Environmental Biology of Fishes

, Volume 48, Issue 1–4, pp 127–155 | Cite as

Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches

  • Vadim J. Birstein
  • Robert Hanner
  • Rob DeSalle


The review of the data on karyology and DNA content in Acipenseriformes shows that both extant families, the Polyodontidae and Acipenseridae, originated from a tetraploid ancestor which probably had a karyotype consisting of 120 macro- and microchromosomes and DNA content of about 3.2–3.8 pg per nucleus. The tetraploidization of the presumed 60-chromosome ancestor seems to have occurred at an early time of evolution of the group. The divergence of the Acipenseridae into Scaphirhyninae and Acipenserinae occurred without polyploidization. Within the genus Acipenser, polyploidization was one of the main genetic mechanisms of speciation by which 8n and 16n-ploid species were formed. Individual gene trees constructed for sequenced partial fragments of the 18S rRNA (230 base pairs, bp), 12S rRNA (185 bp), 16S rRNA (316 bp), and cytochrome b (270 bp) genes of two Eurasian (A. baerii and A. ruthenus) and two American (A. transmontanus and A. medirostris) species of Acipenser, Huso dauricus, Pseudoscaphirhynchus kaufmanni, Scaphirhynchus albus, and Polyodon spathula showed a low level of resolution; the analysis of a combined set of data for the four genes, however, gave better resolution. Our phylogeny based on molecular analysis had two major departures from existing morphological hypotheses: Huso dauricus is a sister-species to Acipenser instead of being basal to all acipenseriforms, and Scaphirhynchus and Pseudoscaphirhynchus do not form a monophyletic group. The phylogenetic tree constructed for the cytochrome b gene fragments (with inclusion of 7 additional species of Acipenser) supported the conclusion that octoploid species appeared at least three times within Acipenser.

sturgeon paddlefish Huso Acipenser Scaphirhynchus Pseudoscaphirhynchus Polyodon Psephurus karyotype chromosome macrochromosome microchromosome genome DNA content 18S rRNA gene cytochrome 12S mtrRNA gene 16s mtrRNA gene rate of molecular evolution phylogeny evolution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Allendorf, F.W. & G.H. Thorgaard. 1984. Tetraploidy and the evolution of salmonid fishes. pp. 1–53. In: B.J. Turner (ed.) Evolutionary Genetics of Fishes, Plenum Press, New York.Google Scholar
  2. Antipa, G. 1909. Fauna ichtiologica a României. Publicatiunile Fondul Vasilie Adamanchi, Academia Româna, Bucureşti 16: 1–294.Google Scholar
  3. Antoniu-Murgoci, A. 1946. Sur l'hybridation chez les estrogeons et description de deux formes nouvelles. Acad. Roum. Bul. Sec. Sci. 29: 308–313.Google Scholar
  4. Arefjev, V.A. 1983. Polykaryogrammic analysis of the ship Acipenser nudiventris Lovetsky (Acipenseridae, Chondrostei). Voprosy Ikhtiologii 23: 209–218 (in Russian, English translation J. Ichthyol. 23: 26–35).Google Scholar
  5. Arefjev, V.A. 1989a. Study of karyotype of the sturgeon Acipenser gueldenstaedti Brandt (Chondrostei). Tsitologia i Genetika 23: 7–10 (in Russian).Google Scholar
  6. Arefjev, V.A. 1989b. Karyotype variability in successive generations after hybridization between the great sturgeon, Huso huso (L.), and the sterlet, Acipenser ruthenus (L.). J. Fish Biol. 35: 819–828.Google Scholar
  7. Arefjev, V.A. 1991. Cytogenetic aspects of differences in the quality of spawners of reciprocal hybrids between bester and beluga sturgeon. pp. 134–150. In: A.D. Gershanovich (ed.) Biological Principles of Commercial Aquaculture of Sturgeons, VNIRO Publishing, Moscow (in Russian).Google Scholar
  8. Arefjev, V.A. 1993. NOR-banding studies of Acipenser baeri karyotype. pp. 30–31. In: International Symposium on Sturgeons, Abstract Bulletin, September 6–11, 1993, VNIRO, Moscow.Google Scholar
  9. Arefjev, V.A. & O.P. Filippova. 1993. Karyotypic analysis of the hybrid between Russian and Siberian sturgeon in relation to its supposed fertility and to cytogenetic aspects of hybridization in Acipenseridae. pp. 80–81. In: International Symposium on Sturgeons, Abstract Bulletin, September 6–11, VNIRO, Moscow.Google Scholar
  10. Arefjev, V.A. & A.I. Nikolaev. 1991. Cytological analysis of the reciprocal hybrids between low-and high-chromosome acipenserids, the great sturgeon, Huso huso (L.), and the Russian sturgeon, Acipenser gueldenstaedti Brandt. Cytologia 56: 495–502.Google Scholar
  11. Arlati, G., L.A. Belysheva & T.I. Kaydanova. 1994. Karyologic analysis of Acipenser naccarii (Bonaparte). pp. 119–123. In: A.D. Gershanovich & T.I.J. Smith (ed.) Proceedings of the International Symposium on Sturgeons, 6–11 September 1993, VNIRO Publishing, Moscow.Google Scholar
  12. Artyukhin, E.N. 1994. On the relationship of the Amur sturgeon, Acipenser schrencki. Sturgeon Quart. 2(3): 7.Google Scholar
  13. Artyukhin, E.N. 1995. On biogeography and relationships within the genus Acipenser. Sturgeon Quart. 3(2): 6–8.Google Scholar
