The extraordinary journey of Peperomia subgenus Tildenia (Piperaceae): Insights into diversification and colonization patterns from its cradle in Peru to the Trans-Mexican Volcanic Belt

Journal of Biogeography

Volumn 38, Issue 12, 2011, Pages 2337-2349

  Symmank, Lars ^a   Samain, Marie Stéphanie ^b   Smith, James F ^c   Pino, Guillermo ^d   Stoll, Alexandra ^e,f   Goetghebeur, Paul ^b   Neinhuis, Christoph ^a   Wanke, Stefan ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b GHENT UNIVERSITY   (Belgium)

^c BOISE STATE UNIVERSITY   (United States)

^d UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS   (Peru)

^e CENTRO DE ESTUDIOS AVANZADOS EN ZONAS ÁRIDAS CEAZA   (Chile)

^f DEPARTAMENTO DE BIOLOGÍA   (Chile)

Author keywords

Amotape Huancabamba Zone; Central Andes; Great American Interchange; Isthmus of Panama; Mexican Transition Zone; Neotropics; Refuge theory; Sierra Madre

Indexed keywords

CLIMATE OSCILLATION; COLONIZATION; DICOTYLEDON; DISPERSAL; DISPERSION; MIOCENE; MOUNTAIN REGION; NEOTROPIC ECOZONE; NORTHERN HEMISPHERE; OROGENY; PHYLOGENETICS; RECONSTRUCTION; REFUGIUM; SOUTHERN HEMISPHERE; TRANSITION ZONE; VICARIANCE; VOLCANIC BELT;

ANDES; ARGENTINA; BOLIVIA; GUATEMALA [CENTRAL AMERICA]; ISTHMUS OF PANAMA; MEXICO [NORTH AMERICA]; PANAMA [CENTRAL AMERICA]; PERU; SIERRA MADRE;

PEPEROMIA; PIPERACEAE; SCYTONEMATOPSIS;

EID: 81255185467     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02586.x     Document Type: Article

References (104)

