Codiversification in an ant-plant mutualism: Stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae)

Evolution

Volumn 58, Issue 3, 2004, Pages 554-570

  Quek, Swee Peck ^a   Davies, Stuart J ^a   Itino, Takao ^b   Pierce, Naomi E ^a  

^a HARVARD UNIVERSITY   (United States)

^b SHINSHU UNIVERSITY   (Japan)

Author keywords

Coevolution; Cospeciation; Decacrema; Macaranga; Myrmecophyte; Phytoecy; Southeast Asia

Indexed keywords

ANT; COEVOLUTION; EVOLUTION; HOST USE; MUTUALISM; MYRMECOPHYTE; PHYLOGENETICS; RECONSTRUCTION;

ANIMALIA; ARTHROPODA; CREMATOGASTER; DECACREMA; EUPHORBIA; EUPHORBIACEAE; FORMICIDAE; HYMENOPTERA; MACARANGA; MYRMICINAE;

EID: 1842580505     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01678.x     Document Type: Article

References (118)

1. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Autom. Contr. 19:716-723.
2. Alvarez, G., I. Armbrecht, E. Jimenez, H. Armbrecht, and P. Ulloa-Chacon. 2001. Ant-plant association in two Tococa species from a primary rain forest of Colombian Choco (Hymenoptera: Formicidae). Sociobiology 38:585-602.
3. André, E. 1896. Fourmis nouvelles d'Asie et d'Australie. Rev. Entomol. 15:251-265.
4. Avise, J. C. 1994. Molecular markers, natural history and evolution. Chapman and Hall, New York.
5. Ayala, F. J., J. K. Wetterer, J. T. Longino, and D. L. Hartl. 1996. Molecular phylogeny of Azteca ants (Hymenoptera: Formicidae) and the colonization of Cecropia trees. Mol. Phylogenet. Evol. 5:423-428.
6. Baldwin, B. G., and M. J. Sanderson. 1998. Age and rate diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA 95:9402-9406.
7. Ballard, J. W. O. 2000. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17: 1126-1130.
8. Beltran, M., C. D. Jiggins, V. Bull, M. Linares, J. Mallet, W. O. McMillan, and E. Bermingham. 2002. Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. Mol. Biol. Evol. 19: 2176-2190.
9. Bequaert, J. 1922. Ants in their diverse relations to the plant world. B. Am. Mus. Nat. Hist. 45:333-584.
10. Blattner, F. R., K. Weising, G. Banfer, U. Maschwitz, and B. Fiala. 2001. Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Mol. Phylogenet. Evol. 19:331-344.
11. Bolton, B. 1995. A new general catalogue of the ants of the world. Harvard Univ. Press, Cambridge, MA.
12. Bremer, K. 1994. Branch support and tree stability. Cladistics 10:295-304.
13. Bronstein, J. L. 1998. The contribution of ant plant protection studies to our understanding of mutualism. Biotropica 30:150-161.
14. Brouat, C., N. Garcia, C. Andary, and D. McKey. 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.
15. Brower, A. V. Z. 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA. 91:6491-6495.
16. Brower, A. V. Z., R. DeSalle, and A. Vogler. 1996. Gene trees, species trees and systematics. Annu. Rev. Ecol. Syst. 27:423-450.
17. Brown, K. S. 1981. The biology of Heticonius and related genera. Annu. Rev. Entomol. 26:427-456.
18. Buckley, T. R., C. Simon, and G. K. Chambers. 2001. Phylogeography of the New Zealand cicada Maoricicada campbelli based on mitochondrial DNA sequences: ancient clades associated with Cenozoic environmental change. Evolution 55:1395-1407.
19. Caccone, A., and V. Sbordoni. 2001. Molecular biogeography of cave life: a study using mitochondrial DNA from Bathysciine beetles. Evolution 55:122-130.
20. Chenuil, A., and D. B. McKey. 1996. Molecular phylogenetic study of a myrmecophyte symbiosis: Did Leonardoxa/ant associations diversify via cospeciation? Mol. Phylogenet. Evol. 6:270-286.
21. Clary, D. O., and D. R. Wolstenholme. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 22:252-271.
