Accelerated rate of molecular evolution for vittarioid ferns is strong and not driven by selection

Systematic Biology

Volumn 63, Issue 1, 2014, Pages 31-54

  Rothfels, Carl J ^a,b   Schuettpelz, Eric ^c,d  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^d DEPARTMENT OF PALEOBIOLOGY   (United States)

Author keywords

Adiantum; Calciphilopteris; codon models; divergence time dating; local clocks; model selection; molecular clock; mutation rate; nucleotide substitution rate; Pteridaceae; rate heterogeneity; relaxed clocks; trigenomic analyses

Indexed keywords

ADIANTUM; FILICOPHYTA; PTERIDACEAE;

ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; FERN; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY;

BAYES THEOREM; EVOLUTION, MOLECULAR; FERNS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION, GENETIC;

EID: 84891358468     PISSN: 10635157     EISSN: 1076836X     Source Type: Journal    
DOI: 10.1093/sysbio/syt058     Document Type: Article

References (147)

1. AkaikeH. 1974. A newlook at the statistical model identification. IEEE T. Automat. Contr. 19:716-723.
2. Baele G., Lemey P., Bedford T., Rambaut A., Suchard M.A., Alekseyenko A.V. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29:2157-2167.
3. Baer C.F., Miyamoto M.M., Denver D.R. 2007. Mutation rate variation in multicellular eukaryotes: Causes and consequences. Nat. Rev. Genet. 8:619-631.
4. Bielawski J.,Yang Z. 2004.Amaximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J. Mol. Evol. 59:121-132.
5. Bininda-Emonds O.R.P. 2007. Fast genes and slowclades: Comparative rates of molecular evolution in mammals. Evol. Bioinform. 3:59-85.
6. Bouma W., Ritchie P. Perrie L. 2010. Phylogeny and generic taxonomy of the New Zealand Pteridaceae ferns from chloroplast rbcL DNA sequences. Aust. Syst. Bot. 23:143-151.
7. Bousquet J., Strauss S., DoerksenA.,Price R. 1992. Extensive variation in evolutionary rate of rbcL gene-sequences among seed plants. PNAS 89:7844-7848.
8. BrandleyM., SchmitzA.,Reeder T. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst. Biol. 54:373-390.
9. Bromham L. 2002. Molecular clocks in reptiles: Life history influences rate of molecular evolution. Mol. Biol. Evol. 19:302-309.
10. Bromham L. 2009. Why do species vary in their rate of molecular evolution? Biol. Letters 5:401-404.
11. BromhamL., Leys R. 2005. Sociality and the rate of molecular evolution. Mol. Biol. Evol. 22:1393-1402.
12. Bromham L., Rambaut A., Harvey P. 1996. Determinants of rate variation in mammalian DNA sequence evolution. J. Mol. Evol. 43:610-621.
13. Bromham L., Woolfit M. 2004. Explosive radiations and the reliability of molecular clocks: Island endemic radiations as a test case. Syst. Biol. 53:758-766.
14. Bromham L., Woolfit M., Lee M., Rambaut A. 2002. Testing the relationship between morphological and molecular rates of change along phylogenies. Evolution 56:1921-1930.
15. Burnham K.P., Anderson D.R. 2002. Model selection and multimodel inference: A practical information-theoretic approach. New York, USA: Springer.
16. Burnham K.P., Anderson D.R. 2004. Multimodel inference: Understanding AIC and BIC in model selection. Sociol. Method. Res. 33:261-304.
17. Cho Y., Mower J., Qiu Y.L., Palmer J. 2004. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. PNAS 101:17741-17746.
18. Crane E.H. 1997. A revised circumscription of the genera of the fern family Vittariaceae. Syst. Bot. 22:509-517.
19. Crane E.H., Farrar D.R.,Wendel J.F. 1995. Phylogeny of theVittariaceae: Convergent simplification leads to a polyphyletic Vittaria. Am. Fern J. 85:283-305.
20. Cronn R., Cedroni M., Haselkorn T., Grover C.,Wendel J.F. 2002. PCRmediated recombination in amplification products derived from polyploid cotton. Theor. Appl. Genet. 104:482-489.
