Large-scale patterns of diversification in the widespread legume genus senna and the evolutionary role of extrafloral nectaries

Evolution

Volumn 64, Issue 12, 2010, Pages 3570-3592

  Marazzi, Brigitte ^a   Sanderson, Michael J ^a  

^a University of Arizona   (United States)

Author keywords

Andes; Ant plant mutualism; Diversification rates; Key innovation; Leguminosae; Radiation

Indexed keywords

ANT; CLADISTICS; EOCENE; EVOLUTIONARY BIOLOGY; INNOVATION; LEGUME; MUTUALISM; NECTAR; OLIGOCENE; SPECIES RICHNESS; TAXONOMY;

ANIMAL; ANT; ARTICLE; CLASSIFICATION; ECOSYSTEM; EVOLUTION; GENETICS; HISTOLOGY; MOLECULAR EVOLUTION; NECTAR; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT GENOME; SENNA; SEQUENCE ALIGNMENT; SYMBIOSIS;

ANIMALS; ANTS; BIOLOGICAL EVOLUTION; ECOSYSTEM; EVOLUTION, MOLECULAR; GENOME, PLANT; PHYLOGENY; PLANT COMPONENTS, AERIAL; PLANT NECTAR; SENNA PLANT; SEQUENCE ALIGNMENT; SYMBIOSIS;

ANDES;

FABACEAE; FORMICIDAE; SENNA;

EID: 78650028282     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.01086.x     Document Type: Article

References (163)

