Skip to main content
Log in

Instability Stabilized: Mechanisms of Evolutionary Stasis and Genetic Diversity Accumulation in Fishes and Lampreys from Environments with Unstable Abiotic Factors

  • Published:
Contemporary Problems of Ecology Aims and scope

Abstract

As studies have shown, individuals from well morphologically distinct groups often represent the same species and may even belong to one population in fishes and lampreys from environments with unstable abiotic factors (Arctic, mountain, and desert regions). Phenotypic plasticity ensures broad variation ranges of morphological traits in unstable conditions, which require rapid transitions from one morphogenetic variant to another. The choice of a morphogenetic pathway can be influenced by the level of individual heterozygosity, changes in the copy numbers of certain DNA sequences, heteroplasmy, and the presence of several allelic variants in the genes that strongly affect the phenotype. A cyclic character is often observed for evolutionary processes driven by these mechanisms, and speciation usually does not take place in unstable environmental conditions. However, mobilization reserve accumulate in a species with a broad reaction norm, and particular morphogenetic pathways may be genetically fixed when its population finds its way into stable environmental conditions, facilitating fast allopatric speciation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Abadía-Cardoso, A., Anderson, E.C., Pearse, D.E., and Garza, J.C., Large-scale parentage analysis reveals reproductive patterns and heritability of spawn timing in a hatchery population of steelhead (Oncorhynchus mykiss), Mol. Ecol., 2013, vol. 22, pp. 4733–4746.

    PubMed  Google Scholar 

  2. Alekseeva, Ya.I. and Makhrov, A.A., Origin of the vendace near Solovetsky Islands: Archive documents in the study if microevolution, Priroda (Moscow), 2017, no. 7, pp. 37–46.

  3. Allendorf, F.W. and Thorgaard, G.H., Tetraploidy and the evolution of Salmonid fishes, in Evolutionary Genetics of Fishes, New York: Plenum, 1984, pp. 1–53.

    Google Scholar 

  4. Altukhov, Yu.P., Geneticheskie protsessy v populyatsiyakh (Genetic Processes in Populations), Moscow: Akademkniga, 2003, 3rd ed.

  5. Arostegui, M.C., Quinn, T.P., Seeb, L.W., Seeb, J.E., and McKinney, G.J., Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout, Mol. Ecol., 2019, vol. 28, pp. 1412–1427.

    CAS  PubMed  Google Scholar 

  6. Artamonova, V.S. and Makhrov, A.A., The influence of genotype on habitat selection of fish and the analysis of population structure, Knowl. Manage. Aquat. Ecosyst., 2016, vol. 417, p. 3.

    Google Scholar 

  7. Artamonova, V.S., Makhrov, A.A., and Popova, E.K., Unintentional selection in captive brood stocks intended for restoring natural populations: description of the phenomenon and a novel method of controlling it, in Stream Restoration: Halting Disturbances, Assisted Recovery and Managed Recovery, Hayes, G.D. and Flores, T.S., Eds., New York: Nova Science, 2010, pp. 149–160.

    Google Scholar 

  8. Artamonova, V.S., Makhrov, A.A., Karabanov, D.P., Rolskiy, A.Yu., Bakay, Yu.I., and Popov, V.I., Hybridization of beaked redfish (Sebastes mentella) with small redfish (S. viviparus) and diversification of redfish (Actinopterygii: Scorpaeniformes) in the Irminger Sea, J. Nat. Hist., 2013, vol. 47, pp. 1791–1801.

    Google Scholar 

  9. Artamonova, V.S., Kucheryavyy, A.V., and Makhrov, A.A., Nucleotide sequence diversity of the mitochondrial cytochrome oxidase subunit I (COI) gene of the Arctic lamprey (Lethenteron camtschaticum) in the Eurasian part of the range, Hydrobiologia, 2015, vol. 757, pp. 197–208.

    CAS  Google Scholar 

  10. Artamonova, V.S., Kolmakova, O.V., Kirillova, E.A., and Makhrov, A.A., Phylogeny of salmonoid fishes (Salmonoidei) based on mtDNA COI gene sequences (barcoding), Contemp. Probl. Ecol., 2018, vol. 11, no. 3, pp. 271–285.