  14. Artyukhin, E.N. & A.E. Andronov. 1990. A morphological study of the green sturgeon, Acipenser medirostris (Chondrostei, Acipenseridae), from the Tumnin (Datta) River and some aspects of the ecology and zoogeography of Acipenseridae. Zoologicheskii Zhurnal 69: 81–91 (in Russian, English translation J. Ichthyol. 30: 11–21).Google Scholar
  15. Asahida, T. & H. Ida. 1989. Karyological notes on four sharks in the order Carcharhiniformes. Japan. J. Ichthyol. 36: 275–280.Google Scholar
  16. Asahida, T. & H. Ida. 1990. Karyotypes of two rays, Torpedo tokionis and Dasyatis matsubarai, and their systematic relationships. Japan. J. Ichthyol. 37: 71–75.Google Scholar
  17. Asahida, T., H. Ida & T. Inoue. 1988. Karyotypes and cellular contents of two sharks in the family Scyliorhinidae. Japan. J. Ichthyol. 35: 215–219.Google Scholar
  18. Asahida, T., H. Ida, H. Terashima & H.Y. Chang. 1993. The karyotype and cellular DNA content of a ray, Mobula japonica. Japan. J. Ichthyol. 40: 317–322.Google Scholar
  19. Avise, J.C. 1992. Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63: 62–76.Google Scholar
  20. BĂnĂrescu, P. 1964. Pisces-Osteichthyes. Fauna Republicii Populare Romîne 13, Editura Academiei Republicii Populare Romîne, Bucureşti. 962 pp.Google Scholar
  21. Bartley, D.M., G.A.E. Gall & B. Bentley. 1985. Preliminary description of the genetic structure of white sturgeon, Acipenser transmontanus, in the Pacific North-West. pp. 105–109. In: F.P. Binkowski & S.I. Doroshov (ed.) North American Sturgeons: Biology and Aquaculture Potential, Dr W. J. Junk Publishers, Dordrecht.Google Scholar
  22. Bemis, W.E., E. Findeis & L. Grande. 1997. An overview of Acipenseriformes. Env. Biol. Fish. (this volume).Google Scholar
  23. Berg, L.S. 1905. Fishes of Turkestan. Scientific results of the Aral expedition, No. 6. St. Petersburg. 261 pp. (in Russian).Google Scholar
  24. Berg, L.S. 1948a. On the position of the Acipenseriformes in the system of fishes. Trudy Zoologicheskogo Instituta 7: 7–57 (in Russian).Google Scholar
  25. Berg, L.S. 1948b. The freshwater fishes of the USSR and adjacent countries, Vol. 1, Part 1. Akademia Nauk USSR, Moscow & Leningrad (in Russian, English translation published by Israel Program for Scientific Translations, Jerusalem. 505 pp.)Google Scholar
  26. Bernardi, G., P. Sordino & D.A. Powers. 1992. Nucleotide sequence of the 18S ribosomal ribonucleic acid gene from two teleosts and two sharks and their molecular phylogeny. Mol. Mar. Biol. Biotechnol. 1: 187–194.Google Scholar
  27. Bernardi, G. & D.A. Powers. 1992. Molecular phylogeny of the prickly shark, Echinorhinus cookei, based on a nuclear (18S rRNA) and a mitochondrial (cytochrome b) gene. Mol. Phylogenet. Evol. 1: 161–167.Google Scholar
  28. Bidwell, C.A., K.J. Kroll, E. Severud, S.I. Doroshov & D.M. Carlson. 1991. Identification and preliminary characterization of white sturgeon (Acipenser transmontanus) vitellogenin mRNA. Gen. Comp. Endocrinol. 83: 415–424.Google Scholar
  29. Birstein, V.J. 1987. Cytogenetic and molecular aspects of vertebrate evolution. Nauka Press, Moscow. 284 pp. (in Russian).Google Scholar
  30. Birstein, V.J. 1993a. Sturgeons and paddlefishes: threatened fishes in need of conservation. Cons. Biol. 7: 773–787.Google Scholar
  31. Birstein, V.J. 1993b. Is Acipenser medirostris one or two species? Sturgeon Quart. 1(2): 8.Google Scholar
  32. Birstein, V.J. & R. DeSalle. 1997. Molecular phylogeny of Acipenserinae. Mol. Phylogenet. Evol. 7 (in press).Google Scholar
  33. Birstein, V.J., A.I. Poletaev & B.F. Goncharov. 1993. The DNA content in Eurasian sturgeon species determined by flow cytometry. Cytometry 14: 377–383.Google Scholar
  34. Birstein, V.J. & V.P. Vasiliev. 1987. Tetraploid-octaploid relationships and karyological evolution in the order Acipenseriformes (Pisces). Karyotypes, nucleoli, and nucleolus-organizer region in four acipenserid species. Genetica 73: 3–12.Google Scholar
  35. Blacklidge, K.H. & C.A. Bidwell. 1993. Three ploidy levels indicated by genome quantification in Acipenseriformes of North America. J. Hered. 84: 427–430.Google Scholar
  36. Bogart, J.P., E.K. Balon & M.N. Bruton. 1994. The chromosomes of the living coelacanth and their remarkable similarity to those of one of the most ancient frogs. J. Hered. 85: 322–325.Google Scholar
  37. Bowen, B.W. & J.C. Avise. 1990. Genetic structure of Atlantic and Gulf of Mexico populations of sea bass, methaden, and sturgeon: influence of zoogeographic factors and life-history patterns. Mar. Biol. 107: 371–381.Google Scholar
  38. Brandt, J.F. 1869/1870. Einige Worte über die europaischen-asiatischen Störarten (Sturionides). Bull. Acad. Imper. Sci. St.-Petersb. 14: 171–175.Google Scholar
  39. Bremer, K. 1988. The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42: 795–803.Google Scholar
