Fig trees at the northern limit of their range: The distributions of cryptic pollinators indicate multiple glacial refugia

Molecular Ecology

Volumn 21, Issue 7, 2012, Pages 1687-1701

  Chen, Yan ^a,b   Compton, Stephen G ^c   Liu, Min ^a   Chen, Xiao Yong ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b MIANYANG NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

co evolution; demographic history; Ficus pumila; fig wasp; glacial refugium; phylogeography; Wiebesia

Indexed keywords

MITOCHONDRIAL DNA; PLANT DNA; RIBOSOMAL SPACER DNA;

ANIMAL; ARTICLE; CHINA; CLIMATE; DNA SEQUENCE; EVOLUTION; FICUS; GENETICS; PHYLOGENY; POLLINATION; POPULATION GENETICS; WASP;

ANIMALS; BIOLOGICAL EVOLUTION; CHINA; CLIMATE; DNA, MITOCHONDRIAL; DNA, PLANT; DNA, RIBOSOMAL SPACER; FICUS; GENETICS, POPULATION; PHYLOGENY; POLLINATION; SEQUENCE ANALYSIS, DNA; WASPS;

AGAONIDAE; ANIMALIA; FICUS (ANGIOSPERM); FICUS PUMILA; WIEBESIA;

EID: 84862804146     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05491.x     Document Type: Article

References (98)