    Google Scholar 

  11. Barson, N.J., Aykanat, T., Hindar, K., Baranski, M., Bolstad, G.H., Fiske, P., Jacq, C., Jensen, A.J., Johnston, S.E., Karlsson, S., Kent, M., Moen, T., Niemelä, E., Nome, T., Næsje, T.F., et al., Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon, Nature, 2015, vol. 528, pp. 405–408.

    CAS  PubMed  Google Scholar 

  12. Bateman K.G., The genetic assimilation of four venation phenocopies, J. Genet., 1959, vol. 56, pp. 443–474.

    Google Scholar 

  13. Bell, M.A. and Aguirre, W.E., Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback, Evol. Ecol. Res., 2013, vol. 15, pp. 377–411.

    Google Scholar 

  14. Bell, M.A. and Andrews, C.A., Evolutionary consequences of postglacial colonization of fresh water by primitively anadromous fishes, in Evolutionary Ecology of Freshwater Animals, Streit, B., Städler, T., and Lively, C.M., Eds., Basel: Birkhäuser, 1997, pp. 323–363.

    Google Scholar 

  15. Berman, D.I. and Leirikh, A.N., The cold hardiness of mass soil invertebrates of Northeastern Asia: 2. The cold hardiness of soil invertebrates as adaptation to climate, Biol. Bull. (Moscow), 2018, vol. 45, pp. 680–690.

    Google Scholar 

  16. Bernatchez, L., On the maintenance of genetic variation and adaptation to environmental change: considerations from population genomics in fishes, J. Fish Biol., 2016, vol. 89, pp. 2519–2556.

    CAS  PubMed  Google Scholar 

  17. Best, C., Ikert H., Kostyniuk D.J., Craig P.M., Navarro-Martin L., Marandel L., and Mennigen, J.A., Epigenetics in teleost fish: From molecular mechanisms to physiological phenotypes, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2018, vol. 224, pp. 210–244.

    CAS  Google Scholar 

  18. Birshtein, Ya.A., Genezis presnovodnoi, peshchernoi i glubokovodnoi faun (Genesis of Freshwater, Cave, and Abyssal Faunas), Moscow: Nauka, 1985.

  19. Bochkarev, N.A., Zuykova, E.I., and Solovyev, M.M., Secondary intergradation of various forms of pidschian-like whitefishes (Coregonus lavaretus sensu lato, Coregonidae) in the water bodies of the Altai-Sayan Mountains, Russ. J. Genet.: Appl. Res., 2018, vol. 8, pp. 178–189.

    CAS  Google Scholar 

  20. Bolotov, I.N., Bespalaya, Yu.V., and Usacheva, O.V., Ecology and evolution of hydrobionts in hot springs of the Subarctic and Arctic: formation of similar assemblages, adaptation of species, and microevolutionary processes, Biol. Bull. Rev., 2012, vol. 2, no. 4, pp. 340–348.

    Google Scholar 

  21. Bolotov, I.N., Aksenova, O.V., Bespalaya, Yu.V., and Spitsyn, V.M., Endemism of freshwater fishe fauna in geothermal regions: a review of molecular-biogeographic studies, Vestn. Sev. (Arkt.) Fed. Univ., Ser.: Estestv. Nauki, 2016a, no. 1, pp. 29–50.

  22. Borovikova, E.A. and Makhrov, A.A., systematic position and origin of whitefishes (Coregonus) of Europe: morphoecological approach, Tr. Karel. Nauchn. Tsentra, Ross. Akad. Nauk, 2013, no. 6, pp. 105-115.

  23. Borovikova, E.A., Gordon, N.Yu., Sharova, Ju.N., and Politov, D.V., Length variation in the mtDNA control region in Coregonus lavaretus nelmuschka from Lake Kubenskoye and related whitefish forms of northwest Russia, Adv. Limnol., 2007, vol. 60, pp. 59–67.

    CAS  Google Scholar 

  24. Borovikova, E.A., Alekseeva, Ya.I., Schreider, M.J., Artamonova, V.S., and Makhrov, A.A., Morphology and genetics of the ciscoes (Actinopterygii: Salmoniformes: Salmonidae: Coregoninae: Coregonus) from the Solovetsky Archipelago (White Sea) as a key to determination of the taxonomic position of ciscoes in Northeastern Europe, Acta Ichthyol. Piscat., 2013, vol. 43, pp. 183–194.

