Beyond aridification: Multiple explanations for the elevated diversification of cacti in the New World Succulent Biome

New Phytologist

Volumn 202, Issue 4, 2014, Pages 1382-1397

  Hernández Hernández, Tania ^a   Brown, Joseph W ^b   Schlumpberger, Boris O ^c   Eguiarte, Luis E ^d   Magallón, Susana ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Herrenhausen Gardens   (Germany)

^d INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Adaptive radiation; BEAST; BiSSE; Cactaceae; Diversification rates; MEDUSA; Pollination syndromes; Succulent Biome

Indexed keywords

CACTACEAE;

BIODIVERSITY; CACTACEAE; EVOLUTION; GENETICS; PHYLOGENY; PHYSIOLOGY;

BIODIVERSITY; BIOLOGICAL EVOLUTION; CACTACEAE; PHYLOGENY;

EID: 84899938368     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12752     Document Type: Article

References (127)

1. Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A, Rabosky DL, Carnevale G, Harmon LJ. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences, USA 106: 13 410-13 414.
2. Ali SS, Yu Y, Pfosser M, Wetschnigl W. 2012. Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies). Annals of Botany 109: 95-107.
3. Antonelli A, Sanmartín I. 2011. Why are there so many plant species in the Neotropics? Taxon 60: 403-414.
4. Applequist WL, Wallace RS. 2000. Phylogeny of the Madagascan endemic family Didiereaceae. Plant Systematics and Evolution 221: 157-166.
5. Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences, USA 108: 8379-8384.
6. Arias S, Terrazas T, Arreola-Nava HJ, Vázquez-Sánchez M, Cameron KM. 2005. Phylogenetic relationships in Peniocereus (Cactaceae) inferred from plastid DNA sequence data. Journal of Plant Research 118: 317-328.
7. Arias S, Terrazas T, Cameron KM. 2003. Phylogenetic analysis of Pachycereus (Cactaceae, Pachycereeae) based on chloroplast and nuclear DNA sequences. Systematic Botany 28: 547-557.
8. Axelrod DI. 1972. Edaphic aridity as a factor in angiosperm evolution. American Naturalist 106: 311-320.
9. Axelrod DI. 1979. Desert vegetation, its age and origin. Goodin JR, Northington DK, eds. Arid land plant resources. Lubbock, TX, USA: International Center for Arid and Semi-Arid Land Studies, 1-72.
10. Bárcenas RT, Yesson C, Hawkins JA. 2011. Molecular systematics of the Cactaceae. Cladistics 27: 1-20.
11. Barthlott W, Hunt DR. 1993. Cactaceae. Kubitzki K, ed. The families and genera of vascular plants. New York, NY, USA: Springer, 161-197.
12. Bruyns PV, Klak C, Hanácek P. 2011. Age and diversity in Old World succulent species of Euphorbia (Euphorbiaceae). Taxon 60: 1717-1733.
13. Butterworth CA, Cota-Sanchez JH, Wallace RS. 2002. Molecular systematics of tribe Cacteae (Cactaceae: Cactoideae): a phylogeny based on rpl16 intron sequence variation. Systematic Botany 27: 257-270.
14. Butterworth CA, Wallace RS. 2004. Phylogenetic studies of Mammillaria (Cactaceae) - insights from chloroplast sequence variation and hypothesis testing using the parametric bootstrap. American Journal of Botany 91: 1086-1098.
15. Butterworth CA, Wallace RS. 2005. Molecular phylogenetics of the leafy cactus genus Pereskia (Cactaceae). Systematic Botany 30: 800-808.
16. Buxbaum F. 1969. Die Entwicklungswege der Kakteen in Südamerika. Fittkau EJ, Illies J, Klineg H, Schwabe GH, Sioli H, eds. Biogeography and ecology in South America. The Hague, the Netherlands: Dr. W. Junk, 583-623.
17. Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R et al. 2008. Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17: 4398-4417.
18. Calsbeek R, Thompson JN, Richardson JE. 2003. Patterns of molecular evolution and diversification in a biodiversity hotspot: the California Floristic Province. Molecular Ecology 12: 1021-1029.
