Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, moraceae)

Evolution

Volumn 66, Issue 12, 2012, Pages 3710-3721

  Moe, Annika M ^a   Weiblen, George D ^b  

^a SYRACUSE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Ceratosolen; Coevolution; Hybridization; Speciation

Indexed keywords

MICROSATELLITE DNA;

CLADISTICS; COEVOLUTION; DECIDUOUS TREE; FITNESS; GENE FLOW; GENETIC MARKER; GENOTYPE; HYBRID; HYBRIDIZATION; MUTUALISM; OVIPOSITION; PLANT-POLLINATOR INTERACTION; POLLINATION; REPRODUCTIVE ISOLATION; SELECTION; SYMPATRY; TAXONOMY; WASP;

ANIMAL; ARTICLE; BAYES THEOREM; EGG LAYING; FICUS; GENE FLOW; GERMINATION; HYBRIDIZATION; PHYSIOLOGY; POLLINATION; REPRODUCTIVE ISOLATION; WASP;

ANIMALS; BAYES THEOREM; FICUS; GENE FLOW; GERMINATION; HYBRIDIZATION, GENETIC; MICROSATELLITE REPEATS; OVIPOSITION; POLLINATION; REPRODUCTIVE ISOLATION; WASPS;

AGAONIDAE; CERATOSOLEN; FICUS (ANGIOSPERM); FICUS HISPIDIOIDES; MORACEAE;

EID: 84870515032     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01727.x     Document Type: Article

References (73)

