Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen
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- 作者：Jane E Stewart (11) (7)
Lavern W Timmer (8)
Christopher B Lawrence (9)
Barry M Pryor (10)
Tobin L Peever (7) - 关键词：Coalescent ; Species delimitation ; Species tree ; Gene tree
- 刊名：BMC Evolutionary Biology
- 出版年：2014
- 出版时间：December 2014
- 年：2014
- 卷：14
- 期：1
- 全文大小：640 KB
- 参考文献：1. Perkins DD: In Praise of Diversity. In / More Gene Manipulations in Fungi. Edited by: Bennett JW, Lasure LL. New York: Academic Press; 1991:3鈥?6.
2. Harrington TC, Rizzo DM: Defining species in the fungi. In / Structure and Dynamics of Fungal Populations. Edited by: Worrall JJ. Dordrecht, The Netherlands: Kluwer Press; 1999:43鈥?1.
3. Maynard Smith J, Szathm谩ry E: / The Major Transitions in Evolution. London: Oxford University Press; 1995.
4. Kohn LM: Mechanisms of fungal speciation. / Annu Rev Phytopathol 2005, 43:279鈥?08.
5. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC: Phylogenetic species recognition and species concepts in fungi. / Fungal Genet Biol 2000, 31:21鈥?2.
6. Hibbett DS, Taylor JW: Fungal systematics: is a new age of enlightenment at hand? / Nat Rev Microbiol 2013, 11:129鈥?33.
7. Hawsworth DL: Integrating Morphological and Molecular Data in Fungal Systematics. In / Systematics and Evolution of Fungi. Edited by: Misra JK, Tewari JP, Deshmukh SK. New York, NY: CRC Press; 2012:1鈥?4.
8. Kohn LM: The clonal dynamic in wild and agricultural plant populations. / Can J Bot 1995, 73:S1231-S1240.
9. Taylor JW, Jacobson DJ, Fisher MC: The evolution of asexual fungi: reproduction, speciation, and classification. / Annu Rev Phytopathol 1999, 37:197鈥?46.
10. Carstens BC, Knowles LL: Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: An example from Melanoplus grasshoppers. / Syst Biol 2007, 56:400鈥?11.
11. Eckert AJ, Carstens BC: Does gene flow destroy phylogenetic signal? The performance of three methods for estimating species phylogeneies in the presence of gene flow. / Mol Phylogenet Evol 2008, 49:832鈥?42.
12. Kubatko LS, Carstens BC, Knowles LL: STEM: species tree estimation using maximum likelihood for gene trees under coalescence. / Bioinformatics 2009, 25:9鈥?73.
13. Kubatko LS, Degnan JH: Inconsistency of phylogenetic estimates from concatenated data under coalescence. / Syst Biol 2007, 56:17鈥?4.
14. Maddison WP: Gene trees in species trees. / Syst Biol 1997, 46:523鈥?36.
15. Hartl DL, Clark AG: / Principles of Population Genetics. 4th edition. Sinauer Associates, Inc: Sunderland, MA; 2007.
16. Degnan JH, Salter LM: Gene tree distributions under the coalescent process. / Evolution 2005, 9:24鈥?7.
17. Maddison WP, Knowles LL: Inferring phylogengy despite incomplete lineage sorting. / Syst Biol 2006, 55:410鈥?31.
18. Lui L, Pearl DK: Species trees from gene trees: Reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. / Syst Biol 2007, 56:504鈥?14.
19. Niemiller ML, Fitzpatrick BM, Miller BT: Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. / Mol Ecol 2008, 17:2258鈥?275.
20. Brumfield RT, Liu L, Lum DE, Edwards SV: Comparison of species tree methods for reconstructing the phylogeny of bearded manikins (Aves: Pipridae: Manacus ) from multilocus sequence data. / Syst Biol 2008, 57:9鈥?31.
21. Cranston KA, Hurwitz B, Ware D, Stein L, Wing RA: Species trees from highly incongruent gene trees in rice. / Syst Biol 2009, 58:489鈥?00.
22. Henk DA, Eagle CE, Brown K, VanDenBerg MA, Dyer PS, Peterson SW, Fisher MC: Speciation despite globally overlapping distributions in Penicillium chyrysogenum : the population genetics of Alexander Fleming鈥檚 lucky fungus. / Mol Ecol 2011, 20:4288鈥?301.