1. Alfaro, M. E., F. Santini, C. D. Brock, H. Alamillo, A. Dornburg, G. Carnevale, D. Rabosky, and L. J. Harmon 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl. Acad. Sci. USA 106:13410-13414.
2. Baldwin, B. G., and M. J. Sanderson 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA 95:9402-9406.
3. Barton, A. M. 1986. Spatial variation in the effect of ants on an extrafloral nectary plant. Ecology 67:495-504.
4. Becerra, J. X., and D. L. Venable 1991. The role of ant-Homoptera mutualisms in the evolution of extrafloral nectaries. Oikos 60:105-106.
5. Bell, C. D., D. E. Soltis, and P. S. Soltis 2005. The age of angiosperms: a molecular timescale without a clock. Evolution 59:1245-1258.
6. Bello, M. A., A. Bruneau, F. Forest, and J. A. Hawkins 2009. Elusive relationships within the order Fabales: phylogenetic analyses using matK and rbcL sequence data. Syst. Bot. 34:102-114.
7. Blüthgen, N., M. Verhaagh, W. Goitia, K. Jaffe, W. Morawetz, and W. Barthlott 2000. How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125:229-240.
8. Bokma, F. 2008. Problems detecting density-dependent diversification on phylogenies. Proc. R. Soc. B 276:993-994.
9. Bond, J. E., and B. D. Opell 1998. Testing adaptive radiation and key innovation hypotheses in spiders. Evolution 52:403-414.
10. Brady, S. G., T. R. Schultz, B. L. Fisher, and P. S. Ward 2006. Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl. Acad. Sci. USA 103:18172-18177.
11. Bronstein, J. L., R. Alarcón, and M. Geber 2006. The evolution of plant-insect mutualisms. New Phytol. 172:412-428.
12. Bruneau, A., M. Mercure, G. P. Lewis, and P. S. Herendeen 2008. Phylogenetic patterns and diversification in the caesalpinioid legumes. Botany 86:697-718.
13. Buchmann, S. L. 1974. Buzz pollination of Cassia quiedondilla (Leguminosae) by bees of the genera Centris and Melipona. Bull. Southern Calif. Acad. Sci. 73:171-173.
14. Buckley, R. 1983. Interactions between ants and membracid bugs decreases growth and seed set of host plant bearing extrafloral nectaries. Oecologia 58:132-136.
15. Budd, G. E. 2006. On the origin and evolution of major morphological characters. Biol. Rev. 81:609-628.
16. Calvillo Canadell, L., and S. R. S. Cevallos-Ferriz 2005. Diverse assemblage of Eocene and Oligocene Leguminosae from Mexico. Int. J. Plant. Sci. 166:671-692.
17. Caspary, R. 1848. De nectariis. Adolphum Marcum, Bonn, Germany [Abstract in Bot. Zeitung 6:628-630 and extensive summaries in Behrens (1879, pp. 19-22) and Nieuwenhuis-von Uxkiull-Giildenbandt (1907, pp. 203-206).
18. Classen-Bockhoff, R., T. Speck, E. Tweraser, P. Wester, S. Thimm, and M. Reith 2004. The staminal lever mechanism in Salvia: a key innovation for adaptive radiation? Org. Div. Evol. 4:189-205.
19. Coddington, J. A. 1994. The roles of homology and convergence in studies of adaptation. Pp. 53-78 in P. Eggleton and R. I. Vane-Wright, eds. Phylogenetics and ecology. The Linnean Society of London, London, UK .
20. Colladon, L. T. F. 1816. Histoire naturelle et médicale des Casses, et particulièrement de la Casse et des Sénés employés en médecine. Jean Martel, Montpellier, France .
21. Cox, D. R., and H. D. Miller 1977. The theory of stochastic processes. Chapman & Hall, London, UK .
22. Crayn, D. M., E. S. Fernando, P. A. Gadeck, and C. J. Quinn 1995. A reassessment of the familial affinity of the Mexican genus Recchia Mocino & Sessé ex DC. Brittonia 47:397-402.
23. Crepet, W. L., and K. J. Nicklas 2009. Dawin's second "abominable mystery": why are there so many angiosperm species? Am. J. Bot. 96:366-381.
24. Darwin, J. H. 1956. The behaviour of an estimator for a simple birth and death process. Biometrika 43:23-31.
25. Davidson, D. W., S. C. Cook, R. R. Snelling, and T. H. Chua 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969-972.
