Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea)

Molecular Phylogenetics and Evolution

Volumn 63, Issue 1, 2012, Pages 28-42

  Aschliman, Neil C ^a,d   Nishida, Mutsumi ^b   Miya, Masaki ^c   Inoue, Jun G ^b   Rosana, Kerri M ^a   Naylor, Gavin J P ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATURAL HISTORY MUSEUM AND INSTITUTE   (Japan)

^d ST AMBROSE UNIVERSITY   (United States)

Author keywords

Batoidea; Convergence; Divergence times; Mass extinction; Mitochondrial genomes; Partition testing

Indexed keywords

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; FOSSIL; GENETICS; HISTOLOGY; MITOCHONDRIAL GENOME; PHYLOGENY; SKATES (FISH);

ANIMALS; BAYES THEOREM; BIOLOGICAL EVOLUTION; CELL NUCLEUS; FOSSILS; GENOME, MITOCHONDRIAL; MODELS, GENETIC; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SKATES (FISH);

BATOIDEA; CHONDRICHTHYES; DASYATIDAE; GNATHOSTOMATA (VERTEBRATE); PISCES; PRISTIDAE; VERTEBRATA;

EID: 84857232002     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.12.012     Document Type: Article

References (98)

1. Adachi J., Hasegawa M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 1996, 42:459-468.
2. Altekar G., Dwarkadas S., Huelsenbeck J.P., Ronquist F. Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 2004, 20:407-415.
3. Amores A., Suzuki T., Yan Y.L., Pomeroy J., Singer A., Amemiya C., Postlethwaite J.H. Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res. 2004, 14:1-10.
4. Benton M.J., Emerson B.C. How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology 2007, 50:23-40.
5. Carroll R.L. Vertebrate Paleontology and Evolution 1988, W.H. Freeman and Company, New York, pp. 62-83.
6. Carvalho M.R. Higher-level elasmobranch phylogeny, basal squaleans, and paraphyly. Interrelationships of Fishes 1996, 35-62. Academic Press, London. M.J. Stiassny, L.R. Parenti, G.D. Johnson (Eds.).
7. Carvalho, M.R., 2004. A Late Cretaceous thornback ray from southern Italy, with a phylogenetic reappraisal of the Platyrhinidae (Chondrichthyes: Batoidea). In: Arriata, G., Tintori, A. (Eds.), Mesozoic Fishes 3. Verlag Dr Friedrich Pfiel, München, pp. 75-100.
8. Chiu C., Amemiya C., Dewer K., Kim C.B., Ruddle F.H., Wagner G.P. Molecular evolution of the HoxA cluster in three major gnathostome lineages. Proc. Natl. Acad. Sci. - Biol. 2002, 99:5492-5497.
9. Chiu C., Dewar K., Wagner G.P., Takahashi K., Ruddle F., Ledje C., Bartsch P., Scemama J.L., Stellwag E., Fried C., Prohaska S.J., Stadler P.F., Amemiya C.T. Bichir HoxA cluster sequence reveals surprising trends in ray-finned fish genomic evolution. Genome Res. 2004, 14:11-17.
10. Compagno L.J.V. Interrelationships of living elasmobranchs. Interrelationships of Fishes 1973, 15-61. Academic Press, London. P.H. Greenwood, R.S. Miles, C. Patterson (Eds.).
11. Compagno, L.J.V., 1999. Systematics and body form. In: Hamlett, W.C. (Ed.), Sharks, Skates, and Rays: The Biology of Elasmobranch Fishes. The Johns Hopkins University Press, Baltimore, MD, pp. 1-42.
12. Compagno, L.J.V., 2005. Checklist of living chondrichthyan fishes. In: Fowler, S.L., Cavanagh, R.D., Camhi, M., Burgess, G.H., Caillet, G.M., Fordham, S.V., Simpfendorfer, C.A., Musick, J.A. (Eds.), Sharks, Rays, and Chimaeras: The Status of the Chondrichthyan Fishes. Status Survey. IUCN, Gland, Switzerland and Cambridge, UK, pp. 401-423.
