Conflicting mitochondrial and nuclear phylogenies for the widely disjunct emys (testudines: emydidae) species complex, and what they tell us about biogeography and hybridization

Systematic Biology

Volumn 58, Issue 1, 2009, Pages 1-20

  Spinks, Phillip Q ^a   Shaffer, H Bradley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actinemys; Clemmys; Emydoidea; Emys; Hnf i ; Nuclear phylogeny; R35; RELN.

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CELL NUCLEUS; CLASSIFICATION; GENETICS; PHYLOGENY; TURTLE;

ANIMALS; CELL NUCLEUS; DNA, MITOCHONDRIAL; PHYLOGENY; TURTLES;

ACTINEMYS; CLEMMYS; EMYDIDAE; EMYDOIDEA; EMYS; EMYS ORBICULARIS; TESTUDINES;

EID: 67449151608     PISSN: 10635157     EISSN: 1076836X     Source Type: Journal    
DOI: 10.1093/sysbio/syp005     Document Type: Article

References (113)

1. Avise J.C., Arnold J., Ball R.M., Bermingham E., Lamb T., Nigel J.E., Reeb CA., Saunders N.C. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann. Rev. Ecol. Syst. 18:489-522.
2. Ballard J.W.O., Kreitman M. 1995. Is mitochondrial DNA a strictly neutral marker? Trends. Evol. Ecol. 12:485-488.
3. Ballard J.W.O., Rand D.M. 2005. The population biology of mitochondrial DNA and its phyiogenetic implications. Ann. Rev. Ecol. Evol. Syst. 36:621-642.
4. Ballard J.W.O., Whitlock M.C. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13:729-744.
5. Bernatchez L., Glémet H., Wilson C.A., Danzmann R.G. 1995. Introgression and fixation of arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 52:179-185.
6. Bhangale T.R., Rieder M.J., Livingston R. J., Nickerson D.A. 2005. Comprehensive identification and characterization of diallelic insertiondeletion polymorphisms in 330 human candidate genes. Hum. Mol. Gen. 14:59-69.
7. Bickham J.W., Lamb T., Minx P., Patton J.C. 1996. Molecular systematics of the genus Clemmys and the intergeneric relationships of emydid turtles. Herpetologica. 52:89-97.
8. Brattstrom B.H., Sturn A. 1959. A new species of fossil turtle from the Pliocene of Oregon, with notes on other fossil Clemmys from western North America. Bull. So. Cal. Acad. Sci. 58:65-71.
9. Brown J.M., Hedtke S.M., Lemmon A.R., Lemmon E.M. 2009. When trees grow too long: investigating the causes of highly inaccurate bayesian branch-length estimates. Syst. Biol. In press.
10. Buckley T.R., Cordeiro M., Marshall D.C., Simon C. 2006. Differentiating between hypotheses of lineage sorting and introgression in New Zealand alpine cicadas (Maoricicada Dugdale). Syst. Biol. 55: 411-425.
11. Burbrink F.T., Lawson R. 2007. How and when did Old World ratsnakes disperse into the New World? Mol. Phylogenet. Evo. 43: 173-189.
12. Burke R.L., Leuteritz T.E., WoIf A.J. 1996. Phyiogenetic relationships of emydine turtles. Herpetologica. 52:572-584.
13. Buschbom J., Barker D. 2006. Evolutionary history of vegetative reproduction in Porpidia s.l. (lichen-forming Ascomycota). Syst. Biol. 55:471-484.
14. ChanK.M.A.,LevinS.A.2005.Leakyprezygoticisolationandporousgenomes: rapidintrogressionofmaternallyinheritedDNA.Evolution.59:720-729. (Pubitemid40589284)
15. Chippindale P.T., Wiens J.J. 1994. Weighting, partitioning, and combining characters in phyiogenetic analysis. Syst. Biol. 43: 278-287.
16. Conant R., Collins J.T. 1991. A field guide to reptiles and amphibians of eastern and central North America. Boston: Houghton Mifflin.
17. Danilov I.G. 2005. Die fossilen Schildkröten Europas. In: Fritz U., editor. Handbuch der Reptilien und Amphibien Europas. Schildkröten II (Cheloniidae, Dermochelyidae, Fossile Schildkröten). Wiebeisheim (Germany): Aula p. 329-441.
18. Degnan J.H., Rosenberg N.A. 2006. Discordance of species trees with their most likely gene trees. PLOS. Genet. 2:762-768.