26. Delgado Salinas, A. O., and M. Sousa Sánchez 1977. Biología floral del genero Cassia en la región de Los Tuxtlas, Veracruz. Bol. Soc. Bot. Mex. 37:5-52.
27. Díaz-Castelazo, C., V. Rico-Gray, F. Ortega, and G. Angeles 2005. Morphological and secretory characterization of extrafloral nectaries in plants of coastal Veracruz, Mexico. Ann. Bot. 96:1175-1189.
28. Donoghue, M. J. 2005. Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny. Paleobiology 31:77-93.
29. Doyle, J. A., and M. J. Donoghue 1993. Phylogenies and angiosperm diversification. Paleobiology 19:141-167.
30. Drummond, A. J., and A. Rambaut 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214-221.
31. Drummond, A. J., S. Y. W. Ho, M. J. Phillips, and A. Rambaut 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
32. Du Puy, D. J. 1995. New combinations in Senna Miller and Chamaecrista Moench (Leguminosae: Caesalpinioideae) from Madagascar. Kew Bull. 50:581-584.
33. Fernandes, A., and P. Bezerra 1984. Uma nova especie de Fabaceae do genero Senna Mill. Bradea 4:49-51.
34. Farrell, B. D., D. E. Dussourd, and C. Mitter 1991. Escalation of plant defense: do latex and resin canals spur plant diversification. Am. Nat. 138:881-900.
35. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
36. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
37. Fleet, R. R., and B. L. Young 2000. Facultative mutualism between imported fire ants (Solenopsis invicta) and a legume (Senna occidentalis). Southwestern Nat. 45:289-298.
38. Friis, E. M., K. R. Pedersen, and P. R. Crane 2006. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeog. Palaeoclim. Palaeoecol. 232:251-293.
39. Fuks, R. 1983. O genero Quillaja Molina (Rosaceae) no Brasil. Arq. Jard. Bot. Rio de Janeiro 26:61-67.
40. Garzione, C. N., G. D. Hoke, J. C. Libarkin, S. Withers, B. MacFadden, J. Eiler, P. Ghosh, and A. Mulch 2008. Rise of the Andes. Science 320:1304-1307.
41. Gianoli, E. 2004. Evolution of a climbing habit promotes diversification in flowering plants. Proc. R. Soc. Lond. B 266:817-824.
42. Govaerts, R. 2003. How many species of seed plants are there?: a response. Taxon 52:583-584.
43. Gottsberger, G., and I. Silberbauer-Gottsberger 1988. Evolution of flower structures and pollination in Neotropical Cassiinae (Caesalpiniaceae) species. Phyton (Horn) 28:293-320.
44. Heil, M., and D. McKey 2003. Protective ant-plant interactions as a model system in ecological and evolutionary research. Annu. Rev. Ecol. Evol. Syst. 34:425-453.
45. Hennig, W. 1966. Phylogenetic systematics. Univ. of Illinois Press, Urbana, IL .
46. Herendeen, P. S. 1992. The fossil history of the Leguminosae from the Eocene of southeastern North America. Pp. 85-160 in P. S. Herendeen and D. L. Dilchner, eds. Advances in legume systematics, part 4, the fossil record. Royal Botanic Gardens, Kew, UK .
47. Hodges, S. A. 1997. Floral nectar spurs and diversification. Int. J. Plant. Sci. 158(Suppl.):S81-S88.
48. Hodges, S. A., and M. L. Arnold 1994. Colombines: a geographically widespread species flock. Proc. Natl. Acad. Sci. USA 91:5129-5132.
49. Hodges, S. A., and M. L. Arnold 1995. Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R. Soc. Lond. B 262:343-348.
50. Huelsenbeck, J. P., and K. A. Crandall 1997. Phylogeny estimation and hypothesis testing using maximum likelihood. Ann. Rev. Ecol. Syst. 28:437-466.
51. Huelsenbeck, J. P., and B. Rannala 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227-232.
52. Hughes, C., and R. Eastwood 2006. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc. Natl. Acad. Sci. USA 103:10334-10339.
53. Hunter, J. P. 1998. Key innovations and the ecology of macroevolution. Trends Ecol. Evol. 13:31-36.
54. Irwin, H. S., and B. L. Turner 1960. Chromosomal relationships and taxonomic considerations in the genus Cassia. Am. J. Bot. 47:309-318.