  40. Brown, J.R., A.T. Beckenbach & M.J. Smith. 1992a. Influence of Pleistocene glaciations and human intervention upon mitochondrial DNA diversity in white sturgeon (Acipenser transmontanus) populations. Can. J. Fish. Aqua. Sci. 49: 358–367.Google Scholar
  41. Brown, J.R., A.T. Beckenbach & M.J. Smith. 1992b. Mitochondrial DNA length variation and heteroplasmy in populations of white sturgeon (Acipenser transmontanus). Genetics 132: 221–228.Google Scholar
  42. Brown, J.R., A.T. Beckenbach & M.J. Smith. 1993. Intraspecific DNA sequence variation of the mitochondrial control region of white sturgeon (Acipenser transmontanus). Mol. Biol. Evol. 10: 326–341.Google Scholar
  43. Brown, J.R., K. Beckenbach, A.T. Beckenbach & M.J. Smith. 1996. Length variation, heteroplasmy and sequence divergence in the mitochondrial DNA of four species of sturgeon (Acipenser). Genetics 142: 525–535.Google Scholar
  44. Brown, J.R., T.L. Gilbert, D.J. Kowbel, P.J. O'Hara, N.E. Buroker, A.T. Beckenbach & M.J. Smith. 1989. Nucleotide sequence of the apocytochrome B gene in white sturgeon mitochondrial DNA. Nucl. Acids Res. 17: 4389.Google Scholar
  45. Buroker, N.E., J.R. Brown, T.A. Gilbert, P.J. O'Hara, A.T. Beckenbach, W.K. Thomas & M.J. Smith. 1990. Length heteroplasmy of sturgeon mitochondrial DNA: an illegitimate elongation model. Genetics 124: 157–163.Google Scholar
  46. Buth, D.G., T.E. Dowling & J.R. Gold. 1991. Molecular and cytological investigations. pp. 83–126. In: I.J. Winfield & J.S. Nelson (ed.) Cyprinid Fishes, Systematics, Biology and Exploitation, Chapman & Hall, London.Google Scholar
  47. Carlson, D.M., M.K. Kettler, S.E. Fisher & G.S. Whitt. 1982. Low genetic variability in paddlefish populations. Copeia 1982: 721–725.Google Scholar
  48. Carpenter, J.M. 1988. Choosing among multiple equally parsimonious cladograms. Cladistics 4: 291–296.Google Scholar
  49. DeSalle, R., A.K. Williams & M. George. 1993. Isolation and characterization of animal mitochondrial DNA. pp. 176–204. In: E.A. Zimmer, T.J. White, R.L. Cann & A.C. Wilson (ed.) Methods in Enzymology, Vol. 224, Molecular Evolution: Producing the Biochemical Data, Academic Press, San Diego.Google Scholar
  50. Dingerkus, G. 1979. Chordate cytogenetic studies: an analysis of their phylogenetic implications with particular reference to fishes and the living coelacanth. Occ. Pap. Calif. Acad. Sci. 134: 111–127.Google Scholar
  51. Dingerkus, G. & W.M. Howell. 1976. Karyotypic analysis and evidence of tetraploidy in the North American paddlefish, Polyodon spathula. Science 177: 664–669.Google Scholar
  52. Donoghue, M.J., R.G. Olmstead, J.F. Smith & J.D. Palmer. 1992. Phylogenetic relationships of Dipsacales based on rbcl sequences. Ann. Missouri Bot. Gard. 79: 333–345.Google Scholar
  53. Ernisse, D.E. & A.G. Kluge. 1993. Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology. Mol. Biol. Evol. 10: 1170–1195.Google Scholar
  54. Ferguson, M.M., L. Bernatchez, M. Gatt, B.R. Konkle, S. Lee, M.L. Malott & R.S. McKinley. 1993. Distribution of mitochondrial DNA variation in lake sturgeon (Acipenser fulvescens) from the Moose River basin, Ontario, Canada. J. Fish Biol. 43(Suppl. A): 91–101.Google Scholar
  55. Ferris, S.D. & G.S. Whitt. 1979. Evolution of the differential regulation of duplicate genes after polyploidization. J. Mol. Evol. 12: 267–317.Google Scholar
  56. Findeis, E.K. 1993. Osteology of the North American shovelnose sturgeon Scaphirhynchus platorynchus Rafinesque 1820, with comparisons to other Acipenseridae and Acipenseriformes. Ph.D. Thesis, University of Massachusetts, Amherst. 449 pp.Google Scholar
  57. Findeis, E.K. 1997. Osteology and phylogenetic interrelationships of sturgeons (Acipenseridae). Env. Biol. Fish. (this volume).Google Scholar
  58. Fitch, W. & T. Smith. 1983. Optimal sequence alignment. Proc. Nat. Acad. Sci. USA 80: 1382–1386.Google Scholar
  59. Fontana, F. 1976. Nuclear DNA content and cytometry of erythrocytes of Huso huso L., Acipenser sturio L., and Acipenser naccarii Bonaparte. Caryologia 29: 127–138.Google Scholar
  60. Fontana, F. 1994. Chromosomal nucleolar organizer regions in four sturgeon species as markers of karyotype evolution in Acipenseriformes (Pisces). Genome 37: 888–892.Google Scholar
  61. Fontana, F. & G. Colombo. 1974. The chromosomes of Italian sturgeons. Experientia 30: 739–742.Google Scholar
  62. Fontana, F., D. Jankovič & S. Živkovič. 1977. Somatic chromosomes of Acipernser ruthenus L. Arh. biol. Nauka 27: 33–35.Google Scholar
  63. Fontana, F., M. Lanfredi, R. Rossi, P. Bronzi & G. Arlati. 1995. Established cell lines from three sturgeon species. Sturgeon Quart. 3(4): 6–7.Google Scholar
  64. Gatesy, J., R. DeSalle & W. Wheeler. 1993. Alignment-ambiguous nucleotide sites and the exclusion of systematic data. Mol. Phylogenet. Evol. 2: 152–157.Google Scholar