1. Baker AJ, (2008) Islands in the sky: the impact of Pleistocene climate cycles on biodiversity. Journal of Biology, 7, 32.
2. Barnosky AD, (2005) Effects of Quaternary climatic change on speciation in mammals. Journal of Mammalian Evolution, 12, 247-264. (Pubitemid 41779903)
3. Beheregaray LB, (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology, 17, 3754-3774.
4. Berg CC, Corner EJH, (2005) Moraceae (Ficus). In: Flora Malesiana. Series I Seed plants (eds, Berg CC, Corner EJH, Nooteboom HP,), pp. 1-727. National Herbarium of the Netherlands, Leiden.
5. Chen JY, Zhou XD, (1993) Relationship between palaeoenvironmental change and soil development in Wuyi Mountains. Geology of Fujian, 12, 228-231.
6. Chen Y, Li HQ, Shao JR, Ma WL, (2008) Pollination of a cultivated fig, Ficus pumila var. awkeotsang in South China. Symbiosis, 45, 33-36. (Pubitemid 351461488)
7. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
8. Compton SG, Holton K, Rashbrook VK, van Noort S, Vincent S, Ware AB, (1991) The biology of Ceratosolen galili, a non pollinating agaonid fig wasp (Hymenoptera, Agaonidae). Biotropica, 23, 188-194.
9. Compton SG, Ball AD, Collinson ME, Hayes P, Rasnitsyn AP, Ross AJ, (2010) Ancient fig wasps indicate at least 34 million years of stasis in their mutualism with fig trees. Biology Letters, 6, 838-842.
10. Cook JM, Segar ST, (2010) Speciation in fig wasps. Ecological Entomology, 35, 54-66.
11. Cruaud A, Jabbour-Zahab R, Genson G, et al. (2010) Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach. Cladistics, 26, 359-387.
12. Drummond AJ, Rambaut A, (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
13. Drummond AJ, Rambaut A, Shapiro B, Pybus OG, (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185-1192. (Pubitemid 40577756)
14. Eckert CG, Samis KE, Lougheed SC, (2008) Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Molecular Ecology, 17, 1170-1188. (Pubitemid 351294604)
15. Elias M, Joron M, Willmott K, et al. (2009) Out of the Andes: patterns of diversification in clearwing butterflies. Molecular Ecology, 18, 1716-1729.
16. Erasmus JC, van Noort S, Jousselin E, Greeff JM, (2007) Molecular phylogeny of fig wasp pollinators (Agaonidae, Hymenoptera) of Ficus section Galoglychia. Zoologica Scripta, 36, 61-78. (Pubitemid 46148247)
17. Excoffier L, (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite island model. Molecular Ecology, 13, 853-864. (Pubitemid 38390591)
18. Excoffier L, Laval G, Schneider S, (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
19. Fu YX, (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
20. Funk DJ, Omland KE, (2003) Species level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34, 397-423. (Pubitemid 38171425)
21. Haine ER, Martin J, Cook JM, (2006) Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evolutionary Biology, 6, 83.
22. Hampe A, Petit RJ, (2005) Conserving biodiversity under climate change: the rear edge matters. Ecology Letters, 8, 461-467. (Pubitemid 40641134)
23. Harrison SP, Yu G, Takahara H, Prentice IC, (2001) Palaeovegetation: diversity of temperate plants in East Asia. Nature, 413, 129-130. (Pubitemid 32867867)
24. Hayward A, Stone GN, (2006) Comparative phylogeography across two trophic levels: the oak gall wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology, 15, 479-489.
25. He KY, (1991) The pollinating fig wasp of Ficus pumial var. awkeotsang. In: Monograph on Ficus pumila var. awkeotsang (ed., Lin TP,), pp. 83-96. Taiwan Forestry Research Institute, Taiwan.
26. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM, (2004) Identification of birds through DNA barcodes. PLoS Biology, 2, 1657-1663.
27. Heled J, Drummond AJ, (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570-580.
28. Herre EA, Jander KC, Machado CA, (2008) Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annual Review of Ecology, Evolution, and Systematics, 39, 439-458.
29. Hewitt GM, (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276. (Pubitemid 26389802)
30. Hewitt GM, (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
31. Hewitt GM, (2001) Speciation, hybrid zones and phylogeography-or seeing genes in space and time. Molecular Ecology, 10, 537-549. (Pubitemid 32406341)
32. Hewitt GM, (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359, 183-195. (Pubitemid 38231471)
33. Hill DS, (1967a) Figs (Ficus spp.) of Hong Kong. Hong Kong University Press, Hong Kong.
34. Hill DS, (1967b) Fig-wasps (Chalcidoidea) of Hong Kong I. Agaonidae. Zoologische Verhandelingen (Leiden), 89, 3-55.
35. Hillis DM, Dixon MT, (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology, 66, 411-453.
36. Jackson AP, Machado CA, Robbins N, Herre EA, (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. (Pubitemid 351461491)