19. Calvente A, Zappi DC, Forest F, Lohmann LG. 2011. Molecular phylogeny, evolution and biogeography of South American epiphytic cacti. International Journal of Plant Sciences 172: 902-914.
20. Catalano SA, Vilardi JC, Tosto D, Saidman BO. 2008. Molecular phylogeny and diversification history of Prosopis (Fabaceae: Mimosoideae). Biological Journal of the Linnean Society 93: 621-640.
21. Cota JH. 1993. Pollination syndromes in the genus Echinocereus: a review. Cactus and Succulent Journal 65: 19-26.
22. Cota JH, Philbrick CT. 1994. Chromosome number variation and polyploidy in the genus Echinocereus (Cactaceae). American Journal of Botany 81: 1054-1062.
23. Cota JH, Wallace RS. 1995. Karyotypic studies in the genus Echinocereus (Cactaceae) and their taxonomic significance. Caryologia 48: 105-122.
24. De-Nova JA, Medina R, Montero JC, Weeks A, Rosell JA, Olson ME, Eguiarte LE, Magallón S. 2012. Insights into the historical construction of species-rich Mesoamerican seasonally dry tropical forests: the diversification of Bursera (Burseraceae, Sapindales). New Phytologist 193: 276-287.
25. Dillon MO, Tu T, Xie L, Quipuscoa Silvestre V, Wen J. 2009. Biogeographic diversification in Nolana (Solanaceae), a ubiquitous member of the Atacama and Peruvian deserts along the western coast of South America. Journal of Systematics and Evolution 47: 457-476.
26. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
27. Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
28. Edwards EJ, Nyffeler R, Donoghue MJ. 2005. Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. American Journal of Botany 92: 1177-1188.
29. Ellis AG, Weis AE. 2006. Coexistence and differentiation of 'flowering stones': the role of local adaptation to soil microenvironment. Journal of Ecology 94: 322-335.
30. Ellis AG, Weis AE, Gaut B. 2006. Evolutionary radiation of "stone plants" in the genus Argyoderma (Aizoaceae): unraveling the effects of landscape, habitat and flowering time. Evolution 60: 39-55.
31. Farrell BD, Dussourd DE, Mitter C. 1991. Escalation of plant defense: do latex and resin canals spur plant diversification? American Naturalist 138: 881-900.
32. Fleming TH, Geiselman C, Kress WJ. 2009. The evolution of bat pollination: a phylogenetic perspective. Annals of Botany 104: 1017-1043.
33. Gascoigne J, Berec L, Gregory S, Courchamp F. 2009. Dangerously few liaisons: a review of mate-finding Allee effects. Population Ecology 51: 355-372.
34. Gentry AH. 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.
35. Ghazoul J. 2005. Implications of plant spatial distribution for pollination and seed production. Burslem D, Pinard M, Hartley S, eds. Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge, UK: Cambridge University Press, 241-266.
36. Gibson AC. 1982. Phylogenetic relationships of Pachycereeae. Barker JSF, Stramer WT, eds. Ecological genetics and evolution: the cactus-yeast-Drosophila model system. New York, NY, USA: Academic Press, 3-16.
37. Gibson AC. 1996. Structure-function relations of warm desert plants. New York, NY, USA: Springer.
38. Gibson AC, Horak KE. 1978. Systematic anatomy and phylogeny of Mexican columnar cacti. Annals of the Missouri Botanical Garden 65: 999-1057.
39. Gibson AC, Nobel PS. 1986. The cactus primer. Cambridge, MA, USA: Harvard University Press.
40. Gómez-Hinostrosa C, Hernández HM. 2000. Diversity, geographical distribution, and conservation of Cactaceae in the Miery Noriega region, Mexico. Biodiversity and Conservation 9: 403-418.
41. Good-Avila SV, Souza V, Gaut BS, Eguiarte LE. 2006. Timing and rate of speciation in Agave (Agavaceae). Proceedings of the National Academy of Sciences, USA 103: 9124-9129.
