Abstract
The palaeotropic genus Macaranga (Euphorbiaceae) is an excellent model system to analyze co-evolutionary processes associated with myrmecophytism, a mutualistic interaction between plants and ants. Ant-plants like Macaranga provide nesting space and feed their partners, whereas the ants protect the plants from herbivores and competitors such as lianas. We used genome-based evidence to investigate speciation mechanisms in Macaranga ant-plants, and their co-evolution with ants from the genus Crematogaster. Our previous work had shown that myrmecophytic Macaranga species show little genetic differentiation, suggesting an adaptive radiation. We hypothesized that the obligatory symbiosis with ants may reduce gene flow among plant populations, eventually enhancing allopatric speciation. To test this hypothesis, we verified the monophyly of the investigated plant lineages by phylogenetic analyses, reconstructed parsimony networks based on chloroplast DNA (cpDNA) variation, and assessed population genetic parameters using nuclear microsatellites and cpDNA haplotypes. Our data provided evidence for vicariant events as well as for hybridization and cpDNA introgression among closely related Macaranga species. The extent of population differentiation within myrmecophytic versus non-myrmecophytic species proved to be in a similar range, indicating that our working hypothesis of enhanced allopatric speciation in myrmecophytes cannot be sustained by the present evidence. Nevertheless, the mutualistic interactions of Macaranga and associated ants may be a key innovation that opened an adaptive zone putatively exploited by the divergence of Macaranga.
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References
Ayala FJ, Wetterer JK, Longino JT, Hartl DL (1996) Molecular phylogeny of Azteca ants (Hymenoptera: Formicidae) and the colonization of Cecropia trees. Mol Phylogenet Evol 5:423–428
Baier C, Guicking D, Prinz K, Fey-Wagner C, Wöhrmann T, Weising K, Debener T, Schie S, Blattner FR (2009) Isolation and characterization of eleven new microsatellite markers for Macaranga (Euphorbiaceae). Mol Ecol Resour 9:1049–1052
Bänfer G, Fiala B, Weising K (2004) AFLP analysis of phylogenetic relationships among myrmecophytic species of Macaranga (Euphorbiaceae) and their allies. Plant Syst Evol 248:213–231
Bänfer G, Moog U, Fiala B, Mohamed M, Weising K, Blattner FR (2006) A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in southeast Asia reveals hybridization, vicariance and long distance dispersals. Mol Ecol 15:4409–4424
Blattner FR, Weising K, Bänfer G, Maschwitz U, Fiala B (2001) Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Mol Phylogenet Evol 19:331–344
Brouat C, Gielly L, McKey D (2001) Phylogenetic relationships in the genus Leonardoxa (Leguminosae: Caesalpinioideae) inferred from chloroplast trnL intron and trnL-trnF intergenic spacer sequences. Am J Bot 88:143–149
Cannon CH, Manos PS (2003) Phylogeography of the Southeast Asian stone oaks (Lithocarpus). J Biogeogr 30:211–226
Chenuil A, McKey DB (1996) Molecular phylogenetic study of a myrmecophyte symbiosis: did Leonardoxa/ant associations diversify via cospeciation? Mol Phylogenet Evol 6:270–286
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant-plant relationships. J Hym Res 2:13–83
Davies SJ (2001) Systematics of Macaranga sects Pachystemon and Pruinosae (Euphorbiaceae). Harv Paper Bot 6:371–448
Davies SJ, Lum SKY, Chan RKG, Wang LK (2001) Evolution of myrmecophytism in western Malesian Macaranga (Euphorbiaceae). Evolution 55:1542–1559
Dorstewitz W (2008) Populationsgenetik von Arten der Gattung Macaranga, Sektion Pachystemon in Südostasien. Diploma Thesis, University of Kassel, Germany
Elias M, Gompert Z, Jiggins C, Willmott K (2008) Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol 6(12):e300