55. Irwin, H. S., and R. C. Barneby 1981. Tribe 2. Cassieae Bronn (1981). Pp. 97-106 in R. M. Pohlhill and P. H. Raven, eds. Advances in legume systematics, part 1. Royal Botanic Gardens, Kew, UK .
56. Irwin, H. S., and R. C. Barneby 1982. The American Cassiinae. Mem. New York Bot. Gard. 35:1-918.
57. Irwin, H. S., and R. C. Barneby 1985 A new species of Senna (Caesalpiniaceae) from coastal northern Bahia, Brazil. Brittonia 37:192-194.
58. Janzen, D. H. 1967. Interaction of the bull's horn acacia (Acacia cornigera L.) with an ant inhabitant (Pseudomyrmex ferruginea F. Smith) in eastern Mexico. Kansas Univ. Sci. Bull. 47:315-558.
59. Kelly, C. A. 1986. Extrafloral nectaries: ants, herbivores and fecundity in Cassia fasciculata. Oecologia 69:600-605.
60. Kendall, D. G. 1949. Stochastic processes and population growth. J. R. Stat. Soc. B 11:230-264.
61. Koptur, S. 1979. Facultative mutualism between weedy vetches bearing extrafloral nectaries and weedy ants in California. Am. J. Bot. 66:1016-1020.
62. Koptur, S. 1984. Experimental evidence for the defense of Inga (Fabaceae, Mimosoideae) saplings by ants. Ecology 66:1787-1793.
63. Koptur, S. 1992. Extrafloral nectary-mediated interactions between insects and plants. Pp. 81-129 in E. Bernays, ed. Insect-plant interactions, volume IV. CRC Press, London, UK .
64. Koptur, S. 1994. Floral and extrafloral nectars of Costa-Rican Inga trees-a comparison of their constituents and composition. Biotropica 26:276-284.
65. Koptur, S. 2004. Visitors to extrafloral nectaries of Senna mexicana var. chapmanii in south Florida. Botany 2004: Annual Meeting of The Botanical Society of America, Snowbird, Utah, USA. [Online abstract nr. 710, .
66. Koptur, S., V. Rico Gray, and M. Palacios Rios 1998. Ant protection of the nectaried fern Polypodium plebeium in central Mexico. Am. J. Bot. 85:317-321.
67. Kubo, J., and Y. Isawa 1995. Inferring the rates of branching and extinction from molecular phylogenies. Evolution 49:694-704.
68. Larsen, K. 1993. Note on the nomenclature of Cassieae (Leguminosae: Caesalpinioideae) in Malaysia. Nordic J. Bot. 13:403-404.
69. Larsen, K., S. S. Larsen, and J. E. Vidal 1984. Leguminosae-Caesalpinioideae. Flora of Thailand vol. 4, part 1. Applied Scientific Research, Bangkok, Thailand .
70. Lavin, M., S. P. Herendeen, and M. F. Wojciechowski 2005. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst. Biol. 54:575-594.
71. Lengyel, S., A. D. Gove, A. M. Latimer, J. D. Majer, and R. R. Dunn 2009. Ants sow the seeds of global diversification in flowering plants. PLoS ONE 4:e5480.
72. Lersten, N. R., and H. T. Horner 2005. Macropattern of styloid and druse crystals in Quillaja (Quillajaceae) bark and leaves. Int. J. Plant Sci. 166:705-711.
73. Lewis, G., B. Schrire, B. Mackinder, and M. Lock 2005. The legumes of the world. Royal Botanic Gardens, Kew, UK .
74. Liem, K. F. 1990. Key evolutionary innovations, differential diversity, and symecomorphosis. Pp. 147-170 in M. Nitecki, ed. Evolutionary innovations. Univ. of Chicago Press, Chicago, USA .
75. Linder, H. P. 2008. Plant species radiations: where, when, why? Phil. Trans. R. Soc. B 363:3097-3105.
76. Linder, H. P., and C. R. Hardy 2004. Evolution of the species-rich Cape flora. Phil. Trans. R. Soc. Lond. B 359:1623-1632.
77. Linder, H. P., C. R. Hardy, and F. Rutschmann 2005. Taxon sampling effects in molecular clock dating: an example from the African Restionaceae. Mol. Phylogenet. Evol. 35:569-582.
78. Lock, J. M. 1988. Cassia sens.lat. (Leguminosae-Caesalpinioideae) in Africa. Kew Bull. 43:333-342.
79. Luckow, M. 1996. The cultivated species of Cassia, Senna, and Chamaecrista (Leguminosae). Baileya. 23:195-241.
80. Magallón, S., and A. Castillo 2009. Angiosperm diversification through time. Am. J. Bot. 96:349-365.