42. Graham A. 2011. The age and diversification of terrestrial New World ecosystems through Cretaceous and Cenozoic time. American Journal of Botany 98: 336-351.
43. Grant V, Grant K. 1979. The pollination spectrum in the southwestern American cactus flora. Plant Systematics and Evolution 133: 29-37.
44. Griffith MP, Porter JM. 2009. Phylogeny of Opuntioideae (Cactaceae). International Journal of Plant Sciences 170: 107-116.
45. Guerrero P, Rosas M, Arroyoa MTK, Wiens JJ. 2013. Evolutionary lag times and recent origin of the biota of an ancient desert (Atacama-Sechura). Proceedings of the National Academy of Sciences, USA 110: 11 469-11 474.
46. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
47. Hartley A, Chong G, Houston J, Mather AE. 2005. 150 million years of climatic stability: evidence from the Atacama Desert, northern Chile. Journal of the Geological Society, London 162: 421-424.
48. Hernández HM, Gómez-Hinostrosa C. 2005. Cactus diversity and endemism in the Chihuahuan Desert Region. Cartron JL, Felger R, Ceballos G, eds. Biodiversity and conservation in Northern Mexico. New York, NY, USA: Oxford University Press, 264-275.
49. Hernández HM, Gómez-Hinostrosa C, Bárcenas R. 2001. Diversity, spatial arrangement, and endemism of Cactaceae in the Huizache area, a hot-spot in the Chihuahuan Desert. Biodiversity and Conservation 10: 1097-1112.
50. Hernández-Hernández T. 2010. Radiaciones evolutivas de linajes de plantas suculentas en el orden Caryophyllales, con énfasis en la familia Cactaceae. Doctoral thesis, Posgrado en Ciencias Biológicas, UNAM, México.
51. Hernández-Hernández T, Hernández HM, De-Nova JA, Puente R, Eguiarte LE, Magallón S. 2011. Phylogenetic relationships and evolution of growth form in Cactaceae (Caryophyllales, Eudicotyledoneae). American Journal of Botany 98: 44-61.
52. Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP et al. 2010. Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931.
53. Horn JW, van Ee BW, Morawetz JJ, Riina R, Steinmann VW, Berry PE, Wurdack KJ. 2012. Phylogenetics and the evolution of major structural characters in the giant genus Euphorbia L. (Euphorbiaceae). Molecular Phylogenetics and Evolution 63: 305-326.
54. Hunt D, Taylor NP, Charles G. 2006. The new cactus lexicon. Milborne Port, UK: DH Books.
55. Johnson SD. 2010. The pollination niche and its role in the diversification and maintenance of the southern Africa flora. Philosophical Transactions of the Royal Society of London B 365: 499-516.
56. Kass RE, Raftery AE. 1995. Bayes factors. Journal of the American Statistical Association 90: 773-795.
57. Kellner A, Ritz CM, Schlittenhardt P, Hellwig FH. 2011. Genetic differentiation in the genus Lithops L. (Ruschioideae, Aizoaceae) reveals a high level of convergent evolution and reflects geographic distribution. Plant Biology 13: 368-380.
58. Klak C, Khunou A, Reeves G, Hedderson T. 2003. A phylogenetic hypothesis for the Aizoaceae (Caryophyllales) based on four plastid DNA regions. American Journal of Botany 90: 1433-1445.
59. Klak C, Reeves G, Hedderson T. 2004. Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427: 63-65.
60. Lavin M, Schrire BP, Lewis G, Pennington RT, Delgado-Salinas A, Thulin M, Hughes CE, BeyraMatos A, Wojciechowski MF. 2004. Metacommunity process rather than continental tectonic history better explains geographically structured phylogenies in legumes. Philosophical Transactions of the Royal Society of London B 359: 1509-1522.
61. Leuenberger BE. 1986. Pereskia (Cactaceae). Memoirs of the New York Botanical Garden 41: 1-141.
62. Livshultz T, Mead JV, Goyder DJ, Brannin M. 2011. Climate niches of milkweeds with plesiomorphic traits (Secamonoideae; Apocynaceae) and the milkweed sister group link ancient African climates and floral evolution. American Journal of Botany 98: 1966-1977.