13. Compagno, L.J.V., Last, P.R., Stevens, J.D., Alava, M.N.R., 2005. Checklist of Philippine Chondrichthyans. CSIRO Marine Laboratories Report 243. CSIRO Marine and Atmospheric Research. p. 61.
14. Crisp M.D., Cook L.G. Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 2009, 63:2257-2265.
15. Cusimano N., Renner S.S. Slowdowns in diversification rates from real phylogenies may not be real. Syst. Biol. 2010, 59:458-464.
16. Davy H. An account of some experiments on the Torpedo. Philos. Trans. Roy. Soc. B 1829, 119:15-18.
17. Delsate D., Candoni L. Description de nouveaux morphotypes dentaires de Batomorphii toarciens (Jurassique inférieur) de Bassin de Paris: Archaeobatidae nov. Fam. Bulletin dela Société Naturelle de Luxembourg 2001, 102:131-143.
18. Do C.B., Mahabhashyam M.S.P., Brudno M., Batzoglou S. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 2005, 15:330-340.
19. Donoghue P.C.J., Benton M.J. Rocks and clocks: calibrating the tree of life using fossils and molecules. Tree 2007, 22:424-431.
20. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
21. Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4:e88.
22. Dulvy N.K., Reynolds J.D. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proc. Roy. Soc. B - Biol. Sci. 1997, 264:1309-1315.
23. Dunn K.A., McEachran J.D., Honeycutt R.L. Molecular phylogenetics of myliobatiform fishes (Chondrichthyes: Myliobatiformes), with comments on the effects of missing data on parsimony and likelihood. Mol. Phylogen. Evol. 2003, 27:259-270.
24. Ellis J.Y., Morrison D.A., Avery D., Johnson A.M. Codon usage and bias among individual genes of the coccidian and piroplasms. Parasitology 1994, 109:265-272.
25. Fedrigo O., Adams D.C., Naylor G.J. DRUIDS-Detection of regions with unexpected internal deviation from stationarity. J. Exp. Zool. B: Mol. Dev. Evol. 2005, 304:119-128.
26. Felsenstein, J., 2004. PHYLIP (Phylogeny Inference Package) version 3.6. http://evolution.genetics.washington.edu/phylip/.
27. Garman S. The Plagiostoma (sharks, skates, and rays). Mem. Mus. Compar. Zoöl. Harvard College 1913, 36:1-528.
28. González-Isáis M., Domínguez H.M.M. Comparative anatomy of the superfamily Myliobatoidea (Chondrichthyes) with some comments on phylogeny. J. Morphol. 2004, 262:517-535.
29. Gould S.J., Raup D.M., Sepkoski J.J., Schopf T.J.M., Simberloff D.S. The shape of evolution: a comparison of real and random clades. Paleobiology 1977, 3:23-40.
30. Heemstra P.C., Smith M.M. Hexatrygonidae, a new family of stingrays (Myliobatiformes: Batoidea) from South Africa, with comments on the classification of batoid fishes. Ichthyological Bulletin of the J.L.B. Smith Inst. Ichthyol. 1980, 43:1-17.
31. Hillis D.M. Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 1998, 47:3-8.
32. Hoegg S., Meyer A. Hox clusters as models for vertebrate genome evolution. Trends Genet. 2005, 21:421-424.
33. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
34. Hugall A.F., Foster R., Lee M.S.Y. Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst. Biol. 2007, 56:543-563.
35. Human B.A., Owen E.P., Compagno L.J.V., Harley E.H. Testing morphologically based phylogenetic theories within the cartilaginous fishes with molecular data, with special reference to the catshark family (Chondrichthyes; Scyliorhinidae) and the interrelationships within them. Mol. Phylogen. Evol. 2006, 39:384-391.
36. Inoue J.G., Miya M., Tsukamoto K., Nishida M. Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the "ancient fish" Mol. Phylogen. Evol. 2003, 26:110-120.
