroxidases were found in EFN, which likely serve as protection from microorganisms. Digestive adaptations were found that make workers of the ant mutualists dependent on the host-derived food sources, a mechanism that likely counteracts the evolution of cheaters. The ants also possessed a high diversity of bacterial associates, several of which appeared involved in nitrogen fixation, thus contributing to the nutrition of these ‘vegetarian’ ants. By contrast, a non-defending ant species that parasitises the host plants appeared physiologically less adapted to the host-derived food rewards; this species, thus, likely is competitively inferior when colony growth is limited by plant-derived rewards. In summary, several physiological adaptations of both host plants and ants stabilise the Acacia–Pseudomyrmex mutualism against exploitation.

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References

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    CAS  PubMed  Google Scholar 

  • Baker HG, Baker I (1975) Studies of nectar-constitution and pollinator-plant coevolution. In: Gilbert F, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 100–140

    Google Scholar 

  • Baker HG, Opler PA, Baker I (1978) A comparison of the amino acid complements of floral and extrafloral nectars. Bot Gaz 139:322–332

    CAS  Google Scholar 

  • Beach RM, Todd JW, Baker SH (1985) Nectaried and nectariless cotton cultivars as nectar sources for the adult soybean looper. J Entomol Sci 20:233–236

    Google Scholar 

  • Bentley BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annu Rev Ecol Syst 8:407–427

    CAS  Google Scholar 

  • Bergstrom CT, Lachmann M (2003) The Red King effect: when the slowest runner wins the coevolutionary race. Proc Natl Acad Sci USA 100:593–598

    CAS  PubMed  Google Scholar 

  • Blüthgen N, Fiedler K (2004) Preferences for sugars and amino acids and their conditionality in a diverse nectar-feeding ant community. J Anim Ecol 73:155–166

    Google Scholar 

  • Boevé JL, Wäckers FL (2003) Gustatory perception and metabolic utilization of sugars by Myrmica rubra ant workers. Oecologia 136:508–514

    PubMed  Google Scholar 

  • Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Google Scholar 

  • Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287. doi:10.1046/j.1461-0248.2001.00218.x

    Google Scholar 

  • Bronstein JL, Huxman T, Horvath B, Farabee M, Davidowitz G (2009) Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator. Ann Bot 103:1435–1443. doi:10.1093/aob/mcp053

    PubMed  Google Scholar 

  • Brouat C, Garcia N, Andary C, McKey D (2001) Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant–plant mutualism. Proc R Soc Lond B 268:2131–2141. doi:10.1098/rspb.2001.1763

    CAS  Google Scholar 

  • Brysch-Herzberg M (2005) Ecology of yeasts in plant–bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 50:87–100

    Google Scholar 

  • Bshary R, Grutter AS (2005) Punishment and partner switching cause cooperative behaviour in a cleaning mutualism. Biol Lett 1:396–399

    PubMed  Google Scholar 

  • Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of co-operation. J Theor Biol 149:63–74. doi:10.1016/S0022-5193(05)80072-4

    CAS  PubMed  Google Scholar 

  • Carter C, Thornburg RW (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci 9:320–324

    CAS  PubMed  Google Scholar 

  • Chandler SM, Wilkinson TL, Douglas AE (2008) Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc R Soc Lond B 275:565–570. doi:10.1098/rspb.2007.1478

    CAS  Google Scholar 

  • Clement LW, Köppen S, Brand WA, Heil M (2008) Strategies of a parasite of the ant–Acacia mutualisms. Behav Ecol Sociobiol 26:953–962. doi:10.1007/s00265-007-0520-1

    Google Scholar 

  • Cornelius ML, Grace JK, Yates JR (1996) Acceptability of different sugars and oils to three tropical ant species (Hymen., Formicidae). Anz Schädlingsk Pflanzensch Umweltsch 69:41–43

    Google Scholar 

  • Dalecky A, Gaume L, Schatz B, McKey D, Kjellberg F (2005) Facultative polygyny in the plant–ant Petalomyrmex phylax (Hymenoptera : Formicinae): sociogenetic and ecological determinants of queen number. Biol J Linn Soc 86:133–151

    Google Scholar 

  • Davidson DW, Patrell-Kim L (1996) Tropical arboreal ants: why so abundant? In: Gibson AC (ed) Neotropical biodiversity and conservation. Mildred E. Mathias Botanical Garden, University of California, Los Angeles, pp 127–140