63. Loera I, Sosa V, Ickert-Bond SM. 2012. Diversification in North American arid lands: niche conservatism, divergence and expansion of habitat explain speciation in the genus Ephedra. Molecular Phylogenetics and Evolution 65: 437-450.
64. Maddison WP, Midford PE, Otto SP. 2007. Estimating a binary character's effect on speciation and extinction. Systematic Biology 56: 701-710.
65. Magallón S, Castillo A. 2009. Angiosperm diversification through time. American Journal of Botany 96: 349-365.
66. Magallón S, Sanderson MJ. 2001. Absolute diversification rates in angiosperm clades. Evolution 55: 1762-1780.
67. Majure LC, Puente R, Griffith MP, Judd WS, Soltis PS, Soltis DE. 2012. Phylogeny of Opuntia s.s. (Cactaceae): clade delineation. American Journal of Botany 99: 847-864.
68. Mandujano MC, Carrillo-Angeles IG, Martínez-Peralta C, Golubov J. 2010. Reproductive biology of Cactaceae. Ramawat KG, ed. Desert plants - biology and biotechnology. Berlin, Germany: Springer, 197-230.
69. McGinnies WG. 1979. General description of desert areas. Goodall DW, Perry RA, eds. Arid land ecosystems, volume I. Cambridge, UK: Cambridge University Press, 5-20.
70. Molina-Freaner F, Eguiarte LE. 2003. The pollination biology of two paniculate agaves (Agavaceae) from northwestern Mexico: contrasting roles of bats as pollinators. American Journal of Botany 90: 1016-1024.
71. Moore MJ, Jansen RK. 2006. Molecular evidence for the age, origin and evolutionary history of the American desert plant genus Tiquilia (Boraginaceae). Molecular Phylogenetics and Evolution 39: 668-687.
72. Morafka DJ. 1977. A biogeographical analysis of the Chihuahuan Desert through its herpetofauna. The Hague, the Netherlands: Dr. W. Junk.
73. Morrone JJ. 2001. Biogeografía de América Latina y el Caribe. Manuales y Tesis SEA 3, Zaragoza, España.
74. Morrone JJ. 2002. Presentación Sintética de un Nuevo Esquema Biogeográfico de América Latina y el Caribe. Costa C, Vanin SA, Lobo JM, Melic A, eds. Hacia un Proyecto CYTED Para el Inventario y Estimación de la Diversidad Entomológica en Iberoamérica: PrIBES, Volumen 2. Zaragoza, España: Monografías Tercer Milenio, 267-275.
75. Morrone JJ. 2006. Biogeographic areas and transition zones of Latin America and the Caribbean Islands based on panbiogeographic and cladistic analyses of the entomofauna. Annual Review of Entomology 51: 467-494.
76. Newton MA, Raftery AE. 1994. Approximate Bayesian inference by the weighted likelihood bootstrap (with discussion). Journal of the Royal Statistical Society, Series B (Methodological) 56: 3-48.
77. van der Niet T, Johnson SD. 2012. Phylogenetic evidence for pollinator driven diversification of angiosperms. Trends Ecology & Evolution 27: 353-361.
78. Nobel PS. 2002. Cacti: biology and uses. Berkeley, CA, USA: University of California Press.
79. Nyffeler R. 2002. Phylogenetic relationships in the cactus family (Cactaceae) based on evidence from trnK/matK and trnL-trnF sequences. American Journal of Botany 89: 312-326.
80. Nyffeler R. 2007. The closest relatives of cacti: insights from phylogenetic analyses of chloroplast and mitochondrial sequences with special emphasis on relationships in the tribe Anacampserotaceae. American Journal of Botany 94: 89-101.
81. Nyffeler R, Eggli U. 2010. An up-to-date familial and suprafamilial classification of succulent plants. Bradleya 28: 125-144.
82. Ocampo G, Columbus JT. 2010. Molecular phylogenetics of suborder Cactineae (Caryophyllales), including insights into photosynthetic diversification and historical biogeography. American Journal of Botany 97: 1827-1847.