22. Crozier, R. H., and Y. C. Crozier. 1993. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133:97-117.
23. Davidson, D. W., and D. McKey. 1993. The evolutionary ecology of symbiotic ant-plant relationships. J. Hym. Res. 2:13-83.
24. Davies, S. J. 2001a. Systematics of Macaranga sections Pachystemon and Pruinosae (Euphorbiaceae). Harv. Pap. Bot. 6: 371-448.
25. _. 2001b. Tree mortality and growth in 11 sympatric Macaranga species in Borneo. Ecology 82:920-932.
26. Davies, S. J., P. A. Palmiotto, P. S. Ashton, H. S. Lee, and J. V. Lafrankie. 1998. Comparative ecology of 11 sympatric species of Macaranga in Borneo: tree distribution in relation to horizontal and vertical resource heterogeneity. J. Ecol. 86:662-673.
27. Davies, S. J., S. K. Y. Lum, R. Chan, and L. K. Wang. 2001. Evolution of myrmecophytism in western Malesian Macaranga (Euphorbiaceae). Evolution 55:1542-1559.
28. Davis, C. C. D., C. D. Bell, P. W. Fritsch, and S. Mathews. 2002. Phylogeny of Acridocarpus-Brachylophon (Malpighiaceae): implications for Tertiary tropical floras and AfroAsian biogeography. Evolution 56:2395-2405.
29. Denno, R. F., M. S. McClure, and J. R. Ott. 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40:297-331.
30. Desdevises, Y., S. Morand, O. Jousson, and P. Legendre. 2002. Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution 56:2459-2471.
31. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
32. Eriksson, T. 2001. Autodecay. Bergius Foundation of the Royal Swedish Academy of Sciences, Stockholm, Sweden.
33. Farrell, B. D. 1998. "Inordinate fondness" explained: Why are there so many beetles? Science 281:555-559.
34. _. 2001. Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. Mol. Phylogenet. Evol. 18:467-478.
35. Farrell, B., and C. Mitter. 1990. Phylogenesis of insect plant interactions: Have Phyllobrotica leaf beetles (Chrysomelidae) and the Lamiales diversified in parallel? Evolution 44:1389-1403.
36. _. 1998. The timing of insect/plant diversification: Might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biol. J. Linn. Soc. 63:553-577.
37. Farrell, B. D., A. S. Sequeira, B. C. O'Meara, B. B. Normark, J. H. Chung, and B. H. Jordal. 2001. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011-2027.
38. Farris, J. S., M. Källersjö, A. C. Kluge, and C. Bult. 1994. Testing significance of incongruence. Cladistics 10:315-319.
39. Federle, W., U. Maschwitz, B. Fiala, M. Riederer, and B. Holldobler. 1997. Slippery ant-plants and skillful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112:217-224.
40. Federle, W., B. Fiala, and U. Maschwitz. 1998. Camponotus (Colobopsis) (Mayr 1861) and Macaranga (Thouars 1806): a specific two-partner ant-plant system from Malaysia. Trop. Zool. 11: 83-94.
41. Federle, W., K. Rohrseitz, and B. Hölldobler. 2000. Attachment forces of ants measured with a centrifuge: better 'wax-runners' have a poorer attachment to a smooth surface. J. Exp. Biol. 203:505-512.
42. Federle, W., U. Maschwitz, and B. Hölldobler. 2002. Pruning of host plant neighbours as defence against enemy ant invasions: Crematogaster ant partners of Macaranga protected by 'wax barriers' prune less than their congeners. Oecologia 132:264-270.
43. Feldhaar, H., B. Fiala, R. bin Hashim, and U. Maschwitz. 2000. Maintaining an ant-plant symbiosis: secondary polygyny in the Macaranga triloba-Crematogaster sp. association. Naturwissenschaften 87:408-411.
44. Feldhaar, H., B. Fiala, J. Gadau, M. Mohamed, and U. Maschwitz. 2003. Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees. Mol. Phylogenet. Evol. 27:441-452.
