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Comparative and phylogenetic perspectives of the cleavage process in tailed amphibians

Published online by Cambridge University Press:  02 September 2014

Alexey G. Desnitskiy*
Affiliation:
Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7/9, 199034, St. Petersburg, Russia.
Spartak N. Litvinchuk
Affiliation:
Institute of Cytology, Russian Academy of Sciences, Tikhoretsky pr. 4, 194064, St. Petersburg, Russia.
*
All correspondence to: Alexey G. Desnitskiy. Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7/9, 199034, St. Petersburg, Russia. Tel: +7812 3289453. e-mail: adesnitskiy@mail.ru

Summary

The order Caudata includes about 660 species and displays a variety of important developmental traits such as cleavage pattern and egg size. However, the cleavage process of tailed amphibians has never been analyzed within a phylogenetic framework. We use published data on the embryos of 36 species concerning the character of the third cleavage furrow (latitudinal, longitudinal or variable) and the magnitude of synchronous cleavage period (up to 3–4 synchronous cell divisions in the animal hemisphere or a considerably longer series of synchronous divisions followed by midblastula transition). Several species from basal caudate families Cryptobranchidae (Andrias davidianus and Cryptobranchus alleganiensis) and Hynobiidae (Onychodactylus japonicus) as well as several representatives from derived families Plethodontidae (Desmognathus fuscus and Ensatina eschscholtzii) and Proteidae (Necturus maculosus) are characterized by longitudinal furrows of the third cleavage and the loss of synchrony as early as the 8-cell stage. By contrast, many representatives of derived families Ambystomatidae and Salamandridae have latitudinal furrows of the third cleavage and extensive period of synchronous divisions. Our analysis of these ontogenetic characters mapped onto a phylogenetic tree shows that the cleavage pattern of large, yolky eggs with short series of synchronous divisions is an ancestral trait for the tailed amphibians, while the data on the orientation of third cleavage furrows seem to be ambiguous with respect to phylogeny. Nevertheless, the midblastula transition, which is characteristic of the model species Ambystoma mexicanum (Caudata) and Xenopus laevis (Anura), might have evolved convergently in these two amphibian orders.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

AmphibiaWeb (2014). Information on amphibian biology and conservation. Electronic database accessible at http://amphibiaweb.org/. Berkeley, California, USA. Accessed on 3 July 2014.Google Scholar
Anderson, P.L. (1943). The normal development of Triturus pyrrhogaster. Anat. Rec. 86, 5973.CrossRefGoogle Scholar
Barbadillo, L.J. (1989). Descripción del desarrollo embrionario de Triturus boscai, Lataste 1879 (Urodela, Salamandridae). Rev. Esp. Herpetol. 3, 209–20.Google Scholar
Beetschen, J.-C. (1996). How did urodele embryos come into prominence as a model system? Int. J. Dev. Biol. 40, 629–36.Google ScholarPubMed
Bell, B.D. (1978). Observations on the ecology and reproduction of the New Zealand leiopelmid frogs. Herpetologica 34, 340–54.Google Scholar
Bell, B.D. & Wassersug, R.J. (2003). Anatomical features of Leiopelma embryos and larvae: implications for anuran evolution. J. Morphol. 256, 160–70.CrossRefGoogle ScholarPubMed
Bonett, R.M., Mueller, R.L. & Wake, D.L. (2005). Why should reacquisition of larval stages by desmognathine salamanders surprise us? Herpetol. Rev. 36, 112–3.Google Scholar