21. Davies T., Savolainen V., Chase M., Moat J., Barraclough T. 2004. Environmental energy and evolutionary rates in flowering plants. P. Roy. Soc. Lond. B Bio. 271:2195-2200.
22. Des Marais D.L., Smith A.R., Britton D.M., Pryer K.M. 2003. Phylogenetic relationships and evolution of extant horsetails, Equisetum, based on chloroplast DNA sequence data (rbcL and trnL-F). Int. J. Plant Sci. 164:737-751.
23. Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: 699-710.
24. Drummond A. J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
25. Drummond A.J., SuchardM.A. 2010. Bayesian random local clocks, or one rate to rule them all. BMC Biol. 8:1-12.
26. Eiserhardt W.L., Rohwer J.G., Russell S.J., Yesilyurt J.C., Schneider H. 2011. Evidence for radiations of cheilanthoid ferns in the Greater Cape Floristic Region. Taxon 60: 1269-1283.
27. Eyre-Walker A., Gaut B. 1997. Correlated rates of synonymous site evolution across plant genomes. Mol. Biol. Evol. 14:455-460.
28. Fan Y., Wu R., Chen M.-H., Kuo L., Lewis P. 2011. Choosing among partition models in Bayesian phylogenetics. Mol. Biol. Evol. 28:523-532.
29. Farrar D. 1974. Gemmiferous fern gametophytes-Vittariaceae. Am. J. Bot. 61:146-155.
30. Fitch W.M., Beintema J. 1990. Correcting parsimonious trees for unseen nucleotide substitutions: The effect of dense branching as exemplified by ribonuclease. Mol. Biol. Evol. 7:438-443.
31. Gastony G.J., Rollo D.R. 1995. Phylogeny and generic circumscriptions of cheilanthoid ferns (Pteridaceae: Cheilanthoideae) inferred from rbcL nucleotide sequences. Am. Fern J. 85:341-360.
32. Gastony G.J., Rollo D.R. 1998. Cheilanthoid ferns (Pteridaceae: Cheilanthoideae) in the southwestern United States and adjacent Mexico-a molecular phylogenetic reassessment of generic lines. Aliso 17:131-144.
33. Gastony G.J., Yatskievych G. 1992. Maternal inheritance of the chloroplast and mitochondrial genomes in cheilanthoid ferns. Am. J. Bot. 79:716-722.
34. Gaut B., Muse S., ClarkW., Clegg M. 1992. Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants. J. Mol. Evol. 35:292-303.
35. Gaya E.,Redelings B.D.,Navarro-RosinésP., Llimona X.,DeCáceres M., Lutzoni F. 2011. Align or not to align? Resolving species complexes within the Caloplaca saxicola group as a case study. Mycologia 103:361-378.
36. Goldman N., Whelan S. 2002. A novel use of equilibrium frequencies in models of sequence evolution. Mol. Biol. Evol. 19: 1821-1831.
37. Goldman N., Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11:725-736.
38. Hebert P., Remigio E., Colbourne J., Taylor D., Wilson C. 2002. Accelerated molecular evolution in halophilic crustaceans. Evolution 56:909-926.
39. Hoegg S., Vences H., Brinkmann H., Meyer A. 2004. Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Mol. Biol. Evol. 21:1188-1200.
40. Hugall A.F., Lee M. S. Y. 2007. The likelihood node density effect and consequences for evolutionary studies of molecular rates. Evolution 61:2293-2307.
41. Hurvich C.M., Tsai C.-L. 1989. Regression and time-series model selection in small samples. Biometrika 76:297-307.
42. Johnson A.K., Rothfels C.J.,Windham M.D., Pryer K. M. 2012. Unique expression of a sporophytic character on the gametophytes of notholaenid ferns (Pteridaceae). Am. J. Bot. 99:1118-1124.
43. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
44. Kirkpatrick R.E.B. 2007. Investigating the monophyly of Pellaea (Pteridaceae) in the context of a phylogenetic analysis of cheilanthoid ferns. Syst. Bot. 32:504-518.
45. Korall P., Schuettpelz E., Pryer K.M. 2010. Abrupt deceleration of molecular evolution linked to the origin of arborescence in ferns. Evolution 64:2786-2792.
