Species diversity is remarkably unevenly distributed among flowering plant lineages. Despite a growing toolbox of research methods, the reasons underlying this patchy pattern have continued to perplex plant biologists for the past two decades. In this review, we examine the present understanding of transitions in flowering plant evolution that have been proposed to influence speciation and extinction. In particular, ploidy changes, transitions between tropical and nontropical biomes, and shifts in floral form have received attention and have offered some surprises in terms of which factors influence speciation and extinction rates. Mating systems and dispersal characteristics once predominated as determining factors, yet recent evidence suggests that these changes are not as influential as previously thought or are important only when paired with range shifts. Although range extent is an important correlate of speciation, it also influences extinction and brings an applied focus to diversification research. Recent studies that find that past diversification can predict present-day extinction risk open an exciting avenue for future research to help guide conservation prioritization.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A. 1.  et al. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. PNAS 106:13410–14 [Google Scholar]
  2. Antonelli A, Zizka A, Silvestro D, Scharn R, Cascales-Miñana B, Bacon CD. 2.  2015. An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics. Front. Genet. 6:130 [Google Scholar]
  3. Armbruster WS.3.  2002. Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. J. Evol. Biol. 15:468–86 [Google Scholar]
  4. Armbruster WS, Debevec EM, Willson MF. 4.  2002. Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. J. Evol. Biol. 15:657–72 [Google Scholar]
  5. Baldwin BG, Sanderson MJ. 5.  1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). PNAS 95:9402–6 [Google Scholar]
  6. Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA. 6.  2016. On the relative abundance of autopolyploids and allopolyploids. New Phytol 210:391–98 [Google Scholar]
  7. Barrett SCH.7.  2013. The evolution of plant reproductive systems: How often are transitions irreversible?. Proc. R. Soc. B 280:20130913 [Google Scholar]
  8. Beaulieu JM, O'Meara BC. 8.  2016. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65:583–601 [Google Scholar]
  9. Bouchenak-Khelladi Y, Onstein RE, Xing Y, Schwery O, Linder HP. 9.  2015. On the complexity of triggering evolutionary radiations. New Phytol 207:313–26 [Google Scholar]
  10. Brochmann C, Brysting AK, Alsos IG, Borgen L, Grundt HH. 10.  et al. 2004. Polyploidy in Arctic plants. Biol. J. Linn. Soc. 82:521–36 [Google Scholar]
  11. Bromham L, Hua X, Cardillo M. 11.  2016. Detecting macroevolutionary self-destruction from phylogenies. Syst. Biol. 65:109–27 [Google Scholar]
  12. Buerki S, Jose S, Yadav SR, Goldblatt P, Manning JC, Forest F. 12.  2012. Contrasting biogeographic and diversification patterns in two Mediterranean-type ecosystems. PLOS ONE 7:e39377 [Google Scholar]
  13. Citerne HL, Jabbour F, Nadot S, Damerval C. 13.  2010. The evolution of floral symmetry. Adv. Bot. Res. 54:85–137 [Google Scholar]
  14. Citerne HL, Reyes E, Le Guilloux M, Delannoy E, Simonnet F. 14.  et al. 2017. Characterization of CYCLOIDEA-like genes in Proteaceae, a basal eudicot family with multiple shifts in floral symmetry. Ann. Bot. 119:367–78 [Google Scholar]
  15. Comes HP, Tribsch A, Bittkau C. 15.  2008. Plant speciation in continental island floras as exemplified by Nigella in the Aegean Archipelago. Phil. Trans. R. Soc. B 363:3083–96 [Google Scholar]
  16. Crane PR, Lidgard S. 16.  1989. Angiosperm diversification and paleolatitudinal gradients in Cretaceous floristic diversity. Science 246:675–78 [Google Scholar]
