Unravelling Species Relationships and Diversification within the Iconic California Floristic Province Sages (Salvia Subgenus Audibertia, Lamiaceae)

Systematic Botany

Volumn 40, Issue 3, 2015, Pages 826-844

  Walker, Jay B ^a,b   Drew, Bryan T ^a,c   Sytsma, Kenneth J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Union Public Schools   (United States)

^c UNIVERSITY OF NEBRASKA AT KEARNEY   (United States)

Author keywords

BAMM; BioGeoBEARS; biogeography; Calosphace; chloroplast capture; Echinosphace; hybridization; staminal evolution

Indexed keywords

EID: 84942878617     PISSN: 03636445     EISSN: 15482324     Source Type: Journal    
DOI: 10.1600/036364415X689285     Document Type: Article

References (109)

1. Ackerly, D. D. 2009. Evolution, origin and age of lineages in the Californian and Mediterranean floras. Journal of Biogeography 36: 1221-1233.
2. Anderson, E. and B. R. Anderson. 1954. Introgression of Salvia apiana and S. mellifera. Annals of the Missouri Botanical Garden 41: 329-338.
3. Axelrod, D. I. 1958. Evolution of the Madro-Tertiary Geoflora. Botanical Review 24: 433-509.
4. Axelrod, D. I. 1973. History of the Mediterranean ecosystem in California. Pp. 225-277 in Mediterranean ecosystems: Origin and structure, eds. F. di Castri and H. A. Mooney. Springer: New York.
5. Axelrod, D. I. 1975. Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Annals of the Missouri Botanical Garden 62: 280-334.
6. Axelrod, D. I. 1977. Outline history of California vegetation. Pp. 139-193 in Terrestrial vegetation of California, eds. M. G. Barbour and J. Major. Wiley: New York.
7. Axelrod, D. I. 1989. Age and origin of chaparral. Pages 7-19 in The California chaparral: Paradigms re-examined, ed. Keeley, S. C.. Science Series no. 34. Los Angeles: Natural History Museum of Los Angeles County.
8. Baikova, E. V. 1998. Floral morphology of some Salvia species as a reflection of its adaptation to pollinators and as a basis for a generic system. Biulleten Moskovskogo Obshchestva Ispytatelei Prirody. Otdel Biologicheskii [Bulletin of Moscow Society of Naturalists: Department of Biology] 103: 52-58.
9. Barnett, J. 1989. Palynology and paleoecology of the Tertiary Weaverville formation, Northwestern California, USA. Palynology 13: 195-246.
10. Bentham, G. 1833. Salvia. Pp. 260-698 in Labiatarum genera et species. London: Ridgeway.
11. Bentham, G. 1876. Verbenaceae and Labiatae. Pp. 1160-1196 in Genera plantarum Vol. 2, eds. G. Bentham and J. D. Hooker. London: Reeve.
12. Bräuchler, C., H. Meimberg, and G. Heubl. 2010. Molecular phylogeny of Menthinae (Lamiaceae, Nepetoideae, Mentheae) -taxonomy, biogeography and conflicts. Molecular Phylogenetics and Evolution 55: 501-523.
13. Briquet, J. 1897. Labiatae. Pp. 183-287 in Die natürlichen pflanzenfamilien Vol. 4/3a, eds. Prantl, K.A. Engler. Leipzig: W. Englemann.
14. Burge, D. O., D. M. Erwin, M. B. Islam, J. Kellermann, S. W. Kembel, D. H. Wilken, and P. S. Manos. 2011. Diversification of Ceanothus (Rhamnaceae) in the California Floristic Province. International Journal of Plant Sciences 172: 1137-1164.
15. Cain, J. W., B. D. Jansen, R. S. Felger, and P. R. Krausman. 2010. Scallopleaf sage (Salvia vaseyi, Lamiaceae) discovered in Arizona. Journal of the Botanical Research Institute of Texas 4: 755-760.
16. Claßen-Bockhoff, R., P. Wester, and E. Tweraser. 2003. The staminal lever arm mechanism in Salvia - a review. Plant Biology 5: 33-41.
17. Claßen-Bockhoff, R., M. Crone, and E. Baikova. 2004a. Stamen development in Salvia: Homology reinvestigated. International Journal of Plant Sciences 165: 475-498.
18. Claßen-Bockhoff, R., T. Speck, E. Tweraser, P. Wester, S. Thimm, and M. Reith. 2004b. The staminal lever mechanism in Salvia: A key innovation for adaptive radiation? Organisms, Diversity & Evolution 4: 189-205.
19. Clebsch, B. 1997. A book of salvias. Sages for every garden. Portland, Oregon: Timber Press.
20. Drew, B. T. 2011. Phylogenetics and biogeography of Lepechinia (Lamiaceae), and evolutionary studies within the Mentheae tribe. Ph. D. thesis. Madison: University of Wisconsin.
