Inferring species-level phylogenies and taxonomic distinctiveness using multilocus data in sistrurus rattlesnakes

Systematic Biology

Volumn 60, Issue 4, 2011, Pages 393-409

  Kubatko, Laura S ^a   Gibbs, H Lisle ^a   Bloomquist, Erik W ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Gene and species trees; genealogical species concept; monophyly based tests for species delimitation; multilocus phylogenetics; Sistrurus rattlesnakes; species tree based divergence times

Indexed keywords

DNA; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; PHYLOGENY; SNAKE; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ANIMALS; CROTALUS; DNA; DNA, MITOCHONDRIAL; GENETIC SPECIATION; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

CROTALUS; SISTRURUS; SISTRURUS CATENATUS; SISTRURUS MILIARIUS;

EID: 79959474470     PISSN: 10635157     EISSN: 1076836X     Source Type: Journal    
DOI: 10.1093/sysbio/syr011     Document Type: Article

References (94)

1. Anderson C.D., Gibbs H.L., Douglas M.E., Holycross A.T. 2009. Conservation genetics of the Desert massasauga rattlesnake (Sistrurus catenatus edwardsii). Copeia. 2009:740-747.
2. Ane C., Larget B., Baum D.A., Smith S.D., Rokas A. 2007. Bayesian estimation of concordance among gene trees. Mol. Biol. Evol. 24: 412-426. (Pubitemid 46204374)
3. Baum D.A. 2007. Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon. 56:417-426. (Pubitemid 47025837)
4. Baum D.A., Shaw K.L. 1995. Genealogical perspectives on the species problem. In: Hoch P.C., Stephenson A.G., editors. Experimental and molecular approaches to plant biosystematics. St. Louis (MO): Missouri Botanical Garden. p. 289-303.
5. Belfore N.M., Liu L., Moritz C. 2008. Multi-locus phylogenetics of a rapid radiation in the Genus Thomomys (Rodentia: Geomyidae). Syst. Biol. 57:294-310.
6. Brumfeld R.T., Beerli P., Nickerson D.A., Edwards S.V. 2003. The utility of single nucleotide polymorphisms in inferences of population history Trends Ecol. Evol. 18:249-256. (Pubitemid 36551230)
7. Brumfeld R.T., Liu L., Lum D.E., Edwards S.V. 2008. Comparison of species tree methods for reconstructing the phylogeny of Bearded Manakins (Aves: Pipridae, Manacus) from multilocus sequence data. Syst. Biol. 57:719-731.
8. Bryson R.W., Pastorini J., Burbrink F.T., Forstner M.R. 2007. A phylogeny of the Lampropeltis mexicana complex (Serpentes: Colubridae) based on mitochondrial DNA sequences suggests evidence for species-level polyphyly within Lampropeltis. Mol. Phylogenet. Evol. 43:674-684. (Pubitemid 46705498)
9. Burbrink F.T., Lawson R., Slowinski J.B. 2000. Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution. 54:2107-2118. (Pubitemid 32113837)
10. Burbrink F.T. 2002. Phylogeographic analysis of the cornsnake (Elaphe guttata) complex as inferred from maximum likelihood and Bayesian analyses. Mol. Phylogenet. Evol. 25:465-476. (Pubitemid 35371654)
11. Campbell J.A., Lamar W. 2004. The venomous reptiles of the western hemisphere. Ithaca (NY): Cornell University Press.
12. Carstens B.C., Dewey T 2010. Species delimitation using a combined coalescent and information-theoretic approach: an example from North American Myotis bats. Syst. Biol. 59:400-414.
13. Carstens B.C., Knowles L. 2007. Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an examplefrom Melanoplus grasshoppers. Syst. Biol. 56:400-411. (Pubitemid 46826903)