1. Ashley, M. V., I. C. Caballero, W. Chaovalitwongse, B. Dasgupta, P. Govindan, S. I. Sheikh, and T. Y. Berger-Wolf. 2009. KINALYZER, a computer program for reconstructing sibling groups. Mol. Ecol. Resour. 9:1127-1131.
2. Azuma, H., R. D. Harrison, K. Nakamura, and Z. H. Su. 2010. Molecular phylogenies of figs and fig-pollinating wasps in the Ryukyu and Bonin (Ogasawara) islands, Japan. Genes Genet. Syst. 85:177-192.
3. Berg, C. C., and E. J. H. Corner. 2005. Moraceae (Ficus). Pages 1-730 in H. P. Nooteboom, eds. Flora Malesiana. Series I, Volume 17 Part 2. National Herbarium Nederland, Leiden, Netherlands.
4. Berger-Wolf, T. Y., S. I. Sheikh, B. DasGupta, M. V. Ashley, I. C. Caballero, W. Chaovalitwongse, and S. L. Putrevu. 2007. Reconstructing sibling relationships in wild populations. Bioinformatics 23:I49-I56.
5. Bronstein, J. L. 1987. Maintenance of species-specificity in a neotropical fig-pollinator wasp mutualism. Oikos 48:39-46.
6. Cavender-Bares, J., K. H. Kozak, P. V. A. Fine, and S. W. Kembel. 2009. The merging of community ecology and phylogenetic biology. Ecol. Lett. 12:693-715.
7. Chen, C., and Q. Song. 2008. Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. J. Chem. Ecol. 34:1536-1544.
8. Chen, C., Q. S. Song, M. Proffit, J. M. Bessiere, Z. B. Li, and M. Hossaert-McKey. 2009. Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct. Ecol. 23:941-950.
9. Cook, J. M., and J.-Y. Rasplus. 2003. Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol. Evol. 18:241-248.
10. Crisp, M. D., and L. G. Cook. 2009. Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 63:2257-2265.
11. Crozier, Y. C., X. C. Jia, J. Y. Yao, A. R. Field, J. M. Cook, and R. H. Crozier. 2007. Microsatellite primers for Ficus racemosa and Ficus rubiginosa. Mol. Ecol. Notes 7:57-59.
12. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611-2620.
13. Gates, D. J., and J. D. Nason. 2012. Flowering asynchrony and mating system effects on reproductive assurance and mutualism persistence in fragmented fig-fig wasp populations. Am. J. Bot. 99: 757-768.
14. Grant, V. 1971. Plant speciation. Columbia Univ. Press, New York.
15. Grison-Pige, L., J.-M. Bessiere, and M. Hossaert-McKey. 2002a. Specific attraction of fig-pollinating wasps: role of volatile compounds released by tropical figs. J. Chem. Ecol. 28:283-295.
16. Grison-Pige, L., M. Hossaert-McKey, J. M. Greef, and J.-M. Bessiere. 2002b. Fig volatile compounds-a first comparative study. Phytochemistry 61:61-71.
17. Haine, E. R., J. Martin, and J. M. Cook. 2006. Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evol. Biol. 6:83.
18. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65-70.
19. Hossaert-McKey, M., M. Gibernau, and J. E. Frey. 1994. Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomol. Exp. Appl. 70:185-191.
20. Irwin, D. E. 2002. Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383-2394.
21. Jackson, A. P., C. A. Machado, N. Robbins, and E. A. Herre. 2008. Multi-locus phylogenetic analysis of neotropical figs does not support co-speciation with the pollinators: the importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45:57-72.
22. Jander, K. C., and E. A. Herre. 2010. Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism. Proc. R. Soc. B Biol. Sci. 277:1481-1488.
23. Janzen, D. H. 1979. How to be a fig. Ann. Rev. Ecol. Syst. 10:13-51.
24. Jousselin, E., J.-Y. Rasplus, and F. Kjellberg. 2003. Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus. Evolution 57:1255-1269.
25. Jousselin, E., S. van Noort, V. Berry, J. Y. Rasplus, N. Ronsted, J. C. Erasmus, and J. M. Greeff. 2008. One fig to bind them all: Host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62:1777-1797.
26. Kay, K. M. 2006. Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:538-552.
27. Kephart, S., and K. Theiss. 2004. Pollinator-mediated isolation in sympatric milkweeds (Asclepias): do floral morphology and insect behavior influence species boundaries? New Phytol. 161:265-277.
28. Kiester, A. R., R. Lande, and D. W. Schemske. 1984. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124:220-243.
29. Lopez-Vaamonde, C., D. J. Dixon, J. M. Cook, and J.-Y. Rasplus. 2002. Revision of the Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host-plant associations. Zool. J. Linn. Soc. 136:637-683.
30. Lu, B., N. Wang, J. H. Xiao, Y. Y. Xu, R. W. Murphy, and D. W. Huang. 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. 9:43.
31. Machado, C. A., N. Robbins, T. P. Gilbert, and E. A. Herre. 2005. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc. Natl. Acad. Sci. USA 102:6558-6565.
32. Marussich, W. A., and C. A. Machado. 2007. Host-specificity and coevolution among pollinating and nonpollinating New World fig wasps. Mol. Ecol. 16:1925-1946.
33. Moe, A. M., and G. D. Weiblen. 2010. Molecular divergence and host conservatism in Ceratosolen (Agaonidae) pollinators of geographically widespread Ficus species (Moraceae). Ann. Entomol. Soc. Am. 103:1025-1037.
34. Moe, A. M., and G. D. Weiblen. 2011. Development and characterization of microsatellite loci in dioecious figs (Ficus, Moraceae). Am. J. Bot. 98:E25-E27.
35. Moe, A. M., D. R. Rossi, and G. D. Weiblen. 2011. Pollinator sharing in dioecious figs (Moraceae). Biol. J. Linn. Soc. 103:546-558.