    Google Scholar 

  • Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972. doi:10.1126/science.1082074

    CAS  PubMed  Google Scholar 

  • Dean MD (2006) A Wolbachia-associated fitness benefit depends on genetic background in Drosophila simulans. Proc R Soc Lond B 273:1415–1420. doi:10.1098/rspb.2005.3453

    CAS  Google Scholar 

  • Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237:187–193

    CAS  PubMed  Google Scholar 

  • Doebeli M, Hauert C (2005) Models of cooperation based on the Prisoner’s Dilemma and the Snowdrift game. Ecol Lett 8:748–766. doi:10.1111/j.1461-0248.2005.00773.x

    Google Scholar 

  • Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680

    CAS  PubMed  Google Scholar 

  • Doebeli M, Hauert C, Killingback T (2004) The evolutionary origin of cooperators and defectors. Science 306:859–862

    CAS  PubMed  Google Scholar 

  • Douglas AE (2008) Conflict, cheats and the persistence of symbioses. New Phytol 177:849–858

    PubMed  Google Scholar 

  • Duarte Rocha CF, Godoy Bergallo H (1992) Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant–plant: Azteca muelleri vs. Coelomera ruficornis on Cecropia pachystachia. Oecologia 91:249–252

    Google Scholar 

  • Edwards DP, Hassall M, Sutherland WJ, Yu DW (2006) Selection for protection in an ant–plant mutualism: host sanctions, host modularity and the principal-agent game. Proc R Soc Lond B 273:595–602. doi:10.1098/rspb.2005.3273

    Google Scholar 

  • Eilmus S, Heil M (2009) Bacterial associates of arboreal ants and their putative functions in an obligate ant–plant mutualism. Appl Environ Microbiol 75:4324–4332. doi:10.1128/AEM.00455-09

    CAS  PubMed  Google Scholar 

  • Federle W, Fiala B, Zizka G, Maschwitz U (2001) Incident daylight as orientation cue for hole-boring ants: prostomata in Macaranga ant–plants. Ins Soc 48:165–177

    Google Scholar 

  • Feldhaar H, Fiala B, bin Hashim R, Maschwitz U (2000) Maintaining an ant–plant symbiosis: secondary polygyny in the Macaranga triloba-Crematogaster sp. association. Naturwissenschaften 87:408–411

    CAS  PubMed  Google Scholar 

  • Ferrière R, Gauduchon M, Bronstein JL (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecol Lett 10:115–126. doi:10.1111/j.1461-0248.2006.01008.x

    PubMed  Google Scholar 

  • Folgarait PJ, Johnson HL, Davidson DW (1994) Responses of Cecropia to experimental removal of Müllerian bodies. Funct Ecol 8:22–28

    Google Scholar 

  • Fonseca CR (1993) Nesting space limits colony size of the plant–ant Pseudomyrmex concolor. Oikos 67:473–482

    Google Scholar 

  • Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293

    CAS  PubMed  Google Scholar 

  • Gaume L, McKey D (1999) An ant–plant mutualism and its host-specific parasite: activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant–ants inhabiting the same myrmecophyte. Oikos 84:130–144

    Google Scholar 

  • Gaume L, Zacharias M, Borges RM (2005) Ant–plant conflicts and a novel case of castration parasitism in a myrmecophyte. Evol Ecol Res 7:435–452

    Google Scholar 

  • González-Teuber M, Heil M (2009) The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists. J Chem Ecol 35:459–468. doi:10.1007/s10886-009-9618-4

    PubMed  Google Scholar 

  • González-Teuber M, Eilmus S, Muck A, Svatos A, Heil M (2009) Pathogenesis-related proteins protect extrafloral nectar from microbial infestation. Plant J 58:464–473. doi:10.1111/j.1365-313X.2009.03790.x

    PubMed  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour I and II. J Theor Biol 7:1–16, 17–52

    Google Scholar 

  • Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61. doi:10.1111/j.1469-8137.2007.02330.x

    CAS  PubMed  Google Scholar 

  • Heil M, McKey D (2003) Protective ant–plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453. doi:10.1146/annurev.ecolsys.34.011802.132410