  65. Gilbert, T.L., J.R. Brown, P.J. O'Hara, N.E. Buroker, A.T. Beckenbach & M.J. Smith. 1988. Sequence of tRNAThe and tRNAPro from white sturgeon (Acipenser transmontanus) mitochondria. Nucl. Acids Res. 16: 11825.Google Scholar
  66. Gold, J.R. 1979. Cytogenetics. pp. 353–405. In: W.S. Hoar, D.J. Randall & J.R. Brett (ed.) Fish Physiology, Vol. 8, Academic Press, New York.Google Scholar
  67. Golubtsov, A.S. & E. Yu. Krysanov. 1993. Karyological study of some cyprinid species from Ethiopia. The ploidy differences between large and small Barbus of Africa. J Fish Biol. 42: 445–455.Google Scholar
  68. Grande, L. & W.E. Bemis. 1991. Osteology and phylogenetic relationships of fossil and recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes. J. Verteb. Paleontol. 11,supplement 1: 1–121.Google Scholar
  69. Grande, L. & W.E. Bemis. 1996. Interrelationships of Acipenseriformes, with comments on “Chondrostei”. pp. 85–115. In: M.L.J. Stiassny, L.R. Parenti & G.D. Johnson (ed.) Interrelationships of Fishes, Academic Press, New York.Google Scholar
  70. Guénette, S., R. Fortin & E. Rassart. 1993. Mitochondrial DNA variation in lake sturgeon (Acipenser fulvescens) from the St. Lawrence River and James Bay drainage basins in Quebec, Canada. Can. J. Fish. Aquat. Sci. 50: 659–664.Google Scholar
  71. Hart, J.L. 1973. Pacific fishes of Canada. Fish. Res. Board Can. Bull. 180, Ottawa. 740 pp.Google Scholar
  72. Hedges, S., C.A. Hass & L.R. Maxson. 1993a. Relations of fish and tetrapods. Nature 363: 501–502.Google Scholar
  73. Hedges, S.B., R.A. Nussbaum & L.R. Maxson. 1993b. Caecilian phylogeny and biogeography inferred from mitochondrial DNA sequences of the 12S rRNA and 16S rRNA genes (Amphibia: Gymnophiona). Herpetological Monographs 7: 64–76.Google Scholar
  74. Hedrick, R.P., T.S. McDowell, R. Rosemark, D. Aronstein & C.N. Lannan. 1991. Two cell lines from white sturgeon. Trans. Amer. Fish. Soc. 120: 528–534.Google Scholar
  75. Hilgendorf, F. 1892. Ŭber eine neue Stör-Art aus Nord-Japan (Acipenser mikadoi). Sitzungsber. Ges. naturf. Freunde, Berlin 7: 98–100.Google Scholar
  76. Hillis, D.M., M.W. Allard & M.M. Miyamoto. 1994. Analysis of DNA sequence data: phylogenetic inference. pp. 456–487. In: E.A. Zimmer, T.J. White, R.L. Cann & A.C. Wilson (ed.) Methods in Enzymology, Vol. 224, Molecular Evolution: Producing the Biochemical Data, Academic Press, San Diego.Google Scholar
  77. Hillis, D.M., A. Larson, S.K. Davis & E.A. Zimmer. 1990. Nucleic acids III: sequencing. pp. 318–370. In: D.M. Hillis & C. Moritz (ed.) Molecular Systematics, Sinauer Associates, Sunderland.Google Scholar
  78. Hinegardner, R. & D.E. Rosen. 1972. Cellular DNA content and the evolution of teleostean fishes. Amer. Nat. 106: 621–644.Google Scholar
  79. Holčík, J., R. Kinzelbach, L.I. Sokolov & V.P. Vasil'ev. 1989. Acipenser sturio Linnaeus, 1758. pp. 366–394. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  80. Ida, H., I. Sato & N. Miyawaki. 1985. Karyotypes of two species in the order Torpediniformes. Japan. J. Ichthyol. 32: 107–111.Google Scholar
  81. Jin, F. 1995. Late Mesozoic acipenseriforms (Osteichthyes: Actinopterygii) in Central Asia and their biogeographical implications. pp. 15–21. In: A. Sun & Y. Wang (ed.) Sixth Symposium on Mesozoic Terresrial Ecosystems and Biota, Short Papers, China Ocean Press, Beijing.Google Scholar
  82. Irwin, D.M., T.D. Kocher & A.C. Wilson. 1991. Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128–144.Google Scholar
  83. Kallersjo, M., J.S. Farris, A.G. Kluge & C. Bult. 1992. Skewness and permutation. Cladistics 8: 275–287.Google Scholar
  84. Kedrova, O.S., N.S. Vladytchenskaya & A.S. Antonov. 1980. Single and repeated sequence divergency in fish genomes. Molekulyarnaya Biologiya 14: 1001–1012 (in Russian, English translation Molec. Biol. 14: 787–797).Google Scholar
  85. Kessler, K.F. 1877. Fishes of the Aralo-Caspian-Pontine region. Trudy Aralo-Kaspiiskoi ekspeditsii 4: 190–196 (in Russian).Google Scholar
  86. Keyvanfar, A. 1988. Étude comparative des protéines sériques et cellulaires de quatre espèces d'esturgeons anadromes de la Mer Caspienne. Ann. Inst. océonagr. (Paris) 64: 25–64.Google Scholar
  87. King, M. 1990. Animal cytogenetics, Vol. 4: Chordata 2. Amphibia. Gebruder Borntraeger, Berlin. 241 pp.Google Scholar
  88. Kinzelbach, R. 1987. Das ehemalige Vorkommen des Störs, Acipenser sturio (Linnaeus, 1758), im Einzugsgebiet des Rheins (Chondrostei: Acipenseridae). Z. Angew. Zool. 74: 167–200.Google Scholar
  89. Kluge, A.G. 1989. A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 38: 7–25.Google Scholar
  90. Kocher, T.D., W.K. Thomas. A. Meyer, S.V. Edwards, S. Pääbo, F.X. Villablanca & A.C. Wilson. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Nat. Acad. Sci. USA 86: 6196–6200.Google Scholar
  91. Kohno, S., M. Kuro-o & C. Ikebe. 1991. Cytogenetics and evolution of hynobiid salamanders. pp. 67–88. In: D.M. Green & S.K. Sessions (ed.). Amphibian Cytogenetics and Evolution, Academic Press, San Diego.Google Scholar