37. Janzen DH, (1979) How to be a fig. Annual Review of Ecology and Systematics, 10, 13-51.
38. Jiang ZF, Huang DW, Zhu CD, Zhen WQ, (2006) New insights into the phylogeny of fig pollinators using Bayesian analyses. Molecular Phylogenetics and Evolution, 38, 306-315.
39. Jousselin E, van Noort S, Berry V, et al. (2008) One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and non-pollinating fig wasps. Evolution, 62, 1777-1797. (Pubitemid 352000103)
40. Kass RE, Raftery AE, (1995) Bayes factors. Journal of the American Statistical Association, 90, 773-795.
41. Kerdelhue C, Le Clainche I, Rasplus JY, (1999) Molecular phylogeny of the Ceratosolen species pollinating Ficus of the subgenus Sycomorus sensu stricto: biogeographical history and origins of the species-specificity breakdown cases. Molecular Phylogenetics and Evolution, 11, 401-414. (Pubitemid 129499278)
42. Larkin MA, Blackshields G, Brown NP, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948. (Pubitemid 350162903)
43. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
44. Lin RC, Yeung CKL, Li SH, (2008) Drastic post-LGM expansion and lack of historical genetic structure of a subtropical fig-pollinating wasp Ceratosolen sp. 1 of Ficus septica in Taiwan. Molecular Ecology, 17, 5008-5022.
45. Lin RC, Yeung CKL, Fong JJ, Tzeng HY, Li SH, (2010) The lack of pollinator specificity in a dioecious fig tree: sympatric fig-pollinating wasps of Ficus septica in Southern Taiwan. Biotropica, 43, 200-207.
46. Lopez-Vaamonde C, Rasplus JY, Weiblen GD, Cook JM, (2001) Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites. Molecular Phylogenetics and Evolution, 21, 55-71. (Pubitemid 32978502)
47. Lu HP, Cai YW, Chen XY, Zhang X, Gu YJ, Zhang GF, (2006) High RAPD but no cpDNA sequence variation in the endemic and endangered plant, Heptacodium miconioides Rehd. (Caprifoliaceae). Genetica, 128, 409-417. (Pubitemid 44544131)
48. Luo GT, Li HQ, Ma WL, Chen Y, (2000) The cooperation of life-stage between Wiebesia pumilae (Hill) Wieb. (Agaoindae) and Ficus pumila L. (Moraceae). Chinese Journal of Ecology, 19, 73-75.
49. Ma WL, Wu X, (1989) A preliminary study of symbioses between Blastophaga pumilae Hill (Hymenoptera) and Ficus pumila L. (Moraceae). Acta Ecologica Sinica, 9, 9-14.
50. Machado CA, Jousselin E, Kjellberg F, Compton SG, Herre EA, (2001) Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proceedings of the Royal Society of London B: Biological Sciences, 268, 685-694. (Pubitemid 32322796)
51. McDonald JH, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654. (Pubitemid 21896661)
52. McLeish M, Guo DN, van Noort S, Midgley G, (2011) Life on the edge: rare and restricted episodes of a pan-tropical mutualism adapting to drier climates. New Phytologist, 191, 210-222.
53. Michaloud G, Michaloud-Pelletier S, Wiebes JT, Berg CC, (1985) The co-occurrence of two pollinating species of fig wasp and one species of fig. Proceedings of the Koninklijke Nederlandse Akademie van Wetenscahppen, C, 88, 93-119.
54. Moe AM, Rossi DR, Weiblen GD, (2011) Pollinator sharing in dioecious figs (Ficus: Moraceae). Biological Journal of the Linnean Society, 103, 546-558.
55. Molbo D, Machado CA, Sevenster JG, Keller L, Herre EA, (2003) Cryptic species of fig-pollinating wasps: implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proceedings of the National Academy of Sciences of the United States of America, 100, 5867-5872. (Pubitemid 36576899)
56. Morgan K, O'Loughlin SM, Fong MY, et al. (2009) Molecular phylogenetics and biogeography of the Neocellia Series of Anopheles mosquitoes in the Oriental Region. Molecular Phylogenetics and Evolution, 52, 588-601.
57. Ni J, Yu G, Harrison SP, Prentice IC, (2010) Palaeovegetation in China during the late Quaternary: biome reconstructions based on a global scheme of plant functional types. Palaeogeography Palaeoclimatology Palaeoecology, 289, 44-61.
58. Nicholls JA, Preuss S, Hayward A, et al. (2010) Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes. Molecular Ecology, 19, 592-609.
59. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL, (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology, 53, 47-67. (Pubitemid 38370420)
60. Posada D, Crandall KA, (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology & Evolution, 16, 37-45. (Pubitemid 32102347)
61. Provan J, Bennett KD, (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564-571.
62. Qian H, Ricklefs RE, (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature, 407, 180-182.
63. Qiu YX, Cheng X, Comes HP, (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world's most diverse temperate flora. Molecular Phylogenetics and Evolution, 59, 225-244.
64. Rambaut A, (2006) FigTree v1.3.1.