    Google Scholar 

  • Heil M, Fiala B, Linsenmair KE, Zotz G, Menke P, Maschwitz U (1997) Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via mutualistic ant partners. J Ecol 85:847–861

    Google Scholar 

  • Heil M, Fiala B, Baumann B, Linsenmair KE (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct Ecol 14:749–757. doi:10.1046/j.1365-2435.2000.00480.x

    Google Scholar 

  • Heil M, Hilpert A, Fiala B, Linsenmair KE (2001a) Nutrient availability and indirect (biotic) defence in a Malaysian ant–plant. Oecologia 126:404–408. doi:10.1007/s004420000534

    Google Scholar 

  • Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001b) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088

    CAS  PubMed  Google Scholar 

  • Heil M, Baumann B, Krüger R, Linsenmair KE (2004a) Main nutrient compounds in food bodies of Mexican Acacia ant–plants. Chemoecology 14:45–52. doi:10.1007/s00049-003-0257-x

    CAS  Google Scholar 

  • Heil M, Greiner S, Meimberg H, Krüger R, Noyer J-L, Heubl G, Linsenmair KE, Boland W (2004b) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208. doi:10.1038/nature02703

    CAS  PubMed  Google Scholar 

  • Heil M, Hilpert A, Krüger R, Linsenmair KE (2004c) Competition among visitors to extrafloral nectaries as a source of ecological costs of an indirect defence. J Trop Ecol 20:201–208. doi:10.1017/S026646740300110X

    Google Scholar 

  • Heil M, Rattke J, Boland W (2005) Post-secretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308:560–563. doi:10.1126/science.1107536

    CAS  PubMed  Google Scholar 

  • Heil M, González-Teuber M, Clement LW, Kautz S, Verhaagh M, Silva Bueno JC (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096. doi:10.1073/pnas.0904304106

    Google Scholar 

  • Herrera CM, Garcia IM, Perez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–2376

    PubMed  Google Scholar 

  • Herrera CM, De Vega C, Canto A, Pozo MI (2009) Yeasts in floral nectar: a quantitative survey. Ann Bot 103:1415–1423. doi:10.1093/aob/mcp026

    PubMed  Google Scholar 

  • Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220. doi:10.1111/j.1574-6968.2008.01110.x

    CAS  PubMed  Google Scholar 

  • Hoeksema JD, Bruna EM (2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125:321–330. doi:10.1007/s004420000496

    Google Scholar 

  • Hoeksema JD, Kummel M (2003) Ecological persistence of the plant-mycorrhizal mutualism: a hypothesis from species coexistence theory. Am Nat 162:S40–S50. doi:10.1086/378644

    PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin

    Google Scholar 

  • Izzo TJ, Vasconcelos HL (2002) Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant–plant. Oecologia 133:200–205. doi:10.1007/s00442-002-1027-0

    Google Scholar 

  • Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275

    Google Scholar 

  • Janzen DH (1974) Swollen-thorn acacias of Central America. Smithsonian Institution Press, Washington

    Google Scholar 

  • Janzen DH (1975) Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188:936–937. doi:10.1126/science.188.4191.936

    CAS  PubMed  Google Scholar 

  • Kautz S, Lumbsch HT, Ward PS, Heil M (2009a) How to prevent cheating: a digestive specialization ties mutualistic plant–ants to their ant–plant partners. Evolution 63:839–853. doi:10.1111/j.1558-5646.2008.00594.x

    CAS  PubMed  Google Scholar 

  • Kautz S, Pauls SU, Ballhorn DJ, Heil M (2009b) Polygynous supercolonies of the acacia–ant Pseudomyrmex peperi, an inferior colony founder. Mol Ecol. doi:10.1111/j.1365-294X.2009.04395.x

  • Kautz S, Schmid VS, Trindl A, Heinze J, Ballhorn DJ, Heil M (2009c) Isolation and characterization of microsatellite loci in the plant–ant Pseudomyrmex ferrugineus (Formicidae: Pseudomyrmecinae) and cross-testing for two congeneric species. Mol Ecol Resources 9:1016–1019. doi:10.1111/j.1755-0998.2009.02569.x

    CAS  Google Scholar 

  • Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume–rhizobium mutualism. Nature 425:78–81. doi:10.1038/nature01931