81. Magallón, S., and M. J. Sanderson 2001. Absolute diversification rates in angiosperms. Evolution 55:1762-1780.
82. Magallón, S., and M. J. Sanderson 2005. Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59:1653-1670.
83. Magallón, S., and M. J. Sanderson 2006. Absolute diversification rates in angiosperms ERRATUM. Evolution 60:2411.
84. Marazzi, B., P. K. Endress, L. Paganucci de Queiroz, and E. Conti 2006a. Phylogenetic relationships within Senna (Leguminosae, Cassiinae) based on three chloroplast regions: patterns in the evolution of floral symmetry and extrafloral nectaries. Am. J. Bot. 93:288-303.
85. Marazzi, B., R. Fortunato, P. K. Endress, and R. Spichiger 2006b. Senna (Cassiinae, Leguminosae) in Paraguay: synopsis, conservation, ecologic role and ethnobotany. Candollea 61:315-329.
86. Marazzi, B., E. Conti, and P. K. Endress 2007. Diversity of anthers and stigmas in the buzz-pollinated genus Senna (Leguminosae, Cassiinae). Int. J. Plant Sci. 168:371-391.
87. Marazzi, B., and P. K. Endress 2008. Patterns and development of floral asymmetry in Senna (Leguminosae, Cassiinae). Am. J. Bot. 95:22-40.
88. Mayhew, P. J. 2007. Why are there so many insect species? Perspectives from fossils and phylogenies. Biol. Rev. Camb. Philos. Soc. 82:425-454.
89. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York, USA .
90. McConway, K. J., and H. J. Sims 2004. A Likelihood-based method for testing for non-stochastic variation of diversification rates in phylogenies. Evolution 58:12-23.
91. McKey, D. 1989. Interactions between ants and leguminous plants. Pp. 673-718 in C. H. Stirton, J. L. Zarucchi, eds. Advances in legume biology. Monogr. Syst. Bot. Mo. Bot. Gard. 29.
92. Moore, B. R., and M. J. Donoghue 2009. A Bayesian approach for evaluating the impact of historical events on rates of diversification. Proc. Natl. Acad. Sci. USA 106:4307-4312.
93. Moreau, C. S., C. D. Bell, R. Vila, S. B. Archibald, and N. E. Pierce 2006. Phylogeny of the ants: diversification in the age of the angiosperms. Science 312:101-104.
94. Müller, F. 1883. Two kinds of stamens with different functions in the same flower, Nature 27:364-365.
95. Nee, M., and R. C. Barneby 1993. A new species of Senna ser. Bacillares (Caesalpiniaceae, Cassiinae) from Bolivia. Brittonia 45:159-161.
96. Nee, S. 2001. Inferring speciation rates from phylogenies. Evolution 55:661-668.
97. Nee, S. 2006. Birth-death models in macroevolution. Annu. Rev. Ecol. Evol. Syst. 37:1-17.
98. Nee, S., A. O. Mooers, and P. H. Harvey 1992. The tempo and mode of evolution revealed from molecular phylogenies. Proc. Natl. Acad. Sci. USA 89:8322-8326.
99. Nee, S., E. C. Holmes, R. M. May, and P. H. Harvey 1994a. Extinction rates can be estimated from molecular phylogenies. Philos. Trans. R. Soc. Lond. B 344:77-82.
100. Nee, S., R. M. May, and P. H. Harvey 1994b. The reconstructed evolutionary process. Philos. Trans. R. Soc. Lond. B 344:305-311.
101. Nee, S., T. G. Barraclough, and P. H. Harvey 1996. Temporal changes in biodiversity: detecting patterns and identifying causes. Pp. 230-252 in K. Gaston, ed. Biodiversity. Oxford Univ. Press, Oxford .
102. Nitecki, M. H. 1990. Evolutionary innovations. Univ. of Chicago Press, Chicago .
103. Oliveira, P. S. 1997. The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct. Ecol. 11:323-330.
104. Oliveira Silva Cardoso, D. B., and L. Paganucci de Queiroz 2008. A new species of Senna (Leguminosae, Caesalpinioideae) from Eastern Brazil. Novon 18:140-143.
105. Persson, C. 2001. Phylogenetic relationships in Polygalaceae based on plastid DNA sequences from the trnL-F region. Taxon 50:763-779.
106. Pie, M. R., and M. K. Tschá 2009. The macroevolutionary dynamics of ant diversification. Evolution 63:3023-3030.
107. Posada, D., and K. A. Crandall 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