1. Antonelli, A. & Sanmartín, I. (2011) Why are there so many plant species in the Neotropics? Taxon, 60, 403-414.
2. Barrier, E., Velasquillo, L., Chavez, M. & Gaulon, R. (1998) Neotectonic evolution of the Isthmus of Tehuantepec (southeastern Mexico). Tectonophysics, 287, 7-96.
3. Barthlott, W., Mutke, J., Rafiqpoor, M.D., Kier, G. & Kreft, H. (2005) Global centres of vascular plant diversity. Nova Acta Leopoldina, 92, 61-83.
4. Bell, C.D., Soltis, D.E. & Soltis, P.S. (2010) The age and diversification of the angiosperms re-revisited. American Journal of Botany, 97, 1296-1303.
5. Bermingham, E. & Martin, A.P. (1998) Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Molecular Ecology, 7, 499-517.
6. Britton, T., Anderson, C.L., Jacquet, D., Lundqvist, S. & Bremer, K. (2007) Estimating divergence times in large phylogenetic trees. Systematic Biology, 56, 741-752.
7. Burnham, R.J. & Graham, A. (1999) The history of Neotropical vegetation: new developments and status. Missouri Botanical Garden, 86, 546-589.
8. Bush, M.B. (1994) Amazonian speciation: a necessarily complex model. Journal of Biogeography, 21, 5-17.
9. Coates, A.G. & Obando, J.A. (1996) The geologic evolution of the Central American Isthmus. Evolution and environment in tropical America (ed. by J.B.C. Jackson, A.F. Budd and A.G. Coates ), pp. 21-56. University of Chicago Press, Chicago.
10. Coates, A.G., Aubry, M.-P., Berggren, W.A. & Collins, L.S. (2003) Early Neogene history of the Central American arc from Bocas del Toro, western Panama. Geological Society of America Bulletin, 115, 271-287.
11. Cody, S., Richardson, J.E., Rull, V., Ellis, C. & Pennington, R.T. (2010) The Great American Biotic Interchange revisited. Ecography, 33, 326-332.
12. Collins, A.C. & Dubach, J.M. (2000) Biogeographic and ecological forces responsible for speciation in Ateles. International Journal of Primatology, 21, 421-444.
13. Cosacov, A., Sérsic, A.N., Sosa, V., De-Nova, J.A., Nylander, S. & Cocucci, A.A. (2009) New insights into the phylogenetic relationships, character evolution, and phytogeographic patterns of Calceolaria (Calceolariaceae). American Journal of Botany, 96, 2240-2255.
14. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
15. Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699-710.
16. Duque-Caro, H. (1990) Neogene stratigraphy, paleoceanography and paleobiogeography in northwest South America and the evolution of the Panama Seaway. Palaeogeography, Paleoclimatology, Palaeoecology, 77, 203-234.
17. Ferrusquia-Villafranca, I. (1993) Geology of Mexico: a synopsis. Biological diversity of Mexico: origins and distribution (ed. by T.P. Ramamoorthy, R. Bye, A. Lot and J. Fa ), pp. 3-107. Oxford University Press, New York.
18. Garzione, C.N. (2008) Surface uplift of Tibet and Cenozoic global cooling. Geology, 36, 1003-1004.
19. Gentry, A.H. (1982) Neotropical floristic diversity: phytogeographical connections between Central and South America. Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden, 69, 557-593.
20. Glor, R.E., Vitt, L.J. & Larson, A. (2001) A molecular phylogenetic analysis of diversification in Amazonian Anolis lizards. Molecular Ecology, 10, 2661-2668.
21. Graham, A. (2009) The Andes: a geological overview from a biological perspective. Annals of the Missouri Botanical Garden, 96, 371-385.
22. Gregory-Wodzicki, K.M. (2000) Uplift history of the Central and Northern Andes: a review. Geological Society of America Bulletin, 112, 1091-1105.
23. Haber, W.A. (2000) Plants and vegetation. Monteverde: ecology and conservation of a tropical cloud forest (ed. by N.M. Nadkarni and N.T. Wheelwright ), pp. 39-94. Oxford University Press, New York.
24. Haffer, J. (1969) Speciation in Amazonian forest birds. Science, 165, 131-137.
25. von Hagen, K.B. & Kadereit, J.W. (2001) The phylogeny of Gentianella (Gentianaceae) and its colonization of the southern hemisphere as revealed by nuclear and chloroplast DNA sequence variation. Organisms Diversity & Evolution, 1, 61-79.
26. von Hagen, K.B. & Kadereit, J.W. (2003) The diversification of Halenia (Gentianaceae): ecological opportunity versus key innovation. Evolution, 57, 2507-2518.