83. Ortega-Baes P, Godínez-Alvarez H. 2006. Global diversity and conservation priorities in the Cactaceae. Biodiversity and Conservation 15: 817-827.
84. Pagel M. 1994. Detecting correlated evolution on phylogenies: a general method for comparative analysis of discrete characters. Proceedings of the Royal Society of London B 225: 37-45.
85. Pagel M. 1997. Inferring evolutionary processes from phylogenies. Zoologica Scripta 26: 331-348.
86. Pagel M, Meade A. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist 167: 808-825.
87. Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633-1644.
88. Phillips SJ, Comus PW. 2000. A natural history of the Sonoran Desert. Tucson, AZ, USA: Arizona-Sonoran Desert Museum Press.
89. Pinkava DJ. 2002. On the evolution of the continental North American Opuntioideae (Cactaceae). Succulent Plant Research 6: 59-98.
90. Placzek C, Quade J, Betancourt JL, Patchett PJ, Rech JA, Latorre C, Matmon A, Holmgren C, Nathan B. 2009. Climate in the dry central Andes over geologic, millennial, and interannual timescales. Annals of the Missouri Botanical Garden 96: 386-397.
91. Porter JM. 1999. Sclerocactus and Pediocactus: a summary of the molecular evidence. Cactus Consensus Initiatives 7: 5-6.
92. Porter JM, Kinney MS, Heil KD. 2000. Relationships between Sclerocactus and Toumeya (Cactaceae) based on chloroplast trnL-trnF sequences. Haseltonia 7: 8-23.
93. Posadas P, Estevez JM, Morrone JJ. 1997. Distributional patterns and endemism areas of vascular plants in the Andean subregion. Fontqueria 48: 1-9.
94. Powell AM, Weedin JF. 2004. Cacti of the Trans-Pecos and adjacent areas. Lubbock, TX, USA: Texas Tech University Press.
95. Prance GT. 1977. Floristic inventory of the tropics: where do we stand? Annals of the Missouri Botanical Garden 64: 659-684.
96. Rabosky DL. 2006. Likelihood methods for detecting temporal shifts in diversification rates. Evolution 60: 1152-1164.
97. Rambaut A, Drummond AJ. 2007. TRACER. [WWW document] URL http://tree.bio.ed.ac.uk/software/tracer/ [accessed 20 April 2012].
98. Raven PH, Axelrod DI. 1974. Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden 61: 539-673.
99. Ree RH. 2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59: 257-265.
100. Ree RH, Smith SA. 2008. Maximum-likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 4-14.
101. Reyes-Agüero JA, Aguirre JR, Valiente-Banuet A. 2006. Reproductive biology of Opuntia: a review. Journal of Arid Environments 64: 549-585.
102. Ritz CM, Martins L, Mecklenburg R, Goremykin V, Hellwig FH. 2007. The molecular phylogeny of Rebutia (Cactaceae) and its allies demonstrates the influence of paleogeography on the evolution of South American mountain cacti. American Journal of Botany 94: 1321-1332.
103. Rull V. 2011. Neotropical biodiversity: timing and potential drivers. Trends in Ecology and Evolution 26: 508-513.
104. Schlumpberger BO. 2012. A survey on pollination modes in cacti and a potential key innovation. Patiny S, ed. Evolution of plant-pollinator interactions. Cambridge, UK: Cambridge University Press, 301-319.
105. Schlumpberger BO, Renner SS. 2012. Molecular phylogenetics of Echinopsis (Cactaceae): polyphyly at all levels and convergent evolution of pollination modes and growth forms. American Journal of Botany 99: 1335-1349.
106. Schnitzler J, Graham CH, Dormann DF, Schiffers K, Linder HP. 2012. Climatic niche evolution and species diversification in the Cape flora, South Africa. Journal of Biogeography 39: 2201-2211.
107. Schrire BD, Lavin M, Lewis GP. 2005. Global distribution patterns of the Leguminosae: insights from recent phylogenies. Friis I, Balslev H, eds. Plant diversity and complexity patterns: local, regional and global dimensions. Viborg, Denmark: Royal Danish Academy of Sciences and Letters, 375-422.