  92. Konstantinov, K.G., N.I. Nikolyukin & N.A. Timofeeva. 1952. On the biology of sturgeon hybrids. Doklady Akademii Nauk SSSR 86: 417–420 (in Russian).Google Scholar
  93. Kozhin, N.I. 1964. Acipenserids of the USSR and their reproduction. Trudy VNIRO 52: 21–59 (in Russian).Google Scholar
  94. Kozlov, V.I. 1970. Natural hybrid between ship sturgeon, Acipenser nudiventris derjavini Borzenko, and Kura River stellate sturgeon, A. stellatus Pallas. Voprosy Ikhtiologii 10: 631–636 (in Russian).Google Scholar
  95. Krykhtin, M.L. & V.G. Svirskii. 1997. Endemic sturgeons of the Amur River: kaluga, Huso dauricus, and Amur sturgeon, Acipenser schrenkii. Env. Biol. Fish. (this volume).Google Scholar
  96. Krylova, V.D. 1980. Morphometric characteristics of a hybrid between the beluga, Huso huso, and the sevruga, Acipenser stellatus. Voprosy Ikhtiologii 20: 875–882 (in Russian, English translation J. Ichthyol. 20: 89–97).Google Scholar
  97. Kutergina, I.G. & G.D. Ryabova. 1990. Genetic analysis of duplicated loci for lactate dehydrogenase Ldh3 and Ldh4 ingeritance in stellate sturgeon. Genetika 26: 952–955 (in Russian).Google Scholar
  98. Kuzmin, Ye. V. 1991. Comparative study of isozymes of muscle malate dehydrogenase of the Ob population of the Siberian sturgeon, Acipenser baeri, and the Don and Kama sterlet, Acipenser ruthenus. Voprosy Ikhtiologii 31: 342–346 (in Russian, English translation J. Ichthyol. 31: 139–144).Google Scholar
  99. Larhammar, D. & C. Risinger. 1994. Molecular genetic aspects of tetraploidy in the common carp, Cyprinus carpio. Mol. Phylogenet. Evol. 3: 59–68.Google Scholar
  100. Le, H.L.V., G. Lecointre & R. Perasso. 1993. A 28S rRNA based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Mol. Phylog. Evol. 2: 31–51.Google Scholar
  101. Legeza, M.I. 1971. On the hybrids of the Caspian Sea acipenserids. Trudy TSNIORKH 3: 196–206 (in Russian).Google Scholar
  102. Li, M.F., V. Marrayatt, C. Annand & P. Odense. 1985. Fish cell culture: two newly developed cell lines from Atlantic sturgeon (Acipenser oxyrhynchus) and guppy (Poecilia reticulata). Can. J. Zool. 63: 2867–2874.Google Scholar
  103. Lindberg, G.U. & M.I. Legeza. 1965. Fishes of the Sea of Japan and adjacent areas of the Okhotsk and Yellow seas, Pt. 2. Nauka Press, Moscow. 391 pp. (in Russian).Google Scholar
  104. Lukyanenko, V.V. & V.I. Lukyanenko. 1994. Ecological-physiological heterogeneity of sturgeons. Uspekhi Sovremennoi Biologii 114: 428–440 (in Russian).Google Scholar
  105. Madsden, C.S., J.E. Brooks, E. de Kloet & S. R. de Kloet. 1994. Sequence conservation of an avian centromeric repeated DNA component. Genome 37: 351–355.Google Scholar
  106. Marshin, V.G., V.V. Ponomarenko & G.P. Smirnova. 1969. Inheritance of some behavior characters in interspecies hybridization of acipenserids. pp. 192–208. In: Genetics, Selection, and Hybridization of Fishes, Nauka Press, Moscow (in Russian).Google Scholar
  107. Martin, A.P., G.J.P. Naylor & S.R. Palumbi. 1992. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357: 153–155.Google Scholar
  108. 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
  109. Meyer, A. 1993. Molecular phylogenetic studies of fishes. pp. 3–41. In: A. R. Beamumont (ed.) Evolution and Genetics of Aquatic Organisms, Chapman and Hall, London.Google Scholar
  110. Meyer, A., C.H. Biermann & G. Orti. 1993. The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: an invitation to the comparative method. Proc. R. Soc. Lond. B 252: 231–236.Google Scholar
  111. Meyer, A. & A.C. Wilson. 1990. Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J. Mol. Evol. 31: 359–364.Google Scholar
  112. Meyer, A., T.D. Kocher, P. Basasibwaki & A. Wilson. 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347: 550–553.Google Scholar
  113. Miracle, A.L. & D.E. Campton. 1995. Tandem repeat sequence variation and length heteroplasmy in the mitochondrial DNA D-loop of the threatened Gulf of Mexico sturgeon, Acipenser oxyrhynchus desotoi. J. Hered. 86: 22–27.Google Scholar
  114. Mirsky, A.E. & H. Ris. 1951. The DNA content of animal cells and its evolutionary significance. J. Gen. Physiol. 34: 451–462.Google Scholar
  115. Miyamoto, M.M. 1985. Consensus cladograms and general classification. Cladistics 1: 186–189.Google Scholar
  116. Morescalchi, A. 1973. Amphibia. pp. 233–348. In: A.B. Chiarelli & E. Capanna (ed.) Cytotaxonomy and Vertebrate Evolution, Academic Press, London.Google Scholar
  117. Morescalchi, A., G. Odierna & E. Olmo. 1979. Karyology of the primitive salamanders, family Hynobiidae. Experientia 35: 1434–1435.Google Scholar
  118. Nelson, J.S. 1994. Fishes of the World, 3rd edition. John Wiley & Sons, Toronto. 600 pp.Google Scholar