  17. Crepet WL.17.  1984. Advanced (constant) insect pollination mechanisms: pattern of evolution and implications vis-a-vis angiosperm diversity. Ann. Mo. Bot. Gard. 71:607–30 [Google Scholar]
  18. Crepet WL, Niklas KJ. 18.  2009. Darwin's second “abominable mystery”: Why are there so many angiosperm species?. Am. J. Bot. 96:366–81 [Google Scholar]
  19. Crisp MD, Arroyo MTK, Cook LG, Gandolfo MA, Jordan GJ. 19.  et al. 2009. Phylogenetic biome conservatism on a global scale. Nature 458:754–56 [Google Scholar]
  20. Cubas P.20.  2004. Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:1175–84 [Google Scholar]
  21. Daru BH, Yessoufou K, Mankga LT, Davies TJ. 21.  2013. A global trend towards the loss of evolutionarily unique species in mangrove ecosystems. PLOS ONE 8:e66686 [Google Scholar]
  22. Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V. 22.  2004. Darwin's abominable mystery: insights from a supertree of the angiosperms. PNAS 101:1904–9 [Google Scholar]
  23. Davies TJ, Barraclough TG, Savolainen V. 23.  2004. Environmental causes for plant biodiversity gradients. Philos. Trans. R. Soc. B 359:1645–56 [Google Scholar]
  24. Davies TJ, Smith GF, Bellstedt DU, Boatwright JS, Bytebier B. 24.  et al. 2011. Extinction risk and diversification are linked in a plant biodiversity hotspot. PLOS Biol 9:e1000620 [Google Scholar]
  25. De Bodt S, Maere S, Van de Peer Y. 25.  2005. Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 20:591–97 [Google Scholar]
  26. Drummond CS, Eastwood RJ, Miotto STS, Hughes CE. 26.  2012. Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling. Syst. Biol. 61:443–60 [Google Scholar]
  27. Endress PK.27.  1982. Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31:48–52 [Google Scholar]
  28. Endress PK.28.  2001. Evolution of floral symmetry. Curr. Opin. Plant Biol. 4:86–91 [Google Scholar]
  29. Endress PK.29.  2001. Origins of flower morphology. J. Exp. Zool. 291:105–15 [Google Scholar]
  30. Endress PK.30.  2006. Angiosperm floral evolution: morphological developmental framework. Adv. Bot. Res. 44:1–61 [Google Scholar]
  31. Endress PK.31.  2010. Flower structure and trends of evolution in eudicots and their major subclades. Ann. Mo. Bot. Gard. 97:541–83 [Google Scholar]
  32. Endress PK.32.  2011. Evolutionary diversification of the flowers in angiosperms. Am. J. Bot. 98:370–96 [Google Scholar]
  33. Fawcett JA, Maere S, Van de Peer Y. 33.  2009. Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. PNAS 106:5737–42 [Google Scholar]
  34. FitzJohn RG.34.  2010. Quantitative traits and diversification. Syst. Biol. 59:619–33 [Google Scholar]
  35. FitzJohn RG.35.  2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3:1084–92 [Google Scholar]
  36. FitzJohn RG, Maddison WP, Otto SP. 36.  2009. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58:595–611 [Google Scholar]
  37. Foster CSP, Sauquet H, van der Merwe M, McPherson H, Rossetto M, Ho SYW. 37.  2017. Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Syst. Biol. 66:338–51 [Google Scholar]
  38. Freeling M.38.  2017. Picking up the ball at the K/Pg boundary: the distribution of ancient polyploidies in the plant phylogenetic tree as a spandrel of asexuality with occasional sex. Plant Cell 29:202–6 [Google Scholar]
  39. Gentry AH.39.  1988. Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann. Mo. Bot. Gard. 75:1–34 [Google Scholar]
  40. Givnish TJ, Barfuss MHJ, Van Ee B Riina R, Schulte K. 40.  et al. 2014. Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Mol. Phylogenetics Evol. 71:55–78 [Google Scholar]
  41. Goldberg EE, Igić B. 41.  2012. Tempo and mode in plant breeding system evolution. Evolution 66:3701–9 [Google Scholar]