27. van der Hammen, T. & Hooghiemstra, H. (2000) Neogene and Quaternary history of vegetation. Quaternary Science Reviews, 19, 725-742.
28. Haq, B.U., Hardenbol, J. & Vail, P.R. (1987) Chronology of fluctuating sea levels since the Triassic. Science, 235, 1156-1166.
29. Hartley, A.J. (2003) Andean uplift and climate change. Journal of the Geological Society, 160, 7-10.
30. Hill, A.W. (1906) The morphology and seedling structure of the geophilous species of Peperomia, together with some views on the origin of monocotyledons. Annals of Botany, 20, 395-427.
31. Hill, A.W. (1907) A revision of the geophilous species of Peperomia with some additional notes on their morphology and seedling structure. Annals of Botany, 21, 141-160.
32. Ho, S.Y.W. (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. Journal of Avian Biology, 38, 409-414.
33. Hooghiemstra, H. & Van der Hammen, T. (2004) Quaternary Ice-Age dynamics in the Colombian Andes: developing an understanding of our legacy. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 173-181.
34. Hoorn, C., Guerrero, J., Sarmiento, G.A. & Lorente, M.A. (1995) Andean tectonics as a cause of changing drainage patterns in Miocene northern South America. Geology, 23, 237-240.
35. Horn, S.P., Sanford, R.L., Dilcher, D., Lott, T.A., Renne, P.R., Wiemann, M.C., Cozadd, D. & Vargas, O. (2003) Pleistocene plant fossils in and near La Selva Biological Station, Costa Rica. Biotropica, 35, 434-441.
36. Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754-755.
37. Hughes, C. & Eastwood, R. (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences USA, 103, 10334-10339.
38. Hungerbühler, D., Steinmann, M., Winkler, W., Seward, D., Eguez, A., Peterson, D.E., Helg, U. & Hammer, C. (2002) Neogene stratigraphy and Andean geodynamics of southern Ecuador. Earth-Science Reviews, 57, 75-124.
39. Iturralde-Vinent, M.A. & MacPhee, R.D.E. (1999) Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bulletin of the American Museum of Natural History, 238, 1-95.
40. Keigwin, L.D. (1978) Pliocene closing of the Isthmus of Panama based on biostratigraphic evidence from nearby Pacific and Caribbean sea cores. Geology, 6, 630-634.
41. Kodandaramaiah, U. (2010) Use of dispersal-vicariance analysis in biogeography - a critique. Journal of Biogeography, 37, 3-11.
42. Kreft, H. & Jetz, W. (2007) Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences USA, 104, 5925-5930.
43. Krzywinski, J., Wilkerson, R.C. & Besansky, N.J. (2001) Toward understanding Anophelinae (Diptera, Culicidae) phylogeny: insights from nuclear single-copy genes and weight of evidence. Systematic Biology, 50, 540-556.
44. Lovejoy, N.R., Albert, J.S. & Crampton, W.G.R. (2006) Miocene marine incursions and marine/freshwater transitions. Journal of South American Earth Sciences, 21, 5-13.
45. MacPhail, M.K., Partridge, A.D. & Truswell, E.M. (1999) Fossil pollen records of the problematical primitive angiosperm family Lactoridaceae in Australia. Plant Systematics and Evolution, 214, 199-210.
46. Magallón, S. (2010) Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology, 59, 384-399.
47. Magallón, S. & Sanderson, M.J. (2001) Absolute diversification rates in angiosperm clades. Evolution, 55, 1762-1780.
48. Marshall, C.J. & Liebherr, J.K. (2000) Cladistic biogeography of the Mexican transition zone. Journal of Biogeography, 27, 203-216.
49. Mathieu, G., Symmank, L., Callejas, R., Wanke, S., Neinhuis, C., Goetghebeur, P. & Samain, M.S. (2011) New geophytic Peperomia (Piperaceae) species from Mexico, Belize and Costa Rica. Revista Mexicana de Biodiversidad, 82, 357-382.
50. McLoughlin, S. (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Australian Journal of Botany, 49, 271-300.
51. Miller, K.G., Fairbanks, R.G. & Mountain, G.S. (1987) Tertiary oxygen isotope synthesis, sea level history and continental margin erosion. Paleoceanography, 2, 1-19.
52. Moore, M.J., Tye, A. & Jansen, R.K. (2006) Patterns of long-distance dispersal in Tiquilia subg. Tiquilia (Boraginaceae): implications for the origin of amphitropical disjuncts and Galápagos Islands endemics. American Journal of Botany, 93, 1163-1177.