46. Lanfear R. 2010. The local-clock permutation test: A simple test to compare rates of molecular evolution on phylogenetic trees. Evolution 65:606-611.
47. Lanfear R., Calcott B., Ho S.Y.W., Guindon S. 2012. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29:1695-1701.
48. Lanfear R., Ho S.Y.W., Davies T.J., Moles A.T., Aarssen L., Swenson N.G., Warmann L., Zanne A.E., Allen A.P. 2013. Taller plants have lower rates of molecular evolution. Nat. Commun. 4:1-29.
49. Lanfear R., Thomas J.A., Welch J.J., Brey T., Bromham L. 2007. Metabolic rate does not calibrate the molecular clock. PNAS 104: 15388-15393.
50. Lanfear R.,Welch J. J., Bromham L. 2010.Watching the clock: Studying variation in rates of molecular evolution between species. Trends Ecol. Evol. 25:496-503.
51. Laroche J., Li P., Maggia L., Bousquet J. 1997. Molecular evolution of angiosperm mitochondrial introns and exons. PNAS 94:5722-5727.
52. Lartillot N., Philippe H. 2006. Computing Bayes factors using thermodynamic integration. Syst. Biol. 55:195-207.
53. Lartillot N., Poujol R. 2010. A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. Mol. Biol. Evol. 28:729-744.
54. Lewis P.O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50:913-925.
55. Lewis P.O., Holder M.T., Swofford D.L. 2010. Phycas. Available from: URL www.phycas.org (last accessed January 1, 2012).
56. Lewis L., Mishler B.D., Vilgalys R. 1997. Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Mol. Phylogenet. Evol. 7:377-393.
57. Li W.-H., Ellsworth D.L., Krushkal J., Chang B.H.J., Hewett-Emmett D. 1996. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol. Phylogenet. Evol. 5:182-187.
58. Li F.-W., Kuo L.-Y., Rothfels C.J., Ebihara A., Chiou W.-L., Windham M.D., Pryer K.M. 2011. rbcL and matK earn two thumbs up as the core DNA barcode for ferns. PLoS ONE 6:e26597.
59. Lu J.-M., Li D.-Z., Lutz S., SoejimaA., Yi T.,Wen J. 2011a. Biogeographic disjunction between eastern Asia and North America in the Adiantum pedatum complex (Pteridaceae). Am. J. Bot. 98:1680-1693.
60. Lu J.-M., Wen J., Lutz S., Wang Y.-P., Li D.-Z. 2011b. Phylogenetic relationships of Chinese Adiantum based on five plastid markers. J. Plant Res. 125:1-13.
61. Lumbsch H., Hipp A.L., Divakar P.K., Blanco O., Crespo A. 2008. Accelerated evolutionary rates in tropical and oceanic parmelioid lichens (Ascomycota). BMC Evol. Biol. 8:257.
62. Lutzoni F., Pagel M. 1997. Accelerated evolution as a consequence of transitions to mutualism. PNAS 94:11422-11427.
63. Maddison W.P., Maddison D.R. 2011. Mesquite: A modular system for evolutionary analysis. Available from: URL mesquiteproject.org (last accessed January 1, 2012).
64. Martin W., Lydiate D., Brinkmann H., Forkmann G., Saedler H. and Cerff R. 1993. Molecular phylogenies in angiospermevolution. Mol. Biol. Evol. 10:140-162.
65. Mayrose I., Otto S.P. 2011. A likelihood method for detecting traitdependent shifts in the rate of molecular evolution. Mol. Biol. Evol. 28:759-770.
66. McCoy S.R., Kuehl J. V., Boore J. L., Raubeson L.A. 2008. The complete plastid genome sequence of Welwitschia mirabilis: An unusually compact plastome with accelerated divergence rates. BMC Evol. Biol. 8:130.
67. Meyer-Gauen G., Schnarrenberger C., Cerff R., Martin W. 1994. Molecular characterization of a novel, nuclear-encoded, NAD+dependent glyceraldehyde-3- phosphate dehydrogenase in plastids of the gymnosperm Pinus sylvestris L. Plant Mol. Biol. 26:1155-1166.
68. Moncalvo J., Drehmel D., Vilgalys R. 2000. Variation in modes and rates of evolution in nuclear and mitochondrial ribosomal DNA in the mushroom genus Amanita (Agaricales, Basidiomycota): Phylogenetic implications. Mol. Phylogenet. Evol. 16:48-63.
69. Mooers A.∅., Harvey P.H. 1994. Metabolic rate, generation time, and the rate of molecular evolution in birds. Mol. Phylogenet. Evol. 3:344-350.
