Abstract
Elasmobranch fishes (sharks and rays) have proven valuable for inferring general and specific properties of molecular evolution through comparative studies with crown group vertebrates because they are the most ancient group of gnathostomes. Recent studies have questioned the conventional phylogenetic placement of sharks in the vertebrate tree, however. In this paper I review the importance of the basal position of Chondrichthyes for comparative biology and compile evidence from multiple, independent genes to evaluate the phylogenetic placement of sharks. The results suggests that alternative phylogenetic hypotheses of the relationships among the Chondrichthyes, Actinopterygii and Sarcopterygii can not be refuted with available data, implying that the assumption of the basal placement of sharks in the vertebrate tree is suspect. Resolving the phylogeny of basal vertebrates is important for testing hypotheses about the evolution of vertebrates, and the current lack of a robust phylogeny limits evolutionary inferences that can be gained from comparative studies that include sharks and rays.
Similar content being viewed by others
References
Amores, A., A. Force, Y.L. Yan, L. Joly, C. Amemiya, A. Fritz, R.K. Ho, J. Rangeland, V. Prince, Y.L. Yang, M. Westerfield, M. Ekker & J.H. Postlethwait, 1998. Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711–1714.
Anderson, M.K., X. Sun, A.L. Miracle, G.W. Litman & E.V. Rothenberg, 2001. Evolution of hematopoiesis: three members of the PU.1 transcription factor family in a cartilaginous fish, Raja eglanteria. Proc. Natl. Acad. Sci. USA 98: 553–558.
Baldauf, S.L., A.J. Roger, I. Wenk-Siefert & W. F. Doolittle, 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972–977.
Bartl, S., 1998. What sharks can tell us about the evolution of MHC genes. Immuno. Rev. 166: 317–331.
Bernardi, G., 2000. Isochores and the evolutionary genomics of vertebrates. Gene 241: 3–17.
Bernstein, R.M., S.F. Schluter, S. Shen & J.J. Marchalonis, 1996. A new high molecular weight immunoglobulin class from the carcharhine shark: implications for the properties of the primordial immunoglobulin. Proc. Natl. Acad. Sci. USA 93: 3289–3293.
Cantatore, P., M. Roberti, G. Pesole, A. Ludovico, F. Milella, M.N. Gadaleta & C. Saccone, 1994. Evolutionary analysis of cytochrome b sequences in some Perciformes: evidence for a slower rate of evolution than in mammals. J.Mol. Evol. 39: 589–597.
Endo, Y., M. Takahashi, M. Nakao, H. Saiga, H. Sekine, M. Matsushita, M. Nonaka & T. Fujita, 2000. Two lineages of mannose-binding lectin-associated serine protease (MASP) in vertebrates. J. Immunol. 161: 4924–4930.
Felsenstein, J., 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27: 401–410.
Foster, P.G. & D.A. Hickey, 1999. Compositional bias may affect both DNA-based and protein-based phylogenetic reconstructions. J. Mol. Evol. 48: 284–290.
Graybeal A., 1998. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47: 9–17.
Hahn, M.E., S.I. Karchner, M. A. Shapiro & S.A. Perera, 1997.
Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. USA 94: 13743–13748.
Haire, R.N., A.L. Miracle, J.P. Rast & G.W. Litman, 2000. Members of the ikaros gene family are present in early primitive vertebrates. J. Immunol. 165: 306–312.
Kim, C.-B., C. Amemiya, W. Bailey, K. Kawasaki, J. Mezey, W. Miller, S. Minoshima, N. Shimizu, G. Wagner & F. Ruddle, 2000. Hox cluster genomics in the horn shark, Heterodontus francisci. PNAS 97: 1655–1660.
Lockhart, P.J., C.J. Howe, D.A. Bryant, T.J. Beanland & A.W.D. Larkum, 1992. Substitutional bias confounds inference of cyanelle origins from sequence data. J. Mol. Evol. 34: 153–162.
Lynch, M. & J.S. Conery. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155.
Martin, A.P., 1999a. Nucleotide substitution rates in organelle and nuclear genes of sharks: implicating metabolic rate (again). Mol. Biol. Evol. 16: 996–1002.
Martin, A.P., 1999b. Increasing genomic complexity by gene duplication and the origin of vertebrates. Am. Nat. 154: 111–128.
Martin, A.P., 2000. Choosing among alternative trees of multigene families. Mol. Phylogen. Evol. 16: 430–439.
Martin, A.P. & S.R. Palumbi, 1993. Protein evolution in different cellular environments: cytochrome b in sharks and mammals. Mol. Biol. Evol. 10: 873–891.
Martin, A.P., G.J.P. Naylor & S.R. Palumbi, 1992. Rates of mitochondrial DNA evolution are slow in sharks compared to mammals. Nature 357: 153–155.