45. Fiala, B., and U. Maschwitz. 1990. Studies on the Southeast Asian ant-plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insectes Soc. 37:212-231.
46. Fiala, B., U. Maschwitz, T. Y. Pong, and A. J. Helbig. 1989. Studies of a Southeast Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463-470.
47. Fiala, B., U. Maschwitz, and K. E. Linsenmair. 1996. Macaranga caladiifolia, a new type of ant-plant among Southeast Asian myrmecophytic Macaranga species. Biotropica 28:408-412.
48. Fiala, B., A. Jakob, and U. Maschwitz. 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.
49. Forel, A. 1910. Glanures myrmécologiques. Ann. Soc. Entomol. Belg. 54:6-32.
50. _. 1911. Fourmis de Bornéo, Singapore, Ceylan, etc. Rev. Suisse Zool. 19:23-62.
51. Harley, R. 1991. The greasy pole syndrome. Pp. 430-433 in C. R. Huxley and D. F. Cutler, eds. Ant-plant interactions. Oxford Univ. Press, Oxford, U.K.
52. Heckroth, H. P., B. Fiala, P. J. Gullan, A. H. Idris, and U. Maschwitz. 1998. The soft scale (Coccidae) associates of Malaysian ant-plants. J. Trop. Ecol. 14:427-443.
53. Heil, M., B. Fiala, K. E. Linsenmair, and T. Boller. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86:146-149.
54. Hoelzer, G. A. 1997. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51:622-626.
55. Holmquist, R. 1983. Transitions and transversions in evolutionary descent: an approach to understanding. J. Mol. Evol. 19:134-144.
56. Huelsenbeck, J. P., and B. Rannala. 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227-232.
57. Huelsenbeck, J. P., and F. Ronquist. 2000. MrBayes: Bayesian inference of phylogeny. Department of Biology, Univ. of Rochester, Rochester, NY.
58. Itino, T., and T. Itioka. 2001. Interspecific variation and ontogenetic change in anti-herbivore defense in myrmecophytic Macaranga species. Ecol. Res. 16:765-774.
59. Itino, T., S. J. Davies, H. Tada, Y. Hieda, M. Inoguchi, T. Itioka, S. Yamane, and T. Inoue. 2001. Cospeciation of ants and plants. Ecol. Res. 16:787-793.
60. Itioka, T., M. Nomura, Y. Inui, T. Itino, and T. Inoue. 2000. Difference in intensity of ant defense among three species of Macaranga myrmecophytes in a Southeast Asian dipterocarp forest. Biotropica 32:318-326.
61. Iturralde-Vinent, M. A., and R. D. E. MacPhee. 1996. Age and paleogeographical origin of Dominican amber. Science 273: 1850-1852.
62. Jaenike, J. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21:243-273.
63. Janzen, D. H. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249-275.
64. _. 1974. Swollen-thorn acacias of Central America. Smithson. Contrib. Bot. 13:1-131.
65. Jousselin, E., J. Y. Rasplus, and Kjellberg. 2003. Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus. Evolution 57:1255-1269.
66. Kelley, S. T., and B. D. Farrell. 1998. Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution 52:1731-1743.
67. Knowlton, N., and L. A. Weigt. 1998. New dates and new rates for divergence across the Isthmus of Panama. Proc. R. Soc. Lond. B 265:2257-2263.
68. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA 2.1: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
69. Labandeira, C. C., D. L. Dilcher, D. R. Davis, and D. L. Wagner. 1994. Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proc. Natl. Acad. Sci. USA. 91:12278-12282.
70. Larget, B., and D. Simon. 1999. Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol. Biol. Evol. 16:750-759.
71. Legendre, P., R. Galzin, and M. L. Harmelin-Vivien. 1997. Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78:547-562.