  42. Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igić B. 42.  2010. Species selection maintains self-incompatibility. Science 330:493–95 [Google Scholar]
  43. Goldberg EE, Lancaster LT, Ree RH. 43.  2011. Phylogenetic inference of reciprocal effects between geographic range evolution and diversification. Syst. Biol. 60:451–65 [Google Scholar]
  44. Goldberg EE, Otto SP, Vamosi JC, Mayrose I, Sabath N. 44.  et al. 2017. Macroevolutionary synthesis of flowering plant sexual systems. Evolution 71:898–912 [Google Scholar]
  45. Gonzalez-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N. 45.  et al. 2016. Phylogenetic approaches reveal biodiversity threats under climate change. Nat. Clim. Change 6:1110–14 [Google Scholar]
  46. Grant V.46.  1981. Plant Speciation New York: Columbia Univ. Press [Google Scholar]
  47. Hileman LC.47.  2014. Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philos. Trans. R. Soc. B 369:20130348 [Google Scholar]
  48. Hodges SA, Arnold ML. 48.  1995. Spurring plant diversification: Are floral nectar spurs a key innovation?. Proc. R. Soc. B 262:343–48 [Google Scholar]
  49. Hohmann N, Wolf EM, Lysak MA, Koch MA. 49.  2015. A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell 27:2770–84 [Google Scholar]
  50. Huang D, Goldberg EE, Roy K. 50.  2015. Fossils, phylogenies, and the challenge of preserving evolutionary history in the face of anthropogenic extinctions. PNAS 112:4909–14 [Google Scholar]
  51. Huelsenbeck JP, Nielsen R, Bollback JP. 51.  2003. Stochastic mapping of morphological characters. Syst. Biol. 52:131–58 [Google Scholar]
  52. Hughes C, Eastwood R. 52.  2006. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. PNAS 103:10334–39 [Google Scholar]
  53. Hunter JP. 53.  Key innovations and the ecology of macroevolution. Trends Ecol. Evol. 13:31–36 [Google Scholar]
  54. Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM. 54.  2007. Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLOS ONE 3:e296 [Google Scholar]
  55. Jabbour F, Damerval C, Nadot S. 55.  2008. Evolutionary trends in the flowers of Asteridae: Is polyandry an alternative to zygomorphy?. Ann. Bot. 102:153–65 [Google Scholar]
  56. Jablonski D, Roy K, Valentine JW. 56.  2006. Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314:102–6 [Google Scholar]
  57. Jansson R, Davies TJ. 57.  2008. Global variation in diversification rates of flowering plants: energy vs. climate change. Ecol. Lett. 11:173–83 [Google Scholar]
  58. Jansson R, Dynesius M. 58.  2002. The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annu. Rev. Ecol. Evol. Syst. 33:741–77 [Google Scholar]
  59. Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR. 59.  et al. 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biol 13:R3 [Google Scholar]
  60. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L. 60.  et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100 [Google Scholar]
  61. Käfer J, de Boer HJ, Mousset S, Kool A, Dufay M, Marais GAB. 61.  2014. Dioecy is associated with higher diversification rates in flowering plants. J. Evol. Biol. 27:1478–90 [Google Scholar]
  62. Kai MAC, Moore BR. 62.  2002. Whole-tree methods for detecting differential diversification rates. Syst. Biol. 51:855–65 [Google Scholar]
  63. Kay KM, Voelckel C, Yang JY, Hufford KM, Kaska DD, Hodges SA. 63.  2006. Floral characters and species diversification. Ecology and Evolution of Flowers LD Harder, SCH Barrett 311–25 Oxford: Oxford Univ. Press [Google Scholar]
  64. Kerkhoff AJ, Moriarty PE, Weiser MD. 64.  2014. The latitudinal species richness gradient in New World woody angiosperms is consistent with the tropical conservatism hypothesis. PNAS 111:8125–30 [Google Scholar]