    Google Scholar 

  25. Borovikova, E.A., Kodukhova, Yu.V., and Semenova, A.V., High level of allometry, phenotypic plasticity of osteological features of the migratory and lake ecological forms of Coregonus lavaretus (Linnaeus, 1758), and evidences of the unlawfulness of the isolation of the species C. pidschian,Sib. Ekol. Zh., 2020 (in press).

  26. Brochmann, C., Brysting, A.K., Alsos, I.G., Borgen, L., Grundt, H.H., Scheen, A.-C., and Elven, R., Polyploidy in arctic plants, Biol. J. Linn. Soc., 2004, vol. 82, pp. 521–536.

    Google Scholar 

  27. Brzuzan, P., Tandemly repeated sequences in mtDNA control region of whitefish, Coregonus lavaretus,Genome, 2000, vol. 43, pp. 584–587.

    CAS  PubMed  Google Scholar 

  28. Cadrin, S.X., Bernreuther, M., Daníelsdóttir, A.K., Hjörleifsson, E., Johansen, T., Kerr, L., Kristinsson, K., Mariani, S., Nedreaas, K., Pampoulie, C., Planque, B., Reinert, J., Saborido-Rey, F., Sigurðsson, T., and Stransky, C., Population structure of beaked redfish, Sebastes mentella: evidence of divergence associated with different habitats, ICES J. Mar. Sci., 2010, vol. 67, pp. 1617–1630.

    Google Scholar 

  29. Casacuberta, E. and González, J., The impact of transposable elements in environmental adaptation, Mol. Ecol., 2013, vol. 22, pp. 1503–1517.

    CAS  PubMed  Google Scholar 

  30. Chapman, J.R., Nakagawa, S., Coltman, D.W., Slate, J., and Sheldon, B.C., A quantitative review of heterozygosity—fitness correlations in animal populations, Mol. Ecol., 2009, vol. 18, pp. 2746–2765.

    CAS  PubMed  Google Scholar 

  31. Chernov, V.M. and Borkhsenius, S.N., Quantitative analysis of genome homology between species of Pacific salmons of genus Oncorhynchus and intraspecific forms of sockeye salmon, Sb. Nauchn. Tr.-Gos. Nauchno-Issled. Inst. Ozern. Rechn. Rybn. Khoz., 1987, no. 261, pp. 84–94.

  32. Czorlich, Y., Aykanat, T., Erkinaro, J., Orell, P., and Primmer, C.R., Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon, Nat. Ecol. Evol., 2018, vol. 2, pp. 1800–1807.

    PubMed  PubMed Central  Google Scholar 

  33. Cucherousset, J., Ombredane, D., Charles, K., Marchand, F., and Baglinière, J.-L., A continuum of life history tactics in a brown trout (Salmo trutta) population, Can. J. Fish. Aquat. Sci., 2005, vol. 62, pp. 1600–1610.

    Google Scholar 

  34. Dai, Y. and Han, H., Karyological analysis of two species in the subfamily schizothoracinae (Cypriniformes: Cyprinidae) from China, with notes on karyotype evolution in schizothoracinae, Turk. J. Fish. Aquat. Sci., 2018, vol. 18, pp. 175–186.

    Google Scholar 

  35. de Graaf, M., Megens, H.-J., Samallo, J., and Sibbing, F., Preliminary insight into the age and origin of the Labeobarbus fish species flock from Lake Tana (Ethiopia) using the mtDNA cytochrome b gene, Mol. Phylogenet. Evol., 2010, vol. 54, pp. 336–343.

    PubMed  Google Scholar 

  36. Denys, G.P.J., Geiger, M.F., Persat, H., Keith, P., and Dettai, A., Invalidity of Gasterosteus gymnurus (Cuvier, 1829) (Actinopterygii, Gasterosteidae) according to integrative taxonomy, Cybium, 2015, vol. 39, pp. 37–45.

    Google Scholar 

  37. Dgebuadze, Yu.Yu., Ekologicheskie zakonomernosti izmenchivosti rosta ryb (Ecological Pattern of Growth Variability of Fishes), Moscow: Nauka, 2001.