37. Inoue J., Donoghue P.C.J., Yang Z. The impact of the representation of fossil calibrations on Bayesian estimation of species divergence times. Syst. Biol. 2010, 59:74-89.
38. Inoue, J.G., Miya, M., Lam, K., Tay, B.-H., Danks, J.A., Bell, J., Walker, T.I., Venkatesh, B., 2010b. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol. Biol. Evol., Advance Access 10.1093/molbev/msq147.
39. Kim C.B., Amemiya C., Bailey W., Kawasaki K., Mezey J., Miller W., Minoshima S., Shimizu N., Wagner G., Ruddle F. Hox cluster genomics in the horn shark, Heterodontus francisci. Proc. Nat. Acad. Sci. USA 2000, 97:1655-1660.
40. Kriwet, J., 2004. The systematic position of the Cretaceous sclerorhynchid sawfishes (Elasmobranchii, Pristiorajea). In: Arriata, G., Tintori, A. (Eds.), Mesozoic Fishes 3. Verlag Dr Friedrich Pfiel, München, pp. 57-73.
41. Kriwet J., Benton M.J. Neoselachian (Chondrichthyes, Elasmobranchii) diversity across the Cretaceous-Tertiary boundary. Palaeogeogr. Palaeocl. 2004, 214:181-194.
42. Last P.R., Séret B. Three new legskates of the genus Sinobatis (Rajoidei: Anacanthobatidae) from the Indo-West Pacific. Zootaxa 2008, 1671:33-58.
43. Last P.R., Stevens J.D. Sharks and Rays of Australia 2009, CSIRO Publishing, Australia, 640pp.
44. Lemmon A.R., Brown J.M., Stanger-Hall K., Lemmon E.M. The effect of ambiguous data on phylogenetic estimates obtained by Maximum Likelihood and Bayesian inference. Syst. Biol. 2009, 58:130-145.
45. Leviton A.E., Gibbs R.H., Heal E., Dawson C.E. Standards in herpetology and ichthyology: part 1 Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia 1985, 1985:802-832.
46. Li C., Ortí G., Zhang G., Lu G. A practical approach to phylogenomics: The phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 2007, 7:44.
47. Li C., Lu G., Ortí G. Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci. Syst. Biol. 2008, 57:519-539.
48. Lisney T.J., Yopak K.E., Montgomery J.C., Collin S.C. Variation in brain organization and cerebellar foliation in chondrichthyans: batoids. Brain Behav. Evol. 2008, 72:262-282.
49. Long M., Gillespie J. Codon usage divergence of homologous vertebrate genes and codon usage clock. J. Mol. Evol. 1991, 32:6-15.
50. Lovejoy N.R. Systematics of myliobatoid elasmobranchs: with emphasis on the phylogeny and historical biogeography of neotropical freshwater stingrays (Potamotrygonidae: Rajiformes). Zool. J. Linn. Soc. - Lond. 1996, 117:207-257.
51. Lovejoy N.R., Bermingham E., Martin A.P. Marine incursion into South America. Nature 1998, 296:421-422.
52. Maisey, J.G., Naylor, G.J.P., Ward, D.J., 2004. Mesozoic elasmobranchs, neoselachian phylogeny and the rise of modern elasmobranch diversity. In: Arriata, G., Tintori, A. (Eds.), Mesozoic Fishes 3. Verlag Dr Friedrich Pfiel, München, pp. 17-56.
53. Manzanares M., Bel-Vialar S., Ariza-McNaughton L., Ferretti E., Marshall H., Maconochie M.M., Blasi F., Krumlauf R. Independent regulation of initiation and maintenance of phases of Hoxa3 expression in the vertebrate hindbrain involve auto- and cross-regulatory mechanisms. Development 2001, 128:3595-3607.
54. Marshall C. A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibration points. Am. Nat. 2008, 171:726-742.
55. McComb D.M., Kajiura S.M. Visual fields for four batoid fishes: a comparative study. J. Exp. Biol. 2008, 211:482-490.