65. Rambaut A, Drummond AJ, (2007) Tracer v1.4.
66. Ramirez WB, (1974) Coevolution of Ficus and Agaonidae. Annals of the Missouri Botanical Garden, 61, 770-780.
67. Rogers AR, (1995) Genetic evidence for a Pleistocene population explosion. Evolution, 49, 608-615.
68. Rogers AR, Harpending H, (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552-569.
69. Ronsted N, Weiblen GD, Clement WL, Zerega NJC, Savolainen V, (2008) Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis, 45, 45-55. (Pubitemid 351461490)
70. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
71. Shafer ABA, Cullingham CI, Côté SD, Coltman DW, (2010) Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Molecular Ecology, 19, 4589-4621.
72. Shanahan M, So S, Compton SG, Corlett R, (2001) Fig-eating by vertebrate frugivores: a global review. Biological Reviews of the Cambridge Philosophical Society, 76, 529-572. (Pubitemid 33089593)
73. Shen L, Chen XY, Zhang X, Li YY, Fu CX, Qiu YX, (2005) Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR-RFLPs: inference of glacial refugia. Heredity, 94, 396-401.
74. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P, (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Annals of the Entomological Society of America, 87, 651-701.
75. Slatkin M, Hudson RR, (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555-562.
76. Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PDN, (2006) DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America, 103, 3657-3662. (Pubitemid 43376611)
77. Soltis DE, Morris AB, Mclachlan JS, Manos PS, Soltis PS, (2006) Comparative phylogeography of unglaciated eastern North America. Molecular Ecology, 15, 4261-4293. (Pubitemid 44749551)
78. Song YC, (1999) Perspecitve of the vegetation zonation of forest region in eastern China. Acta Botanica Sinica, 41, 545-552.
79. Song H, Buhay JE, Whiting MF, Crandall KA, (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America, 105, 13486-13491.
80. Su ZH, Iino H, Nakamura K, Serrato A, Oyama K, (2008) Breakdown of the one-to-one rule in Mexican fig-wasp associations inferred by molecular phylogenetic analysis. Symbiosis, 45, 73-81. (Pubitemid 351461492)
81. Suchard MA, Weiss RE, Sinsheimer JS, (2001) Bayesian selection of continuous-time Markov chain evolutionary models. Molecular Biology and Evolution, 18, 1001-1013. (Pubitemid 32520473)
82. Sun XJ, Xiao JH, Cook JM, Feng G, Huang DW, (2011) Comparisons of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity. BMC Evolutionary Biology, 11, 86.
83. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595. (Pubitemid 19274682)
84. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: molecular evolutionary genetics analysis MEGA software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. (Pubitemid 47236692)
85. Wang X, Liu YK, (1994) Theories and Practice in Biodiversity. China Environmental Science Press, Beijing.
86. Wang J, Gao P, Kang M, Lowe AJ, Huang H, (2009a) Refugia within refugia: the case study of a canopy tree Eurycorymbus cavaleriei in subtropical China. Journal of Biogeography, 36, 2156-2164.
87. Wang R, Ai B, Gao BQ, Yu S, Li YY, Chen XY, (2009b) Spatial genetic structure and restricted gene flow in a functionally dioecious fig'Ficus pumila L. pumila (Moraceae). Population Ecology, 51, 307-315.
88. Warren M, Robertson MP, Greeff JM, (2010) A comparative approach to understanding factors limiting abundance patterns and distributions in a fig tree-fig wasp mutualism. Ecography, 33, 148-158.
89. Weiblen GD, (2002) How to be a fig wasp. Annual Review of Entomology, 47, 299-330. (Pubitemid 34108584)
90. Wiebes JT, (1979) Co-evolution of figs and their insect pollinators. Annual Review of Ecology and Systematics, 10, 1-12.
91. Wiebes JT, (1994) The Indo-Australian Agaoninae Pollinators of Figs. North-Holland, Amsterdam, Oxford, New York, Tokyo.
92. Wu ZY, (1980) Vegetation of China. Science Press, Beijing.
93. Wu WS, Chen YL, (2008) Comparison of reproduction ecology of different Ficus awkeotsang strains. Acta Ecologica Sinica, 28, 2692-4702.
94. Wu ZY, Raven PH, (1994) Floral of China. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, MO.
95. Xiao JH, Wang NX, Li YW, et al. (2010) Molecular approaches to identify cryptic species and polymorphic species within a complex community of fig wasps. PLoS ONE, 5, e15067.
96. Yu G, Chen X, Ni J, et al. (2000) Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. Journal of Biogeography, 27, 635-664. (Pubitemid 32122056)
97. Zhao ZB, (1982) A preliminary study on the evolution of Taiwan Strait. Taiwan Strait, 1, 20-24.
98. Zhou SZ, Li JJ, Zhang SQ, Zhao JD, Cui JX, (2004) Quaternary glaciations in China. In: Developments in Quaternary Science (eds, Ehlers J, Gibbard PL,), pp. 105-113. Elsevier, Amsterdam.