21. Drew, B. T. and K. J. Sytsma. 2011. Testing the monophyly and placement of Lepechinia in the tribe Mentheae (Lamiaceae). Systematic Botany 36: 1038-1049.
22. Drew, B. T. and K. J. Sytsma. 2012. Phylogenetics, biogeography, and staminal evolution in the tribe Mentheae (Lamiaceae). American Journal of Botany 99: 933-953.
23. Drew, B. T. and K. J. Sytsma. 2013. Phylogenetics, biogeography, and evolution of dioecy in South American Lepechinia (Lamiaceae). Botanical Journal of the Linnean Society 171: 171-190.
24. Emboden, W. A. 1964. Pollen morphology of the genus Salvia section Audibertia. Pollen & Spores 6: 527-536.
25. Emboden, W. A. 1969. Detection of palynological introgression in Salvia. Contributions in Science. Los Angeles County Museum of Natural History 156: 1-10.
26. Emboden, W. A. 1971. The role of introgressive hybridization in the development of Salvia sect. Audibertia. Contributions in Science. Los Angeles County Museum of Natural History 208: 1-15.
27. Emboden, W. A. and H. Lewis. 1967. Terpenes as taxonomic characters in Salvia section Audibertia. Brittonia 19: 152-160.
28. Epling, C. 1938. The Californian salvias: A review of Salvia, section Audibertia. Annals of the Missouri Botanical Garden 25: 95-188.
29. Epling, C. 1939. A revision of Salvia, subgenus Calosphace. Beihefte Feddes Repertorium Specierum Novarum Regni Vegetabilis 110: 1-383.
30. Epling, C. 1940. Supplementary notes on Salvia: Audibertia. Annals of the Missouri Botanical Garden 27: 259-263.
31. Epling, C. 1944. The living mosaic. Los Angeles: University of California Press.
32. Epling, C. 1947. Natural hybridization of Salvia apiana and S. mellifera. Evolution 1: 69-78.
33. Epling, C., H. Lewis, and P. Raven. 1962. Chromosomes of Salvia: Section Audibertia. Aliso 5: 217-221.
34. Faegri, K. and L. Van Der Pijl. 1979. The principles of pollination ecology. Oxford: Pergamon Press.
35. Farris, J. S., M. Källersjö, A. G. Kluge, and C. Bult. 1995. Testing significance and congruence. Cladistics 10: 315-319.
36. Felger, R .S. 2000. Flora of the Gran Desierto and Río Colorado of Northwestern Mexico. Tucson: University of Arizona Press.
37. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
38. Graham, A. 1999. Late Cretaceous and Cenozoic history of North American vegetation, north of Mexico. Oxford: Oxford University Press.
39. Grant, V. 1981. Plant speciation, 2nd ed. New York: Columbia University Press.
40. Grant, V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proceedings of the National Academy of Sciences USA 91: 3-10.
41. Grant, K. A. and V. Grant. 1964. Mechanical isolation of Salvia apiana and Salvia mellifera. Evolution 18: 196-212.
42. Greene, E. 1892. On certain California Labiatae. Pittonia 2: 233v236.
43. Hashemi, A., A. Estilai, and J. Carapetian. 1993. Characterization of isozymes in Salvia columbariae. Euphytica 67: 101-104.
44. Hedge, I. C. 1982. Labiatae. Pp. 403-476 in Flora Iranica, ed. C. H. Rechinger. Graz, Austria: Akademische Drukund Verlagsanstalt.
45. Himmelbaur, W. and E. Stibal. 1933-1935. Entwicklungsrichtungen in der Blutenregion der Gattung Salvia. I-III. Biologia Generalis 8: 449-474
46. 9: 129-150
47. 10: 17-48.
48. J. C. Hickman (ed.). 1993. The Jepson manual: Vascular plants of California. Berkeley, California: University of California Press.
49. Hipp, A. L., J. C. Hall, and K. J. Sytsma. 2004. Congruence versus phylogenetic accuracy: Revisiting the incongruence length difference test. Systematic Biology 53: 81-89.
50. Hodges, S. A. and M. L. Arnold. 1994. Columbines: A geographically widespread species flock. Proceedings of the National Academy of Sciences USA 91: 5129-5132.
51. Huck, R. B. 1992. Overview of pollination biology in the Lamiaceae. Pp. 167-181 in Advances in Labiatae science, eds. Harley, R. M. and T. Reynolds. Kew: Royal Botanic Garden.
52. Huelsenbeck, J. P. and F. R. Ronquist. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
53. Jenks, A. A., J. B. Walker, and S.-C. Kim. 2012. Phylogeny of New World Salvia subgenus Calosphace (Lamiaceae) based on cpDNA (psbAtrnH) and nrDNA (ITS) sequence data. Journal of Plant Research 126: 483-496.