23. Pollard DA, Iyer VN, Moses AM, Eisen MB: Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. / PLoS Genet 2006, 2:e173.
24. Browne AGP, Fisher MC, Henk DA: Species-specific PCR to describe local-scale distribution of four cryptic species in the Penicillium chrysogenum complex. / Fungal Ecol 2013, 6:419鈥?29.
25. Pamilo P, Nei M: Relationships between gene trees and species trees. / Mol Biol Evol 1988, 5:568鈥?83.
26. Leache AD: Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards ( Sceloporus ). / Syst Biol 2008, 56:547鈥?59.
27. Linnen CR: / Species tree estimation for complex divergence histories: a case study in Neodiprion sawflies. In Estimating Species Trees. Edited by Knowles LL, Kubatko L. New York: Wiley-Blackwell; 2010.
28. Andrew M, Peever TL, Pryor BM: An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex. / Mycologia 2009, 101:95鈥?09.
29. Stewart JE, Thomas KA, Lawrence CB, Dang H, Pryor BM, Peever TL: Signatures of recombination in clonal lineages of the citrus brown spot pathogen, Alternaria alternata sensu lato. / Phytopathology 2013, 103:741鈥?49.
30. Pierce NB: Black rot of oranges. / Bot Gazelle 1902, 33:234鈥?3.
31. Neergaard P: / Danish Species of Alternaria and Stemphylium. London: Oxford University Press; 1945:560.
32. Ellis MB: / Dematiaceous Hyphomycetes. Kew: Commonwealth Mycological Institute; 19.
33. Kusaba M, Tsuge T: Nuclear ribosomal DNA variation and pathogenic specialization in Alternaria fungi known to produce host-specific toxins. / Appl Environ Microbiol 1994, 60:3055鈥?062.
34. Simmons EG: Alternaria themes and variations (226鈥?35): Classification of citrus pathogens. / Mycotaxon 1999, 70:263鈥?23.
35. Peever TL, Iba帽ez A, Akimitsu K, Timmer LW: Worldwide Phylogeography of the citrus brown spot pathogen, Alternaria alternata . / Phytopathology 2002, 92:794鈥?02.
36. Peever TL, Su G, Carpenter-Boggs L, Timmer LW: Molecular systematics of citrus-associated Alternaria spp. / Mycologia 2004, 96:119鈥?34.
37. Kingman JFC: The coalescent. / Stoch Process Appl 1982, 13:235鈥?48.
38. Peever TL, Canihos Y, Olsen L, Ibanez A, Liu Y鈥揅, Timmer LW: Population genetic structure and host specificity of Alternaria spp. causing brown spot on Minneola tangelo and rough lemon in Florida. / Phytopathology 1999, 92:794鈥?02.
39. Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H: Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata . / Mol Plant-Microbe Interact 2001, 14:749鈥?57.
40. Peever TL, Carpenter-Boggs L, Timmer LW, Carris LM, Bhatia A: Citrus black rot is caused by phylogenetically distinct lineages of Alternaria alternata . / Phytopathology 2005, 95:512鈥?18.
41. Su G, Peever TL, Timmer LW: Molecular systematics of citrus-associated Alternaria sp . / Phytopathology 2001, 91:S190.
42. Andrew M: / Molecular systematics of small-spored Alternaria species. MS Thesis: Washington State University; 2006.
43. Tran-Dinh N, Hocking A: Isolation and characterization of polymorphic microsatellite markers for Alternaria alternata . / Mol Ecol Resour 2006, 6:405鈥?07.
44. Rozen S, Skaletsky H, Krawetz S, Misener S: Primer3 on the WWW for general users and for biologist programmers. / In bioinformatics Methods and Protocols 2000, 365鈥?86.
45. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. / Syst Biol 2003, 52:696鈥?07.
46. Huelsenbeck JP, Ronquist F: MrBayes: Bayesian inference of phylogenetic trees. / Bioinformatics 2001, 17:754鈥?55.
47. Minin V, Abdo Z, Joyce P, Sullivan J: Performance-based selection of likelihood models for phylogeny estimation. / Syst Biol 2003, 52:674鈥?83.
48. Heled J, Drummond AJ: Bayesian inference of species trees from multilocus data. / Mol Biol Evol 2010,2010(27):570鈥?80.
49. Shimodaira H, Hasegawa M: Multiple comparisons of loglikelihoods with applications to phylogenetic inference. / Mol Biol Evol 1999, 16:1114鈥?116.
