Advertisement

Russian Journal of Developmental Biology

, Volume 49, Issue 6, pp 327–338 | Cite as

Lampreys, “Living Fossils,” in Research on Early Development and Regeneration in Vertebrates

  • A. V. BayramovEmail author
  • G. V. Ermakova
  • A. V. Kucheryavyy
  • A. G. Zaraisky
REVIEWS

Abstract

Agnathans, the most ancient of the extant vertebrates, evoke steadily increasing interest as the object of research on the basic processes of vertebrate ontogeny. Lampreys have been more accessible to researchers than myxines (hagfish), representatives of the other class of jawless vertebrates, for more than 100 years. Studies on the functional and evolutionary aspects of early ontogeny in lamprey at the molecular level became possible in the past two decades. Studies on the distinctive features of lampreys as the ancient representatives of vertebrates and comparison to gnathostomes, the more modern vertebrates, are of great interest. Molecular studies of lampreys can provide insight into the evolutionary mechanisms for the emergence and development of individual unique structures of vertebrates. The appearance of the telencephalon, which was first detected in lampreys, was one of the most important aromorphoses of vertebrates. Development and advancement of the telencephalon in the course of evolution enabled the implementation of higher forms of nervous activity in vertebrates, including humans. Research on the molecular mechanisms of basic ontogenetic events, such as early embryonic differentiation and neural induction, in the lamprey and other vertebrates is also important. Studies on the well-developed regeneration capacity of lampreys, in turn, give hope for at least partial use of the knowledge gained in future medical practice. This article is a review of recent data on the molecular aspects of the early development of the telencephalon, early embryonic differentiation, and regeneration of lampreys.

Keywords:

cyclostomes lampreys telencephalon development neural induction early embryonic differentiation regeneration 

Notes

ACKNOWLEDGMENTS

The work was supported by a grant from the Russian Foundation for Basic Research (project no. 18-04-00015). Experiments on the creation of the tail regeneration model in the river lamprey (Fig. 4) were supported by a grant from the Russian Science Foundation (project no. 14-50-00131).