72. Legendre, P., Y. Desdevises, and E. Bazin. 2002. A statistical test for host-parasite coevolution. Syst. Biol. 51:217-234.
73. Longino, J. T. 1989. Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica. Biotropica 21:126-132.
74. _. 2003. The Crematogaster (Hymenoptera, Formicidae, Myrmicinae) of Costa Rica. Zootaxa 151:1-150.
75. Lutzoni, F., and M. Pagel. 1997. Accelerated evolution as a consequence of transitions to mutualism. Proc. Natl. Acad. Sci. USA 94:11422-11427.
76. Machado, C. A., E. Jousselin, F. Kjellberg, S. G. Compton, and E. A. Herre. 2001. Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proc. R. Soc. Lond. B 268:685-694.
77. Maddison, W. P. 1997. Gene trees in species trees. Syst. Biol. 46: 523-536.
78. Maddison, W. P., and D. R. Maddison. 1992. MacClade: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA.
79. Maschwitz, U., and B. Fiala. 1995. Investigations on ant plant associations in the Southeast Asian genus Neonauclea Merr (Rubiaceae). Acta Oecol. 16:3-18.
80. Maschwitz, U., B. Fiala, S. J. Davies, and L. E. Linsenmair. 1996. A Southeast Asian myrmecophyte with two alternative inhabitants: Camponotus or Crematogaster as partners of M. lamellata. Ecotropica 2:29-40.
81. Miller, D. G., and B. Crespi. 2003. The evolution of inquilinism, host-plant use and mitochondrial substitution rates in Tamalia gall aphids. J. Evol. Biol. 16:731-743.
82. Miura, T., Y. Roisin, and T. Matsumoto. 2000. Molecular phylogeny and biogeography of the nasute termite genus Nasutitermes (Isoptera: Termitidae) in the Pacific tropics. Mol. Phylogenet. Evol. 17:1-10.
83. Molbo, D., C. A. Machado, J. G. Sevenster, L. Keller, and E. A. Herre. 2003. Cryptic species of fig-pollinating wasps: implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proc. Natl. Acad. Sci. USA 100:5867-5872.
84. Moore, W. S. 1995. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718-726.
85. _. 1997. Mitochondrial-gene trees versus nuclear-gene trees, a reply to Hoelzer. Evolution 51:627-629.
86. Morley, R. J. 2000. Origin and evolution of tropical rain forests. John Wiley and Sons, Chichester, U.K.
87. Mueller, U. G., T. R. Schultz, C. R. Currie, R. M. M. Adams, and D. Malloch. 2001. The origin of the attine ant-fungus mutualism. Q. Rev. Biol. 76:169-197.
88. Murphy, W. J., T. N. P. Nguyen, E. B. Taylor, and G. E. Collier. 1999. Mitochondrial DNA phylogeny of West African aplocheiloid killifishes (Cyprinodontiformes, Aplocheilidae). Mol. Phylogenet. Evol. 11:343-350.
89. Nichols, R. 2001. Gene trees and species trees are not the same. Trends Ecol. Evol. 16:358-364.
90. Page, R. D. M. 1994a. Maps between trees and cladistic analysis of historical associations among genes, organisms and areas. Syst. Biol. 42:58-77.
91. _. 1994b. TreeMap 1.0. Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, Univ. of Glasgow, Glasgow, U.K.
92. Page, R. D. M., and M. A. Charleston. 2002. TreeMap versus BPA (again): a response to Dowling. Technical Reports in Taxonomy 02-02. Available via http://taxonomy.zoology.gla.ac.uk/publications/tech-reports.
93. Parker, J. D., and S. W. Rissing. 2002. Molecular evidence for the origin of workerless social parasites in the ant genus Pogonomyrmex. Evolution 56:2017-2028.
94. Pellmyr, O., and J. Leebens-Mack. 1999. Forty million years of mutualism: evidence for Eocene origin of the yucca-yucca moth association. Proc. Natl. Acad. Sci. USA 96:9178-9183.
95. Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitutions. Bioinformatics 14:817-818.
96. Rambaut, A., and M. Charleston. 2002. TreeEdit 1.0 alpha 10: phylogenetic tree editor. Dept. of Zoology, Univ. of Oxford, Oxford, U.K.