54. Jepson Flora Project (eds.). 2014. Jepson eFlora, http://ucjeps.berkeley.edu/IJM.html [accessed on October 23, 2014].
55. Jepson, W. L. 1925. A manual of the flowering plants of California. Berkeley, California: University of California Press.
56. Johnson, L. A. and D. E. Soltis. 1994. matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Systematic Botany 19: 143-156.
57. Kraft, N. J. B., B. G. Baldwin, and D. D. Ackerly. 2010. Range size, taxon age and hotspots of neoendemism in the California flora. Diversity & Distributions 16: 403-413.
58. Lancaster, L. T. and K. M. Kay. 2013. Origin and diversification of the California flora: Re-examining classic hypotheses with molecular phylogenies. Evolution 67: 1041-1054.
59. Maddison, D. R. and W. P. Maddison. 2005. MacClade 4: Analysis of phylogeny and character evolution, v. 4.08a. http://macclade.org.
60. Matzke, N. J. 2013. Probabilistic historical biogeography: New models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers of Biogeography 4: 242-247.
61. Matzke, N. J. 2014. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63: 951-970.
62. Meyn, O. and W. A. Emboden. 1987. Parameters and consequences of introgression in Salvia apiana X S. mellifera (Lamiaceae). Systematic Botany 12: 390-399.
63. Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. Pp. 1-8 in Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, Louisiana: Gateway Computing.
64. Mivart, S. G. 1871. On the genesis of species. London: MacMillan and Co.
65. Mix, H. T., A. Mulch, M. L. Kent-Corson, and C. P. Chamberlain. 2011. Cenozoic migration of topography in the North American Cordillera. Geology 39: 87-90.
66. Mulch, A., A. M. Sarna-Wojcicki, M. E. Perkins, and C. P. Chamberlain. 2008. A Miocene to Pleistocene climate and elevation record of the Sierra Nevada (California). Proceedings of the California Academy of Sciences 105: 6819-6824.
67. Muller, C. H. 1965. Inhibitory terpenes volatized from Salvia shrubs. Bulletin of the Torrey Botanical Club 92: 38-45.
68. Muller, C. H. 1966. The role of chemical inhibition (allelopathy) in vegetational composition. Bulletin of the Torrey Botanical Club 93: 332-351.
69. Muller, C. H. and R. Hauge. 1967. Volatile growth inhibitors produced by Salvia leucophylla: Effect on seedling anatomy. Bulletin of the Torrey Botanical Club 94: 182-191.
70. Muller, H. M. and C. H. Muller. 1964. Volatile growth inhibitors produced by Salvia species. Bulletin of the Torrey Botanical Club 91: 327-330.
71. Muller, C. H., R. B. Hanawalt, and J. K. McPherson. 1968a. Allelopathic control of herb growth in the fire cycle of California chaparral. Bulletin of the Torrey Botanical Club 95: 225-231.
72. Muller, C. H., P. Lorber, and B. Haley. 1968b. Volatile growth inhibitors produced by Salvia leucophylla: Effect on seedling growth and respiration. Bulletin of the Torrey Botanical Club 95: 415-422.
73. Munz, P. A. 1927. The southern California species of Salvia. Southern California Academy of Sciences 26: 17-29.
74. Munz, P. A. 1935. Manual of southern California botany. San Francisco, California: J. W. Stacy.
75. Neisess, K. R. 1983. Evolution, systematics and terpene relationships of Salvia section Audibertia. Ph. D. Thesis. Riverside, California: University of California.
76. Neisess, K. R. 1984. Heterostyly in Salvia brandegeei. Madroño 31: 252-254.
77. Neisess, K. R., R. W. Scora, and J. Kumamoto. 1987. Volatile leaf oils of California salvias. Journal of Natural Products 50: 515-517.
78. Olmstead, R. G., B. Bremer, K. M. Scott, and J. D. Palmer. 1993. A parsimony analysis of the Asteridae sensu lato based on rbcL sequences. Annals of the Missouri Botanical Garden 80: 700-722.
79. Oxelman, B., M. Liden, and D. Berglund. 1997. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Systematics and Evolution 206: 393-410.
80. Pagel, M. 1994. Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London. Series B, Biological Sciences 255: 37-45.
81. Pagel, M. and A. Meade. 2007. BayesTraits, version 1.0. Computer program and documentation distributed by the author, website: http://www.evolution.rdg.ac.uk(accessed 13 May 2014).
82. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
83. Plummer, M., N. Best, K. Cowles, and K. Vines. 2006. CODA: Convergence diagnosis and output analysis for MCMC. R News 6: 7-11.
84. Posada, D. and K. A. Crandall. 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics 14: 817-818.
85. R Development Core Team. 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Austria. URL http://www.R-project.org/.
86. Rabosky, D. L., M. Grundler, C. Anderson, P. Title, J. J. Shi, J. W. Brown, H. Huang, and J. G. Larson. 2014. BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution 5: 701-707.
87. Raven, P. H. 1973. The evolution of Mediterranean floras. Pp. 213-224 in Mediterranean ecosystems: Origin and structure, eds. di Castri, F. and H. A. Mooney. Springer: New York.
88. Raven, P. H. and D. Axelrod. 1978. Origin and relationships of the California flora. Berkeley: University of California Press.
89. Ree, R. H. and S. A. Smith. 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 4-14.
90. Ree, R. H., B. R. Moore, C. O. Webb, and M. J. Donoghue. 2005. A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59: 2299-2311.
91. Reith, M., G. Baumann, R. Claßen-Bockhoff, and T. Speck. 2007. New insights into the functional morphology of the lever mechanism of Salvia pratensis (Lamiaceae). Annals of Botany 100: 393-400.
92. Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution 19: 101-109.
93. Shaw, J., E. B. Lickey, J. T. Beck, S. B. Farmer, W. Liu, J. Miller, K. C. Siripun, C. T. Winder, E. E. Schilling, and R. L. Small. 2005. The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92: 142-166.
94. Shimodaira, H. and M. Hasegawa. 1999. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114-1116.
95. Spalink, D., B. T. Drew, M. C. Pace, J. G. Zaborsky, J. R. Starr, K. M. Cameron, and K. J. Sytsma. Historical biogeography and diversification of the cosmopolitan Cyperaceae. Journal of Biogeography (in press).
96. Stewart, W. S. 1939. Chromosome numbers of California salvias. American Journal of Botany 26: 730-732.
97. Strachan, J. L. 1982. A revision of the Salvia dorrii complex (Lamiaceae). Brittonia 34: 151-169.
98. Swofford, D. L. 2003. PAUP∗ Phylogenetic analysis using parsimony (∗and othermethods),v.4.0b10.Sunderland, Massachusetts: Sinauer Associates.
99. Sytsma, K. J., J. Morawetz, J. C. Pires, M. Nepokroeff, E. Conti, M. Zjhra, J. C. Hall, and M. W. Chase. 2002. Urticalean rosids: Circumscription, rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. American Journal of Botany 89: 1531-1546.
100. Taylor, R. M. and T. J. Ayers. 2006. Systematics of Salvia pachyphylla. Madroño 53: 11-24.
101. Templeton, A. R. 1980. The theory of speciation via the founder principle. Genetics 94: 1011-1038.
102. Walker, J. B. 2006. Systematics of the genus Salvia. Ph.D. dissertation. Madison: University of Wisconsin.
103. Walker, J. B. and K. J. Sytsma. 2007. Staminal evolution in the genus Salvia (Lamiaceae): Molecular phylogenetic evidence for multiple origins of the staminal lever. Annals of Botany 100: 375-391.
104. Walker, J. B., K. J. Sytsma, J. Treutlein, and M. Wink. 2004. Salvia is not monophyletic: Implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. American Journal of Botany 91: 1115-1125.
105. Wernicke, B., R. Clayton, M. Ducea, C. H. Jones, S. Park, S. Ruppert, J. Saleeby, J. K. Snow, L. Squires, M. Fliedner, G. Jiracek, R. Keller, S. Klemperer, J. Luetgart, P. Malin, K. Miller, W. Mooney, H. Oliver, and R. Phinney. 1996. Origin of high mountains in the continents: The southern Sierra Nevada. Science 271: 190-193.
106. Wester, P. and R. Claßen-Bockhoff. 2006. Bird pollination in South African Salvia species. Flora 201: 396-406.
107. Wester, P. and R. Claßen-Bockhoff. 2007. Floral diversity and pollen transfer mechanisms in bird-pollinated Salvia species. Annals of Botany 100: 401-421.
108. Whistler, R. L. 1982. Industrial gums from plants: Guar and chia. Economic Botany 36: 195-202.
109. Zwickl, D. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph. D. thesis. Austin: University of Texas.