REFERENCES

  1. 1.
    Arendt, D. and Nübler-Jung, K., Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs, Mech Dev., 1999, vol. 81(1–2), pp. 3–22.Google Scholar
  2. 2.
    Arias, A.M. and Steventon, B., On the nature and function of organizers, Development, 2018, vol. 145, p. dev159525.Google Scholar
  3. 3.
    Bachvarova, R. F., Skromne, I., and Stern, C.D., Induction of primitive streak and Hensen’s node by the posterior marginal zone in the early chick embryo, Development, 1998, vol. 125, pp. 3521–3534.Google Scholar
  4. 4.
    Bayramov, A.V., Martynova, N.Yu., Eroshkin, F.M., et al., The homeodomain-containing transcription factor X-nkx-5.1 inhibits expression of the homeobox gene Xanf-1 during the Xenopus laevis forebrain development, Mech Dev., 2004, vol. 121, pp. 1425–1441.Google Scholar
  5. 5.
    Bayramov, A.V., Ermakova, G.V., Eroshkin, F.M., et al., The presence of the Anf/Hesx1 homeobox in lampreys indicates that it may play important role in telencephalon emergence, Sci. Rep., 2016, vol. 6, p. 39849.Google Scholar
  6. 6.
    Bayramov, A.V., Ermakova, G.V., Eroshkin, F.M., et al., Presence of a homeobox gene of the Anf class in Pacific lamprey Lethenteron camtschaticum confirms the hypothesis about the importance of Anf gene emergence for the origin of telencephalon in vertebrate evolution, Russ. J. Dev. Biol., 2017, vol. 48, no. 4, pp. 241–251.Google Scholar
  7. 7.
    Beddington, R.S., Induction of a second neural axis by the mouse node, Development, 1994, vol. 120, pp. 613–620.Google Scholar
  8. 8.
    Bertolotti, E., Malagoli, D., and Franchini, A., Skin wound healing in different aged Xenopus laevis, J. Morphol., 2013, vol. 274, pp. 956–964.Google Scholar
  9. 9.
    Bjornson, C.R., Griffin, K.J., Farr, G.H., et al., Eomesodermin is a localized maternal determinant required for endoderm induction in zebrafish, Dev. Cell, 2005, vol. 9(4), pp. 523–533.Google Scholar
  10. 10.
    Cardozo, M.J., Mysiak, K.S., Becker, T., et al., Reduce, reuse, recycle - Developmental signals in spinal cord regeneration, Dev Biol., 2017, vol. 432(1), pp. 53–62.Google Scholar
  11. 11.
    Cattell, M.V., Garnett, A.T., Klymkowsky, M.W., et al., A maternally established SoxB1/SoxF axis is a conserved feature of chordate germ layer patterning, Evol Dev., 2012, vol. 14(1), pp. 104–115.Google Scholar
  12. 12.
    Chandran, V., Coppola, G., Nawabi, H., et al., A systems-level analysis of the peripheral nerve intrinsic axonal growth program, Neuron, 2016, vol. 89, pp. 956–970.Google Scholar
  13. 13.
    Chen, Y., Love, N.R., and Amaya, E., Tadpole tail regeneration in Xenopus, Biochem Soc Trans., 2014, vol. 3, pp. 617–623.Google Scholar
  14. 14.
    Cohen, A., Mackler, S., and Selzer, M., Behavioral recovery following spinal transections: functional regeneration in the lamprey CNS, Trends Neurosci., 1988, vol. 11, pp. 227–231.Google Scholar
  15. 15.
    De Robertis, E. M., Wessely, O., Oelgeschlager, M., et al., Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer, Int. J. Dev. Biol., 2001, vol. 45, pp. 189–197.Google Scholar
  16. 16.
    Derobert, Y., Baratte, B., Lepage, M., et al., Pax6 expression patterns in Lampetra fluviatilis and Scyliorhinus canicula embryos suggest highly conserved roles in the early regionalization of the vertebrate brain, Brain Res Bull., 2002, vol. 1, no. 57(3–4), pp. 277–280.Google Scholar
  17. 17.
    Diaz Quiroz, J.F. and Echeverri, K., Spinal cord regeneration: where fish, frogs and salamanders lead the way, can we follow?, Biochem. J., 2013, vol. 451, pp. 353–364.Google Scholar
  18. 18.
    Edwards-Faret, G., Munoz, R., Mendez-Olivos, E.E., et al., Spinal cord regeneration in Xenopus laevis, Nat. Protoc., 2017, vol. 12, pp. 372–389.Google Scholar