14. Castoe TA., Spencer C., Parkinson C.L. 2007. Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert biogeography Mol. Phylogenet. Evol. 42:193-212. (Pubitemid 44750714)
15. Creer S., Malhotra A., Thorpe R.S., Pook C.E. 2005. Targeting optimal introns for phylogenetic analyses in non-model taxa: experimental results in Asian pitvipers. Cladistics. 21:390-395. (Pubitemid 43899606)
16. Cummings M.P, Neel M.C., Shaw K.L. 2008. A genealogical approach to quantifying lineage divergence. Evolution. 62:2411-2422.
17. Dettman J.R., Jacobson DJ., Taylor J.W. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution. 57:2703-2720. (Pubitemid 38078353)
18. Douglas M.E., Douglas M.R., Schuett G.W., Porras L.W., Holycross A.T 2002. Phylogeography of the western rattlesnake (Crotalus viridis) complex, with emphasis on the Colorado Plateau. In: Schuett G. W., Hoggren M., Douglas M. E., Greene H. W., editors.) Biology of the vipers. Eagle Mountain (Utah): Eagle Mountain Publishing, LC. p. 11-50.
19. Douglas M.E., Douglas M.R., Schuett G.W., Porras L.W. 2006. Evolution of rattlesnakes (Viperidae: Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and Quaternary climate change. Mol. Ecol. 15:3353-3374. (Pubitemid 44379737)
20. Douglas M.E., Douglas M.R., Schuett G.W., Porras L.W., Thomason B.L. 2007. Genealogical concordance between mitochondrial and nuclear DNAs supports species recognition of the Panamint rattlesnake (Crotalus mitchellii stephensi). Copeia. 2007:920-932.
21. Drummond A.J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
22. Eckert A.J., Carstens B.C. 2008. Does gene fow destroy phylogenetic signal? The performance of three methods for estimating species phylogenies in the presence of gene fow. Mol. Phylogenet. Evol. 49:832-842.
23. Edwards S.V. 2009. Is a new and general theory of molecular systematics emerging? Evolution. 63:1-19.
24. Edwards S.V., Beerli P. 2000. Gene divergence, population divergence, and the variance in coalescent time in phylogeographic studies. Evolution. 54:1839-1854. (Pubitemid 32113816)
25. Edwards S.V., Liu L., Pearl D.K. 2007. High-resolution species trees without concatenation. Proc. Natl. Acad. Sci. U.S.A. 104:5936-5941. (Pubitemid 47175637)
26. Evans PD., Gloyd H.K. 1948. The subspecies of the massasauga, Sistrurus catenatus, in Missouri. Bull. Chicago Acad. Sci. 8:225-232.
27. Fontanella F.M., Feldman C.R., Siddall M.E., Burbrink F.T. 2008. Phylogeography of Diadophis punctatus: extensive lineage diversity and repeated patterns of historical demography in a trans-continental snake. Mol. Phylogenet. Evol. 46:1049-1070. (Pubitemid 351391938)
28. Friesen V.L., Congdon B.C., Kidd M.G., Birt T.P. 1999. Polymerase chain reaction (PCR) primers for the amplifcation of fve nuclear introns in vertebrates. Mol. Ecol. 8:2141-2152.
29. Gibbs H.L., Corey SJ., Blouin-Demers G., Prior K.A., Weatherhead PJ. 2006. Hybridization between mtDNA-defned phylogeographic lineages of black ratsnakes (Pantherophis sp.). Mol. Ecol. 15:3755-3767. (Pubitemid 44564283)
30. Gibbs H.L., Diaz J. 2010. Identifcation of single copy nuclear DNA markers for North American pit vipers. Mol. Ecol. Resour. 10:177-180.
31. Gibbs H.L., Murphy M., Chiucchi J. 2011. Genetic identity of endangered massasauga rattlesnakes (Sistrurus sp.) in Missouri. Conserv Genet. doi:10.1007/s10592-010-0151-3.
32. Gibbs H.L., Prior K., Weatherhead PJ., Johnnson G. 1997. Genetic structure of populations of the threatened eastern massasauga rattlesnake, Sistrurus c. catenatus: evidence from microsatellite DNA markers. Mol. Ecol. 6:1123-1132.