Ennos RA, Sinclair WT, Hu XS, Langdon A (1999) Using organelle markers to elucidate the history, ecology and evolution of plant populations. In: Hollingsworth PM, Bateman RM, Gornall RJ (eds) Molecular systematics and plant evolution. Taylor & Francis, London, pp 1–19
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50
Federle W, Maschwitz U, Fiala B, Riederer M, Hölldobler B (1997) Slippery ant-plants and skillful climbers: Selection and protection of the specific partner ants by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112:217–224
Federle W, Fiala B, Zizka G, Maschwitz U (2001) Incident daylight as orientation cure for hole-boring ants: prostomata in Macaranga ant-plants. Insect Soc 48:165–177
Feldhaar H, Fiala B, Gadau J, Mohamed M, Maschwitz U (2003a) Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees. Mol Phylogenet Evol 27:441–452
Feldhaar H, Fiala B, Rosli BH, Maschwitz U (2003b) Patterns of the Crematogaster-Macaranga association: the ant partner makes the difference. Insect Soc 50:9–19
Fiala B, Maschwitz U (1991) Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism. Biol J Linn Soc 44:287–305
Fiala B, Maschwitz U (1992a) Domatia as most important preadaptations in the evolution of myrmecophytes in a paleotropical tree genus. Plant Syst Evol 180:53–64
Fiala B, Maschwitz U (1992b) Food bodies and their significance for obligate ant-association in the tree genus Macaranga (Euphorbiaceae). Bot J Linn Soc 110:61–75
Fiala B, Maschwitz U, Tho YP, Helbig AJ (1989) Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463–470
Fiala B, Jakob A, Maschwitz U, Linsenmair KE (1999) Diversity, evolutionary specialization and geographic distribution of a mutualistic ant–plant complex: Macaranga and Crematogaster in South East Asia. Biol J Linn Soc 66:305–331
Guicking D, Tikam SR, Blattner FR, Weising K (2006) Microsatellite markers for the palaeotropic pioneer tree genus Macaranga (Euphorbiaceae) and their cross-species transferability. Mol Ecol Notes 6:245–248
Guicking D, Kröger-Kilian T, Weising K, Blattner FR (2008) Single nucleotide sequence analysis: a cost- and time-effective protocol for the analysis of microsatellite- and indel-rich chloroplast DNA regions. Mol Ecol Resour 8:62–65
Heckroth HP, Fiala B, Gullan PJ, Idris AHJ, Maschwitz U (1998) The soft scale (Coccidae) associates of Malaysian ant-plants. J Trop Ecol 14:427–443
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
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 symbiotic ant partners. J Ecol 85:847–861
Heil M, Fiala B, Kaiser W, Linsenmair KE (1998) Chemical contents of Macaranga food bodies: physiological adaptations to their role in ant attraction and nutrition. Funct Ecol 12:117–122
Heil M, Fiala B, Boller T, Linsenmair KE (1999) Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86:146–149
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001a) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defense response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088
Heil M, Fiala B, Maschwitz U, Linsenmair KE (2001b) On the benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126:394–403
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53
Jakob SS, Blattner FR (2006) A chloroplast genealogy of Hordeum (Poaceae): long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Mol Biol Evol 23:1602–1612
Jolivet P (1996) Ants and plants: an example of coevolution (enlarged edition). Backhuys, Leiden
Kröger-Kilian T (2006) Vergleichende Untersuchungen zur genetischen Diversität und Populationsstruktur der Ameisenpflanzenarten Macaranga hypoleuca und Macaranga beccariana (Euphorbiaceae) in Südostasien. Diploma Thesis, University of Kassel, Germany
Kulju KKM, Sierra SEC, Draisma SGA, Samuel R, van Welzen PC (2007) Molecular phylogeny of Macaranga, Mallotus, and related genera. Am J Bot 94:1726–1743
Lewis T (1973) Thrips: their biology, ecology and economic importance. Academic, New York
Léotard G, Saltmarsh A, Kjellberg F, McKey D (2008) Mutualism, hybrid inviability and speciation in a tropical ant-plant. J Evol Biol 21:1133–1143