  19. 19.
    Ermakova, G.V., Alexandrova, E.M., Kazanskaya, O.V., et al., The homeobox gene, Xanf-1, can control both neural differentiation and patterning in the presumptive anterior neurectoderm of the Xenopus laevis embryo, Development, 1999, vol. 126, pp. 4513–4523.Google Scholar
  20. 20.
    Ermakova, G.V., Solovieva, E.A., Martynova, N.Y., et al., The homeodomain factor Xanf represses expression of genes in the presumptive rostral forebrain that specify more caudal brain regions, Dev. Biol., 2007, vol. 307, pp. 483–497.Google Scholar
  21. 21.
    Eroshkin, F., Kazanskaya, O., Martynova, N., et al., Characterization of cis-regulatory elements of the homeobox gene Xanf-1, Gene, 2002, vol. 285, pp. 279–286.Google Scholar
  22. 22.
    Feinberg, T.E. and Mallatt, J., The evolutionary and genetic origins of consciousness in the Cambrian Period over 500 million years ago, Front Psychol., 2013, vol. 4, p. 667. doi 10.3389/fpsyg.2013.00667Google Scholar
  23. 23.
    Feiner, N., Meyer, A., and Kuraku, S., Evolution of the vertebrate Pax4/6 class of genes with focus on its novel member, the Pax10 gene, Genome Biol. Evol., 2014, vol. 6, pp. 1635–1651.Google Scholar
  24. 24.
    Force, A., Amores, A., and Postlethwait, J.H., Hox cluster organization in the jawless vertebrate Petromyzon marinus, J Exp Zool., 2002, vol. 15, no. 294(1), pp. 30–46.Google Scholar
  25. 25.
    Gess, R.W., Coates, M.I., and Rubidge, B.S., A lamprey from the Devonian period of South Africa, Nature, 2006, vol. 443, no. 7114, pp. 981–984.Google Scholar
  26. 26.
    Godwin, J., The promise of perfect adult tissue repair and regeneration in mammals: learning from regenerative amphibians and fish, Bioessays, 2014, vol. 36, pp. 861–871.Google Scholar
  27. 27.
    Golichenkov, V.A., Ivanov, E.A., and Nikeryasova, E.N., Embriologiya (Embryology), Moscow: Izd. dom Akademiya, 2004, pp. 164–174.Google Scholar
  28. 28.
    Green, S.A., and Bronner, M.E., The Lamprey: A jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits, Differentiation, 2014, vol. 87, pp. 44–51.Google Scholar
  29. 29.
    Gurtner, G.C., Werner, S., Barrandon, Y., et al., Wound repair and regeneration, Nature, 2008, vol. 453, pp. 314–321.Google Scholar
  30. 30.
    Harland, R. and Gerhar, J., Formation and function of Spemann’s organizer, Annu. Rev. Cell Dev. Biol., 1997, vol.13, pp. 611–667.Google Scholar
  31. 31.
    Herman, P.E., Papatheodorou, A., Bryant, S.A., et al., Highly conserved molecular pathways, including Wnt signaling, promote functional recovery from spinal cord injury in lampreys, Sci. Rep., 2018, vol. 5, no. 8(1), p. 742.Google Scholar
  32. 32.
    Hugnot, J.P. and Franzen, R., The spinal cord ependymal region: a stem cell niche in the caudal central nervous system, Front Biosci (Landmark Ed), 2011, vol. 16, pp. 1044–1059.Google Scholar
  33. 33.
    Hume, J.B., Adams, C.E., Mable, B., et al., Post-zygotic hybrid viability in sympatric species pairs: a case study from European lampreys, Biol. J. Linn. Soc., 2013, vol. 108, no. 2, pp. 378–383.Google Scholar
  34. 34.
    Janvier, P., Modern look for ancient lamprey, Nature, 2006, vol. 433, pp. 921–924.Google Scholar
  35. 35.
    Kumamoto, T. and Hanashima, C., Evolutionary conservation and conversion of Foxg1 function in brain development, Dev. Growth Differ., 2017, vol. 59, no. 4, pp. 258–269.Google Scholar
  36. 36.
    Kuraku, S. and Kuratani, S., Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences, Zoolog Sci., 2006, vol. 23, no. 12, pp. 1053–1064.Google Scholar
  37. 37.