    CAS  PubMed  Google Scholar 

  • Kobayashi S, Asai T, Fujimoto Y, Kohshima S (2008) Anti-herbivore structures of Paulownia tomentosa: morphology, distribution, chemical constituents and changes during shoot and leaf development. Ann Bot 101:1035–1047. doi:10.1093/aob/mcn033

    CAS  PubMed  Google Scholar 

  • Koptur S (1992) Extrafloral nectary-mediated interactions between insects and plants. In: Bernays EA (ed) Insect–plant interactions, vol IV. CRC Press, Boca Raton, pp 81–129

    Google Scholar 

  • Lanza J, Vargo EL, Pulim S, Chang YZ (1993) Preferences of the fire ants Solenopsis invicta and S. geminata (Hymenoptera: Formicidae) for amino acid and sugar components of extrafloral nectars. Environ Entomol 22:411–417

    CAS  Google Scholar 

  • Letourneau DK (1990) Code of ant–plant mutualism broken by parasite. Science 248:215–217. doi:10.1126/science.248.4952.215

    CAS  PubMed  Google Scholar 

  • Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350

    CAS  PubMed  Google Scholar 

  • Mithöfer A (2002) Suppression of plant defence in rhizobia–legume symbiosis. Trends Plant Sci 10:440–444

    Google Scholar 

  • Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225

    Google Scholar 

  • Mondor EB, Addicott JF (2003) Conspicuous extra-floral nectaries are inducible in Vicia faba. Ecol Lett 6:495–497

    Google Scholar 

  • Morris WF, Bronstein JL, Wilson WG (2003) Three-way coexistence in obligate mutualist-exploiter interactions: the potential role of competition. Am Nat 161:860–875

    PubMed  Google Scholar 

  • Nardi JB, Mackie RI, Dawson JO (2002) Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J Insect Physiol 48:751–763

    CAS  PubMed  Google Scholar 

  • Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87:912–921

    CAS  PubMed  Google Scholar 

  • Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Heidelberg, pp 215–263

    Google Scholar 

  • Palmer TM (2004) Wars of attrition: colony size determines competitive outcomes in a guild of African acacia ants. Anim Behav 68:993–1004

    Google Scholar 

  • Pellmyr O, Huth CJ (1994) Evolutionary stability of mutualism between yuccas and yucca moth. Nature 372:257–260

    CAS  Google Scholar 

  • Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc R Soc Lond B 273:2097–2106. doi:10.1098/rspb.2006.3541

    Google Scholar 

  • Pulice CE, Packer AA (2008) Simulated herbivory induces extrafloral nectary production in Prunus avium. Funct Ecol 22:801–807. doi:10.1111/j.1365-2435.2008.01440.x

    Google Scholar 

  • Raine NE, Gammans N, Macfadyen IJ, Scrivner GK, Stone GN (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant–plant. Ecol Entomol 29:345–352. doi:10.1111/j.0307-6946.2004.00608.x

    Google Scholar 

  • Rickson FR (1969) Developmental aspects of the shoot apex, leaf, and Beltian bodies of Acacia cornigera. Am J Bot 56:195–200

    Google Scholar 

  • Rickson FR (1975) The ultrastructure of Acacia cornigera L. Beltian body tissue. Am J Bot 62:913–922

    Google Scholar 

  • Risch SJ, Rickson F (1981) Mutualism in which ants must be present before plants produce food bodies. Nature 291:149–150. doi:10.1038/291149a0

    Google Scholar 

  • Roesch C, Bothe H (2005) Improved assessment of denitrifying, nitrogen-fixing, and total-community bacteria by terminal restriction fragment length polymorphism [tRFLP] analysis using multiple restriction enzymes. Appl Environ Microbiol 71:2026–2035

    CAS  Google Scholar 

  • Rogers WE, Siemann E, Lankau RA (2003) Damage induced production of extrafloral nectaries in native and invasive seedlings of Chinese tallow tree (Sapium sebiferum). Am Midl Natural 149:413–417

    Google Scholar 

  • Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. doi:10.1016/j.tree.2006.06.018

    PubMed  Google Scholar 

  • Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135–160

    PubMed  Google Scholar 

  • Sandhu DK, Waraich MK (1985) Yeast associated with pollinating bees and flower nectar. Microbial Ecol 11:51–58

    Google Scholar 

  • Segraves K, Althoff D, Pellmyr O (2005) Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths. Proc R Soc Lond B 272:2195–2201