108. Silvera K, Santiago LS, Cushman JC, Winter K. 2009. Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiology 149: 1838-1847.
109. Smith CI, Pellmyr O, Althoff DM, Bálcazar-Lara M, Leebens-Mack J, Segraves KA. 2008. Pattern and timing of diversification in Yucca (Agavaceae): specialized pollination does not escalate rates of diversification. Proceedings of the Royal Society of London B 275: 249-258.
110. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodríguez NF, Walker JB, Moore MJ, Carlsward BS et al. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. American Journal of Botany 98: 704-730.
111. Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
112. Thiv M, Van der Niet T, Rutschmann F, Thulin M, Brune T, Linder HP. 2011. Old-New World and trans-African disjunctions of Thamnosma (Rutaceae): intercontinental long- distance dispersal and local differentiation in the succulent biome. American Journal of Botany 98: 76-87.
113. Tidwell WD, Nambudiri EMV. 1989. Tomlisonia thomassonii, gen et sp. nov., a permineralized grass from the upper Miocene Ricardo Formation, California. Review of Palaeobotany and Palynology 60: 165-177.
114. Valiente-Banuet A, Arizmendi MC, Rojas-Martínez A, Domínguez-Canseco I. 1996. Ecological relationships between columnar cacti and nectar feeding bats in Mexico. Journal of Tropical Ecology 12: 103-119.
115. Van Devender TR. 2000. The deep history of the Sonoran Desert. Phillips SJ, Comus PW, eds. A natural history of the Sonoran Desert. Tucson, AZ, USA: Arizona-Sonoran Desert Museum Press, 61-69.
116. Verboom GA, Archibald JK, Bakker FT, Bellstedt DU, Conrad F, Dreyer LL, Forest F, Galley C, Goldblatt P, Henning JF et al. 2009. Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Molecular Phylogenetics and Evolution 51: 44-53.
117. Wallace RS. 1995. Molecular systematic study of the Cactaceae: using chloroplast DNA variation to elucidate cactus phylogeny. Bradleya 13: 1-12.
118. Wallace RS. 2002. The phylogeny and systematics of columnar cacti: an overview. Fleming TH, Valiente-Banuet A, eds. Columnar cacti and their mutualists: evolution, ecology and conservation. Tucson, AZ, USA: The University of Arizona Press, 42-65.
119. Wallace RS, Cota JH. 1996. An intron loss in the chloroplast gene rpoC1 supports a monophyletic origin of the subfamily Cactoideae of the Cactaceae. Current Genetics 29: 275-281.
120. Wallace RS, Dickie SL. 2002. Systematic implications of chloroplast DNA sequence variation in subfam. Opuntioideae (Cactaceae). Succulent Plant Research 6: 9-24.
121. Wallace RS, Gibson AC. 2002. Evolution and systematics. Nobel PS, ed. Cacti, biology and uses. Los Angeles, CA, USA: University of California Press, 1-21.
122. Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE. 2009. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proceedings of the National Academy of Sciences, USA 106: 3853-3858.
123. Xu S, Schlüter PM, Schiestl FP. 2012. Pollinator-driven speciation in sexually deceptive orchids. International Journal of Ecology 2012: Article ID 285081.
124. Yu Y, Harris AJ, He X-J. 2010. S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution 56: 848-850.
125. Yu Y, Harris AJ, He X-J. 2011. RASP (Reconstruct Ancestral State in Phylogenies) 2.0 beta. [WWW document] URL http://mnh.scu.edu.cn/soft/blog/RASP [accessed 10 February 2013].
126. Zachos JC, Dickens GR, Zeebe RE. 2008. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451: 279-283.
127. Ziegler AM, Eshel G, Rees PM, Rothfus TA, Rowley DB, Sunderlin D. 2003. Tracing the tropics across land and sea: permian to present. Lethaia 36: 227-254.