50. Swofford DL: / PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates; 2003.
51. Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis. / Nucleic Acids Symp Ser 1999, 41:95鈥?8.
52. Librado P, Rozas J: DnaSP v5: A software for comprehensive analysis of DNA polymorphism. / Bioinformatics 2009, 25:1451鈥?452.
53. Rozas J, Sanchez-Del J, Barrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. / Bioinformatics 2003, 19:2496鈥?497.
54. Hudson RR, Kaplan NL: Statistical properties of the number of recombination events in the history of a sample of DNA sequences. / Genetics 1985, 111:147鈥?64.
55. Jakobsen IB, Easteal S: A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. / Comput Appl Biosci 1996, 12:291鈥?95.
56. Price EW, Carbone I: SNAP: workbench management tool for evolutionary population genetics analysis. / Bioinformatics 2005, 21:402鈥?04.
57. Aylor DL, Price EW, Carbone I: SNAP: combine and map modules for multilocus population genetics analysis. / Bioinformatics 2006, 22:1399鈥?401.
58. Hey J, Wakely J: A coalescent estimator of the population recombination rate. / Genetics 1997, 145:833鈥?46.
59. Griffiths RC, Marjoram P: Ancestral inference from samples of DNA sequences with recombination. / J Comput Biol 1996, 3:479鈥?02.
60. Lawrence DP, Gannibal PB, Peever TL, Pryor BM: The sections of Alternaria: formalizing species-group concepts. / Mycologia 2013, 105:530鈥?46.
61. Bahlo M, Griffiths RC: Inference from gene trees in a subdivided population. / Theor Popul Biol 2000, 57:79鈥?5.
62. Griffiths RC, Tavar茅 S: Ancestral inference in population genetics. / Stat Sci 1994, 9:307鈥?19.
63. Lyngso RB, Song YS, Hein J: Minimum Recombination Histories by Branch and Bound. In / Algorithms in Bioinformatics, Proceedings. Berlin: Springer-Verlag Berlin; 2005:239鈥?50.
64. Oliver JC: AUGIST: inferring species trees while accommodating gene tree uncertainty. / Bioinformatics 2008, 24:2932鈥?933.
65. Avise JC, Ball RM Jr: Principles of genealogical concordance in species concepts and biological taxonomy. / Oxf Surv Evol Biol 1990, 7:45鈥?7.
66. Alfaro ME, Zoller S, Lutzoni F: Bayes or bootstrap? A simulation studying comparing the performance of Bayseian markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. / Mol Biol Evol 2003, 20:255鈥?66.
67. Maddison WP, Maddison DR: Mesquite: a modular system for evolutionary analysis. Version 2.73. 2010. http://mesquiteproject.org.
68. Yule GU: A mathematical theory of evolution, based on the conclusions of Dr. J.C. Willis, F.R.S. / Philos Trans R Soc Lond Biol 1925, 213:21鈥?7.
69. Rannala B, Yang Z: Probability distribution of molecular evolutionary tree: a new methods for phylogenetic inference. / J Mol Evol 1996, 43:304鈥?11.
70. Rambaut A: FigTree, a graphical viewer of phylogenetic trees. 2008. http://tree.bio.ed.ac.uk/software/figtree.
71. Berbee ML, Payne BP, Zhang G, Roberts RG, Turgeon BG: Shared ITS DNA substitutions in isolates of opposite mating type reveal a recombining history for three presumed asexual species in the filamentous ascomycete genus Alternaria . / Mycol Res 2003, 107:169鈥?82.
72. Kasuga T, White TJ, Taylor JW: Estimation of nucleotide substitution rates in Eurotiomycete fungi. / Mol Biol Evol 2002, 19:2318鈥?324.
73. Nishimura S, Kohmoto K: Host-specific toxins and chemical structures from Alternaria species. / Annu Rev Phytopathol 1983, 21:87鈥?16.
74. Chaverri P, Castlebury LA, Samuels GJ, Geiser DM: Multilocus phogenetics structure within the Trichoderma harzianum / Hypocrea lixii complex. / Mol Phylogenet Evol 2003, 27:302鈥?13.
75. Miller AN, Huhndorf SM: Using phylogenetic species recognition to delimit species boundaries and species relationships within Lasiosphaeria . / Mycologia 2004, 96:302鈥?13.