108. Pybus, O. G., and P. H. Harvey 2000. Testing macro-evolutionary models using incomplete molecular phylogenies. Proc. R. Soc. Lond. B 267:2267-2272.
109. Rabosky, D. L. 2006a. LASER: a maximum likelihood toolkit for inferring temporal shifts in diversification rates. Evol. Bioinform. Online 2:257-260.
110. Rabosky, D. L. 2006b. Likelihood methods for detecting temporal shifts in diversification rates. Evolution 60:1152-1164.
111. Rabosky, D. L. 2009. Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecol. Lett. 12:735-743.
112. Rabosky, D. L., S. C. Donnellan, A. L. Talaba, and I. J. Lovette 2007. Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade. Proc. R. Soc. Lond. B 274:2915-2923.
113. Rabosky, D. L., and I. J. Lovette 2008. Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution 62:1866-1875.
114. Randell, B. R. 1988. Revision of the Cassiinae in Australia. 1. Senna Miller sect. Chamaefistula (Colladon) Irwin and Barneby. J. Adelaide Bot. Gard 11:19-49.
115. Randell, B. R. 1989. Revision of the Cassiinae in Australia. 2. Senna Miller sect. Psilorhegma (J. Vogel) Irwin and Barneby. J. Adelaide Bot. Gard 12:165-272.
116. Randell, B. R. 1990. Revision of the Cassiinae in Australia. 3. Senna Miller sect. Senna. J. Adelaide Bot. Gard. 13:1-16.
117. Randell, B. R., and B. A. Barlow 1998. Senna. Flora of Australia 12:89-138.
118. Ree, R. H. 2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59:257-265.
119. Richardson, J. E., R. T. Pennington, T. D. Pennington, and P. M. Hollingsworth 2001. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293:2242-2245.
120. Ricklefs, R. E. 2007. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22:601-610.
121. Rudgers, J. A. 2004. Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85:192-205.
122. Rutter, M. T., and M. D. Rausher 2004. Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait. Evolution 58:2657-2668.
123. Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19:101-109.
124. Sanderson, M. J. 2003. r8s; inferring absolute rates of evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301-302.
125. Sanderson, M. J., and G. Barathan 1993. Does cladistic information affect inferences about branching rates? Syst. Biol. 42:1-17.
126. Sanderson, M. J., and M. J. Donoghue 1994. Shifts in diversification rate with the origin of angiosperms. Science 264:1590-1593.
127. Sanderson, M. J., and M. J. Donoghue 1996. Reconstructing shifts in diversification on phylogenetic trees. Trends Ecol. Evol. 11:15-20.
128. Sanderson, M. J., and L. Hufford 1996. Homoplasy: the recurrence of similarity in evolution. Academic Press, New York .
129. Sanderson, M. J., and M. S. Wojciechowski 1996. Diversification rates in a temperate legume clade: are there "so many species" of Astragalus? Am. J. Bot. 83:1488-1502.
130. Sauquet, H., P. H. Weston, C. L. Anderson, N. P. Barker, D. J. Cantrill, A. R. Mast, and V. Savolainen 2009. Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proc. Natl. Acad. Sci. USA 106:221-225.
131. Sargent, R. D. 2004. Floral symmetry affects speciation rates in angiosperms. Proc. R. Soc. Lond. B 271:603-608.
132. Scherson, R. A., R. Vidal, and M. J. Sanderson 2008. Phylogeny, biogeography, and rates of diversification of New World Astragalus (Leguminosae) with an emphasis on South American radiations. Am. J. Bot. 95:1030-1039.
133. Schupp, E. W., and D. H. Feener 1991. Phylogeny, life form, and habitat dependence of ant-defended plants in a Panamanian forest. Pp. 175-197 in C. R. Huxley and D. F. Cutler, eds. Ant-plant interactions. Oxford Univ. Press, Oxford .
134. Scotland, R. W., and M. J. Sanderson 2004. The significance of few versus many in the Tree of Life. Science 303:643.
135. Scotland, R. W., and A. H. Wortley 2003. How many species of seed plants are there? Taxon 52:101-104.