  119. Nesov, L.A. & M.N. Kaznyshkin. 1983. New sturgeons from the Cretacious and Paleogene of the USSR. pp. 68–76. In: V.V. Menner (ed.) Contemporary Problems of Paleoichthyology, Nauka Press, Moscow (in Russian).Google Scholar
  120. Nguyen, T.M., T.P. Mommsen, S.M. Mims & J.M. Conlon. 1994. Characterization of insulins and proglucagon-derived peptides from a phylogenetically ancient fish, the padlefish (Polyodon spathula). Biochem. J. 300: 339–345.Google Scholar
  121. Nikolyukin, N.I. 1970. Hybridization within the family Acipenseridae and perspectives of its use in sturgeon breeding. Trudy VNIRO 76: 56–69 (in Russian).Google Scholar
  122. Nikonorov, S.I., G.D. Ryabova, I.G. Kutergina & M.V. Ofitserov. 1985. Electrophoretic analysis of genetic variability of the starred sturgeon Acipenser stellatus. Doklady Akademii Nauk SSSR. Seriya Biologiya 284: 209–211 (in Russian; English translation Doklady Biological Sciences 284: 570–572).Google Scholar
  123. Normark, B.B., A.R. McCune & R.G. Harrison. 1991. Phylogenetic relationships of neopterygian fishes, inferred from mitochondrial DNA sequences. Mol. Biol. Evol. 8: 819–834.Google Scholar
  124. Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, Heidelberg. 160 pp.Google Scholar
  125. Ohno, S., J. Muramoto, C. Stenius, L. Christian, W.A. Kittrel & N.B. Atkin. 1969. Microchromosomes in holocephalian, chondrostean, and holostean fishes. Chromosoma 26: 35–40.Google Scholar
  126. Ojima Y. & T. Yamano. 1980. A chromosome study of the holostean long nose gar Lepisosteus osseus. Chrom. Inform. Serv. 28: 7–8.Google Scholar
  127. Olmo, E., V. Stingo, O. Cobror, T. Capriglione & G. Odierna. 1982. Repetitive DNA and polyploidy in selachians. Comp. Biochem. Physiol. 73B: 739–745.Google Scholar
  128. Ong, T.-L., J. Stabile, I. Wirgin & J.R. Waldman. 1996. Genetic divergence between Acipenser oxyrinchus oxyrinchus and A. o. desotoi as assessed by mitochondrial DNA sequencing analysis. Copeia 1996: 464–469.Google Scholar
  129. Ovsyannikov, F.V. 1870. On the artificial breeding of the sterlet. pp. 191–200. In: Trudy II Syezda Russkikh Estesvoispytatelei, Pt. 2, Moscow (in Russian).Google Scholar
  130. Palumbi, S.R., A.P. Martin, W.O. McMillan, S.R. Romano, G. Grabowsky & L. Stice. 1991. The simple fools guide to PCR, version 2. Department of Zoology, University of Hawaii, Honolulu. 15 pp.Google Scholar
  131. Patarnello, T., L. Bargelloni, F. Caldara & L. Colombo. 1994. Cytochrome b and 16S rRNA sequence variation in the Salmo trutta (Salmonidae, Teleostei) species complex. Molec. Phylogenet. Evol. 3: 69–74.Google Scholar
  132. Patterson, C. 1973. Interrelationships of holosteans. pp. 233–305. In: P.H. Greenwood, R.S. Miles & C. Patterson (ed.) Interrelationships of Fishes, Academic Press, London.Google Scholar
  133. Patterson, C. 1982. Morphology and interrelationships of primitive actinopterygian fishes. Amer. Zool. 22: 241–259.Google Scholar
  134. Patterson, C., D.M. Williams & C.J. Humphries. 1993. Congruence between molecular and morphological phylogenies. Annu. Rev. Ecol. Syst. 24: 153–188.Google Scholar
  135. Phelps, S.R. & F. Allendorf. 1983. Genetic identity of pallid and shovelnose sturgeon (Scaphirhynchus albus and S. platorynchus). Copeia 1983: 696–700.Google Scholar
  136. Pirogovskii, M.I., L.I. Sokolov & V.P. Vasil'ev. 1989. Huso huso (Linnaeus, 1758). pp. 156–200. In:: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  137. Rab, P. 1986. A note on the karyotype of the sterlet, Acipenser ruthenus (Pisces, Acipenseridae). Folia Zool. 35: 73–78.Google Scholar
  138. Risinger, C. & D. Larhammar. 1993. Multiple loci for synapse protein SNAP-25 in the tetraploid goldfish. Proc. Nat. Acad. Sci. USA 90: 10598–10602.Google Scholar
  139. Rochard, E., P. Williot, G. Castelnaud & M. Lepage. 1991. Éléments de systèmatique et de biologie des populations sauvages d'esturgeons. pp. 475–507. In: P. Williot (ed.) Acipenser, CEMAGREF Publ., Bordeaux.Google Scholar
  140. Rossi, R., G. Grandi, R. Trisolini, P. Franzoni, A. Carrieri, B.S. Dezfuli & E. Vecchietti. 1991. Osservazioni sulla biologia e la pesca della storione cobice Acipenser naccarii Bonaparte nella parte terminale del fiume Po. Atti Soc. Ital. Sci. Nat. Mus. Civ. Stir. Natur. Milano 132: 121–142.Google Scholar
  141. Ruban, G.I. 1997. Species structure, contemporary distribution and status of the Siberian sturgeon, Acipenser baerii. Env. Biol. Fish. (this volume).Google Scholar
  142. Ryabova, G.D. & I.G. Kutergina. 1990. Analysis of allozyme variability in the stellate sturgeon, Acipenser stellatus (Pallas), from the northern Caspian Sea. Genetika 26: 902–911 (in Russian).Google Scholar
  143. Schwartz, F.J. & M.B. Maddock. 1986. Comparison of karyotypes and cellular DNA contents within and between major lines of elasmobranchs. pp. 148–157. In: T. Uyeno, R. Arai, T. Tanuichi & K. Matsuda (ed.) Indo-Pacific Fish Biology: Proceedings of the Second International Conference on Indo-Pacific Fishes, Ichthyol. Soc. Japan, Tokyo.Google Scholar
