Chloroplast DNA phylogeography of a distylous shrub (Palicourea padifolia, Rubiaceae) reveals past fragmentation and demographic expansion in Mexican cloud forests

Molecular Phylogenetics and Evolution

Volumn 61, Issue 3, 2011, Pages 603-615

  Gutiérrez Rodríguez, Carla ^a   Ornelas, Juan Francisco ^a   Rodríguez Gómez, Flor ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Chloroplast; Genetic variation; Isthmus of Tehuantepec; Phylogeography; Pleistocene; Refugia

Indexed keywords

CHLOROPLAST DNA;

ARTICLE; FLOWER; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLOTYPE; MEXICO; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; POPULATION DYNAMICS; RUBIACEAE; TIME; TREE;

DNA, CHLOROPLAST; FLOWERS; GENETIC VARIATION; HAPLOTYPES; MEXICO; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; POPULATION DYNAMICS; RUBIACEAE; TIME FACTORS; TREES;

AVES; PALICOUREA PADIFOLIA; RUBIACEAE;

EID: 80055119876     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.08.023     Document Type: Article

References (110)

1. Avise J.C. Phylogeography: The History and Formation of Species 2000, Harvard University Press, Cambridge, MA.
2. Bohonak A.J. IBD (Isolation by Distance): a program for population genetic analyses of isolation by distance. J. Hered. 2002, 93:153-154.
3. Bonaccorso E., Navarro-Sigüenza A.G., Sánchez-González L., Peterson T.A., García-Moreno J. Genetic differentiation of the Chlorospingus ophthalmicus complex in Mexico and Central America. J. Avian Biol. 2008, 39:311-321.
4. Bossart J.L., Prowell D.P. Genetic estimates of population structure and gene flow: limitations, lessons and new directions. TREE 1998, 13:202-206.
5. Bush M.B., Colinvaux P.A. A pollen record of a complete glacial cycle from lowland Panama. J. Veg. Sci. 1990, 1:105-118.
6. Cadena C.D., Klicka J., Ricklefs R.E. Evolutionary differentiation in the Neotropical montane region: molecular phylogenetics and phylogeography of Buarremon brush-finches (Aves, Emberizidae). Mol. Phylogenet. Evol. 2007, 44:993-1016.
7. Carstens B.C., Knowles L.L. Shifting distribution and speciation: species divergence during rapid climate change. Mol. Ecol. 2007, 16:619-627.
8. Castelloe J., Templeton A.R. Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol. Phylogenet. Evol. 1994, 3:102-113.
9. Castoe T.A., Daza J.M., Smith E.N., Sasa M.M., Kuck U., Campbell J.A., Chippindale P.T., Parkinson C.L. Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. J. Biogeogr. 2009, 36:88-103.
10. Cavander-Bares, J., González-Rodríguez, A., Pahlich, A., Koehler, K., Deacon, N., 2011. Phylogeography and climatic niche evolution in live oaks (Quercus series Virentes) from the tropics to the temperate zone. J. Biogeogr. doi:10.1111/j.1365-2699.2010.02451.x.
11. Cavers S., Navarro C., Lowe A.J. Chloroplast DNA phylogeography reveals colonization history of a Neotropical tree, Cedrela odorata L., in Mesoamerica. Mol. Ecol. 2003, 12:1451-1460.
12. Clement M., Posada D., Crandall K.A. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 2000, 9:1657-1659.
13. Colinvaux P.A., De Oliveira P.E., Bush M.B. Amazonian and Neotropical plant communities on glacial time-scales: the failure of the aridity and refuge hypotheses. Quaternary Sci. Rev. 2000, 19:141-169.
14. Conroy C.J., Cook J.A. Phylogeography of a post-glacial colonizer: Microtus longicaudus (Rodentia:Muridae). Mol. Ecol. 2000, 9:165-175.
15. Contreras P.S., Ornelas J.F. Reproductive conflicts of Palicourea padifolia (Rubiaceae), a distylous shrub of a tropical cloud forest in Mexico. Plant Syst. Evol. 1999, 219:225-241.
16. Cortés-Rodríguez N., Hernández-Baños B.E., Navarro-Sigüenza A.G., Peterson A.T., García-Moreno J. Phylogeography and population genetics of the Amethyst- throated Hummingbird (Lampornis amethystinus). Mol. Phylogenet. Evol. 2008, 48:1-11.