70. Muse S.V. 2000. Examining rates and patterns of nucleotide substitution in plants. Plant Mol. Biol. 42:25-43.
71. Muse S., Gaut B. 1997. Comparing patterns of nucleotide substitution rates among chloroplast loci using the relative ratio test. Genetics 146:393-399.
72. Muse S., Weir B. 1992. Testing for equality of evolutionary rates. Genetics 132:269-276.
73. Nabholz B., Glémin S., Galtier N. 2008. Strong variations of mitochondrial mutation rate across mammals-the longevity hypothesis. Mol. Biol. Evol. 25:120-130.
74. Neiman M., Hehman G., Miller J.T., Logsdon J.M. Jr., Taylor D.R. 2010. Accelerated mutation accumulation in asexual lineages of a freshwater snail. Mol. Biol. Evol. 27:954-963.
75. Nielsen R., Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
76. Nikolaev S.I., Montoya-Burgos J.I., Popadin K., Parand L., Margulies E.H., Antonarakis S.E. 2007. Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. PNAS 104:20443-20448.
77. PagelM.,Venditti C., MeadeA. 2006. Large punctuational contribution of speciation to evolutionary divergence at the molecular level. Science 314:119-121.
78. Parkinson C.L.,Mower J.P., Qiu Y.L., ShirkA.J., Song K.M., YoungN.D., dePamphilis C.W., Palmer J.D. 2005. Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evol. Biol. 5:73.
79. Peterson J., Brinkmann H., Cerff R. 2003. Origin, evolution, and metabolic role of a novel glycolytic GAPDH enzyme recruited by land plant plastids. J. Mol. Evol. 57:16-26.
80. Posada D. 2008. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
81. Prado J., Rodrigues C.D.N., Salatino A., Salatino M.L.F. 2007. Phylogenetic relationships among Pteridaceae, including Brazilian species, inferred from rbcL sequences. Taxon 56:355-368.
82. Pryer K.M., Schuettpelz E.,Wolf P.G., Schneider H., SmithA.R., Cranfill R. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am. J. Bot. 91:1582-1598.
83. Rambaut, A., Drummond A.J. 2007. Tracer. Available from: URL http://tree.bio.ed.ac.uk/software/tracer/(last accessed January 1, 2012).
84. Redelings B.D., Suchard M.A. 2007. Incorporating indel information into phylogeny estimation for rapidly emerging pathogens. BMC Evol. Biol. 7:40.
85. Ronquist F., Huelsenbeck J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
86. Rothfels C.J., Larsson A., Kuo L.-Y., Korall P., Chiou W.-L., Pryer K.M. 2012. Overcoming deep roots, fast rates, and short internodes to resolve the ancient rapid radiation of eupolypod II ferns. Syst. Biol. 61:490-509.
87. Rothfels C.J., Larsson A., Li F.-W., Sigel E.M., Huiet L., Burge D.O., Ruhsam M., Graham S.W., Stevenson D.W., Wong G.K.-S., Korall P., Pryer K.M. 2013a. Transcriptome-mining for single-copy nuclear markers in ferns. PLoS ONE, in press.
88. Rothfels C.J., Windham M.D., Grusz A.L., Gastony G.J., Pryer K.M. 2008. Toward a monophyletic Notholaena (Pteridaceae): Resolving patterns of evolutionary convergence in xeric-adapted ferns. Taxon 57:712-724.
89. Rothfels C.J., Windham M.D., Pryer K.M. 2013b. A plastid phylogeny of the cosmopolitan fern family Cystopteridaceae (Polypodiopsida). Syst. Bot. 38:295-306.
90. Ruhfel B., Lindsay S., Davis C.C. 2008. Phylogenetic placement of Rheopteris and the polyphyly of Monogramma (Pteridaceae s.l.): Evidence from rbcL sequence data. Syst. Bot. 33: 37-43.
91. Sanderson M.J. 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol. Biol. Evol. 19:101-109.
92. Sanderson M.J. 2003. r8s: Inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301-302.
93. Sarich V.M., Wilson A.C. 1967. Immunological time scale for hominid evolution. Science 158:1200.
94. Schneider H., Smith A., Cranfill R., Hildebrand T., Haufler C., Ranker T. 2004. Unraveling the phylogeny of polygrammoid ferns (Polypodiaceae and Grammitidaceae): Exploring aspects of the diversification of epiphytic plants. Mol. Phylogenet. Evol. 31:1041-1063.