Bordzilovskaya, N.P., Dettlaff, T.A., Duhon, S.T. & Malacinski, G.M. (1989). Developmental-stage series of axolotl embryos. In Developmental Biology of the Axolotl (eds Armstrong, J.B. & Malacinski, G.M.), pp. 201–19. New York: Oxford University Press.Google Scholar
Brinkmann, H., Denk, A., Zitzler, J., Joss, J.J. & Meyer, A. (2004a). Complete mitochondrial genome sequences of the South American and the Australian lungfish: testing of the phylogenetic performance of mitochondrial data sets for phylogenetic problems in tetrapod relationships. J. Mol. Evol. 59, 834–48.CrossRefGoogle ScholarPubMed
Brinkmann, H., Venkatesh, B., Brenner, S. & Meyer, A. (2004b). Nuclear protein-coding genes support lungfish and not the coelacanth as the closest living relatives of land vertebrates. Proc. Natl Acad. Sci. USA 101, 4900–5.CrossRefGoogle Scholar
Brown, H.A. (1989). Developmental anatomy of the tailed frog (Ascaphus truei): a primitive frog with large eggs and slow development. J. Zool. 217, 525–37.CrossRefGoogle Scholar
Callery, E.M. (2006). There's more than one frog in the pond: a survey of the Amphibia and their contributions to developmental biology. Sem. Cell Dev. Biol. 17, 8092.CrossRefGoogle Scholar
Chippindale, P.T., Bonett, R.M., Baldwin, A.S. & Wiens, J.J. (2004). Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders. Evolution 58, 2809–22.Google Scholar
Collart, C., Allen, G.E., Bradshaw, C.R., Smith, J.C. & Zegerman, P. (2013). Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341, 893–6.CrossRefGoogle ScholarPubMed
Collazo, A. & Keller, R. (2010). Early development of Ensatina eschscholtzii: an amphibian with a large, yolky egg. Evodevo 1, 6. doi: 10.1186/2041-9139-1-6.CrossRefGoogle ScholarPubMed
Collazo, A. & Marks, S.B. (1994). Development of Gyrinophilus porphyriticus: identification of the ancestral developmental pattern in the salamander family Plethodontidae. J. Exp. Zool. 268, 239–58.CrossRefGoogle Scholar
D’Amen, M., Vignoli, L. & Bologna, M.A. (2006). The normal development and the chromosome No. 1 syndrome in Triturus carnifex carnifex (Caudata, Salamandridae). Ital. J. Zool. 73, 325–33.CrossRefGoogle Scholar
Davenport, J.M. & Summers, K. (2010). Environmental influences on egg and clutch sizes in lentic- and lotic-breeding salamanders. Phyllomedusa 9, 8798.CrossRefGoogle Scholar
de Bussy, L.P. (1905). Die ersten Entwicklungsstadien des Megalobatrachus maximus. Zool. Anz. 28, 523–36.Google Scholar
del Pino, E.M. & Loor-Vela, S. (1990). The pattern of early cleavage of the marsupial frog Gastrotheca riobambae. Development 110, 781–9.Google Scholar
Dempster, W.T. (1933). Growth in Amblystoma punctatum during the embryonic and early larval period. J. Exp. Zool. 64, 495511.Google Scholar
Dent, J.N. (1942). The embryonic development of Plethodon cinereus as correlated with the differentiation and functioning of the thyroid gland. J. Morphol. 71, 577601.CrossRefGoogle Scholar
Desnitskiy, A.G. (2011). On the diversity of the primary steps of embryonic development in the caudate amphibians. Russ. J. Dev. Biol. 42, 207–11.CrossRefGoogle Scholar
Desnitskiy, A.G. (2014). On the classification of the cleavage patterns in amphibian embryos. Russ. J. Dev. Biol. 45, 110.CrossRefGoogle Scholar
Duellman, W.E. & Trueb, L. (1994). The Biology of Amphibians, 2nd edn. Baltimore & London: Johns Hopkins University Press.CrossRefGoogle Scholar
Elinson, R.P. (1986). Fertilization in amphibians: the ancestry of the block to polyspermy. Int. Rev. Cytol. 101, 59100.CrossRefGoogle ScholarPubMed