  65. Kiester AR, Lande R, Schemske DW. 65.  1984. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124:220–43 [Google Scholar]
  66. Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC. 66.  2016. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol 210:1430–42 [Google Scholar]
  67. Larson-Johnson K.67.  2016. Phylogenetic investigation of the complex evolutionary history of dispersal mode and diversification rates across living and fossil Fagales. New Phytol 209:418–35 [Google Scholar]
  68. Levin DA.68.  1975. Minority cytotype exclusion in local plant populations. Taxon 24:35–43 [Google Scholar]
  69. Levin DA.69.  1983. Polyploidy and novelty in flowering plants. Am. Nat. 122:1–25 [Google Scholar]
  70. Lewis PO.70.  2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50:913–25 [Google Scholar]
  71. Li Z, Defoort J, Tasdighian S, Maere S, Van de Peer Y, De Smet R. 71.  2016. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28:326–44 [Google Scholar]
  72. Mace GM, Lande R. 72.  1991. Assessing extinction threats: toward a reevaluation of IUCN threatened species categories. Conserv. Biol. 5:148–57 [Google Scholar]
  73. Maddison W, FitzJohn R. 73.  2015. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64:127–36 [Google Scholar]
  74. Maddison WP, Midford PE, Otto SP. 74.  2007. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56:701–10 [Google Scholar]
  75. Magallón S, Castillo A. 75.  2009. Angiosperm diversification through time. Am. J. Bot. 96:349–65 [Google Scholar]
  76. Magallón S, Crane PR, Herendeen PS. 76.  1999. Phylogenetic pattern, diversity, and diversification of eudicots. Ann. Mo. Bot. Gard. 86:297–372 [Google Scholar]
  77. Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T. 77.  2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol 207:437–53 [Google Scholar]
  78. Magallón S, Sanderson MJ. 78.  2001. Absolute diversification rates in angiosperm clades. Evolution 55:1762–80 [Google Scholar]
  79. Magnuson-Ford K, Otto S. 79.  2012. Linking the investigations of character evolution and species diversification. Am. Nat. 180:225–45 [Google Scholar]
  80. May MR, Moore BR. 80.  2016. How well can we detect lineage-specific diversification-rate shifts? A simulation study of sequential AIC methods. Syst. Biol. 65:1076–84 [Google Scholar]
  81. Mayrose I, Barker MS, Otto SP. 81.  2010. Probabilistic models of chromosome number evolution and the inference of polyploidy. Syst. Biol. 59:132–44 [Google Scholar]
  82. Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS. 82.  et al. 2011. Recently formed polyploid plants diversify at lower rates. Science 333:1257 [Google Scholar]
  83. Merckx VSFT, Hendriks KP, Beentjes KK, Mennes CB, Becking LE. 83.  et al. 2015. Evolution of endemism on a young tropical mountain. Nature 524:347–50 [Google Scholar]
  84. Meudt HM, Rojas-Andrés BM, Prebble JM, Low E, Garnock-Jones PJ, Albach DC. 84.  2015. Is genome downsizing associated with diversification in polyploid lineages of Veronica?. Bot. J. Linn. Soc. 178:243–66 [Google Scholar]
  85. Meyers LA, Levin DA. 85.  2006. On the abundance of polyploids in flowering plants. Evolution 60:1198–206 [Google Scholar]
  86. Moore BR, Höhna S, May MR, Rannala B, Huelsenbeck JP. 86.  2016. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. PNAS 113:9569–74 [Google Scholar]
  87. Morlon H, Parsons TL, Plotkin JB. 87.  2011. Reconciling molecular phylogenies with the fossil record. PNAS 108:16327–32 [Google Scholar]
  88. Nee S, Holmes EC, May RM, Harvey PH. 88.  1994. Extinction rates can be estimated from molecular phylogenies. Philos. Trans. R. Soc. B 344:77–82 [Google Scholar]
  89. Nowell RW, Laue BE, Sharp PM, Green S. 89.  2016. Comparative genomics reveals genes significantly associated with woody hosts in the plant pathogen Pseudomonas syringae. Mol. Plant Pathol 17:1409–24 [Google Scholar]