95. Schon I., Martens K., Van Doninck K., Butlin R.K. 2003. Evolution in the slow lane: Molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda). Biol. J. Lin. Soc. 79:93-100.
96. Schuettpelz E., Grusz A.L., Windham M.D., Pryer K.M. 2008. The utility of nuclear gapCp in resolving polyploid fern origins. Syst. Bot. 33:621-629.
97. Schuettpelz E., Korall P., Pryer K.M. 2006. Plastid atpA data provide improved support for deep relationships among ferns. Taxon 55:897-906.
98. Schuettpelz E., Pryer K.M. 2006. Reconciling extreme branch length differences: Decoupling time and rate through the evolutionary history of filmy ferns. Syst. Biol. 55:485-502.
99. Schuettpelz E., Pryer K.M. 2007. Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037-1050.
100. Schuettpelz E., Pryer K.M. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. PNAS 106:11200-11205.
101. Schuettpelz E., Schneider H., Huiet L.,Windham M.D., Pryer K. M. 2007. A molecular phylogeny of the fern family Pteridaceae: Assessing overall relationships and the affinities of previously unsampled genera. Mol. Phylogenet. Evol. 44:1172-1185.
102. Shao R., Dowton M., Murrell A., Barker S. 2003. Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol. Biol. Evol. 20:1612-1619.
103. Shapiro B., Rambaut A., Drummond A.J. 2005. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol. Biol. Evol. 23:7-9.
104. Simmons M.P., Ochoterena H. 2000. Gaps as characters in sequencebased phylogenetic analyses. Syst. Biol. 49:369-381.
105. Singh N.D., Arndt P., Clark A.G., Aquadro C.F. 2009. Strong evidence for lineage and sequence specificity of substitution rates and patterns in Drosophila. Mol. Biol. Evol. 26:1591-1605.
106. Small R., Ryburn J., Cronn R., Seelanan T.,Wendel J. 1998. The tortoise and the hare: Choosing between noncoding plastome and nuclear Adh sequences for phylogeny reconstruction in a recently diverged plant group. Am. J. Bot. 85:1301-1315.
107. Smith S.A., Donoghue M.J. 2008. Rates of molecular evolution are linked to life history in flowering plants. Science 322:86-89.
108. Soltis P.S., Soltis D.E., Savolainen V., Crane P.R., Barraclough T.G. 2002. Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils. PNAS 99:4430-4435.
109. Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
110. Stamatakis A., Hoover P., Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57:758-771.
111. Suchard M.A., Redelings B.D. 2006. BAli-Phy: Simultaneous Bayesian inference of alignment and phylogeny. Bioinformatics 22:2047-2048.
112. Swofford D.L. 2002. PAUP: Phylogenetic analysis using parsimony (and other methods). Sunderland (MA): Sinauer.
113. Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Am. Math. Soc. Lect. Math. Life Sci. 17:57-86.
114. Thiers B. [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. Available from: URL http://sweetgum.nybg.org/ih/(last accessed January 1, 2013).
115. Thomas J., Welch J.J., Woolfit M., Bromham L. 2006. There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. PNAS 103:7366-7371.
116. Tryon R.M. 1942. A revision of the genus Doryopteris. Contrib. Gray Herb. 143:1-80.
117. Tryon R.M., Tryon A.F., Kramer K.U. 1990. Pteridaceae. In: Kramer K.U., Green P.S., editors. The families and genera of vascular plants. Berlin: Springer. p. 230-256.
118. Vangerow S., Teerkorn T., Knoop V. 1999. Phylogenetic information in the mitochondrial nad5 gene of pteridophytes: RNA editing and intron sequences. Plant Biol. 1:235-243.
119. Venditti C., Meade A., Pagel M. 2006. Detecting the node-density artifact in phylogeny reconstruction. Syst. Biol. 55:637-643.