17. De Cserna S. An Outline of the Geology of Mexico, the Geology of North America: An Overview 1989, The Geological Society of America, Boulder, Colorado.
18. Dick C.W., Bermingham E., Lemes M.R., Gribel R. Extreme long-distance dispersal of the lowland rainforest tree Ceiba pentandra L. (Malvaceae) in Africa and the Neotropics. Mol. Ecol. 2007, 16:3039-3049.
19. Domínguez C.A., Abarca C.A., Eguiarte L.E., Molina-Freaner F. Local genetic differentiation among populations of the mass-flowering tropical shrub Erythroxylum havanense (Erythroxylaceae). New Phytol. 2005, 166:663-672.
20. Doyle J.J., Doyle J.L. A rapid DNA isolation procedure from small quantities of fresh leaf tissue. Phytochem. Bull. 1987, 19:11-15.
21. Dupanloup I., Schneider S., Excoffier L. A simulated annealing approach to define the genetic structure of populations. Mol. Ecol. 2002, 12:2571-2581.
22. Edwards C.W., Bradley R.D. Molecular systematics and historical phylogeography of the Neotoma mexicana species group. J. Mammal. 2002, 83:20-30.
23. Excoffier L., Smouse P.E., Quattro J.M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131:479-491.
24. Fehlberg S., Ranker T.A. Evolutionary history and phylogeography of Encelia farinosa (Asteraceae) from the Sonoran, Mojave, and Peninsular Deserts. Mol. Phylogenet. Evol. 2009, 50:326-335.
25. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 1981, 17:368-376.
26. Ferrusquía-Villafranca I. Geology of Mexico, a synopsis. Biological Diversity of Mexico: Diversity and Distributions 1993, 3-108. Oxford University Press, New York, NY. T.P. Ramamoorthy, R.A. Bye, A. Lot, J. Fa (Eds.).
27. Fu Y.-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selections. Genetics 1997, 174:918-925.
28. García-Moreno J., Navarro-Sigüenza A.G., Peterson A.T., Sánchez-González L.A. Genetic variation coincides with geographic structure in the common bush-tanager (Chlorospingus ophthalmicus) complex from Mexico. Mol. Phylogenet. Evol. 2004, 33:186-196.
29. Ge X.-J., Chiang Y.-C., Chou C.-H., Chiang T.-Y. Nested clade analysis of Dunnia sinensis (Rubiaceae), a monotypic genus from China based on organelle DNA sequences. Conserv. Genet. 2002, 3:351-365.
30. González C., Ornelas J.F., Jiménez L. Between-year changes in functional gender expression of Palicourea padifolia (Rubiaceae), a distylous, hummingbird-pollinated shrub. Ann. Bot. 2005, 95:371-378.
31. González C., Ornelas J.F., Gutiérrez-Rodríguez C. Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the wedge-tailed sabrewing (Campylopterus curvipennis). BMC Evol. Biol. 2011, 11:38.
32. González-Astorga J., Vovides A.P., Ferrer M.M., Iglesias C. Population genetics of Dioon edule Lindl. (Zamiaceae, Cycadales): biogeographical and evolutionary implications. Biol. J. Linn. Soc. 2003, 80:457-467.
33. González-Rodríguez A., Bain J.F., Golden J.L., Oyama K. Chloroplast DNA in the Quercus affinis-Q. Laurina complex in Mexico: geographical structure and associations with nuclear and morphological variation. Mol. Ecol. 2004, 13:3467-3476.
34. Graham A. Tropical American Tertiary floras and paleoenvironments: Mexico, Costa Rica and Panama. Am. J. Bot. 1987, 74:1519-1531.
35. Graham A. The tertiary history of the northern temperate element in the northern Latin America biota. Am. J. Bot. 1999, 86:32-38.
36. Haffer J. Speciation in Amazonian forest birds. Science 1969, 165:131-137.
37. Hamrick J.L., Godt M.J.W. Effects of life the history traits on genetic diversity in plants. Phil. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:1291-1298.
38. Harpending R.C. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum. Biol. 1994, 66:591-600.
39. Hernández A., Ornelas J.F. Correlación morfo-específica en flores de Palicourea padifolia (Rubiaceae). Bol. Soc. Bot. Méx. 2003, 73:35-41.