  38. Dunbar, M.J., Ecological Development in Polar Regions. A Study in Evolution, Englewood Cliffs, NJ: Prentice-Hall, 1968.

    Google Scholar 

  39. Dynesius, M. and Jansson, R., Evolutionary consequences of changes in species’ geographical distributions driven by Milankovitch climate oscillations, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 9115–9120.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Dzerzhinskii, K.F., Shkil, F.N., Abdissa, B., Zelalem, W., and Mina, M., Spawning of large barbus (Barbus intermedins Complex) in a small river of the Lake Tana basin (Ethiopia) and relationships of some putative species, J. Ichthyol., 2007, vol. 47, pp. 639–646.

    Google Scholar 

  41. Esin, E.V. and Markevich, G.N., Gol’tsy roda Salvelinus aziatskoi chasti Severnoi Patsifiki: proiskhozhdenie, evolyutsiya i sovremennoe raznoobrazie (Chars of Genus Salvelinus from Asian Part of Northern Pacific: Origin, Evolution, and Modern Diversity), Petropavlovsk-Kamchatski: Kamchatpress, 2017.

  42. Etheridge, E.C., Adams, C.E., Bean, C.W., Durie, N.C., Gowans, A.R.D., Harrod, C., Lyle, A.A., Maitland, P.S., and Winfield, I.J., Are phenotypic traits useful for differentiating among a priori Coregonus taxa? J. Fish Bio-l., 2012, vol. 80, pp. 387–407.

    CAS  Google Scholar 

  43. Ferguson, A., Reed, T.E., Cross, T.F., McGinnity, P., and Prodöhl, P.A., Anadromy, potamodromy and residency in brown trout Salmo trutta: the role of genes and the environment, J. Fish Biol., 2019, vol. 95, pp. 692–718.

    PubMed  PubMed Central  Google Scholar 

  44. Frolov, S.V., Specific karyotype of endemic fish Salvethymus svetovidovi,Dokl. Akad. Nauk, 1993, vol. 329, no. 3, pp. 363–364.

    Google Scholar 

  45. Gause, G.F., The relation of adaptability to adaptation, Quat. Rev. Biol., 1942, vol. 17, pp. 99–114.

    Google Scholar 

  46. Gauze, G.F., Ecology and origin of the species, in Ekologiya i evolyutsionnaya teoriya (Ecology and the Theory of Evolution), Leningrad: Nauka, 1984, pp. 5–105.

  47. Gauze, G.F. and Alpatov, V.V., The inverse relationship between the acquired and innate properties of organisms, Dokl. Akad. Nauk SSSR, 1941, vol. 30, no. 3, pp. 252–253.

    Google Scholar 

  48. Gershenzon, S.M., “Mobilization reserve” of intraspecific variability, Zh. Obshch. Biol., 1941, vol. 2, no. 1, pp. 85–107.

    Google Scholar 

  49. Golubtsov, A.S., Vnutripopulyatsionnaya izmenchivost’ zhivotnykh i belkovyi polimorfizm (Intrapopulation Variability of Animals and Protein Polymorphism), Moscow: Nauka, 1988.

  50. Golubtsov, A.S. and Krysanov, E.Yu., Karyological study of some cyprinid species from Ethiopia. The ploidy differences between large and small Barbus of Africa, J. Fish Biol., 1993, vol. 42, pp. 445–455.

    Google Scholar 

  51. Gunter, H.M., Schneider, R.F., Karner, I., Sturmbauer, C., and Meyer, A., Molecular investigation of genetic assimilation during the rapid adaptive radiations of East African cichlid fishes, Mol. Ecol., 2017, vol. 26, pp. 6634–6653.

    CAS  PubMed  Google Scholar 

  52. Hume, J.B., Recknagel, H., Bean, C.W., Adams, C.E., and Mable, B.K., RADseq and mate choice assays reveal unidirectional gene flow among three lamprey ecotypes despite weak assortative mating: insights into the formation and stability of multiple ecotypes in sympatry, Mol. Ecol., 2018, vol. 27, pp. 4572–4590.