Maschwitz U, Fiala B, Davies SJ, Linsenmair KE (1996) A south-east Asian myrmecophyte with two alternative inhabitants: Camponotus or Crematogaster as partners of Macaranga lamellata. Ecotropica 2:29–40
Maschwitz U, Fiala B, Dumpert K (2004) An unusual myrmecophytic Macaranga association, occurring in a disjunct area in the monsoon zone of Southeast Asia: phenology and description of the ant species. Ecotropica 10:33–49
McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM (2001) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55:703–711
Moog U (2002) Die Reproduktion von Macaranga (Euphorbiaceae) in Südostasien: Bestäubung durch Thripse und Kastration durch Pflanzenameisen. PhD thesis, University of Frankfurt
Moog U, Fiala B, Federle W, Maschwitz U (2002) Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia. Am J Bot 89:50–59
Mound LA, Marullo R (1996) The thrips of Central and South America: an introduction. Mem Entomol Int 6:1–488
Nason JD, Herre EA, Hamrick JL (1998) The breeding structure of a tropical keystone plant resource. Nature 391:685–687
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Pierce NE (1987) The evolution and biogeography of associations between lycaenid butterflies and ants. Oxford Surv Evol Biol 4:89–116
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quek SP, Davies SJ, Itino T, Pierce NE (2004) Codiversification in an ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution 58:554–570
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352
Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Mol Ecol 7:465–474
Schemske DW (2002) Ecological and evolutionary perspectives on the origins of tropical diversity. In: Chazdon RL, Whitmore TC (eds) Foundations of tropical forest biology. University of Chicago Press, Chicago, pp 163–173
Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Vogel M, Bänfer G, Moog U, Weising K (2003) Development and characterization of chloroplast microsatellite markers in Macaranga (Euphorbiaceae). Genome 46:845–857
Weising K, Gardner RG (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19
Whitmore TC (1975) Macaranga. In: Airy Shaw HK (ed) The Euphorbiaceae of Borneo. Kew Bull Add Ser 4:140–159
Whitmore TC (1982) Macaranga Thou. Kew Bull 36:312–323
Whitmore TC (1987) Biogeographical evolution of the Malay Archipelago. Clarendon, Oxford
Whitmore TC (2008) The genus Macaranga - a prodromus. Kew Publishing, Kew
Acknowledgments
We acknowledge financial support by Deutsche Forschungsgemeinschaft (grants We 1830/4, Fi 606/5 and Bl 462/2) within priority program SPP1127. Permission to conduct research in Malaysia was kindly granted by the Economic Planning Unit (EPU) of the Prime Minister´s Office, Kuala Lumpur and EPU in Kota Kinabalu, Sabah, as well as the Danum Valley Management Committee and the Forest Department, Sarawak. The permit to work in Brunei was obtained by Universiti Brunei Darussalam and Brunei Museum. We thank our counterparts and colleagues in Malaysia and Brunei for their cooperation and support, especially Prof. Datin Dr. Maryati Mohamed, Dr. Rosli bin Hashim, Dr. Kamariah Abu Salim, and members of Sabah Parks, namely Dr. Jamili Nais and Dr. Maklarin bin Lakim. Logistic support and help in many other ways by Prof. Dr. K. Eduard Linsenmair is gratefully acknowledged. We thank Dr. Ferry Slik and Prof. Dr. Ulrich Maschwitz for the kind supply of plant material, and Dr. Heike Feldhaar for fruitful discussions on ant–plant interactions. Two anonymous reviewers provided valuable suggestions.
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Weising, K. et al. (2010). Mechanisms of Speciation in Southeast Asian Ant-Plants of the Genus Macaranga (Euphorbiaceae). In: Glaubrecht, M. (eds) Evolution in Action. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12425-9_9
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