136. Simon, M. 2008. Systematics and evolution of Mimosa L. (Leguminosae) and the assembly of a Neotropical plant diversity hotspot. PhD dissertation. Univ. of Oxford, Oxford, UK .
137. Simpson, G. G. 1953. The major features of evolution. Columbia Univ. Press, New York .
138. Sims, H. J., and K. J., McConway 2003. Non-stochastic variation of species-level diversification rates within angiosperms. Evolution 57:460-479.
139. Sing, V. 2001. Monograph on Indian subtribe Cassiinae (Caesalpiniaceae). Scientific Editions, Jodhpur, India .
140. Slowinski, J. B., and C. Guyer 1989. Testing the stochasticity of patterns of organismal diversity: an improved null model. Am. Nat. 134:907-921.
141. Slowinski, J. B., and C. Guyer 1993. Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction. Am. Nat. 142:1019-1024.
142. Smith, J. F. 2001. High species diversity in fleshy-fruited tropical understory plants. Am. Nat. 157:646-653.
143. Stanley, S. M. 1979. Macroevolution. W. H. Freeman, San Francisco, CA .
144. Stephenson, A. G. 1982. The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63:663-669.
145. Strathmann, R. R., and M. Slatkin 1983. The improbability of animal phyla with few species. Paleobiology 9:97-106.
146. Swofford, D. L. 2002. PAUP*: phylogenetic analyses using parsimony (*and other methods). Sinauer, Sunderland, MA, USA .
147. Swofford, D. L., G. J. Olsen, P. J. Waddell, and D. M. Hillis 1996. Phylogenetic inference. Pp. 407-514 in D. M. Hillis, C. Moritz, and B. K. Mable, eds. Molecular systematics. 2nd ed. Sinauer Associates, Sunderland, MA, USA .
148. Tamura, K., J. Dudley, M. Nei, and S. Kumar 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
149. The International Plant Names Index. 2009. Available at: [accessed April-May 2009.
150. Thompson, J. D., D. G. Higgins, and T. J. Gibson 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
151. Venkatesh, C. S. 1957. The form, structure and special ways of dehiscence in anthers of Cassia. III. Subgenus Senna. Phytomorphology 7:253-273.
152. W3Tropicos. 2009. Tropicos.org. Missouri Botanical Garden <> [accessed April-May 2009.
153. Walker, J. B., K. J. Sytsma, J. Treutlein, and M. Wink 2004. Salvia (Lamiaceae) is not monophyletic: implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. Am. J. Bot. 91:1115-1125.
154. Wagner, A. 2008. Gene duplications, robustness and evolutionary innovations. BioEssays 30:367-373.
155. Wagner, D., and A. Kay 2002. Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evol. Ecol. Res. 4:293-305.
156. Wang, H., M. J. Moore, P. S. Soltis, C. D. Bell, S. F. Brockington, R. Alexandre, C. C. Davis, M. Latvis, S. R. Manchester, and D. E. Soltis 2009. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc. Natl. Acad. Sci. USA 106:3853-3858.
157. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford Univ. Press, New York .
158. West-Eberhard, M. J. 2005. Developmental plasticity and the origin of species differences. Proc. Natl. Acad. Sci. USA 102(Suppl. 1):6543-6549.
159. Westerkamp, C. 2004. Ricochet pollination in cassias-and how bees explain enantiostyly: preliminary communication. Pp. 225-230 in B. M. Freitas and J. O. P. Pereira, eds. Solitary bees: conservation, rearing and management for pollination. Imprensa Universitária, Fortaleza, Brazil .
160. Winkler, D. W. 2000. The Phylogenetic approach to avian life histories: an important complement to within population studies. Condor 102:52-59.
161. Wojciechowski, M. S. 2005. Astragalus (Fabaceae): a molecular phylogenetic perspective. Brittonia 57:382-396.
162. Wojciechowski, M. S., M. Lavin, and M. J. Sanderson 2004. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am. J. Bot. 91:1846-1862.
163. Yule, G. U. 1924. A mathematical theory of evolution, based on the conclusions of Dr. J.C. Willis, F.R.S. Phil. Trans. R. Soc. Lond. B 213:21-87.