40. Hernández A., Ornelas J.F. Disassortative pollen transfer in distylous Palicourea padifolia (Rubiaceae), a hummingbird-pollinated shrub. Ecoscience 2007, 14:8-16.
41. Hewitt G.M. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 1999, 68:87-112.
42. Hewitt G.M. The genetic legacy of the Quaternary ice ages. Nature 2000, 405:907-913.
43. Hey J. On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol. 2005, 3:965-975.
44. Hey J., Nielsen R. Multilocus methods for estimating population sizes, migration rates and diverge time, with applications to the divergence of Drosophila pseudoobscura and D. Persimilis. Genetics 2004, 167:747-760.
45. Hey J., Nielsen R. Integration with the Felsestein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. USA 2007, 104:2785-2790.
46. Hillis D.M., Mable B.K., Moritz C. Application of molecular systematics: the state of the field and look to the future. Molecular Systematics 1996, 515-543. Sinauer and Associates, Sunderland, Massachusetts. D.M. Hillis, C. Moritz, B.K. Mable (Eds.).
47. Hodgins K.A., Barrett S.C.H. Population structure and genetic diversity in tristylous Narcissus triandrus: insights from microsatellite and chloroplast DNA variation. Mol. Ecol. 2007, 16:2317-2332.
48. Huidobro L., Morrone J.J., Villalobos J.L., Alvarez F. Distributional patterns of freshwater taxa (fishes, crustaceans and plants) from the Mexican Transition Zone. J. Biogeogr. 2006, 33:731-741.
49. Jacquemyn H., Honnay O., Galbusera P., Roldán-Ruiz I. Genetic structure of the forest herb Pimula elatior in a changing landscape. Mol. Ecol. 2004, 13:211-219.
50. Jaramillo-Correa J.P., Beaulieu J., Ledig F.T., Bousquet J. Decoupled mitochondrial and chloroplast DNA population structure reveals Holocene collapse and population isolation in a threatened Mexican-endemic conifer. Mol. Ecol. 2006, 15:2787-2800.
51. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16:111-120.
52. Kuhner M.K., Smith L.P. Comparing likelihood and Bayesian coalescent estimation of population parameters. Genetics 2007, 175:155-165.
53. Lambeck K., Chappell J. Sea level change through the last glacial cycle. Science 2001, 292:679-686.
54. León-Paniagua L., Navarro-Singüenza A.G., Hernández-Baños B.E., Morales J.C. Diversification of the arboreal mice of the genus Habromys (Rodentia; Cricetidae:Neotominae) in the Mesoamerican highlands. Mol. Phylogenet. Evol. 2007, 42:653-664.
55. Loiselle B.A., Sork V.L., Graham C. Comparison of genetic variation in bird-disperse shrubs of a tropical wet forest. Biotropica 1995, 27:487-494.
56. Marshall C.J., Liebherr J.K. Cladistic biogeography of the Mexican transition zone. J. Biogeogr. 2000, 27:203-216.
57. Moreno-Letelier A., Piñero D. Phylogeographic structure of Pinus strobiformis Engelm, across the Chihuahuan desert filter-barrier. J. Biogeogr. 2009, 36:121-131.
58. Morris A.B., Ickert-Bond S.M., Brunson D.B., Soltis D.E., Soltis P.S. Phylogeographical structure and temporal complexity in American sweetgum (Liquidambar styraciflua; Altingiaceae). Mol. Ecol. 2008, 17:3889-3900.
59. Morris A.B., Graham C.H., Soltis D.E., Soltis P.S. Reassessment of phylogeographical structure in an eastern North American tree using Monmonier's algorithm and ecological niche modeling. J. Biogeogr. 2010, 37:1657-1667.
60. Navarro-Sigüenza A.G., Peterson A.T., Nyari A., García-Deras G.M., García-Moreno J. Phylogeography of the Buarremon brush-finch complex (Aves, Emberizidae) in Mesoamerica. Mol. Phylogenet. Evol. 2008, 47:21-35.
61. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
62. Nei M. Age of the common ancestor of human mitochondrial DNA. Mol. Biol. Evol. 1992, 9:1179-1180.
63. Nielsen R., Wakeley J. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 2001, 158:885-896.