19. Doyle J.A., Donoghue M.J. 1993. Phytogenies and angiosperm diversification. Paleobiology. 19:141-167.
20. Edwards S.V., Liu L., Pearl D.K. 2007. High-resolution species trees without concatenation. Proc. Natl. Acad. Sci. USA. 104:5936-5941.
21. Engstrom T.N., Shaffer H.B., McCord W.P. 2004. Multiple data sets, high homoplasy, and the phytogeny of softshell turtles (Testudines: Trioinychidae). Syst. Biol. 53:693-710. (Pubitemid 39568274)
22. Ernst C.H., Barbour R.W. 1989. Turtles of the world. Washington (DC): Smithsonian Institution Press.
23. Ernst C.H., Lovich J.E., Barbour R.W. 1994. Turtles of the United States and Canada. Washington, D.C.: Smithsonian Institution Press.
24. Feldman C.R., Parham J.F. 2002. Molecular phylogenetics of emydine turtles: taxonomic revision and the evolution of shell kinesis. Mol. Phylogenet. Evol. 22:388-398.
25. Felsenstein J. 1985. Confidence limits on phytogenies: an approach using the bootstrap. Evolution. 39:783-791.
26. Felsenstein J. 1988. Phytogenies from molecular sequences: inference and reliability. Ann. Rev. Genet. 22:521-565.
27. Felsenstein J. 1993. PHYLIP: phyiogenetic inference package. Version 3.5d. Seattle (WA): University of Washington.
28. Ferris S.D., Sage R.D., Huang C., Nielsen J.T., Ritte U., Wilson A.C. 1983. Flow of mitochondrial DNA across a species boundary. Proc. Natl. Acad. Sci. USA. 80:2290-2294.
29. Fritz U. 1998. Introduction to zoogeography and subspecific differentiation in Emys orbicularis (Linnaeus, 1758). Proceedings of the Emys symposium; 1996 Oct. 4-6; Dresden, Germany. Rheinbach (Germany): Deutsche Gesellschaft fr Herpetologie und Terrarienkunde, p. 1-28.
30. Fritz U., d'Angelo S., Pennisi M.G., Lo Valvo M. 2006. Variation of Sicilian pond turtles, Emys trinacris-what makes a species cryptic? Amphibia-Reptilia. 27:513-529.
31. Fritz U., Fattizzo T., Guicking D., Tripepi S., Pennisi M.G., Lenk P., Roger U., Wink M. 2005. A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudnies, Emydidae). Zool. Scripta. 34:351-371.
32. Fujita M.F., Engstrom T.N., Starkey D.E., Shaffer H.B. 2004. Turtle phytogeny: insights from a novel nuclear intron. Mol. Phylogenet. Evol. 31:1031-1040.
33. Funk D.J., Omland K.E. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Ann. Rev. Ecol. Evol. Syst. 34:397-423.
34. Gadagkar S.R., Rosenberg M.S, Kumar S. 2005. Inferring species phytogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J. Exp. Zool. 304B:64-74. (Pubitemid 40346325)
35. Gaffney E.S., Meylan P.A. 1988. A phytogeny of turtles. In: Benton M.J., editor. Phytogeny and classification of the tetrapods. Oxford: Clarendon Press.p. 157-219.
36. Gerber A.S., Loggins R., Kumar S., Dowling T.E. 2001. Does nonneutral evolution shape observed patterns of DNA variation in animal mitochondrial genomes? Ann. Rev. Genet. 35:539-566.
37. Good J.M., Hird S., Reid N., Demboski J., Steppan S.J., MartinNims T.R., Sullivan J. 2008. Ancient hybridization and mitochondrial capture between two species of chipmunks. Mol. Ecol. 17: 1313-1327.
38. Graur D., Martin W. 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends. Genet. 20:80-86.
39. Gustafson E.P. 1978. The vertebrate faunas of the Pliocene Ringold Formation, south-central Washington. Bull. Mus. Nat. Hist. Oregon. 23:1-62.
40. Hedges S.B., Kumar S. 2004. Precision of molecular time estimates. Trends. Genet. 20:242-247.
41. Hey J. 2004. HKA (a computer program for tests of natural selection). Available from: URL http://lifesci.rutgers.edu/heylab/~heylab/ heylabsoftware.htm#HKA. Newark (NJ): Rutgers University.