  90. O'Meara B, Smith S, Armbruster W, Harder L, Hardy C. 90.  et al. 2016. Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity Proc. R. Soc. B 283:20152304 [Google Scholar]
  91. Ohno S.91.  1970. Evolution by Gene Duplication New York: Springer [Google Scholar]
  92. Ojeda DI, Valido A, Fernández de Castro AG, Ortega-Olivencia A, Fuertes-Aguilar J. 92.  et al. 2016. Pollinator shifts drive petal epidermal evolution on the Macaronesian Islands bird-flowered species. Biol. Lett. 12:20160022–24 [Google Scholar]
  93. Onstein RE, Jordan GJ, Sauquet H, Weston PH, Bouchenak-Khelladi Y. 93.  et al. 2016. Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Glob. Ecol. Biogeogr. 25:1239–51 [Google Scholar]
  94. Osborne CP, Freckleton RP. 94.  2009. Ecological selection pressures for C4 photosynthesis in the grasses. Proc. R. Soc. B 276:1753–60 [Google Scholar]
  95. Otto SP.95.  2007. The evolutionary consequences of polyploidy. Cell 131:452–62 [Google Scholar]
  96. Otto SP, Whitton J. 96.  2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34:401–37 [Google Scholar]
  97. Pagel M.97.  1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. B 255:37–45 [Google Scholar]
  98. Pagel M.98.  1997. Inferring evolutionary processes from phylogenies. Zool. Scr. 26:331–48 [Google Scholar]
  99. Pagel M.99.  1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48:612–22 [Google Scholar]
  100. Pagel M, Meade A. 100.  2006. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167:808–25 [Google Scholar]
  101. Pennington RT, Lavin M, Särkinen T, Lewis GP, Klitgaard BB, Hughes CE. 101.  2010. Contrasting plant diversification histories within the Andean biodiversity hotspot. PNAS 107:13783–87 [Google Scholar]
  102. Pimm SL, Raven PH. 102.  2017. The fate of the world's plants. Trends Ecol. Evol. 32:317–20 [Google Scholar]
  103. Rabosky DL.103.  2010. Extinction rates should not be estimated from molecular phylogenies. Evolution 64:1816–24 [Google Scholar]
  104. Rabosky DL.104.  2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLOS ONE 9:e89543 [Google Scholar]
  105. Rabosky DL, Donnellan SC, Grundler M, Lovette IJ. 105.  2014. Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Syst. Biol. 63:610–27 [Google Scholar]
  106. Rabosky DL, Goldberg EE. 106.  2015. Model inadequacy and mistaken inferences of trait-dependent speciation. Syst. Biol. 64:340–55 [Google Scholar]
  107. Rabosky DL, Lovette IJ. 107.  2008. Explosive evolutionary radiations: decreasing speciation or increasing extinction through time?. Evolution 62:1866–75 [Google Scholar]
  108. Rabosky DL, Mitchell JS, Chang J. 108.  2017. Is BAMM flawed? Theoretical and practical concerns in the analysis of multi-rate diversification models. Syst. Biol. 66:477–98 [Google Scholar]
  109. Ramsey J, Ramsey TS. 109.  2014. Ecological studies of polyploidy in the 100 years following its discovery. Philos. Trans. R. Soc. B 369:20130352 [Google Scholar]
  110. Ramsey J, Schemske DW. 110.  2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33:589–639 [Google Scholar]
  111. Rausch JH, Morgan MT. 111.  2005. The effect of self-fertilization, inbreeding depression, and population size on autopolyploid establishment. Evolution 59:1867–75 [Google Scholar]
  112. Ree RH.112.  2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59:257–65 [Google Scholar]
  113. Renner SS.113.  2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101:1588–96 [Google Scholar]
  114. Reyes E, Morlon H, Sauquet H. 114.  2015. Presence in Mediterranean hotspots and floral symmetry affect speciation and extinction rates in Proteaceae. New Phytol 207:401–10 [Google Scholar]