64. Nybom H., Batish I. Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Persp. Plant Ecol. Syst. 2000, 3:93-114.
65. Ornelas J.F., Jiménez L., González C., Hernández A. Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds' effectiveness as pollen vectors. Am. J. Bot. 2004, 91:1052-1060.
66. Ornelas J.F., González C., Jiménez L., Lara C., Martínez J.A. Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. II. Attracting and rewarding mutualistic and antagonistic visitors. Am. J. Bot. 2004, 91:1061-1069.
67. Ornelas J.F., Ruiz-Sánchez E., Sosa V. Phylogeography of Podocarpus matudae (Podocarpaceae): pre-Quaternary relicts in northern Mesoamerican cloud forests. J. Biogeogr. 2010, 37:2384-2396.
68. Ortíz-Medrano A., Moreno-Letelier A., Piñero D. Fragmentación y expansión demográfica en las poblaciones mexicanas de Pinus ayacahuite var. ayacahuite. Bol. Soc. Bot. Méx. 2008, 83:25-36.
69. Parra-Olea G., García-París M., Wake D.B. Phylogenetic relationships among the salamanders of the Botiglossa macrinni species group (Amphibia: Plethodontidae), with descriptions of two new species from Oaxaca (México). J. Hepetol. 2002, 36:356-366.
70. Pennington R.T., Prado D.E., Pendry C.A. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 2000, 27:261-273.
71. Pérez-Nasser N., Eguiarte L.E., Piñero D. Mating system and genetic structure of the distylous tropical tree Psychotria faxlucens (Rubiaceae). Am. J. Bot. 1993, 80:45-52.
72. Peterson A.T., Soberón J., Sánchez-Cordero V. Conservatism of ecological niches in evolutionary time. Science 1999, 285:1265-1267.
73. Petit R.J., Pineau E., Desmesure B., Bacilieri R., Ducousso A., Kremer A. Chloroplast DNA footprints of postglacial recolonization by oaks. Proc. Natl. Acad. Sci., USA 1997, 94:9996-10001.
74. Piperno D.R., Moreno J.E., Iriarte J., Holst I., Lachniet M., Jones J.G., Ranere A.J., Castanzo R. Late Pleistocene and Holocene environmental history of the Iguala Valley, Central Balsas watershed of Mexico. Proc. Natl. Acad Sci., USA 2007, 104:11874-11881.
75. Pons O., Petit R.J. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 1996, 144:1237-1245.
76. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
77. Prance G.T. A review of the phytogeographic evidences for Pleistocene climate changes in the Neotropics. Ann. Missou. Bot. Gard. 1982, 69:594-624.
78. Ree R.H. Pollen flow, fecundity, and the adaptive significance of heterostyly in Palicourea padifolia (Rubiaceae). Biotropica 1997, 29:298-308.
79. Richardson J.E., Pennington R.T., Pennington T.D., Hollingsworth P.M. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 2001, 293:2242-2245.
80. Rico Y., Lorenzo C., González-Cózatl F.X., Espinoza E. Phylogeography and population structure of the endangered Tehuantepec jackrabbit Lepus flavigularis: implications for conservation. Conserv. Genet. 2008, 9:1467-1477.
81. Rogers A.R. Genetic evidence for a Pleistocene population explosion. Evolution 1995, 49:608-615.
82. Rogers A.R., Harpending H. Population growth makes waves in the distribution of pairwise differences. Mol. Biol. Evol. 1992, 9:552-569.
83. Ronquist F., Huelsenbeck J.P. MrBAyes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
84. Rousset F. Genetic differentiation and estimation of gene flow from F-Statistics under isolation by distance. Genetics 1997, 145:1219-1228.
85. Rzedowski J. Diversity and origins of the phanerogamic Flora of Mexico. Biological Diversity of Mexico: Diversity and Distributions 1993, 129-144. Oxford University Press, New York, NY. T.P. Ramamoorthy, R.A. Bye, A. Lot, J. Fa (Eds.).
86. Schneider S., Excoffier L. Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetics 1999, 152:1079-1089.
87. Schneider, S., Roessli, D., Excoffier, L., 2000. ARLEQUIN, Version 2.00: A Software for Population Genetics Data Analysis, University of Geneva, Geneva.