56. McEachran J.D., Aschliman N. Phylogeny of Batoidea. Biology of Sharks and Their Relatives 2004, 79-113. CRC Press, Boca Raton, FL. J.C. Carrier, J.A. Musick, M.R. Heithaus (Eds.).
57. McEachran J.D., Dunn K.A. Phylogenetic analysis of skates, a morphologically conservative clade of elasmobranchs (Chondrichthyes: Rajidae). Copeia 1998, 1998:271-290.
58. McEachran, J.D., Miyake, T., 1990. Phylogenetic interrelationships of skates: a working hypothesis (Chondrichthyes: Rajoidei). In: Pratt, H.L., Gruber, S.H., Taniuchi T. (Eds.), NOAA Technical Report NMFS 90, Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries, pp. 285-304.
59. McEachran J.D., Dunn K.A., Miyake T. Interrelationships of the batoid fishes (Chondrichthyes: Batoidea). Interrelationships of Fishes 1996, 63-82. Academic Press, London. M.J. Stiassny, L.R. Parenti, G.D. Johnson (Eds.).
60. Miya M., Nishida M. Organization of the mitochondrial genome of a deep-sea fish, Gonostoma gracile (Teleostei: Stomiiformes): first example of transfer RNA gene rearrangements in bony fishes. Mar. Biotechnol. 1999, 1:416-426.
61. Miya M., Takeshima H., Endo H., Ishiguro N.B., Inoue J.G., Mukai T., Satoh T.P., Yamaguchi M., Kawaguchi A., Mabuchi K., Shirai S.M., Nishida M. Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol. Phylogen. Evol. 2003, 26:121-138.
62. Naylor G.J.P., Ryburn J.A., Fedrigo O., Lopez A. Phylogenetic relationships among the major lineages of modern elasmobranchs. Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, batoids, and chimaeras 2005, vol. 3:1-25. Science Publishers, Inc., Enfield, NH.
63. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T., Last, P.R. (accepted for publication). A DNA sequence based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull. Amer. Mus. Nat. Hist.
64. Near T.J., Sanderson M.J. Assessing the quality of molecular divergence time estimates by fossil calibrations and fossil-based model selection. Philos. Trans. Roy. Soc. B - Biol. Sci. 2004, 359:1477-1483.
65. Near T.J., Meylan P.A., Shaffer H.B. Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am. Nat. 2005, 165:137-146.
66. Nelson, J.S., 2006. Fishes of the world, fourth ed. John Wiley and Sons, Inc. Hoboken, New Jersey, USA, 601p.
67. Neyt C., Jagla K., Thisse C., Thisse B., Haines L., Currie P.D. Evolutionary origins of vertebrate appendicular muscle. Nature 2000, 408:82-86.
68. Nishida K. Phylogeny of the suborder Myliobatoidei. Mem. Facul. Fish., Hokkaido Univ. 1990, 37:1-108.
69. Nylander J.A.A., Wilgenbush J.C., Warren D.L., Swofford D.L. AWTY (Are We There Yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 2008, 24:581-583.
70. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
71. Powers T.P., Amemiya C.T. Evolutionary plasticity of vertebrate Hox genes. Curr. Genomics 2004, 5:459-472.
72. Robinson-Rechavi M., Boussau B., Laudet V. Phylogenetic dating and characterization of gene duplications in vertebrates: the cartilaginous fish reference. Mol. Biol. Evol. 2004, 21:580-586.
73. Rokas A., Kruger D., Carroll S.B. Animal evolution and the molecular signature of radiations compressed in time. Science 2005, 310:1933-1938.
74. Ronquist F., Huelsenbeck J.P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
75. Ronquist, F., Huelsenbeck, J.P., van der Mark, P., 2005. MrBayes 3.1 Manual. http://mrbayes.csit.fsu.edu/.
76. Rosenberger L.J. Pectoral fin locomotion in batoid fishes: undulation versus oscillation. J. Exp. Biol. 2001, 204:379-394.