97. Rand, D. B., A. Heath, T. Suderman, and N. E. Pierce. 2000. Phylogeny and life history evolution of the genus Chrysoritis within the Aphnaeini (Lepidoptera: Lycaenidae), inferred from mitochondrial cytochrome oxidase I sequences. Mol. Phylogenet. Evol. 17:85-96.
98. Ridsdale, C. E. 1989. A revision of Neonauclea (Rubiaceae). Blumea 34:177-275.
99. Rocha-Olivares, A., C. A. Kimbrell, B. J. Eitner, and R. D. Vetter. 1999. Evolution of a mitochondrial cytochrome b gene sequence in the species-rich genus Sebastes (Teleostei, Scorpaenidae) and its utility in testing the monophyly of the subgenus Sebastomus. Mol. Phylogenet. Evol. 11:426-440.
100. Sanderson, M. J. 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14:1218-1231.
101. Savolainen, R., and K. Vepsäläinen. 2003. Sympatric speciation through intraspecific social parasitism. Proc. Natl. Acad. Sci. USA 100:7169-7174.
102. Schemske, D. W. 1983. Limits to specialization and coevolution in plant-animal mutualisms. Pp. 67-109 in M. H. Nitecki, ed. Coevolution. Univ. of Chicago Press, Chicago.
103. Schubart, C. D., R. Diesel, and S. B. Hedges. 1998. Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363-365.
104. Shaw, K. L. 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc. Natl. Acad. Sci. USA 99:16122-16127.
105. Sota, T., and A. P. Vogler. 2001. Incongruence of mitochondrial and nuclear gene trees in the carabid beetles Ohomopterus. Syst. Biol. 50:39-59.
106. Swofford, D. L. 1999. PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinaur Associates, Sunderland, MA.
107. Szidat, L. 1940. Beiträge zum aubfau eines natürlichen systems der Trematoden. I. Die entwicklung von Echinocercaria choanophila U. Szidat zu Cathaemasia hians und die ableitung der Fasciolidae von den Echinostomidae. Z. Parasitenkd. 11:239-283.
108. Thompson, J. N. 1989. Concepts of coevolution. Trends Ecol. Evol. 4:179-183.
109. Wahlberg, N., R. Oliveira, and J. A. Scott. 2003. Phylogenetic relationships of Phyciodes butterfly species (Lepidoptera: Nymphalidae): complex mtDNA variation and species delimitations. Syst. Entomol. 28:257-273.
110. Walsh, P. S., D. A. Metzger, and R. Higuchi. 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506-513.
111. Ward, P. S. 1991. Phylogenetic analysis of pseudomyrmecine ants associated with domatia-bearing plants. Pp. 335-352 in C. R. Huxley and D. F. Cutler, eds. Ant-plant interactions. Oxford Univ. Press, New York.
112. _. 1993. Systematic studies on Pseudomyrmex acacia-ants (Hymenoptera: Formicidae: Pseudomyrmecinae). J. Hym. Res. 2:117-168.
113. _. 1999. Systematics, biogeography and host plant associations of the Pseudomyrmex viduus group (Hymenoptera: Formicidae), Triplaris-and Tachigali-inhabiting ants. Zool. J. Linn. Soc. 126:451-540.
114. Weiblen, G. D., and G. L. Bush. 2002. Speciation in fig pollinators and parasites. Mol. Ecol. 11:1573-1578.
115. Wiens, J. J., and T. A. Penkrot. 2002. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51:69-91.
116. Wilson, E. O. 1988. The biogeography of the West Indian ants (Hymenoptera: Formicidae). Pp. 214-230 in J. K. Liebherr, ed. Zoogeography of Caribbean insects. Cornell Univ. Press, Ithaca, NY.
117. Yamane, S. 1997. A list of Bornean ants. Pp. 104-111 in T. Inoue and A. A. Hamid, eds. General flowering of tropical rainforests in Sarawak. Center for Ecological Research, Kyoto Univ., Kyoto, Japan.
118. Yu, D. W., and D. W. Davidson. 1997. Experimental studies of species-specificity in Cecropia-ant relationships. Ecol. Monogr. 67:273-294.