120. Weisrock D.W. 2012. Concordance analysis in mitogenomic phylogenetics. Mol. Phylogenet. Evol. 65:194-202.
121. Welch J.J., Bininda-Emonds O.R.P., Bromham L. 2008. Correlates of substitution rate variation in mammalian protein-coding sequences. BMC Evol. Biol. 8:53.
122. Wertheim J.O., Sanderson M.J., Worobey M., Bjork A. 2010. Relaxed molecular clocks, the bias-variance trade-off, and the quality of phylogenetic inference. Syst. Biol. 59:1-8.
123. Wikström N., Pryer K.M. 2005. Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Mol. Phylogenet. Evol. 36:484-493.
124. Windham M.D., Huiet L., Schuettpelz E., GruszA.L.,Rothfels C.J., Beck J. 2009. Using plastid and nuclearDNAsequences to redrawgeneric boundaries and demystify species complexes in cheilanthoid ferns. Am. Fern J. 99:68-72.
125. Wolf P.G. 1997. Evaluation of atpB nucleotide sequences for phylogenetic studies of ferns and other pteridophytes. Am. J. Bot. 84:1429-1440.
126. Wolfe K.H., LiW.-H., Sharp P.M. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. PNAS 84:9054-9058.
127. Wolfe K.H., Sharp P., Li W.H. 1989a. Mutation rates differ among regions of the mammalian genome. Nature 337:283-285.
128. Wolfe K.H., Sharp P.M., Li W.-H. 1989b. Rates of synonymous substitution in plant nuclear genes. J. Mol. Evol. 29:208-211.
129. Wong W.S.W., Yang Z., Goldman N., Nielsen R. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168:1041-1051.
130. Woolfit M., Bromham L. 2003. Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol. Biol. Evol. 20:1545-1555.
131. Woolfit M., BromhamL. 2005. Population size and molecular evolution on islands. P. Roy. Soc. B-Biol. Sci. 272:2277-2282.
132. Xiang Q.-Y., Thorne J.L., Seo T.-K., Zhang W., Thomas D.T., Ricklefs R.E. 2008. Rates of nucleotide substitution in Cornaceae (Cornales)-Pattern of variation and underlying causal factors. Mol. Phylogenet. Evol. 49:327-342.
133. Xie W.Lewis P.Fan Y.Kuo L.Chen M.-H. 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. 60:150-160.
134. Yang Z. 1996. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol. Evol. 11:367-372.
135. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
136. Yang Z. 2007. PAML 4: A program package for phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586-1591.
137. Yang Z., Nielsen R. 1998. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J. Mol. Evol. 46: 409-418.
138. Yang Z., Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19:908-917.
139. Yang Z., Nielsen R., Goldman N., Pedersen A.-M.K. 2000. Codonsubstitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.
140. Yang Z., Rannala B. 2006. Bayesian estimation of species divergence times under amolecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23:212-226.
141. Yang Z.,WongW.S.W., Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22:1107-1118.
142. Yesilyurt J.C., Schneider H. 2010. The new fern genus Calciphilopteris (Pteridaceae). Phytotaxa 7:52-59.
143. YoderA.D., Yang Z. 2000. Estimation of primate speciation dates using local molecular clocks. Mol. Biol. Evol. 17:1081-1090.
144. Zhang G., Zhang X., Chen Z., Liu H., YangW. 2007. First insights in the phylogeny of Asian cheilanthoid ferns based on sequences of two chloroplast markers. Taxon 56:369-378.
145. Zoller S., Lutzoni F. 2003. Slow algae, fast fungi: Exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Mol. Phylogenet. Evol. 29:629-640.
146. Zuckerkandl E., Pauling L. 1962. Molecular disease, evolution, and genetic heterogeneity. In: Kasha M., Pullman B., editors. Horizons in biochemistry. New York: Academic Press. p. 189-225.
147. Zuckerkandl E., Pauling L. 1965. Evolutionary divergence and convergence in proteins. In: Bryson V., Vogel H.J., editors. Evolving genes and proteins. New York: Academic Press. p. 97-165.