  115. Reyes E, Sauquet H, Nadot S. 115.  2016. Perianth symmetry changed at least 199 times in angiosperm evolution. Taxon 65:945–64 [Google Scholar]
  116. Ricklefs RE.116.  2007. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22:601–10 [Google Scholar]
  117. Robertson K, Goldberg EE, Igić B. 117.  2011. Comparative evidence for the correlated evolution of polyploidy and self-compatibility in Solanaceae. Evolution 65:139–55 [Google Scholar]
  118. Rolland J, Condamine FL, Jiguet F, Morlon H. 118.  2014. Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. PLOS Biol 12:e1001775 [Google Scholar]
  119. Sabath N, Goldberg EE, Glick L, Einhorn M, Ashman T-L. 119.  et al. 2016. Dioecy does not consistently accelerate or slow lineage diversification across multiple genera of angiosperms. New Phytol 209:1290–300 [Google Scholar]
  120. Sánchez-Reyes LL, Morlon H, Magallón S. 120.  2017. Uncovering higher-taxon diversification dynamics from clade age and species-richness data. Syst. Biol. 66:367–78 [Google Scholar]
  121. Sanderson MJ, Donoghue MJ. 121.  1994. Shifts in diversification rate with the origin of angiosperms. Science 264:1590–93 [Google Scholar]
  122. Sargent RD.122.  2004. Floral symmetry affects speciation rates in angiosperms. Proc. R. Soc. B 271:603–8 [Google Scholar]
  123. Sauquet H, von Balthazar M, Magallón S, Doyle J, Endress P. 123.  et al. 2017. The ancestral flower of angiosperms and its early diversification. Nature Commun 8:16047 [Google Scholar]
  124. Savolainen V, Anstett M-C, Lexer C, Hutton I, Clarkson JJ. 124.  et al. 2006. Sympatric speciation in palms on an oceanic island. Nature 441:210–13 [Google Scholar]
  125. Scarpino SV, Levin DA, Meyers LA. 125.  2014. Polyploid formation shapes flowering plant diversity. Am. Nat. 184:456–65 [Google Scholar]
  126. Schluter D, Price T, Mooers AO, Ludwig D. 126.  1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–711 [Google Scholar]
  127. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R. 127.  2004. Ferns diversified in the shadow of angiosperms. Nature 428:553–57 [Google Scholar]
  128. Schranz ME, Mohammadin S, Edger PP. 128.  2012. Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr. Opin. Plant Biol. 15:147–53 [Google Scholar]
  129. Schultz RJ.129.  1980. Role of polyploidy in the evolution of fishes. Polyploidy: Biological Relevance WH Lewis 313–40 New York: Plenum [Google Scholar]
  130. Segraves KA.130.  2017. The effects of genome duplications in a community context. New Phytol 215:57–69 [Google Scholar]
  131. Silvestro D, Cascales-Miñana B, Bacon CD, Antonelli A. 131.  2015. Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytol 207425–36 [Google Scholar]
  132. Slowinski JB, Guyer C. 132.  1989. Testing the stochasticity of patterns of organismal diversity: an improved null model. Am. Nat. 134:907–21 [Google Scholar]
  133. Slowinski JB, Guyer C. 133.  1993. Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction. Am. Nat. 142:1019–24 [Google Scholar]
  134. Smith SA, Beaulieu JM, Stamatakis A, Donoghue MJ. 134.  2011. Understanding angiosperm diversification using small and large phylogenetic trees. Am. J. Bot. 98:404–14 [Google Scholar]
  135. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH. 135.  et al. 2009. Polyploidy and angiosperm diversification. Am. J. Bot. 96:336–48 [Google Scholar]
  136. Soltis DE, Segovia-Salcedo MC, Jordon-Thaden I, Majure L, Miles NM. 136.  et al. 2014. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytol 202:1105–17 [Google Scholar]
  137. Stebbins GL Jr. 137.  1938. Cytological characteristics associated with the different growth habits in the dicotyledons. Am. J. Bot. 25:189 [Google Scholar]
  138. Stebbins GL Jr. 138.  1950. Variation and Evolution in Plants New York: Columbia Univ. Press [Google Scholar]