42. Holbrook J.E. 1842. North American herpetology. Facsimile Reprints in Herpetology [reprinted in 1976 by Society for the Study of Amphibians and Reptiles]. Philadelphia (PA): J. Dobson.
43. Holder M.T., Anderson J.A., Holloway A.K. 2001. Difficulties in detecting hybridization. Syst. Biol. 50:978-982.
44. Holman J.A. 1995. A new species of Emydoidea (Reptilia: Testudines) from the late Barstovian (Medial Miocene) of Cherry County, Nebraska. J. Herpetol. 29:548-553.
45. Holman J.A. 2002. The status of Emydoidea hutchisoni Holman, 1995 (Testudines:Emydidae). Mich. Academician. 2:393-394.
46. Holman J.A., Fritz U. 2001. A new emydine species from the Medial Miocene (Barstovian) of Nebraska, USA with a new generic arrangement for the species of Clemmys sunsu McDowell (1964) (Reptilia: Testudines: Emydidae). Zool. Abh. 51:321-344.
47. Holman J.A., Parmlee D. 2005. Noteworthy turtle remains from the Late Miocene (Late Hemphillian) of northeastern Nebraska. Tex. J. Sci. 57:307-310.
48. Hudson R.R., Kreitman M., Aquadé M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics. 116: 153-159.
49. Hudson R.R., Coyne J.A. 2002. Mathematical consequences of the genealogical species concept. Evolution. 56:1557-1565.
50. Huelsenbeck J.P., Rannala B. 2004. Frequentist properties of Bayesian posterior probabilities of phyiogenetic trees under simple and complex substitution models. Syst. Biol. 53:904-913.
51. Huelsenbeck J.P., Ronquist F. 2001. MRBAYES: Bayesian inference of phytogeny. Bioinformatics. 17:754-755.
52. Hutchison J. 1981. Emydoidea (Emydinae, Testudines) from the Barstovian (Miocene) of Nebraska. Paleobios. 37:1-6.
53. Kass R.E., Raftery A.E. 1995. Bayes factors. J. Am. Stat. Assoc. 90: 773-795.
54. KelloggE.A.,AppelsR.,Mason-GamerR.J.1996.Whengenestelldifferentstories: thediploidgeneraofTriticeae(Gramineae).Syst.Bot.21:321-347.(Pubitemid27185796)
55. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
56. Krenz J.G., Naylor G.J.P., Shaffer H.B., Janzen F.J. 2005. Molecular phylogenetics and evolution of turtles. Mol. Phylogenet. Evol. 37: 178-191.
57. Leaché A.D., McGuire J.A. 2006. Phyiogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: evidence for a misleading mitochondrial gene tree. Mol. Phylogenet. Evol. 39:628-644.
58. Lenk P., Fritz U., Joger U., Wink M. 1999. Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Mol. Ecol. 8:1911-1922.
59. Linnen CR., Farrell B.D. 2007. Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera:Diprionidae) sawflies. Evolution. 61:1417-1438.
60. Liu L., Pearl D.K. 2007. Species trees from gene trees: reconstructing Bayesian posterior distributions of species phytogeny using estimated gene tree distributions. Syst. Biol. 56:504-514.
61. Maddison W.P., Maddison D.R. 2003. MacClade. Sunderland (MA): Sinauer Associates.
62. Marshall D.C., Simon C., Buckley T.R. 2006. Accurate branch length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch length priors. Syst. Biol. 55:993-1003.
63. Melo-Ferreira J., Boursot P., Randi E., Kryukov A., Suchentrunk F., Ferrand N., Alves P.C. 2007. The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Mol. Ecol. 16: 605-618.
64. Melo-Ferreira J., Boursot P., Suchentrunk F., Ferrand N., Alves P.C. 2005. Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in Northern Iberia. Mol. Ecol. 14:2459-2464.
65. Miller R.E., Buckley T.R., Manos P.S. 2002. An examination of the monophyly of morning glory taxa using Bayesian phyiogenetic inference. Syst. Biol. 51:740-753.
66. Minin V., Abdo Z., Joyce P., Sullivan J. 2003. Performance-based selection of likelihood models for phytogeny estimation. Syst. Biol. 52:674-683.