53. Moore, M.J., Bell, C.D., Soltis, P.S. & Soltis, D.E. (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences USA, 104, 19363-19368.
54. Moritz, C., Patton, J.L., Schneider, C.J. & Smith, T.B. (2000) Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology and Systematics, 31, 533-563.
55. Mosblech, N.A.S., Bush, M.B. & van Woesik, R. (2011) On metapopulations and microrefugia: palaeoecological insights. Journal of Biogeography, 38, 419-429.
56. Müller, K. (2005) SeqState: primer design and sequence statistics for phylogenetic DNA data sets. Applied Bioinformatics, 4, 65-69.
57. Noble, D.C., McKee, E.H., Mourier, T. & Mégard, F. (1990) Cenozoic stratigraphy, magmatic activity, compressive deformation and uplift in northern Peru. Geological Society of America Bulletin, 102, 1105-1113.
58. Pennington, R.T. & Dick, C.W. (2004) The role of immigrants in the assembly of the South American rainforest tree flora. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 1611-1622.
59. Pennington, R.T., Prado, D.A. & Pendry, C. (2000) Neotropical seasonally dry forests and Pleistocene vegetation changes. Journal of Biogeography, 27, 261-273.
60. Pennington, R.T., Lavin, M., Prado, D.E., Pendry, C.A., Pell, S.K. & Butterworth, C.A. (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 515-538.
61. Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
62. Rahbek, C. & Graves, G.R. (2001) Multiscale assessment of patterns of avian species richness. Proceedings of the National Academy of Sciences USA, 98, 4534-4539.
63. Rambaut, A. (2009) FigTree v1.2.3. Available at: .
64. Rambaut, A. & Drummond, A.J. (2009) Tracer v1.5. Available at: .
65. Raven, P.H. (1963) Amphitropical relationships in the floras of North and South America. Quarterly Review of Biology, 38, 151-177.
66. Raven, P.H. & Axelrod, D.I. (1974) Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden, 61, 539-673.
67. Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4-14.
68. Ree, R.H., Moore, B.R., Webb, C.O. & Donoghue, M.J. (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution, 59, 2299-2311.
69. Renner, S.S. (2005) Relaxed molecular clocks for dating historical plant dispersal events. Trends in Plant Science, 10, 550-558.
70. Richter, M., Diertl, K.-H., Emck, P., Peters, T. & Beck, E. (2009) Reasons for an outstanding plant diversity in the tropical Andes of southern Ecuador. Landscape Online, 12, 1-35.
71. Ronquist, F. (1996) DIVA, version 1.1. Computer program and manual available by anonymous FTP from Uppsala University, Uppsala, Sweden. Available at: or .
72. Ronquist, F. (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 45, 195-203.
73. Rull, V. (2009) Microrefugia. Journal of Biogeography, 36, 481-484.
74. Samain, M.S., Vanderschaeve, L., Chaerle, P., Goetghebeur, P., Neinhuis, C. & Wanke, S. (2009) Is morphology telling the truth about the evolution of the species rich genus Peperomia (Piperaceae)? Plant Systematics and Evolution, 278, 1-21.
75. Samain, M.S., Mathieu, G., Pino, G., Symmank, L., Cieza, N., Neinhuis, C., Goetghebeur, P. & Wanke, S. (2011) The geophytic Peperomia subgenus Tildenia (Piperaceae) in the Andes with the description of new species in a phylogenetic framework. Plant Ecology and Evolution, 144, 148-176.
76. Sanderson, M.J. (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101-109.
77. Sanderson, M.J., Thorne, J.L., Wikstrom, N. & Bremer, K. (2004) Molecular evidence on plant divergence times. American Journal of Botany, 91, 1656-1665.
78. Sanmartín, I. & Ronquist, F. (2004) Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology, 53, 216-243.
79. Santos, C., Jaramillo, C., Bayona, G., Rueda, M. & Torres, V. (2008) Late Eocene marine incursion in north-western South America. Palaeogeography, Palaeoclimatology, Palaeoecology, 264, 140-146.
80. Simmons, M.P. & Ochoterena, H. (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology, 49, 369-381.
81. Simpson, B.B., Tate, J.A. & Weeks, A. (2005) The biogeography of Hoffmannseggia (Leguminosae, Caesalpinioideae, Caesalpinieae): a tale of many travels. Journal of Biogeography, 32, 15-27.
82. Simpson, G.G. (1980) Splendid isolation: the curious history of South American mammals. Yale University Press, New Haven, CT.