Mehta, K.D., R. Chang & J. Norman, 1996. Chiloscyllium plagiosum low-density lipoprotein receptor: evolutionary conservation of five different function domains. J. Mol. Evol. 42: 264–272.
Naylor, G.J.P. & W.M. Brown, 1998. Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Syst. Biol. 47: 61–76.
Nei, M., I.B. Rogozin & H. Piontkivska, 2000. Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc. Natl. Acad. Sci. USA 97: 10866–10871.
Nonaka, M., C. Namikawa, Y. Kato, M. Sasaki, L. Salter-Cid & M.F. Flajnik, 1997. Major histocompatibility complex gene mapping in the amphibian Xenopus implies a primordial organization. Proc. Natl. Acad. Sci. USA 94: 5789–5791.
Ohta, Y., K. Okamura, E.C. McKinney, S. Bartl, K. Hashimoto & M.F. Flajnik, 2000. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc. Natl. Acad. Sci. USA 97: 4712–4717.
Ono-Koyanagi, K., H. Suga, K. Katoh & T. Miyata, 2000. Protein tyrosine phosphatases from amphioxus, hagfish, and ray: divergence of tissue-specific isoform genes in the early evolution of vertebrates. J. Mol. Evol. 50: 302–311.
Pan, F.-M., M.-H. Chuang & S.-H. Chiou, 1997. Characterization of gammaS-crystallin isoforms from lip shark (Chiloscyllium colax): evolutionary comparison between gammaS and Beta/ Delta crystallins. Biochem. Biophys. Res. Comm. 240: 51–56.
Rasmussen, A.-S. & U. Arnason, 1999. Phylogenetic studies of complete mitochondrial DNA molecules place cartilaginous fishes within the tree of bony fishes. J. Mol. Evol. 48: 118–123.
Rast, J.P., M.K. Anderson, S.J. Strong, C. Luer, R.T. Litman & G.W. Litman, 1997. Alpha, beta, gamma, and delta T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6: 1–11.
Ruvolo M., 1997. Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets. Mol. Biol. Evol. 14: 248–265.
Sato, A., F. Figueroa, B.W. Murray, E. Malaga-Trillo, Z. Zaleska-Rutczynska, H. Sultmann, S. Toyosawa, C. Wedekind, N. Steck & J. Klein, 2000. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51: 108–116.
Schaffeld M, A. Lobbecke, B. Lieb & J. Markl, 1998. Tracing keratin evolution: catalog, expression patterns and primary structure of shark (Scyliorhinus stellaris) keratins. Eur. J. Cell Biol. 77: 69–80.
Shimeld, S.M. & P.W.H. Holland, 2000. Vertebrate innovations. Proc. Natl. Acad. Sci. USA 97: 4449–4452.
Singer, G.A. & D.A. Hickey, 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol. Biol. Evol. 17: 1581–1588.
Sokal, R.R. & F.J. Rohlf, 1981. Biometry. Freeman and Co., NY, 2nd edn.
Stock, D.W. & D.A. Power, 1995. The cDNA sequence of the lactate dehydrogenase-A of the spiny dogfish (Squalus acanthias): corrections to the amino acid sequence and an analysis of the vertebrate lactate dehydrogenases. Mol. Mar. Biol. Biotech. 4: 284–294.
Stock, D.W. & D.A. Powers, 1998. A monophyletic origin of heart-predominant lactate dehydrogenase (LDH) isozymes of gnathostome vertebrates: evidence from the cDNA sequence of the spiny dogfish (Squalus acanthias) LDH-B. Mol. Mar. Biol. Biotech. 7: 160–164.
Suga H, D. Hoshiyama, S. Kuraku, K. Katoh, K. Kubokawa & T. Miyata, 1999. Protein tyrosine kinase cDNAs from amphioxus, hagfish, and lamprey: isoform duplications around the divergence of cyclostomes and gnathostomes. J. Mol. Evol. 49: 601–608.
Suzuki, N., K. Ueda, H. Sakamoto & S. Sasayama. 1999. Fish calcitonin genes: primitive bony fish genes have been conserved in some lower vertebrates. Gen. Comp. Endo. 113: 369–373.
Swofford, D.S., 1999. Phylogenetic Analysis Using Parsimony and other Methods. Sinauer Press, Sunderland, MA.
Thompson, J.D., D.G. Higgins & T.J. Gibson, 1997. CLUSTAL X: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalities and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.
Tracy, M.R. & S.B. Hedges, 2000. Evolutionary history of the enolase gene family. Gene 259: 129–138.
Venkatesh, B., Y. Ning & S. Brenner, 1999. Late changes in spliceosomal introns define clades in vertebrate evolution. Proc. Natl. Acad. Sci. USA 96: 10267–10271.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Martin, A. The phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies. Genetica 111, 349–357 (2001). https://doi.org/10.1023/A:1013747532647
Issue date:
DOI: https://doi.org/10.1023/A:1013747532647