    Kuratani, S., Nobusada, Y., Horigome, N., et al., Embryology of the lamprey and evolution of the vertebrate jaws: insights from molecular and developmental perspectives, Philos, Trans R Soc., Lond., B Biol., Sci., 2001, vol. 356, no. 1414, pp. 1615–1632.Google Scholar
  38. 38.
    Lerch, J.K., Martinez-Ondaro, Y.R., Bixby, J.L., et al., cJun promotes CNS axon growth, Mol. Cell Neurosci., 2014, vol. 59, pp. 97–105.Google Scholar
  39. 39.
    Li, J., Zhang, S., and Amaya, E., The cellular and molecular mechanisms of tissue repair and regeneration as revealed by studies in Xenopus, Regeneration (Oxf), 2016, vol. 3, no. 4, pp. 198–208.Google Scholar
  40. 40.
    Lurie, D.I. and Selzer, M.E., Axonal regeneration in the adult lamprey spinal cord, J. Comp. Neurol., 1991, vol. 306, pp. 409–416.Google Scholar
  41. 41.
    Luttrell, S. M., Gotting, K., Ross, E., et al., Head regeneration in hemichordates is not a strict recapitulation of development, Dev Dyn., 2016, vol. 245, pp. 1159–1175.Google Scholar
  42. 42.
    Marín, O. and Rubenstein, J.L., A long, remarkable journey: tangential migration in the telencephalon, Nat. Rev. Neurosci., 2001, vol. 2, no. 11, pp. 780–790.Google Scholar
  43. 43.
    Martini, F. H. and Flescher, D., Hagfishes. Order Myxiniformes. In Fishes of the Gulf of Maine, 3rd Ed., Bigehow, H.B. and Schmeder, W.C., Eds., Washington: Smithsonian Institution Press, 2002, pp. 9–16.Google Scholar
  44. 44.
    Martynova, N.Yu., Eroshkin, F.M., Ermakova, G.V., et al., Patterning the forebrain: FoxA4a/Pintallavis and Xvent-2 determine the posterior limit of the Xanf-1 expression in the neural plate, Development, 2004, vol. 131, p. 2329–2338.Google Scholar
  45. 45.
    McCauley, D.W., Docker, M.F., Whyard, S., et al., Lampreys as diverse model organisms in the genomics era, Bioscience, 2015, vol. 65(11), pp. 1046–1056.Google Scholar
  46. 46.
    Medina, L., Evolution and Embryological Development of Forebrain, Brain Inflammation: Biomedical Imaging, 2009, pp. 1172–1192.Google Scholar
  47. 47.
    Mehta, T.K., Ravi, V., Yamasaki, S., et al., Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum), Proc. Natl. Acad. Sci. USA., 2013, vol. 110, pp.16044–16049.Google Scholar
  48. 48.
    Murakami, Y., Ogasawara, M., Sugahara, F., et al., Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates, Development, 2001, vol. 128(18), pp. 3521–3531.Google Scholar
  49. 49.
    Murakami, Y, Uchida, K, Rijli, F.M., et al., Evolution of the brain developmental plan: Insights from agnathans, Dev Biol., 2005, vol. 280, p. 249–259.Google Scholar
  50. 50.
    Myojin, M., Ueki, T., Sugahara, F., et al., Isolation of Dlx and Emx gene cognates in an agnathan species, Lampetra japonica, and their expression patterns during embryonic and larval development: conserved and diversified regulatory patterns of homeobox genes in vertebrate head evolution, J. Exp. Zool., 2001, vol. 15, no. 291(1), pp. 68–84.Google Scholar
  51. 51.
    Neidert, A.H., Virupannavar, V., Hooker, G.W., et al., Lamprey Dlx genes and early vertebrate evolution, Proc Natl Acad Sci U S A, 2001, vol. 13, no. 98(4), pp. 1665–1670.Google Scholar
  52. 52.
    Niazi, I.A., The histology of tail regeneration in the ammocoetes, Can. J. Zool., 1963, vol. 41.Google Scholar
  53. 53.
    Oisi, Y., Ota, K.G., Kuraku, S., et al., Craniofacial development of hagfishes and the evolution of vertebrates, Nature, 2013, vol. 10, no. 493(7431), pp. 175–180.Google Scholar
  54. 54.
    Osório, J. and Rétaux, S., The lamprey in evolutionary studies, Dev Genes Evol., 2008, vol. 218(5), pp. 221–235.Google Scholar
  55. 55.
    Ota, K.G. and Kuratani, S., The history of scientific endeavors towards understanding hagfish embryology, Zoolog Sci., 2006, vol. 23(5), pp. 403–418.Google Scholar