67. Mockford S.W., Herman T.B., Snyder M., Wright J.M. 2006. Conservation genetics of Blanding's turtle (Emydoidea blandingii) and its application in the identification of evolutionarily significant units. Conserv. Gen. 8:209-219.
68. Mockford S.W., McEachern L., Herman T.B., Snyder M., Wright J.M. 2005. Population genetic structure of a disjunct population of Blanding's turtle (Emydoidea blandingii) in Nova Scotia. Biol. Conserv. 123:373-380.
69. Moritz C., Dowling T.E., Brown W.M. 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Ann. Rev. Ecol. Syst. 18:269-292.
70. Near T.J., Meylan P.A., Shaffer H.B. 2005. Assessing concordance of fossil calibration points in molecular clock studies: An example using turtles. Am. Nat. 165:137-146.
71. Nee S., May R.M., Harvey P.H. 1994. The reconstructed evolutionary process. Phil. Trans. R. Soc. Lond. B, 344:305-311.
72. Nylander J.A.A., Ronquist F., Huelsenbeck J.P., Nieves-Aldrey J.L. 2004. Bayesian phyiogenetic analysis of combined data. Syst. Biol. 53:47-67.
73. Pamilo P., Nei M. 1988. Relationships between gene trees and species trees. Mol. Biol. Evol. 5:568-583.
74. Parham J.F., Feldman C.R. 2002. Generic revisions of emydine turtles. Turtle Tortoise Newslett. 6:28-30.
75. Parham J.F., Feldman C.R., Boore J.L. 2006. The complete mitochondrial genome of the enigmatic bigheaded turtle (Platystemon): description of unusual genomic features and the reconciliation of phyiogenetic hypotheses based on mitochondrial and nuclear DNA. BMC. Evol. Biol. 6:11.
76. Parham J.F., Türkozan O., Stuart B.L., Arakelyan M., Shafei S., Papenfuss T.J. 2006. Genetic evidence for premature taxonomie inflation in Middle Eastern tortoises. Proc. Cal. Acad. Sci. 57:955-964.
77. Peters J.L., Zhuravlev Y., Fefelov L., Logie A., Omland K.E. 2007. Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.). Evolution 61:1992-2006.
78. Pollard D., Iyer V.N., Moses A.M., Eisen M.B. 2006. Whole genome phytogeny of the Drosophila melanogaster species subgroup: widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. PLoS. Genet. 2(10):el73.
79. PosadaD.,CrandallK.A.1998.Modeltest:testingthemodelofDNAsubstitution. Bioinformatics.14:817-818.(Pubitemid28552116)
80. Primmer C.R., Borge T., Lindell J., Saatre G.P. 2002. Single nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol. Ecol. 11:603-612.
81. Rambaut A., Drummond A.J. 2007. Tracer version 1.4. Available from: URL http://beast.bio.ed.ac.uk/Tracer.
82. Rand D.M. 2001. The units of selection on mitochondrial DNA. Ann. Rev. Ecol. Syst. 32:415-448.
83. Robertson A.V., Ramsden C., Niedzwiecki J., Fu J., Bogart J.P. 2006. An unexpected recent ancestor of unisexual Ambystoma. Mol. Ecol. 15:3339-3351. (Pubitemid 44379736)
84. Ronquist F., Huelsenbeck J.P. 2003. MRBAYES 3: Bayesian phyiogenetic inference under mixed models. Bioinformatics. 19:1572-1574. (Pubitemid 37038874)
85. 4 photosynthetic syndrome. Plant. Biol. 3:202-213.
86. Sambrook J., Russell D.W. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
87. Sanderson M.J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19:101-109.
88. 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. (Pubitemid 36181923)
89. Sanderson M.J., Shaffer H.B. 2002. Troubleshooting molecular phyiogenetic analyses. Ann. Rev. Ecol. Syst. 33:49-72.
90. Sanmarti I., Enghoff H., Ronquist F. 2001. Patterns of animal dispersal, vicariance and diversification in the holarctic. Bio. J. Linn. Soc. 73:345-390.
91. Shaffer H.B., Clark J.M, Kraus F. 1991. When molecules and morphology clash: a phyiogenetic analysis of the North American ambystomatid salamanders (Caudata: Ambystomatidae). Syst. Biol. 40:284-303.
92. Shaffer H.B., Meylan P., McKnight M.L. 1997. Tests of turtle phytogeny: molecular, morphological, and paleontological approaches. Syst. Biol. 46:235-268.