33. Gibbs H.L., Rossiter W 2008. Rapid evolution by positive selection and gene gain and loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J. Mol. Evol. 66:151-166.
34. Gibbs H.L., Sanz L., Calvete J.J. 2009. Snake population venomics: proteomics-based analyses of individual variation reveals signifcant gene regulation effects on venom protein expression in Sistrurus rattlesnakes. J. Mol. Evol. 68:113-125.
35. Gloyd H.K. 1935. The subspecies of Sistrurus miliarius. Occasional Papers, Museum of Zoology, University of Michigan 322:1-7.
36. Gloyd H.K. 1940. The Rattlesnakes, Genera Sistrurus and Crotalus. Special Publ. Chicago Acad. Sci. 4:104-118.
37. Gloyd H.K. 1955. A review of the massasaugas, Sistrurus catenatus, of the southwestern United States (Serpentes: Crotalidae). Bull. Chicago Acad. Sci. 10:83-98.
38. Gonçalvesa H., Mart́nez-Solanod I., Ferranda N., Garća-Paŕsc M. 2007. Conficting phylogenetic signal of nuclear vs mitochondrial DNA markers in midwife toads (Anura, Discoglossidae, Alytes): deep coalescence or ancestral hybridization? Mol. Phylogenet. Evol. 44:494-500.
39. Guiher TJ., Burbrink F.T. 2008. Demographic and phylogeographic histories of two venomous North American snakes of the genus Agkistrodon. Mol. Phylogenet. Evol. 48:543-553.
40. Harrigan RJ., Mazza M.E., Sorenson M.D. 2008. Computation versus cloning: evaluation of two methods for haplotype determination. Mol. Ecol. Resour. 8:1239-1248.
41. Heled J., Drummond A.J. 2010. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 27:570-580.
42. Hey J., Nielsen R. 2007. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. U.S.A. 104:2785-2790. (Pubitemid 46327957)
43. Holycross A.T, Mackessy S.P 2002. Variation in the diet of Sistrurus catenatus (massasauga) with emphasis on Sistrurus catenatus edwardsii (desert massasauga). J. Herpetol. 36:454-464. (Pubitemid 35161849)
44. Hudson R.R. 1992. Gene trees, species trees and the segregation of ancestral alleles. Genetics. 131:509-512.
45. Hudson R.R., Coyne J.A. 2002. Mathematical consequences of the genealogical species concept. Evolution. 56:1557-1565.
46. Hudson R.R., Turelli M. 2003. Stochasticity overrules the "three-times"rule: genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution. 57:182-190. (Pubitemid 36234340)
47. Huelsenbeck J.P, Hillis D.M., Nielsen R. 1996. A likelihood ratio test of monophyly Syst. Biol. 45:546-558.
48. Jennings W.B., Edwards S.V. 2005. Speciational history of Australian grass fnches (Poephila) inferred from 30 gene trees. Evolution. 59:2033-2047. (Pubitemid 41384386)
49. Klauber L.M. 1972. Rattlesnakes: their habits, life histories, and infuence on mankind. 2nd ed. Berkeley (CA): University of Califoria Press.
50. Knowles L.L., Carstens B.C. 2007. Delimiting species without monophyletic gene trees. Syst. Biol. 56:887-895. (Pubitemid 350129639)
51. Knowles L.L., Kubatko L.S. 2010. Estimating species trees: practical and theoretical aspects. Hoboken (NJ): Wiley-Blackwell.
52. Kosakovsky Pond S.L., Posada D., Gravenor M.B., Woelk C.H., Frost S.D.W. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol. 23:1891-1901. (Pubitemid 44412875)
53. Kubatko L.S., Carstens B.C., Knowles L.L. 2009. STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics. 25:971-973.
54. Kubatko L., Degnan J. 2007. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56(1): 17-24.