  56. 56.
    Ota, K.G., Kuraku, S., and Kuratani, S., Hagfish embryology with reference to the evolution of the neural crest, Nature, 2007, vol. 446, pp. 672–675.Google Scholar
  57. 57.
    Parker, D., The lesioned spinal cord is a “new” spinal cord: evidence from functional changes after spinal injury in lamprey, Front Neural Circuits, 2017, vol. 11, p. 84.Google Scholar
  58. 58.
    Pavlov, D.S., Nazarov, D.Yu., Zvezdin, A.O., and Kucheryavyi, A.V., Downstream migration of early larvae of the European river lamprey Lampetra fluviatilis, Dokl. Biol. Sci., 2014, vol. 459, no. 1, pp. 344–347.Google Scholar
  59. 59.
    Piavis, G.W., Embryological stages in the sea lamprey and effects of temperature on development, U.S. Fish Wildl. Serv. Biol. Bull., 1961, vol. 182, no. 61, pp. 111–143.Google Scholar
  60. 60.
    Putnam, N.H., Butts, T., Ferrier, D.E., et al., The amphioxus genome and the evolution of the chordate karyotype, Nature, 2008, vol. 453, pp. 1064–1071.Google Scholar
  61. 61.
    Renaud, C.B., Lampreys of the world. An annotated and illustrated catalogue of lamprey species known to date, FAO Species Catalogue for Fishery Purposes, 2011, vol. 5, p. 109.Google Scholar
  62. 62.
    Reyes, R.C., Embryogenesis and ammocoete morphological development of the Pacific lamprey (Entosphenus tridentatus Gairdner, 1836) from the American River, California, Tracy Technical Bull., 2008, vol. 3, p. 28.Google Scholar
  63. 63.
    Richardson, M.K. and Wright, G.M., Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus), J. Morph., 2003, vol. 257, no. 3, pp. 348–363.Google Scholar
  64. 64.
    Richardson, M.K., Admiraal, J., and Wright, G.M., Developmental anatomy of lampreys., Biol Rev Camb Philos Soc., 2010, vol. 85, no. 1, pp. 1–33.Google Scholar
  65. 65.
    Seifert, A.W. and Maden, M., New insights into vertebrate skin regeneration, Int. Rev. Cell Mol. Biol., 2014, vol. 310, pp. 129–169.Google Scholar
  66. 66.
    Shih, J., and Fraser, S. E., Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage, Development, 1996, vol. 122, pp. 1313–1322.Google Scholar
  67. 67.
    Smith, A.J., Howell, J.H., and Piavis, G.W., Comparative embryology of five species of lamprey of the Upper Great Lakes, Copeia, 1968, vol. 3, pp. 461–469.Google Scholar
  68. 68.
    Smith, R.P., Lerch-Haner, J.K., Pardinas, J.R., et al., Transcriptional profiling of intrinsic PNS factors in the postnatal mouse, Mol Cell Neurosci., 2011, vol. 46, pp. 32–44.Google Scholar
  69. 69.
    Smith, J.J., Kuraku, S., Holt, C., et al., Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution, Nat Genet., 2013, vol. 45, p. 415–421.Google Scholar
  70. 70.
    Spemann, H. and Mangold, H., Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren, Arch. Mikrosk. Anat. Entwicklungsmechanik, 1924, vol. 100, pp. 599–638.Google Scholar
  71. 71.
    Square, T., Romášek, M., Jandzik, D., et al., CRISPR/ Cas9-mediated mutagenesis in the sea lamprey Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates, Development, 2015, vol. 142, no. 23, pp. 4180–4187.Google Scholar
  72. 72.
    Strand, N.S., Hoi, K.K., Phan, T.M.T., et al., Wnt/β-catenin signaling promotes regeneration after adult zebrafish spinal cord injury, Biochem Biophys Res Commun., 2016, vol. 477, no. 4, pp. 952–956.Google Scholar
  73. 73.
    Suda, Y., Kurokawa, D., Takeuchi, M., et al., Evolution of Otx paralogue usages in early patterning of the vertebrate head, Dev Biol. 2009, vol. 325, no. 1, pp. 282–295.Google Scholar
  74. 74.
    Sugahara, F., Murakami, Y., and Kuratani, S., Gene expression analysis of lamprey embryo, N. Y.: Springer, 2015.Google Scholar
  75. 75.