Elinson, R.P. & del Pino, E.M. (2012). Developmental diversity of amphibians. WIREs Dev. Biol., 1, 345–69.CrossRefGoogle ScholarPubMed
Epperlein, H.H. & Junginger, M. (1982). The normal development of the newt, Triturus alpestris (Daudin). Amphibia–Reptilia 2, 295308.CrossRefGoogle Scholar
Eycleshymer, A.C. (1895). The early development of Amblystoma, with observations on some other vertebrates. J. Morphol. 10, 343418.CrossRefGoogle Scholar
Eycleshymer, A.C. (1904). Bilateral symmetry in the egg of Necturus. Anat. Anz. 25, 230–40.Google Scholar
Eycleshymer, A.C. & Wilson, J. M. (1910). Normal Plates of the Development of Necturus maculosus. Jena, Germany: Verlag von Gustav Fischer.Google Scholar
Fankhauser, G. (1967). Urodeles. In: Methods in Developmental Biology. (eds Wilt, F.H. & Wessels, N.K.), pp. 8599. New York: Thomas Y. Crowell Company.Google Scholar
Feng, X.I.E., Liang, F.E.I., Cheng, L.I. & Chang-Yuan, Y.E. (2001). The preliminary studies on the early development of the Chinhai salamander, Echinotriton chinhaiensis. Chin. J. Zool. 36, 21–5.Google Scholar
Ferrier, V. (1974). Chronologie du développement de l’amphibien urodèle Tylototriton verrucosus Anderson (Salamandridae). Annal. Embryol. Morphogen. 7, 407–16.Google Scholar
Gallien, L. & Bidaud, O. (1959). Table chronologique du développement chez Triturus helveticus Razoumowsky. Bull. Soc. Zool. France 84, 2232.Google Scholar
Gallien, L. & Durocher, M. (1957). Table chronologique du développement chez Pleurodeles waltlii Michah. Bull. Biol. France Belg. 91, 97114.Google Scholar
Gasser, F. (1964). Observations sur les stades initiaux du développement de l’ urodèle Pyrénéen Euproctus asper. Bull. Soc. Zool. France 89, 423–8.Google Scholar
Goodale, H.D. (1911). The early development of Spelerpes bilineatus (Green). Am. J. Anat. 12, 173247.CrossRefGoogle Scholar
Grönroos, H. (1895). Zur Entwickelungsgeschichte des Erdsalamanders (Salamandra maculosa Laur.). Anat. Hefte 6, 153247.CrossRefGoogle Scholar
Gurdon, J.B. & Hopwood, N. (2000). The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int. J. Dev. Biol. 44, 4350.Google ScholarPubMed
Hara, K. (1977). The cleavage pattern of the axolotl egg studied by cinematography and cell counting. Roux's Arch. Dev. Biol. 181, 7387.CrossRefGoogle Scholar
Harrison, R.G. (1962). Amblystoma punctatum. In: Experimental Embryology. Techniques and Procedures, 3rd edn (ed. Rugh, R.), pp. 8287. Minneapolis, Minnesota: Burgess Publishing Company.Google Scholar
Hilton, W.A. (1909). General features of the early development of Desmognathus fusca. J. Morphol. 20, 533–59.CrossRefGoogle Scholar
Hirsch, N., Zimmerman, L.B. & Grainger, R.M. (2002). Xenopus, the next generation: X. tropicalis genetics and genomics. Dev. Dyn. 225, 422–33.CrossRefGoogle ScholarPubMed
Humphrey, R.R. (1928). Ovulation in the four-toed salamander, Hemidactylium scutatum, and the external features of cleavage and gastrulation. Biol. Bull. 54, 307–23.CrossRefGoogle Scholar
Irisarri, I., San Mauro, D., Green, D.M. & Zardoya, R. (2010). The complete mitochondrial genome of the relict frog Leiopelma archeyi: insights into the root of the frog tree of life. Mitoch. DNA. 21, 173–82.CrossRefGoogle ScholarPubMed
Iwasawa, H. & Kera, Y. (1980). Normal stages of development of the Japanese lungless salamander, Onychodactylus japonicus (Houttuyn). Jap. J. Herpetol. 8, 7389.CrossRefGoogle Scholar