76. Kohmoto K, Otani H, Tsuge T: Alternaria alternata Pathogens. In / Pathogenesis and Host Specificity in Plant Diss: Histopathological, Biochemical, Genetic and Molecular Bases. Vol. II, Eukaryotes. Edited by: Kohmoto K, Singh US, Singh RP. Oxford: Pergamon Press; 1995:51鈥?3.
77. Timmer LW, Peever TL, Solel Z, Akimitsu K: Alternaria diseases of citrus 鈥?Novel pathosystems. / Phytopathol Mediterrian 2003, 42:3鈥?6.
78. Nishimura S, Kohmoto K, Otani H, Ramachandran P, Tamura F: Pathological and epidemiological aspects of Alternaria alternata infection depending on a host-specific toxin. In / Plant infection: the Physiological and Biochemical Basis. Edited by: Asada Y, Bushnell WR, Ouchi S, Vance CP. Tokyo; Berlin: Japan Scientific Societies Press; Springer-Verlag; 1982:199鈥?1.
79. Akamatsu H, Taga M, Kodama M, Johnson R, Otani H, Kohmoto K: Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxin. / Curr Genet 1999, 35:647鈥?56.
80. Masunaka A, Ohtani K, Peever TL, Timmer LW, Tsuge T, Yamamoto M, Akimitsu K: An isolate of Alternaria alternata that is pathogenic to both tanginess and rough lemon produces two host-selective toxins ACT and ACR toxins. / Phytopathology 2005, 95:241鈥?47.
81. Masunaka A, Tanaka A, Tsuge T, Peever TL, Timmer LW, Yamamoto M, Yamamoto H, Akimitsu K: Distribution and characterization of AKT homologs in the tangerine pathotype of Alternaria alternata . / Phytopathology 2000, 90:762鈥?68.
82. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Mayumi E, Yamamoto M, Otani H: Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata . / FEMS Microbiol Rev 2013, 37:44鈥?6.
83. Li W-H, Tanimura M, Sharp PM: An evaluation of the molecular clock hypothesis using mammalian DNA sequences. / J Mol Evol 1987, 25:330鈥?42.
84. Scora RW: On the history and origin of citrus. / Torrey Bot Club 1975, 102:369鈥?75.
85. O鈥橠onnell K: Molecular phylogeny of the Nectria haematococca 鈥?/strong> Fusarium solani species complex. / Mycologia 2000, 92:919鈥?38.
86. O鈥橠onnell K, Kistler HC, Tacke BK, Casper HH: Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum , the fungus causing wheat scab. / Proc Natl Acad Sci U S A 2000, 97:7905鈥?910.
87. Steenkamp ET, Wingfield BD, Desjardins AE: Cryptic speciation in Fusarium subglutinans . / Mycologia 2002, 94:1032鈥?043.
88. Koufopanou V, Burt A, Taylor JW: Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidioides immitis . / Proc Natl Acad Sci U S A 1997, 94:5478鈥?482.
89. Kasuga T, Taylor JW, White TJ: Phylogenetic relationships of varieties and geographical groups of the human pathogenic fungus, Histoplasma capsulatum Darling. / J Clin Microbiol 1999, 37:653鈥?63.
90. Cruse M, Telerant R, Gallagher T, Lee T, Taylor JW: Cryptic species in Stachybotrys chartarum . / Mycologia 2002, 94:814鈥?22.
91. Fisher MC, Koenig G, White TJ, Taylor JW: Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non-California population of Coccidioides immitis . / Mycologia 2002, 94:73鈥?4.
92. Couch BC, Kohn LM: A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae , from M. grisea. / Mycologia 2002, 94:683鈥?93.
93. O鈥橠onnell K, Ward TJ, Geiser DM, Kistler HC, Aoki T: Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. / Fungal Genet Biol 2004, 41:600鈥?23.
94. Degnan JH, Rosenberg NA: Discordance of species trees with their most likely gene trees. / PLoS Genet 2006, 2:762鈥?68.
95. Rosenberg NA, Tao R: Discordance of species trees with their most likely gene trees: the case of five taxa. / Syst Biol 2008, 57:131鈥?40.
96. Sen D, Brown CJ, Top EM, Sullivan J: Inferring the evolutionary history of IncP-1 plasmids despite incongruence among backbone gene trees. / Mol Biol Evol 2013, 30:154鈥?66.
97. Belfiore NM, Liu L, Moritz C: Multilocus phylogenetics of a rapid radiation in the genus Thomomys (Rodentia: Geomyidae). / Syst Biol 2008, 57:294.