88. Shaw J., Lickey E.B., Beck J.T., Farmer S.B., Liu W., Miller J., Siripun K.C., Winder C.T., Schilling E.E., Small R.L. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am. J. Bot. 2005, 92:142-166.
89. Shaw J., Lickey E.B., Schilling E.E., Small R.L. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am. J. Bot. 2007, 94:257-288.
90. Slatkin M., Hudson R.R. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 1991, 129:555-562.
91. Soltis D.E., Gitzendanner M.M., Strenge D.D., Soltis P.S. Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Syst. Evol. 1997, 206:353-373.
92. Sosa V., Ruiz-Sánchez E., Rodríguez-Gómez F.C. Hidden phylogeographic complexity in the Sierra Madre Oriental: the case of the Mexican tulip puppy Hunnemannia fumariifolia (Papaveraceae). J. Biogeogr. 2009, 36:18-27.
93. Sullivan J., Markert J.A., Kilpatrick C.W. Phylogeography and molecular systematics of the Peromyscus aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Syst. Biol. 1997, 46:426-440.
94. Sullivan J., Arellano E., Rogers D.S. Comparative phylogeography of Mesoamerican highland rodents: concerted versus independent response to past climatic fluctuations. Am. Nat. 2000, 155:755-768.
95. Taberlet P., Fumagalli L., Wust-Saucy A.-G., Cosson J.-F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 1998, 7:453-464.
96. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
97. Tajima F. Measurement of DNA polymorphism. Mechanisms of Molecular Evolution. Introduction to Molecular Paleopopulation Biology 1993, 37-59. Scientific Societies Press, Sinauer Associates, Inc., Japan Tokyo, Sunderland, MA. N. Takahata, A.G. Clark (Eds.).
98. Tajima F. The amount of DNA polymorphism maintained in a finite population when the neutral mutation varies among sites. Genetics 1996, 143:1457-1465.
99. Taylor C.M. Revision of Palicourea (Rubiaceae) in Mexico and Central America. Syst. Bot. Monogr. 1989, 26:1-102.
100. Templeton A.R., Crandall K.A., Sing C.F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNAsequence data. III. Cladogram estimation. Genetics 1992, 132:619-633.
101. Toledo V.M. Pleistocene changes of vegetation in tropical Mexico. Biological Diversification in the Tropics: Proceedings of the 5th International Symposium of the Association for Tropical Biology, Caracas 1982, 93-111. Columbia University Press, New York. G.T. Prance (Ed.).
102. Van der Velde M., Bijlsma R. Phylogeography of five Polytrichum species within Europe. Biol. J. Linn. Soc. 2003, 78:203-213.
103. Wendt T. Las selvas de Uxpanapa, Veracruz-Oaxaca, México: evidencia de refugios florísticos Cenozoicos. Anales del Instituto de Biología, UNAM, Serie Botánica 1987, 58:29-54.
104. Whitmore T.C., Prance G.T. Biogeography and Quaternary History in Tropical America 1987, Oxford Science Publications, Oxford.
105. Wolf K.H., Li W.H., Sharp P.M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNA. Proc. Natl. Acad. Sci., USA 1987, 84:9054-9058.
106. Won Y.-J., Hey J. Divergence population genetics of chimpanzees. Mol. Biol. Evol. 2005, 22:297-307.
107. Worth J.R.P., Jordan G.J., Martrick J.R., Mckinnon G.E., Vaillancourt R.E. Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmania lanceolata (Winteraceae). Mol. Ecol. 2010, 19:2949-2963.
108. Yuan Q.J., Zhang Z.Y., Peng H., Ge S. Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in southwest China and northern Vietnam. Mol. Ecol. 2008, 17:1054-1065.
109. Zink R.M., Barrowclough G.G., Atwood J.L., Blackwell-Rago R.C. Genetics, taxonomy and conservation of the threatened California Gnatcatcher. Conserv. Biol. 2000, 14:1394-1405.
110. Zurawski G., Clegg M.T., Brown A.H.D. The nature of nucleotide sequence divergence between barley and maize chloroplast DNA. Genetics 1984, 106:735-749.