Iwasawa, H. & Yamashita, K. (1991). Normal stages of development of a hynobiid salamander, Hynobius nigrescens Stejneger. Jap. J. Herpetol. 14, 3962.CrossRefGoogle Scholar
Jordan, E.O. (1893). The habits and development of the newt (Diemictylus viridescens). J. Morphol. 8, 269366.CrossRefGoogle Scholar
Kemp, A. (1982). The embryological development of the Queensland lungfish, Neoceratodus forsteri (Krefft). Mem. Queensland Mus. 20, 553–97.Google Scholar
Khan, P.A. & Liversage, R.A. (1995). Development of Notophthalmus viridescens embryos. Dev. Growth Differ. 37, 529–37.CrossRefGoogle ScholarPubMed
Khokha, M.K., Chung, C., Bustamante, E.L., Gaw, L.W.K., Trott, K.A., Yeh, J., Lim, N., Lin, J.C.Y., Taverner, N., Amaya, E., Papalopulu, N., Smith, J.C., Zorn, A.M., Harland, R.M. & Grammer, T.C. (2002). Techniques and probes for the study of Xenopus tropicalis development. Dev. Dyn. 225, 499510.CrossRefGoogle Scholar
Kimelman, D., Kirschner, M. & Scherson, T. (1987). The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48, 399407.CrossRefGoogle ScholarPubMed
Knight, F.C.E. (1938). Die Entwicklung von Triton alpestris bei verschiedenen Temperaturen, mit Normentafel. Roux's Arch. Entwicklungsmech. Org. 137, 461–73.CrossRefGoogle Scholar
Kung, C.-C., Chang, C.-M. & Tsai, B. (1960). Observations on the early development of Cynops orientalis (David). Acta Zool. Sinica 12, 175–83.Google Scholar
Kunitomo, K. (1910). Über die Entwickelungsgeschichte des Hynobius nebulosus. Anat. Hefte 40, 193283.CrossRefGoogle Scholar
Lefresne, J., Andeol, Y. & Signoret, J. (1998). Evidence for introduction of a variable G1 phase at the midblastula transition during early development in axolotl. Dev. Growth Differ. 40, 497508.CrossRefGoogle ScholarPubMed
Liozner, L.D. & Dettlaff, T.A. (1991). The newts Triturus vulgaris and Triturus cristatus. In: Animal Species for Developmental Studies. Vol. 2 (eds Dettlaff, T.A. & Vassetzky, S.G.), pp. 145–65. New York: Consultants Bureau.CrossRefGoogle Scholar
Luo, J., Xiao, Y., Luo, K., Huang, X., Peng, L. & Liu, Y. (2007). Embryonic development and organogenesis of Chinese giant salamander, Andrias davidianus. Progr. Nat. Sci. 17, 1303–11.Google Scholar
Marks, S.B. & Collazo, A. (1998). Direct development in Desmognathus aeneus (Caudata: Plethodontidae): a staging table. Copeia 1998, 637–48.CrossRefGoogle Scholar
Masui, Y. & Wang, P. (1998) Cell cycle transition in early embryonic development of Xenopus laevis. Biol. Cell 90, 537–48.CrossRefGoogle Scholar
Mi, X.-Q., Deng, X.-J., Guo, K.-J., Niu, Y.-D. & Zhou, Y. (2007). Early embryonic development of Hynobius guabangshanensis. Sichuan J. Zool. 26, 377–8.Google Scholar
Mietchen, D., Jakobi, J.W. & Richter, H.-P. (2005). Cortex reorganization of Xenopus laevis eggs in strong static magnetic fields. BioMagnetic Res. Technol. 3, 2. doi: 10.1186/1477-044X-3-2.CrossRefGoogle ScholarPubMed
Mo, W.-C., Liu, Y., Cooper, H.M. & He, R.-Q. (2012). Altered development of Xenopus embryos in a hypogeomagnetic field. Bioelectromagnetics 33, 238–46.CrossRefGoogle Scholar
Newport, J. & Kirschner, M. (1982a). A major developmental transition in early Xenopus embryos: 1. Characterization and timing of cellular changes at the midblastula stage. Cell 30, 675–86.CrossRefGoogle Scholar
Newport, J. & Kirschner, M. (1982b.) A major developmental transition in early Xenopus embryos: 2. Control of the onset of transcription. Cell 30, 687–96.CrossRefGoogle Scholar
Nieuwkoop, P.D. (1996). What are the key advantages and disadvantages of urodele species compared to anurans as a model system for experimental analysis of early development? Int. J. Dev. Biol. 40, 617–9.Google Scholar