55. Kubatko L.S., Gibbs H.L. 2010. Estimating species relationships and taxon distinctiveness in Sistrurus rattlesnakes using multilocus data. In: Knowles L.L., Kubatko L.S., editors. Estimating species trees: practical and theoretical aspects. Hoboken (NJ): Wiley-Blackwell. p. 193-207.
56. Kuhner M.K. 2006. LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics. 22:768-770.
57. Lawson R. 1987. Molecular studies of thamnophiine snakes. 1. The phylogeny of the genus Nerodia. J. Herpetol. 21:140-157.
58. Leaché A.D. 2009. Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Syst. Biol. 58:547-559.
59. Leaché A.D. 2010. Species trees for spiny lizards (Genus Sceloporus): identifying points of concordance and confict between nuclear and mitochondrial data. Mol. Phylogenet. Evol. 54:162-171.
60. Leaché A.D., McGuire J. 2006. Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: evidence for a misleading mitochondrial gene tree. Mol. Phylogenet. Evol. 39:628-644.
61. Leaché A.D., Reeder T.W. 2002. Molecular systematics of the eastern fence lizard (Sceloporus undulatus): A comparison of parsimony, likelihood, and Bayesian approaches. Syst. Biol. 51:44-68. (Pubitemid 35169407)
62. Linnen C.R., Farrell B.D. 2007. Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera: Diprionidae) sawfies. Evolution. 61:1417-1438. (Pubitemid 46848827)
63. Liu L., Pearl D.K. 2007. Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. Syst. Biol. 56:504-514.
64. Liu L., Yu L., Kubatko L., Pearl D.K., Edwards S.V. 2009a. Coalescent methods for estimating multilocus phylogenetic trees. Mol. Phylogenet. Evol. 53:320-328.
65. Liu L., Yu L., Pearl D.K., Edwards S.V. 2009b. Estimating species phylogenies using coalescence times among sequences. Syst. Biol. 58: 468-477.
66. Mackessy S.P 2005. Desert Massasauga Rattlesnake (Sistrurus catenatus edwardsii): a technical conservation assessment. USDA Forest Service, Rocky Mountain Region. Available from: http://www.fs.fed.us/r2/projects/scp/ assessments/massasauga.pdf.
67. Maddison W.P 1997. Gene trees in species trees. Syst. Biol. 46:523-536.
68. Minin V., Abdo Z., Joyce P, Sullivan J. 2003. Performance-based selection of likelihood models for phylogeny estimation. Syst. Biol. 52:674-683. (Pubitemid 37365048)
69. Murphy R.W., Fu J., Lathrop A., Feltham J.V., Kovak V. 2002. Phylogeny of the rattlesnakes (Crotalus and Sistrurus) inferred from sequences of fve mitochondrial DNA genes. In: Schuett G.W., Hoggren M., Douglas M.E., Greene H.W., editors. Biology of the vipers. Eagle Mountain (Utah): Eagle Mountain Publishing, LC. p. 69-92.
70. O'Meara B.C. 2010. New heuristics methods for joint species tree inference and species delimitation. Syst. Biol. 59:59-73.
71. Parkinson C.L., Chippindale P, Campbell J. 2002. Multigene analyses of pitviper phylogeny with comments on their biogeographical history. In: Schuett G.W., Hoggren M., Douglas M.E., Greene H.W., editors. Biology of the vipers. Eagle Mountain (Utah): Eagle Mountain Publishing, LC. p. 93-110.
72. Parkinson C.L., Zamudio K.R., Greene H.W. 2000. Phylogeography of the pitviper clade Agkistrodon: historical ecology species status, and conservation of cantils. Mol. Ecol. 9:411-420. (Pubitemid 30215330)
73. Parmley D., Holman J.A. 2007. Earliest fossil record of a Pigmy rattlesnake (Viperidae: Sistrurus Garman). J. Herpet. 41:141-144. (Pubitemid 46761214)