    CAS  PubMed  Google Scholar 

  53. Ishikawa, A., Kabeya, N., Ikeya, K., Kakioka, R., Cech, J.N., Osada, N., Leal, M.C., Inoue, J., Kume, M., Toyoda, A., Tezuka, A., Nagano, A.J., Yamasaki, Y.Y., Suzuki, Y., Kokita, T., et al., A key metabolic gene for recurrent freshwater colonization and radiation in fishes, Science, 2019, vol. 364, pp. 886–889.

    CAS  PubMed  Google Scholar 

  54. Jonsson, B. and Jonsson, N., Polymorphism and speciation in Arctic charr, J. Fish Biol., 2001, vol. 58, pp. 605–638.

    Google Scholar 

  55. Karabanov, D.P., Kodukhova, Yu.V., and Kutsokon’, Yu.K., Expansion of Amur stone moroko Pseudorasbora parva (Cypriniformes, Cyprinidae) into reservoirs of Eurasia, Vestn. Zool., 2010, vol. 44, no. 2, pp. 115–124.

    Google Scholar 

  56. Kaufman, Z.S., Adaptation of hydrobionts to conditions of high altitudes, Tr. Karel. Nauchn. Tsentra, Ross. Akad. Nauk, 2015, no. 1, pp. 3–19.

  57. Kekäläinen, J., Oskoei, P., Janhunen, M., Koskinen, H., Kortet, R., and Huuskonen, H., Sperm pre-fertilization thermal environment shapes offspring phenotype and performance, J. Exp. Biol., 2018, vol. 221, art. ID jeb181412.

    PubMed  Google Scholar 

  58. Khlebovich, V.V., Discrete adaptive norms: mechanisms and role in evolution, Tr. Zool. Inst.,Ross. Akad. Nauk, 2009, suppl. 1, pp. 219–231.

  59. Khlebovich, V.V., Ekologiya osobi. Ocherki fenotipicheskikh adaptatsii zhivotnykh (Ecology of a Species: Description of Phenotypic Adaptations of the Animals), St. Petersburg: Zool. Inst., Ross. Akad. Nauk, 2012.

  60. Kirpichnikov, V.S., Geneticheskie osnovy selektsii ryb (Genetic Principles of Fish Breeding), Leningrad: Nauka, 1979.

  61. Klementsen, A., The charr problems revisited: exceptional phetotypic plasticity promotes ecological speciation in postglacial lakes, Freshwater Rev., 2010, vol. 3, pp. 49–74.

    Google Scholar 

  62. Kmiec, B., Woloszynska, M., and Janska, H., Heteroplasmy as a common state of mitochondrial genetic information in plants and animals, Curr. Genet., 2006, vol. 50, pp. 149–159.

    CAS  PubMed  Google Scholar 

  63. Knudsen, R., Klemetsen, A., Alekseyev, S., Adams, C.E., and Power, M., The role of Salvelinus in contemporary studies of evolution, trophic ecology and anthropogenic change, Hydrobiologia, 2016, vol. 783, pp. 1–9.

    Google Scholar 

  64. Kondrashov, A.S. and Mina, M.V., Sympatric speciation: when is it possible? Biol. J. Linn. Soc., 1986, vol. 27, pp. 201–223.

    Google Scholar 

  65. Kosyuk, G.N. and Borkhsenus, S.N., Intrapopulation differences in the genome structure of two species of salmons, Mol. Biol. (Moscow), 1981, vol. 15, no. 3, pp. 547–553.

    Google Scholar 

  66. Kottelat, M. and Freyhof, J., Handbook of European Freshwater Fishes, Gland: World Conserv. Union, IUCN, 2007.

  67. Krysanov, E., Demidova, T., and Nagy, B., Divergent karyotypes of the annual killifish genus Nothobranchius (Cyprinodontiformes; Nothobranchiidae), Comp. Cytogenet., 2016, vol. 10, pp. 439–445.

    PubMed  PubMed Central  Google Scholar 

  68. Laius, D.L. and Laius, Yu.A., Random variability as a independent type of phenotypic variation, in Evolyutsionnaya biologiya: istoriya i teoriya (Evolutionary Biology: History and Theory), St. Petersburg, 2003, no. 2, pp. 117–133.