Nussbaum, R.A. (1985). The evolution of parental care in salamanders. Misc. Publ. Mus. Zool. Univ. Michigan 169, 150.Google Scholar
Nussbaum, R.A. (1987). Parental care and egg size in salamanders: an examination of the safe harbor hypothesis. Res. Popul. Ecol. 29, 2744.CrossRefGoogle Scholar
Pyron, R.A. & Wiens, J.J. (2011). A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61, 543–83.CrossRefGoogle Scholar
Reinhard, S., Voitel, S. & Kupfer, A. (2013). External fertilisation and paternal care in the paedomorphic salamander Siren intermedia Barnes, 1826 (Urodela: Sirenidae). Zool. Anz. 253, 15.CrossRefGoogle Scholar
Rugh, R. (1951). The Frog; Its Reproduction and Development. Philadelphia: Blakiston Company.CrossRefGoogle Scholar
Salthe, S.N. (1969). Reproductive modes and the number and sizes of ova in the urodeles. Am. Midl. Nat. 81, 467–90.CrossRefGoogle Scholar
San Mauro, D. (2010). A multilocus timescale for the origin of extant amphibians. Mol. Phylogenet. Evol. 56, 554–61.CrossRefGoogle ScholarPubMed
Schönmann, W. (1938). Der diploide Bastard Triton palmatus ♀ x Salamandra ♂. Roux's Arch. Entwicklungsmech. Org. 138, 345–75.CrossRefGoogle Scholar
Schrenkenberg, G.M. & Jacobson, A.G. (1975). Normal stages of development of the axolotl Ambystoma mexicanum. Dev. Biol. 42, 391–9.CrossRefGoogle Scholar
Sever, D.M., Doody, J.S., Reddish, C.A., Wenner, M.M. & Church, D.R. (1996). Sperm storage in spermathecae of the great lamper eel, Amphiuma tridactylum (Caudata: Amphiumidae). J. Morphol. 230, 7997.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Shen, X.X., Liang, D., Feng, Y.J., Chen, M.Y. & Zhang, P. (2013). A versatile and highly efficient toolkit including 102 nuclear markers for vertebrate phylogenomics, tested by resolving the higher level relationships of the Caudata. Mol. Biol. Evol. 30, 2235–48.CrossRefGoogle ScholarPubMed
Shi, D.-L. & Boucaut, J.-C. (1995). The chronological development of the urodele amphibian Pleurodeles waltl (Michah). Int. J. Dev. Biol. 39, 427–41.Google ScholarPubMed
Signoret, J. (1977). La cinétique cellulaire au cours de la segmentation du germe d’axolotl: proposition d’un modèle statistique. J. Embryol. Exp. Morphol. 42, 514.Google Scholar
Signoret, J. (1980). Evidence of the first genetic activity required in axolotl development. Res. Probl. Cell Differ. 11, 71–4.CrossRefGoogle ScholarPubMed
Signoret, J. & Lefresne, J. (1971). Contribution à l’étude de la segmentation de l’oeuf d’axolotl: 1. Définition de la transition blastuléenne. Annal. Embryol. Morphogen. 4, 113–23.Google Scholar
Signoret, J. & Lefresne, J. (1976). Le cycle cellulaire au cours de la segmentation du germe d’axolotl. Bull. Soc. Zool. France 101, 123–7.Google Scholar
Smith, B.G. (1906). Preliminary report on the embryology of Cryptobranchus allegheniensis. Biol. Bull. 11, 146–64.CrossRefGoogle Scholar
Smith, B.G. (1912). The embryology of Cryptobranchus allegheniensis, including comparisons with some other vertebrates. 2. General embryonic and larval development, with special reference to external features. J. Morphol. 23, 455565.CrossRefGoogle Scholar
Smith, B.G. (1922). The origin of bilateral symmetry in the embryo of Cryptobranchus allegheniensis. J. Morphol. 36, 357–99.CrossRefGoogle Scholar
Smith, B.G. (1926). The embryology of Cryptobranchus allegheniensis. 3. Formation of the blastula. J. Morphol. Physiol. 42, 197252.CrossRefGoogle Scholar
