Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Log in

The phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies

  • Published:
Genetica Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Bartl, S., 1998. What sharks can tell us about the evolution of MHC genes. Immuno. Rev. 166: 317–331.

    Google Scholar 

  • Bernardi, G., 2000. Isochores and the evolutionary genomics of vertebrates. Gene 241: 3–17.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Felsenstein, J., 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27: 401–410.

    Google Scholar 

  • 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.

    Google Scholar 

  • Graybeal A., 1998. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47: 9–17.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lynch, M. & J.S. Conery. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155.

    Google Scholar 

  • Martin, A.P., 1999a. Nucleotide substitution rates in organelle and nuclear genes of sharks: implicating metabolic rate (again). Mol. Biol. Evol. 16: 996–1002.

    Google Scholar 

  • Martin, A.P., 1999b. Increasing genomic complexity by gene duplication and the origin of vertebrates. Am. Nat. 154: 111–128.

    Google Scholar 

  • Martin, A.P., 2000. Choosing among alternative trees of multigene families. Mol. Phylogen. Evol. 16: 430–439.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Ruvolo M., 1997. Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets. Mol. Biol. Evol. 14: 248–265.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Shimeld, S.M. & P.W.H. Holland, 2000. Vertebrate innovations. Proc. Natl. Acad. Sci. USA 97: 4449–4452.

    Google Scholar 

  • 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.

    Google Scholar 

  • Sokal, R.R. & F.J. Rohlf, 1981. Biometry. Freeman and Co., NY, 2nd edn.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Swofford, D.S., 1999. Phylogenetic Analysis Using Parsimony and other Methods. Sinauer Press, Sunderland, MA.

    Google Scholar 

  • 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.

    Google Scholar 

  • Tracy, M.R. & S.B. Hedges, 2000. Evolutionary history of the enolase gene family. Gene 259: 129–138.

    Google Scholar 

  • 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.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints 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

Download citation

  • Issue date:

  • DOI: https://doi.org/10.1023/A:1013747532647