  144. Scott, W.B. & E.J. Grossman. 1973. Freshwater fishes of Canada. Fish Res. Board Can. Bull. 184, Ottawa. 966 pp.Google Scholar
  145. Serebryakova, E.V. 1969. Some data on chromosome complements of the acipenserids. pp. 105–113. In: Genetics, Selection, and Hybridization of Fishes, Nauka Press, Moscow (in Russian).Google Scholar
  146. Serebryakova, E.V. 1970. Chromosome complements of hybrids between acipenserids with different karyotypes. pp. 413–419. In: Distant Hybridization of Plants and Animals, Vol. 2, Kolos, Moscow (in Russian).Google Scholar
  147. Serebryakova, E.V., V.A. Arefiev, V.P. Vasiliev & L.I. Sokolov. 1983. The study of the karyotype of giant sturgeon, Huso huso (L.) (Acipenseridae, Chondrostei) with reference to their systematic position. pp. 63–69. In: Genetics of Commercial Fishes and Objects of Aquaculture, Legkaya i Pishchevaya Promyshlennost, Moscow (in Russian).Google Scholar
  148. Shedlock, A.M., J.D. Parker, D.A. Crispin, T.W. Pietsch & G.C. Burmer. 1992. Evolution of the salmonid mitochondrial control region. Mol. Phylogenet. Evol. 1: 179–192.Google Scholar
  149. Shmidt, P.Yu. 1950. Fishes of the Sea of Okhotsk. Izdatelstvo Akademii Nauk, Moscow. 370 pp. (in Russian).Google Scholar
  150. Shubina, T.N., A.A. Popova & V.P. Vasilev. 1989. Acipenser stellatus Pallas, 1771. pp. 395–443. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  151. Slynko, V.I. 1976. Multiple molecular forms of malate dehydrogenase and lactate dehydrogenase in Russian sturgeon (Acipenser gueldenstaedti Br.) and beluga (Huso huso L.). Doklady Akademii Nauk SSSR, Seriya Biologiya 228: 470–472 (in Russian; English translation Doklady Biological Sciences 228: 201–204).Google Scholar
  152. Sokolov, L.I. & V.P. Vasilev. 1989a. Acipenser nudiventris Lovetsky, 1828. pp. 206–226. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  153. Sokolov, L.I. & V.P. Vasilev. 1989b. Acipenser ruthenus Linnaeus, 1758. pp. 227–262. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  154. Sokolov, L.I. & V.P. Vasilev. 1989c. Acipenser baeri Brandt, 1869. pp. 263–284. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  155. Stanley, H.P., H.E. Kasinsky & N.C. Bols. 1984. Meiotic chromatin diminution in a vertebrate, the holocephalian fish Hydrolagus colliei (Chondrichthyes, Holocephali). Tissue and Cell 16: 203–215.Google Scholar
  156. Stingo, V. & L. Rocco. 1991. Chondrichthyan cytogenetics: a comparison with teleostean. J. Mol. Evol. 33: 76–82.Google Scholar
  157. Stock, D.W., J.K. Gibbons & G.S. Whitt. 1991a. Strength and limitations of molecular sequence comparisons for inferring the phylogeny of the major groups of fishes. J. Fish Biol. 39(Suppl. A): 225–236.Google Scholar
  158. Stock, D.W., K.D. Moberg, L.R. Maxson & G.S. Whitt. 1991b. A phylogenetic analysis of the 18S ribosomal RNA sequence of the coelacanth Latimeria chalumnae. Env. Biol. Fish. 32: 99–117.Google Scholar
  159. Stock, D.W. & G.S. Whitt. 1992. Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group. Science 257: 787–789.Google Scholar
  160. Suzuki, A. & J. Hirata. 1991. Chromosomes and DNA content of Amia calva. Chromos. Inform. Serv. 50: 34–37.Google Scholar
  161. Suzuki, A., K. Yamanaka, T. Urushido & N. Kondo. 1988. A banding chromosome study of African fish family Polypteridae (Pisces: Polypteriformes). Proc. Japan. Acad. 64B: 299–302.Google Scholar
  162. Suzuki, A., K. Yamanaka, T. Urushido & N. Kondo. 1989. N-banding chromosomes of two polypterids, Polypterus senegalus and Calamoichthys calabaricus (Polypteriformes, Pisces). Chromos. Inform. Serv. 46: 23–25.Google Scholar
  163. Swofford, D.L. 1993. PAUP: Phylogenetc Analysis Using Parsimony: Version 3.1. Computer program distributed by the Illinois Natural History Survey, Champaign. 154 pp.Google Scholar
  164. Tiersch, T.R., R.W. Chandler, S.S. Wachtel & S. Elias. 1989. Reference standards for flow cytometry and application in comparative studies of nuclear DNA content. Cytometry 10: 706–710.Google Scholar
  165. Tortonese, E. 1989. Acipenser naccarii Bonaparte, 1836. pp. 284–293. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  166. Tsoi, S.C.M., S.-C. Lee & W.-C. Chao. 1989. Duplicate gene expression and diploidization in an Asian tetraploid catostomid, Myxocyprinus asiaticus (Cypriniformes, Catostomidae). Comp. Biochem. Physiol. 93B: 27–32.Google Scholar
  167. Ueno, K., A. Nagase & Y.-J. Ye. 1988. Tetraploid origin of the karyotype of the Asian sucker, Myxocyprinus asiaticus. Japan. J. Ichthyol. 34: 512–514.Google Scholar
  168. Uyeno, T. & G.R. Smith. 1972. Tetraploid origin of the karyotype of catostomid fishes. Science 175: 644–646.Google Scholar
  169. Vasiliev, V.P. 1985. Evolutionary karyology of fishes. Nauka Press, Moscow. 298 pp. (in Russian).Google Scholar