36. Moe, A. M., W. L. Clement, and G. D. Weiblen. 2012. Rapid evolution of pollinator-mediated plant reproductive isolation. in R. S. Singh, J. Xu, and R. J. Kulathinal, eds. Rapidly evolving genes and genetic systems Oxford Univ. Press, Oxford, U.K.
37. 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.
38. Moore, J. C., A. M. Dunn, S. G. Compton, and M. J. Hatcher. 2003. Foundress re-emergence and fig permeability in fig tree-wasp mutualisms. J. Evol. Biol. 16:1186-1195.
39. Mopper, S. 1996. Adaptive genetic: structure in phytophagous insect populations. Trends Ecol. Evol. 11:235-238.
40. Novotny, V., Y. Basset, S. E. Miller, G. D. Weiblen, B. Bremer, L. Cizek, and P. Drozd. 2002. Low host specificity of herbivorous insects in a tropical forest. Nature 416:841-844.
41. Ollerton, J. 2006. "Biological Barter": patterns of specialization compared across different multualisms. Pp. 411-435 in N. Waser and J. Ollerton, eds. Plant-pollinator interactions. Univ. of Chcago Press, Chicago, IL.
42. Oyama, R. K., K. N. Jones, and D. A. Baum. 2010. Sympatric sister species of Californian antirrhinum and their transiently specialized pollinators. Am. Midl. Nat. 164:337-347.
43. Parrish, T. L., H. P. Koelewijn, P. J. van Dijk, and M. Kruijt. 2003. Genetic evidence for natural hybridization between species of dioecious Ficus on island populations. Biotropica 35:333-343.
44. Pritchard, J. K., M. Stephens, and P. J. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
45. Proffit, M., C. Chen, C. Soler, J. M. Bessiere, B. Schatz, and M. Hossaert-McKey. 2009. Can chemical signals, responsible for mutualistic partner encounter, promote the specific exploitation of nursery pollination mutualisms? The case of figs and fig wasps. Entomol. Exp. Appl. 131:46-57.
46. Ramirez, W. 1994. Hybridization of Ficus religiosa with F. septica and F. aurea (Moraceae). Rev. Biol. Trop. 42:339-342.
47. Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248-249.
48. Renoult, J. P., F. Kjellberg, C. Grout, S. Santoni, and B. Khadari. 2009. Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol. Biol. 9:248.
49. Revell, L. J., L. J. Harmon, and D. C. Collar. 2008. Phylogenetic signal, evolutionary process, and rate. Syst. Biol. 57:591-601.
50. Ronsted, N., G. D. Weiblen, W. L. Clement, N. J. C. Zerega, and V. Savolainen. 2008. Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis 45:45-55.
51. Rousset, F. 2008. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8:103-106.
52. Silvieus, S. I., W. L. Clement, and G. D. Weiblen. 2008. Cophylogeny of figs, pollinators, gallers and parasitoids. Pp. 225-239 in K. J. Tilmon, ed. Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. Univ. of California Press, Berkeley, CA.
53. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
54. Smith, C. I., C. S. Drummond, W. Godsoe, J. B. Yoder, and O. Pellmyr. 2009. Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae). Mol. Ecol. 18:5218-5229.
55. Stebbins, G. L. 1950. Variation and evolution in plants. Columbia Univ. Press, New York.
56. Su, Z. H., H. Iino, K. Nakamura, A. Serrato, and K. Oyama. 2008. Breakdown of the one-to-one rule in Mexican fig-wasp associations inferred by molecular phylogenetic analysis. Symbiosis 45:73-81.
57. Valdes, A. M., M. Slatkin, and N. B. Freimer. 1993. Allele frequencies at microsatellite loci-the stepwise mutation model revisited. Genetics 133:737-749.
58. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills, and P. Shipley. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4:535-538.
59. Ware, A. B., and S. G. Compton. 1994. Responses of fig wasps to host plant volatile cues. J. Chem. Ecol. 20:785-802.
60. Ware, A. B., P. T. Kaye, S. G. Compton, and S. van Noort. 1993. Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Syst. Evol. 186:147-156.
61. Weiblen, G. D. 2000. Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphology. Am. J. Bot. 87:1342-1357.
62. Weiblen, G. D. 2001. Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology. Syst. Biol. 50:243-267.
63. Weiblen, G. D. 2002. How to be a fig wasp. Ann. Rev. Entomol. 47:299-330.
64. Weiblen, G. D. 2004. Correlated evolution in fig pollination. Syst. Biol. 53:128-139.
65. Weiblen, G. D., and G. L. Bush. 2002a. Speciation in fig pollinators and parasites. Mol. Ecol. 11:1573-1578.
66. Weiblen, G. D., and G. L. Bush. 2002b. Speciation in fig pollinators and parasites. Mol. Ecol. 11:1573-1578.
67. Weiblen, G. D., D. W. Yu, and S. A. West. 2001. Pollination and parasitism in functionally dioecious figs. Proc. R. Soc. Lond. Biol. 268:651-659.
68. Weiblen, G. D., C. O. Webb, V. Novotny, Y. Basset, and S. E. Miller. 2006. Phylogenetic dispersion of host use in a tropical insect herbivore community. Ecology 87:S62-S75.
69. Weiblen, G. D., S. B. Lomascolo, R. Oono, and E. R. Dumont. 2010. Nutritional dimorphism in New Guinea dioecious figs. Biotropica 42:656-663.
70. Weir, B., and C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
71. Wiebes, J. T. 1963. Taxonomy and host preferences of Indo-Australian fig wasps of the genus Ceratosolen (Agaonidae). Tijdschr. Entomol. 106:1-112.
72. Wilson, G. A., and B. Rannala. 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177-1191.
73. Zavodna, M., P. Arens, P. J. Van Dijk, and B. Vosman. 2005. Development and characterization of microsatellite markers for two dioecious Ficus species. Mol. Ecol. Notes 5:355-357.