93. Shaffer H.B., Thomson R.C. 2007. Using single nucleotide polymorphisms (SNPs) to delimit species in recent radiations. Syst. Biol. 56: 896-906.
94. Shaw K. 2002. Conflict between nuclear and mitochondrial DNA phytogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc. Natl. Acad. Sci. USA. 25:16122-16127.
95. Spinks P.Q., Shaffer H.B. 2005. Rangewide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Mol. Ecol. 14: 2047-2064.
96. Spinks P.Q., Shaffer H.B. 2007. Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conserv. Genet. 8:641-657.
97. Spinks P.Q., Shaffer H.B., Iverson J.B., McCord W.P. 2004. Phyiogenetic hypotheses for the turtle family Geoemydidae. Mol. Phylogenet. Evol. 32:164-182.
98. Stamatakis A., Hoover P., Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web-servers. Syst. Biol. 75: 758-771.
99. Steiner S., Tilak M., Douzery E.J.P., Catzeflis F.M. 2005. New DNA data from a transthyretin nuclear intron suggests an Oligocene to Miocene diversification of living South America opossums (Marsupialia: Didelphidae). Mol. Phylogenet. Evol. 35:363-379.
100. Stephens M., Donnelly P. 2003. A comparison of bayesian methods for haplotype reconstruction. Am. J. Hum. Genet. 73:1162-1169.
101. Stephens M., Smith N.J., Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68:978-989.
102. Stephens P.R., Wiens J.J. 2003. Ecological diversification and phytogeny of emydid turtles. Biol. J. Linn. Soc. 79:577-610.
103. *: phyiogenetic analysis using parsimony (*and other methods). Sunderland, MA; Sinauer Associates.
104. Thomson R.C., Shedlock A.M., Edwards S.V., Shaffer H.B. 2008. Developing markers for multilocus phylogenetics in non-model organisms: A test case with turtles. Mol. Phylogenet. Evol. 49:514-525.
105. Turtle Taxonomy Working Group. 2007a. An annotated list of modern turtle terminal taxa, with comments on areas of taxonomic instability and recent change. In: Shaffer H.B., FitzSimmons N.N., Georges A., Rhodin A.G.J., editors. Defining turtle diversity: Proceedings of a workshop on genetics, ethics, and taxonomy of freshwater turtles and tortoises. Chelonian Research Monographs No. 4. Lunenburg (MA): Chelonian Research Foundation, p. 173-199.
106. Turtle Taxonomy Working Group. 2007b. Turtle taxonomy: methodology, recommendations, and guidelines. In: Shaffer H.B., FitzSimmons N.N., Georges A., Rhodin A.G.J., editors. Defining turtle diversity: Proceedings of a workshop on genetics, ethics, and taxonomy of freshwater turtles and tortoises. Chelonian Research Monographs No. 4. Lunenburg (MA): Chelonian Research Foundation, p. 73-84.
107. Webb S.D. 1977. A history of savanna vertebrates in the New World. Part I: North America. Ann. Rev. Ecol. Syst. 8:355-380.
108. Wilson C.C, Bernatchez L. 1998. The ghost of hybrids past: fixation of arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush). Mol. Ecol. Notes. 7:127-132.
109. Yang Z., Rannala, B. 2005. Branch-Length Prior Influences Bayesian Posterior Probability of Phytogeny. Syst. Biol. 54:455-470.
110. Zachos J., Pagani M., Sloan L., Thomas E., Billups K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science. 292:686-693. (Pubitemid 32385533)
111. Zhang A., Sota T. 2007. Nuclear gene sequences resolve species phytogeny and mitochondrial introgression in Leptocarabus beetles showing trans-species polymorphisms. Mol. Phylogenet. Evol. 45:534-546.
112. Zhang D.X., Hewitt G.M. 2003. Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol. Ecol. 12:563-584.
113. Zug G.R. 1969. Fossil Chelonians, Chrysemys and Clemmys, from the Upper Pliocene of Idaho. Great. Basin. Nat. 29:82-87.