  170. Vasiliev, V.P., L.L. Sokolov & E.V. Serebryakova. 1980. Karyotypes of the Siberian sturgeon, Acipenser baeri, of the Lena River and some aspects of karyotype evolution in Acipenseriformes. Voprosy Ikhtiologii 20: 814–822 (in Russian; English translation J. Ichthiol. 20: 37–45).Google Scholar
  171. Vervoort, A. 1980a. Karyotypes of Polypteridae (Osteichthyes). Experientia 36: 646–647.Google Scholar
  172. Vervoort, A. 1980b. Karyotypes and nuclear DNA contents of Polypteridae (Osteichthyes). Experientia 36: 646–647.Google Scholar
  173. Vladykov, V.D. 1955. A comparison of Atlantic sea sturgeon with a new subspecies from the Gulf of Mexico (Acipenser oxyrhynchus desotoi). J. Fish. Res. Board Can. 12: 754–761.Google Scholar
  174. Vladykov, V.D. & J.R. Greeley. 1963. Order Acipenseroidei. pp. 24–60. In: H.B. Bigelow, C.M. Breder, D.M. Cohen, G.W. Mead, D. Merriman, Y.H. Olsen, W.C. Schroeder, L.P. Schultz & J. Tee-Van (ed.) Fishes of the Western North Atlantic, Mem. Sears Found. Mar. Res. 1.Google Scholar
  175. Vlasenko, A.D., A.V. Pavlov, L.I. Sokolov & V.P. Vasilev. 1989a. Acipenser gueldenstaedti Brandt, 1833. pp. 294–344. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  176. Vlasenko, A.D., A.V. Pavlov & V.P. Vasilev. 1989b. Acipenser persicus Borodin, 1897. pp. 345–366. In: J. Holčík (ed.) The Freshwater Fishes of Europe, Vol. 1, Pt. II, General Introduction to Fishes, Acipenseriformes, AULA-Verlag, Wiesbaden.Google Scholar
  177. Wagner, R.P., M.P. Maguire & R.L. Stallings. 1993. Chromosomes. A Synthesis. Wiley-Liss, New York. 523 pp.Google Scholar
  178. Ward, R.D., D.O. Skibinski & M. Woodwark. 1992. Protein heterozygosity, protein structure, and taxonomic differentiation. Evol. Biol. 26: 23–159.Google Scholar
  179. Ward, R.D., M. Woodwark & D.O.F. Skibinski. 1994. A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J. Fish Biol. 44: 213–232.Google Scholar
  180. Waterman M.S., M. Eggert & E. Lander. 1992. Parametric sequence comparisons. Proc. Nat. Acad. Sci. USA 89: 6090–6093.Google Scholar
  181. Watrous, L. & Q. Wheeler. 1981. The out-group comparison method of character analysis. Syst. Zool. 30: 1–11.Google Scholar
  182. Wei, Q., F. Ke, J. Zhang, P. Zhuang, J. Luo, R. Zhou & W. Yang. 1997. Biology, fisheries, and conservation of sturgeons and paddlefish in China. Env. Biol. Fish. (this volume).Google Scholar
  183. Wheeler, W.C. 1995. Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Syst. Biol. 44: 321–331.Google Scholar
  184. Wheeler, W.C., P. Cartwright & C.Y. Hayashi. 1993. Arthropod phylogeny: a combined approach. Cladistics 9: 1–39.Google Scholar
  185. Wheeler, W.C., J. Gatesy & R. DeSalle. 1995. Elision: a method for accomodating multiple molecular sequence alignments with alignment-ambiguous sites. Molec. Phylogenet. Evol. 4: 1–9.Google Scholar
  186. Wheeler, W.C. & D.L. Gladstein. 1993. MALIGN, Version 1.85. Program and documentation. AMNH, New York. 27 pp.Google Scholar
  187. Williot, P., P. Bronzi & G. Arlati. 1993. A very brief survey of status and prospects of freshwater sturgeon farming in Europe (EEC). pp. 32–36. In: P. Kestmont & R. Billard (ed.) Workshop on Aquaculture of Freshwater Species (except Salmonids), Spec. Publ. No. 20, Europ. Aquacult. Soc., Ghent.Google Scholar
  188. Wirgin, I.I., J.E. Stabile & J.R. Waldman. 1997. Molecular analysis in the conservation of sturgeons and paddlefish. Env. Biol. Fish. (this volume).Google Scholar
  189. Yakovlev, V.N. 1977. Phylogenesis of acipenseriforms. pp. 116–146. In: V.V. Menner (ed.) Essays on Phylogeny and Systematics of Fossil Fishes and Agnathans, Akademiya Nauk SSSR, Moscow (in Russian).Google Scholar
  190. Yakovlev, V.N. 1986. Fishes. pp. 178–179. In: L.P. Tatarinov (ed.) Insects in the Early Cretaceous Ecosystems of the West Mongolia, The Soviet-Mongolian Palaeontological Expedition Transactions, Vol. 28, Nauka Press, Moscow (in Russian).Google Scholar
  191. Yasuda, A., K. Yamaguchi, T. Noso, H. Papkoff, A.L. Polenov, C.S. Nicoll & H. Kawaguchi. 1992. The complete sequence of growth hormone from sturgeon (Acipenser guldenstaedti). Biochim. Biophys. Acta 1120: 297–304.Google Scholar
  192. Yu, X., T. Zhou, K. Li, Y. Li. & M. Zhou. 1987. On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica 72: 225–236.Google Scholar
  193. Yu, X.-Y. & X.-J. Yu. 1990. A schizothoracine fish species, Diptychus dipogon, with a very high number of chromosomes. Chrom. Inform. Serv. 48: 17–18.Google Scholar
  194. Zograf, N.Yu. 1887. Materials to understanding of the organization of the sterlet. Izvestiya Obschestva Lyubitelei Estestoznaniya, Antropologii i Etnographii 52(3). 72 pp. (in Russian).Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Vadim J. Birstein
    • 1
  • Robert Hanner
    • 2
  • Rob DeSalle
    • 3
  1. 1.The Sturgeon SocietyNew YorkU.S.A
  2. 2.Department of BiologyUniversity of OregonEugeneU.S.A
  3. 3.Department of EntomologyAmerican Museum of Natural HistoryNew YorkU.S.A

Personalised recommendations