Suzuki, A., Kuwabara, Y. & Kuwana, T. (1976). Analysis of cell proliferation during early embryogenesis. Dev. Growth Differ. 18, 447–55.CrossRefGoogle ScholarPubMed
Svensson, G.S.O. (1938). Zur Kenntnis der Furchung bei den Gymnophionen. Acta Zool. 19, 191207.CrossRefGoogle Scholar
Sytina, L.A., Medvedeva, I.M. & Godina, L.B. (1987). Development of Siberian Newt. Moscow, Russia: Nauka Press.Google Scholar
Tarkhnishvili, D.N. & Serbinova, I.A. (1997). Normal development of the Caucasian salamander (Mertensiella caucasica). Adv. Amphib. Res. Former Soviet Union 2, 1330.Google Scholar
Tripepi, S., Rossi, F. & Peluso, G. (1998). Embryonic development of the newt Triturus italicus in relation to temperature. Amphibia–Reptilia 19, 345–55.CrossRefGoogle Scholar
Twitty, V.C. & Bodenstein, D. (1962). Triturus torosus. In: Experimental Embryology. Techniques and Procedures, 3rd edn (ed. Rugh, R.), p. 90. Minneapolis, Minnesota: Burgess Publishing Company.Google Scholar
Valles, J.M. (2002). Model of magnetic field-induced mitotic apparatus reorientation in frog eggs. Biophys. J. 82, 1260–5.CrossRefGoogle ScholarPubMed
Valles, J.M., Wasserman, S.R.R.M., Schweidenback, C., Edwardson, J., Denegre, J.M. & Mowry, K.L. (2002). Processes that occur before second cleavage determine third cleavage orientation in Xenopus. Exp. Cell Res. 274, 112–8.CrossRefGoogle Scholar
Vassetzky, S.G. (1991). The Spanish newt Pleurodeles waltlii. In Animal Species for Developmental Studies. Vol. 2 (eds Dettlaff, T.A. & Vassetzky, S.G.), pp. 167201. New York: Consultants Bureau.CrossRefGoogle Scholar
Vieites, D., Román, S.N., Wake, M.H. & Wake, D.B. (2011). A multigenic perspective on phylogenetic relationships in the largest family of salamanders, the Plethodontidae. Mol. Phylogenet. Evol. 59, 623–35.CrossRefGoogle ScholarPubMed
Wake, D.B. & Hanken, J. (1996). Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40, 859–69.Google ScholarPubMed
Wiens, J.J., Kuczynski, C.A., Duellman, W.E. & Reeder, T.W. (2007). Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61, 1886–99.CrossRefGoogle ScholarPubMed
Wiens, J.J., Sparreboom, M. & Arntzen, J.W. (2011). Crest evolution in newts: implications for reconstruction methods, sexual selection, phenotypic plasticity and the origin of novelties. J. Evol. Biol. 24, 2073–86.CrossRefGoogle ScholarPubMed
Wilder, H.H. (1904). The early development of Desmognathus fusca. Am. Nat. 38, 117–25.CrossRefGoogle Scholar
Wunderer, H. (1910). Die Entwicklung der äußern Körperform des Alpensalamanders (Salamandra atra Laur). Zool. Jahrb. Abt. Anat. Ontog. Tiere 29, 367414.Google Scholar
Yamazaki-Yamamoto, K., Takata, K. & Kato, Y. (1984). Changes of chromosome length and constitutive heterochromatin in association with cell division during early development of Cynops pyrrhogaster embryo. Dev. Growth Differ. 26, 295302.CrossRefGoogle ScholarPubMed
Zhang, P., Liang, D., Mao, R.L., Hillis, D.M., Wake, D.B. & Cannatella, D.C. (2013). Efficient sequencing of anuran mtDNAs and a mitogenomic exploration of the phylogeny and evolution of frogs. Mol. Biol. Evol. 30, 1899–915.CrossRefGoogle Scholar
Zheng, Y., Peng, R., Kuro-O, M. & Zeng, X. (2011). Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of salamanders (order Caudata). Mol. Biol. Evol. 28, 2521–35.CrossRefGoogle Scholar
Zheng, Y., Peng, R., Murphy, R.W., Kuro-O, M., Hu, L. & Zeng, X. (2012). Matrilineal genealogy of Hynobius (Caudata: Hynobiidae) and a temporal perspective on varying levels of diversity among lineages of salamanders on the Japanese Islands. Asian Herpetol. Res. 3, 288302.Google Scholar