    Sugahara, F., Pascual-Anaya, J., Oisi, Y., et al., Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain, Nature, 2016, vol. 531, pp. 97–100.Google Scholar
  76. 76.
    Sugahara, F., Murakami, Y., Pascual-Anaya, J., et al., Reconstructing the ancestral vertebrate brain, Dev. Growth Differ., 2017, vol. 59(4), pp.163–174.Google Scholar
  77. 77.
    Sussel, L., Marin, O., Kimura, S., et al., Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum, Development, 1999, vol. 126, pp. 3359–3370.Google Scholar
  78. 78.
    Tahara, Y., Normal stages of development in the lamprey, Lampetra reissneri (Dybowski), Zool. Sci., 1988, vol. 5, p. 109–118.Google Scholar
  79. 79.
    Takeuchi, M., Takahashi, M., Okabe, M., et al., Germ layer patterning in bichir and lamprey; an insight into its evolution in vertebrates, Dev Biol., 2009, vol. 332, no. 1, pp. 90–102.Google Scholar
  80. 80.
    Tanaka, E.M. and Ferretti, P., Considering the evolution of regeneration in the central nervous system, Nat Rev Neurosci., 2009, vol. 10, pp. 713–723.Google Scholar
  81. 81.
    Tank, E.M., Dekker, R.G., Beauchamp, K., et al., Patterns and consequences of vertebrate Emx gene duplications, Evol Dev., 2009, vol. 11, no. 4, pp. 343–353.Google Scholar
  82. 82.
    Tomsa, J.M. and Langeland, J.A., Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw, Dev Biol., 1999, vol. 207, no. 1, pp. 26–37.Google Scholar
  83. 83.
    Tsimbalov, I.A., Kucheryuavyi, A.V., and Pavlov, D.S., Results of hybridization between anadromous and resident forms of European river lamprey Lampetra fluviatilis, J. Ichthyol., 2018, vol. 58, no. 1, pp. 122–125.Google Scholar
  84. 84.
    Vergara, M.N., Arsenijevic, Y., and Del Rio-Tsonis, K., CNS regeneration: a morphogen’s tale, J. Neurobiol., 2005, vol. 64, pp. 491–507.Google Scholar
  85. 85.
    Wullimann, M.F., Mueller, T., Distel, M., et al., The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis, Front. Neuroanat., 2011, vol. 5, p. 27.Google Scholar
  86. 86.
    Xu, P.F., Houssin, N., Ferri-Lagneau, K.F., et al., Construction of a vertebrate embryo from two opposing morphogen gradients, Science, 2014, vol. 344, pp. 87–89.Google Scholar
  87. 87.
    Xuan, S., Baptista, C.A., Balas, G., et al., Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres, Neuron, 1995, vol. 14, no. 6, pp. 1141–1152.Google Scholar
  88. 88.
    Yang, X.U., Si-Wei, Z.H.U., and Qing-Wei, L.I., Lamprey: a model for vertebrate evolutionary research, Dongwuxue Yanjiu, 2016, vol. 37, no. 5, pp. 263–269.Google Scholar
  89. 89.
    Yokoyama, H., Maruoka, T., Aruga, A., et al., Prx-1 expression in Xenopus laevis scarless skin-wound healing and its resemblance to epimorphic regeneration, J. Invest.Dermatol., 2011, vol. 131, pp. 2477–2485.Google Scholar
  90. 90.
    Zhang, H., Ravi, V., Tay, B.H., et al., Lampreys, the jawless vertebrates, contain only two ParaHox gene clusters, Proc Natl Acad Sci U S A, 2017, vol. 114, no. 34, p. 9146–9151.Google Scholar
  91. 91.
    Zhang, J., Houston, D.W., King, M.L., et al., The role of maternal VegT in establishing the primary germ layers in Xenopus embryos, Cell, 1998, vol. 94, no. 4, pp. 515–524.Google Scholar
  92. 92.
    Zu, Y., Zhang, X., Ren, J., et al., Biallelic editing of a lamprey genome using the CRISPR/Cas9 system, Sci Rep., 2016, vol. 6, p. 23496.Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • A. V. Bayramov
    • 1
    Email author
  • G. V. Ermakova
    • 1
  • A. V. Kucheryavyy
    • 2
  • A. G. Zaraisky
    • 1
  1. 1.Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesMoscowRussia
  2. 2.Severtsov Institute of Ecology and Evolution, Russian Academy of SciencesMoscowRussia

Personalised recommendations