    Google Scholar 

  • Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs JL, Urbina M, Tausczik Y (2006) An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction. Proc R Soc Lond B 273:77–81

    Google Scholar 

  • Stapel JO, Cortesero AM, DeMoraes CM, Tumlinson JH, Lewis WJ (1997) Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environ Entomol 26:617–623

    Google Scholar 

  • Stoll S, Gadau J, Gross R, Feldhaar H (2007) Bacterial microbiota associated with ants of the genus Tetraponera. Biol J Linn Soc 90:399–412. doi:10.1111/j.1095-8312.2006.00730.x

    Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542

    CAS  PubMed  Google Scholar 

  • Thornburg RW (2007) Molecular biology of the Nicotiana floral nectary. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and Nectar. Springer, Heidelberg, pp 265–287

    Google Scholar 

  • Thornburg RW, Carter C, Powell A, Mittler R, Rizhsky L, Horner HT (2003) A major function of the tobacco floral nectary is defense against microbial attack. Plant Syst Evol 238:211–218

    Google Scholar 

  • Tillberg CV (2004) Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis. Oecologia 140:506–515. doi:10.1007/s00442-004-1601-8

    PubMed  Google Scholar 

  • Tobin JE (1995) Ecology and diversity of tropical forest canopy ants. In: Lowman MD, Nadkarni NM (eds) Forest canopies. Academic Press, San Diego, pp 129–147

    Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Google Scholar 

  • Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    PubMed  Google Scholar 

  • Vander Meer RK, Lofgren CS, Seawright JA (1995) Specificity of the red imported fire ant (Hymenoptera, Formicidae) phagostimulant response to carbohydrates. Florida Entomol 78:144–154

    CAS  Google Scholar 

  • Wäckers FL, Wunderlin R (1999) Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomol Exp Appl 91:149–154

    Google Scholar 

  • Ward PS (1993) Systematic studies on Pseudomyrmex acacia–ants (Hymenoptera: Formicidae: Pseudomyrmecinae). J Hym Res 2:117–168

    Google Scholar 

  • Werren JH, Windsor D, Guo LR (1995) Distribution of Wolbachia among neotropical arthropods. Proc R Soc Lond B 262:197–204

    Google Scholar 

  • West SA, Kiers ET, Simms EL, Denison RF (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc Lond B Biol Sci 269:685–694

    Google Scholar 

  • Wooley SC, Donaldson JR, Gusse AC, Lindroth RL, Stevens MT (2007) Extrafloral nectaries in aspen (Populus tremuloides): Heritable genetic variation and herbivore-induced expression. Ann Bot 100:1337–1346. doi:10.1093/aob/mcm220

    PubMed  Google Scholar 

  • Yu DW (2001) Parasites of mutualisms. Biol J Linn Soc 72:529–546

    Google Scholar 

  • Yu DW, Pierce NE (1998) A castration parasite of an ant–plant mutualism. Proc R Soc Lond B 265:375–382. doi:10.1098/rspb.1998.0305

    Google Scholar 

  • Zientz E, Beyaert N, Gross R, Feldhaar H (2006) Relevance of the endosymbiosis of Blochmannia floridanus and carpenter ants at different stages of the life cycle of the host. Schriftenr Vegetationskunde 72:6027–6033

    CAS  Google Scholar 

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Acknowledgments

We thank Rosa Maria Adame-Álvarez, Ralf Krüger and Juan Carlos Silva Bueno for help with field work, Doyle McKey for many valuable comments on an earlier version of this manuscript and the German Research Foundation (DFG grant He3169/4-2) and CONACyT for financial support.

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  1. Departamento de Ingeniería Genética, CINVESTAV-Irapuato, Km. 9.6 Libramiento Norte, CP 36821, Irapuato, Guanajuato, Mexico

    Martin Heil & Domancar Orona-Tamayo

  2. Department of General Botany-Plant Ecology, FB BioGeo, University of Duisburg-Essen, Universitätsstraße 5, 45117, Essen, Germany

    Sascha Eilmus, Stefanie Kautz & Marcia González-Teuber

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Correspondence to Martin Heil.

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Heil, M., Orona-Tamayo, D., Eilmus, S. et al. Chemical communication and coevolution in an ant–plant mutualism. Chemoecology 20, 63–74 (2010). https://doi.org/10.1007/s00049-009-0036-4

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