  139. Stebbins GL Jr. 139.  1971. Relationships between adaptive radiation, speciation and major evolutionary trends. Taxon 20:3–16 [Google Scholar]
  140. Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE. 140.  et al. 2015. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol 207:454–67 [Google Scholar]
  141. Thompson JN, Merg KF. 141.  2008. Evolution of polyploidy and the diversification of plant–pollinator interactions. Ecology 89:2197–206 [Google Scholar]
  142. Uribe-Convers S, Tank DC. 142.  2015. Shifts in diversification rates linked to biogeographic movement into new areas: an example of a recent radiation in the Andes. Am. J. Bot. 102:1854–69 [Google Scholar]
  143. Uyeda JC, Zenil-Ferguson R, Pennell MW. 143.  2017. Rethinking phylogenetic comparative methods. bioRxiv222729 https://doi.org/10.1101/222729 [Crossref] [Google Scholar]
  144. Vamosi JC, Dickinson TA. 144.  2006. Polyploidy and diversification: a phylogenetic investigation in Rosaceae. Int. J. Plant. Sci. 167:349–58 [Google Scholar]
  145. Vamosi JC, McEwen JR. 145.  2012. Origin, elevation, and evolutionary success of hybrids and polyploids in British Columbia, Canada. Botany 91:182–88 [Google Scholar]
  146. Vamosi JC, Vamosi SM. 146.  2010. Key innovations within a geographical context in flowering plants: towards resolving Darwin's abominable mystery. Ecol. Lett. 13:1270–79 [Google Scholar]
  147. Vamosi JC, Vamosi SM. 147.  2011. Factors influencing diversification in angiosperms: at the crossroads of intrinsic and extrinsic traits. Am. J. Bot. 98:460–71 [Google Scholar]
  148. Vamosi JC, Wilson JRU. 148.  2008. Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecol. Lett. 11:1047–53 [Google Scholar]
  149. Vamosi SM, Vamosi JC. 149.  2012. Causes and consequences of range size variation: the influence of traits, speciation, and extinction. Front. Biogeogr. 4:167–77 [Google Scholar]
  150. Vanneste K, Maere S, Van de Peer Y. 150.  2014. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos. Trans. R. Soc. B. 369:20130353 [Google Scholar]
  151. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T. 151.  et al. 2012. Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-Box gene and species diversification. Mol. Biol. Evol. 29:3793–806 [Google Scholar]
  152. Wagner WH Jr. 152.  1970. Biosystematics and evolutionary noise. Taxon 19:146–51 [Google Scholar]
  153. Wang W, Lin L, Xiang X-G, del C, Ortiz R, Liu Y. 153.  et al. 2016. The rise of angiosperm-dominated herbaceous floras: insights from Ranunculaceae. Sci. Rep. 6:27259 [Google Scholar]
  154. Weir JT, Schluter D. 154.  2007. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315:1574–76 [Google Scholar]
  155. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. 155.  2008. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. PNAS 105:17029–33 [Google Scholar]
  156. Wolfe JA, Upchurch GR. 156.  1986. Vegetation, climatic and floral changes at the Cretaceous–Tertiary boundary. Nature 324:148–52 [Google Scholar]
  157. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 157.  2009. The frequency of polyploid speciation in vascular plants. PNAS 106:13875–79 [Google Scholar]
  158. Xing Y, Gandolfo MA, Onstein RE, Cantrill DJ, Jacobs BF. 158.  et al. 2016. Testing the biases in the rich Cenozoic angiosperm macrofossil record. Int. J. Plant Sci. 177:371–88 [Google Scholar]
  159. Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA. 159.  et al. 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92 [Google Scholar]
  160. Zhan SH, Drori M, Goldberg EE, Otto SP, Mayrose I. 160.  2016. Phylogenetic evidence for cladogenetic polyploidization in land plants. Am. J. Bot. 1031252–58 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error