77. Sanderson M.J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 2002, 19:101-109.
78. Sanderson M.J. R8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 2003, 19:301-302.
79. Schaefer J.T., Summers A.P. Batoid wing skeletal structure: novel morphologies, biomechanical implications, and phylogenetic patterns. J. Morphol. 2005, 264:298-313.
80. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114-1116.
81. Shirai S. Squalean Phylogeny: A New Framework of Squaloid Sharks and Related Taxa 1992, Hokkaido University Press, Sapporo, pp. 1-138.
82. Shirai S. Phylogenetic interrelationships of neoselachians (Chondrichthyes: Euselachii). Interrelationships of Fishes 1996, 9-34. Academic Press, London. M.J. Stiassny, L.R. Parenti, G.D. Johnson (Eds.).
83. Siverson M., Cappetta H. A skate in the lowermost Maastrichtian of southern Sweden. Palaeontology 2001, 44:431-445.
84. Stamatakis A. RAxML-VI-HPC: maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
85. Stiassny, M.L.J., Wiley, E.O., Johnson, G.D., de Carvalho, M.R., 2004. Gnathostome fishes. In: Cracraft, J., Donoghue, M.J. (Eds.), Assembling the Tree of Life. Oxford University Press, pp. 410-429.
86. Sullivan J., Swofford D.L., Naylor G.J.P. The effect of taxon sampling on estimating rate-heterogeneity parameters of maximum-likelihood models. Mol. Biol. Evol. 1999, 16:1347-1356.
87. *and other Methods), Version 4.0b10 2003, Sinauer Associates, Sunderland, MA.
88. Tanaka M., Münsterberg A., Anderson W.G., Prescott A.R., Hazon N., Tickle C. Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 2002, 416:527-531.
89. Toffoli D., Hrbek T., Araújo M.L.G., Almeida M.P., Charvet-Almeida P., Farias I.P. A test of the utility of DNA barcoding in the radiation of the freshwater stingray genus Potamotrygon (Potamotrygonidae, Myliobatiformes). Genet. Mol. Biol. 2008, (Suppl. 1):324-336.
90. Tümpel S., Maconochie M.M., Wiedemann L.M., Krumlauf R. Conservation and diversity in the cis-regulatory networks that integrate information controlling expression of Hoxa2 in hindbrain and cranial neural crest cells in vertebrates. Dev. Biol. 2002, 246:45-56.
91. Underwood C.J. Diversification of the Neoselachii (Chondrichthyes) during the Jurassic and Cretaceous. Paleobiology 2006, 32:215-235.
92. Vélez-Zuazo, X., Agnarsson, I., 2010. Shark tales: a molecular species-level phylogeny of sharks (Selachimorpha, Chondrichthyes). Mol. Phylogenet. Evol. 2010 November 30 (Epub ahead of prin).
93. Venkatesh B., Ning Y., Brenner S. Late changes in spliceosomal introns define clades in vertebrate evolution. Proc. Natl. Acad. Sci. - Biol. 1999, 96:10267-10271.
94. Venkatesh B., Erdmann M.V., Brenner S. Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc. Natl. Acad. Sci. - Biol. 2001, 98:11382-11387.
95. Venkatesh B., Kirkness E.F., Loh Y.H., Halpern A.L., Lee A.P., Johnson J., Dandona N., Viswanathan L.D., Tay A., Venter J.C., Strausberg R.L., Brenner S. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol. 2007, 5:932-944.
96. Walker, J.D., Geissman, J.W., compilers., 2009. Geologic Time Scale: Geological Society of America. Product code CTS004R2C.
97. Wilga C.A.D., Lauder G.V. Biomechanics of locomotion in sharks, rays and chimaeras. Biology of Sharks and Their Relatives 2004, 139-164. CRC Press, Boca Raton, FL. J.C. Carrier, J.A. Musick, M.R. Heithaus (Eds.).
98. Wright F. The 'effective number of codons' used in a gene. Gene 1990, 87:23-29.