83. Smith, J.F., Stevens, A.C., Tepe, E.J. & Davidson, C. (2008) Placing the origin of two species-rich genera in the late Cretaceous with later species divergence in the Tertiary: a phylogenetic, biogeographic and molecular dating analysis of Piper and Peperomia (Piperaceae). Plant Systematics and Evolution, 275, 9-30.
84. Smith, S.Y. & Stockey, R.A. (2007) Establishing a fossil record for the perianthless Piperales: Saururus tuckerae sp. nov. (Saururaceae) from the Middle Eocene Princeton Chert. American Journal of Botany, 94, 1642-1657.
85. Somoza, R. (1998) Updated Nazca (Farallon)-South America relative motions during the last 40 My: implications for mountain building in the central Andean region. Journal of South American Earth Science, 11, 211-215.
86. Stehli, F. & Webb, S. (1985) The Great American Biotic Interchange. Plenum Press, New York.
87. Steinberg, M. & Taylor, M. (2008) Guatemala's Altos de Chiantla: changes on the high frontier. Mountain Research and Development, 28, 255-262.
88. Stern, S.R., Tepe, E.J. & Bohs, L.A. (2008) Checklist of Solanum of north-central Peru: a hotspot of biological diversity. Arnoldoa, 15, 277-284.
89. Stöver, B.C. & Müller, K.F. (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics, 11, 7.
90. Toledo, V.M. (1976) Los cambios climáticos del Pleistoceno y sus efectos sobre la vegetación tropical cálida y húmeda de México. Master's Thesis, Universidad Nacional Autónoma de México, Mexico City.
91. Torsvik, T.H. & Van der Voo, R. (2002) Refining Gondwana and Pangea palaeogeography: estimates of Phanerozoic non-dipole (octupole) fields. Geophysical Journal International, 151, 771-794.
92. Trelease, W. (1930) The geography of American peppers. Proceedings of the American Philosophical Society, 69, 309-327.
93. Véliz, M. (2007) Nuevas especies del género Peperomia (Piperaceae) de Centro América. Cactus Aventuras Internacional, 73, 2-13.
94. Vovides, A.P., Pérez-Farrera, M.A., González-Astorga, J. & Iglesias, C. (2008) A new species of Ceratozamia (Zamiaceae) from Oaxaca, Mexico with comments on habitat and relationships. Botanical Journal of the Linnaean Society, 157, 169-175.
95. Wanke, S., Samain, M.S., Vanderschaeve, L., Mathieu, G., Goetghebeur, P. & Neinhuis, C. (2006) Phylogeny of the genus Peperomia (Piperaceae) inferred from the trnK/matK region (cpDNA). Plant Biology, 8, 93-102.
96. Wanke, S., Jaramillo, M.A., Borsch, T., Samain, M.S., Quandt, D. & Neinhuis, C. (2007) Evolution of Piperales -matK gene and trnK intron sequence data reveal lineage specific resolution contrast. Molecular Phylogenetics and Evolution, 42, 477-497.
97. Weigend, M. (2002) Observations on the biogeography of the Amotape-Huancabamba Zone in Northern Peru. The Botanical Review, 68, 38-54.
98. Weigend, M. (2004) Additional observations on the biogeography of the Amotape-Huancabamba zone in northern Peru: defining the south-eastern limits. Revista Peruana de Biología, 11, 127-134.
99. Weigend, M., Gottschling, M., Hilger, H.H. & Nürk, N.M. (2010) Five new species of Lithospermum L. (Boraginaceae tribe Lithospermeae) in Andean South America: another radiation in the Amotape-Huancabamba Zone. Taxon, 59, 1161-1179.
100. Wendt, T. (1987) Las selvas de Uxpanapa, Veracruz-Oaxaca, México: evidencia de refugios florísticos Cenozoicos. Anales del Instituto de Biología UNAM (Series Botánica), 58, 29-54.
101. Westerhold, T., Bickert, T. & Rohl, U. (2005) Middle to late Miocene oxygen isotope stratigraphy of ODP site 1085 (SE Atlantic): new constrains on Miocene climate variability and sea-level fluctuations. Palaeogeography, Palaeoclimatology, Palaeoecology, 217, 205-222.
102. Wilf, P., Cúneo, N.R., Johnson, K.R., Hicks, J.F., Wing, S.L. & Obradovich, J.D. (2003) High plant diversity in Eocene South America: evidence from Patagonia. Science, 300, 122-125.
103. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. (2001) Trends, rhythms, and aberrations in global climate 65Ma to present. Science, 292, 686-693.
104. Zavada, M.S. & Benson, J.M. (1987) First fossil evidence for the primitive angiosperm family Lactoridaceae. American Journal of Botany, 74, 1590-1594.