98. Yun SH, Berbee ML, Yoder OC, Turgeon BG: Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. / Proc Natl Acad Sci U S A 1999, 96:5592鈥?597.
99. Stewart JE, Kawabe M, Abdo Z, Arie T, Peever TL: Contrasting Codon usage patterns and purifying selection at the mating locus in putatively asexual Alternaria fungal species. / PLoS ONE 2011, 6:e20083.
100. Roberts RG: Alternaria yaliinficiens sp. nov. on Ya Li pear fruit: from interception to identification. / Plant Dis 2005, 89:134鈥?45.
101. Boykin LM, Armstrong KF, Kubatko L, DeBarro P: Species delimitation and global biosecurity. / Evol Bioinformatics 2012, 8:1鈥?7.
102. Rossman AY, Palm-Hern谩ndez ME: Systematics of plant pathogenetic fungi: why it matters? / Plant Dis 2008, 92:1376鈥?386.
103. Elena K: Alternaria brown spot of Minneola in Greece; evaluation of citrus species susceptibility. / Plant Pathol Eur J Plant Pathol 2006, 115:259鈥?62.
104. Golmohammadi M, Andrew M, Peever TL, Peres NA, Timmer LW: First report of brown spot of tangerine hybrid cultivars Minneola, page and fortune caused by Alternaria alternata in Iran. / Plant Pathol 2006, 12:2005鈥?098.
105. Mar铆n JE, Fern谩ndez H, Peres NA, Andrew M, Peever TL, Timmer LW: First report of Alternaria brown spot of citrus caused by Alternaria alternata in Peru. / Plant Dis 2006, 90:686. - 作者单位：Jane E Stewart (11) (7)
Lavern W Timmer (8)
Christopher B Lawrence (9)
Barry M Pryor (10)
Tobin L Peever (7)
11. Department of Plant Pathology, University of Georgia, Athens, Georgia
7. Department of Plant Pathology, Washington State University, Pullman, WA, USA
8. Citrus Research and Education Center, University of Florida, Lake Alfred, FL, USA
9. Virginia Bioinformatics Institute, Blacksburg, VA, USA
10. Division of Plant Pathology and Microbiology, School of Plant Sciences, University of Arizona, Tucson, AZ, USA - ISSN：1471-2148
文摘
Background Traditional morphological and biological species concepts are difficult to apply to closely related, asexual taxa because of the lack of an active sexual phase and paucity of morphological characters. Phylogenetic species concepts such as genealogical concordance phylogenetic species recognition (GCPSR) have been extensively used; however, methods that incorporate gene tree uncertainty into species recognition may more accurately and objectively delineate species. Using a worldwide sample of Alternaria alternata sensu lato, causal agent of citrus brown spot, the evolutionary histories of four nuclear loci including an endo-polygalacturonase gene, two anonymous loci, and one microsatellite flanking region were estimated using the coalescent. Species boundaries were estimated using several approaches including those that incorporate uncertainty in gene genealogies when lineage sorting and non-reciprocal monophyly of gene trees is common. Results Coalescent analyses revealed three phylogenetic lineages strongly influenced by incomplete lineage sorting and recombination. Divergence of the citrus 2 lineage from the citrus 1 and citrus 3 lineages was supported at most loci. A consensus of species tree estimation methods supported two species of Alternaria causing citrus brown spot worldwide. Based on substitution rates at the endo-polygalacturonase locus, divergence of the citrus 2 and the 1 and 3 lineages was estimated to have occurred at least 5, 400 years before present, predating the human-mediated movement of citrus and associated pathogens out of SE Asia. Conclusions The number of Alternaria species identified as causing brown spot of citrus worldwide using morphological criteria has been overestimated. Little support was found for most of these morphospecies using quantitative species recognition approaches. Correct species delimitation of plant-pathogenic fungi is critical for understanding the evolution of pathogenicity, introductions of pathogens to new areas, and for regulating the movement of pathogens to enforce quarantines. This research shows that multilocus phylogenetic methods that allow for recombination and incomplete lineage sorting can be useful for the quantitative delimitation of asexual species that are morphologically indistinguishable. Two phylogenetic species of Alternaria were identified as causing citrus brown spot worldwide. Further research is needed to determine how these species were introduced worldwide, how they differ phenotypically and how these species are maintained.