74. Pook C.E., Wuster W., Thorpe R.S. 2000. Historicalbiogeography of the western rattlesnake (Serpentes: Viperidae: Crotalus viridis) inferred from mitochondrial DNA sequence information. Mol. Phylogenet. Evol. 15:269-282. (Pubitemid 30343204)
75. Ronquist F, Huelsenbeck J.P 2003. MrBayes 3: Bayesian phylogenetic inferenceundermixedmodels. Bioinformatics. 19:1572-1574.
76. Rosenberg N.A. 2003. The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model. Evolution. 57:1465-1477. (Pubitemid 36953636)
77. Rosenberg N.A. 2007. Statistical tests for taxonomic distinctiveness from observations of monophyly Evolution. 61:317-323. (Pubitemid 46411604)
78. Rozas J., Sanchez-Delbarrio J.C., Messeguer X., Rozas J. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19:2496-2497. (Pubitemid 38016658)
79. Sanz L., Gibbs H.L., Mackessy S.P, Calvete J.J. 2006. Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J. Proteome Res. 5:2098-2112. (Pubitemid 44330802)
80. Schelly R., Salzburger W., Koblmuller S., Duftner N., Sturmbauer C. 2005. Phylogenetic relationships of the lamprologine cichlid genus Lepidiolamprologus (Teleostei: Perciformes) based on mitochondrial and nuclear sequences, suggesting introgressive hybridization. Mol. Phylogenet. Evol. 38:426-438. (Pubitemid 43069387)
81. Schluter D. 2000. The ecology of adaptive radiation. Oxford (UK): Oxford University Press.
82. Serb J.M., Phillips C.A., Iverson J.B. 2001. Molecular phylogeny and biogeography of Kinosternon avescens based on complete mitochondrial control region sequences. Mol. Phylogenet. Evol. 18:149-162. (Pubitemid 32113886)
83. Soltis D.E., Morris A.B., McLachlan J.S., Manos P.S., Soltis P.S. 2006. Comparative phylogeography of unglaciated eastern North America. Mol. Ecol. 15:4261-4293. (Pubitemid 44749551)
84. Stephens M., Smith N., Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68:978-989. (Pubitemid 32289743)
85. Swofford D.L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland (MA): Sinauer Associates.
86. Szymanski J. 1998. Status assessment for the Eastern Massasauga (Sistrurus c. catenatus) 1998. Fort Snelling (MN): U.S. Fish and Wildlife Service, Endangered Species Division.
87. Than C., Nakhleh L. 2009. Species tree inference by minimizing deep coalescences. PLOS Comput. Biol. 5(9):e1000501.
88. US Federal Register 1996. Policy regarding the recognition of distinct vertebrate population segments under the Endangered Species Act. 61:4722. US Federal Register 1999. Endangered and threatened wildlife and plants. 64:57534.
89. Vidal N., Hedges S.B. 2002. Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies 325:987-995. (Pubitemid 35428761)
90. Weisrock D.W., Shaffer H.B., Storz B.L., Storz S.R., Voss S.R. 2006. Multiple nuclear gene sequences identify phylogenetic species boundaries in the rapidly radiating clade of Mexican ambystomatid salamanders. Mol. Ecol. 15:2489-2503. (Pubitemid 44050719)
91. Wiens J.J., Kuczynski C.A., Smith S.A., Mulcahy D.G., Sites Jr. J.W., Townsend T.M., Reeder T.W. 2008. Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Syst. Biol. 57:420-431. (Pubitemid 351882203)
92. Wiens J.J., Penkrot T.A. 2002. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51:69-91. (Pubitemid 35169408)
93. Yang Z. 2002. Likelihood and Bayes estimation of ancestral population sizes in Hominoids using data from multiple loci. Genetics. 162:1811-1823. (Pubitemid 36114665)
94. Yang Z., Rannala B. 2010. Bayesian species delimitation using multilocus sequence data. Proc. Natl. Acad. Sci. U.S.A. 107:9264-9269.