  69. Lajus, D.L., Graham, J.H., and Kozhara, A.V., Developmental instability and the stochastic component of total phenotypic variance, in Developmental Instability: Causes and Consequences, Polak, M., Ed., Oxford: Oxford Univ. Press, 2003, pp. 243–363.

    Google Scholar 

  70. Leary, R.F., Allendorf, F.W., and Knudsen, K.L., Major morphological effects of a regulatory gene: Pgm1-t in rainbow trout, Mol. Biol. Evol., 1984, vol. 1, pp. 183–194.

    CAS  PubMed  Google Scholar 

  71. Levin, B.A., Casal-Lóez, M., Simonov, E., Dgebuadze, Yu.Y., Mugue, N.S., Tiunov, A.V., Doadrio, I., and Golubtsov, A.S., Adaptive radiation of barbs of the genus Labeobarbus (Cyprinidae) in an East African river, Freshwater Biol., 2019, vol. 64, pp. 1721–1736.

  72. Lowe, S., Browne, M., Boudjelas, S., and De Poorter, M., 100 of the World’s Worst Invasive Alien Species A selection from the Global Invasive Species Database, Auckland: Invasive Species Spec. Group, 2004.

  73. Lunt, D.H., Whipple, L.E., and Hyman, B.C., Mitochondrial DNA variable number tandem repeats (VNTRs): utility and problems in molecular ecology, Mol. Ecol., 1998, vol. 7, pp. 1441–1455.

    CAS  PubMed  Google Scholar 

  74. Makhrov, A.A., A narrowing of the phenotypic diversity range after large rearrangements of the karyotype in Salmonidae: the relationship between saltational genome rearrangements and gradual adaptive evolution, Genes, 2017, vol. 8, p. 297.

    PubMed Central  Google Scholar 

  75. Makhrov, A.A. and Bolotov, I.N., Ecological causes of high morphological plasticity of members of a taxon inhabiting the center of its origin (exemplified by the noble salmons, genus Salmo), Biol. Bull. (Moscow), 2019, vol. 46, pp. 38–46.

    Google Scholar 

  76. Makhrov, A.A. and Popov, I.Yu., Life forms of lampreys (Petromyzontidae) as a manifestation of intraspecific diversity of ontogenesis, Russ. J. Dev. Biol., 2015, vol. 46, pp. 196–207.

    Google Scholar 

  77. Makhrov, A.A., Kuzishin, K.V., and Novikov, G.G., Genetic differentiation of brown trout Salmo trutta L. from streams flowing into the Velikaya Salma streit (White Sea), Russ. J. Genet., 1999, vol. 35, pp. 830–836.

    CAS  Google Scholar 

  78. Makhrov, A.A., Artamonova, V.S., Sumarokov, V.S., Pashkov, A.N., Reshetnikov, S.I., Ganchenko, M.V. and Kulyan, S.A., Variation in the timing of spawning of the Black Sea brown trout Salmo trutta labrax Pallas under artificial and natural conditions, Biol. Bull. (Moscow), 2011a, vol. 38, pp. 138–145.

    Google Scholar 

  79. Makhrov, A.A., Artamonova, V.S., Popov, V.I., Rolskiy, A.Yu., and Bakay, Yu.I., Comment on: Cadrin et al. (2010) “Population structure of beaked redfish, Sebastes mentella: evidence of divergence associated with different habitats. ICES Journal of Marine Science, 67: 1617–1630”, ICES J. Mar. Sci., 2011b, vol. 68, pp. 2013–2015.

    Google Scholar 

  80. Makhrov, A.A., Artamonova, V.S., Bobrov, V.V., Koblik, E.A., Lebedev, V.S., Pavlova, S.V., and Sheftel’, B.I., Journey thought Qinling Mountains and eastern margin of Tibet: from subtropics to taiga and tundra-steppes, Priroda (Moscow), 2019a, no. 3, pp. 70–83.

  81. Makhrov, A.A., Bolotov, I.N., Spitsyn, V.M., Gofarov, M.Yu., and Artamonova, V.S., Resident and anadromous forms of arctic charr (Salvelinus alpinus) from North-East Europe: an example of high ecological variability without speciation, Dokl. Biochem. Biophys., 2019b, vol. 485, no. 2, pp. 119–122.

    CAS  PubMed  Google Scholar 

  82. Markov, A.V. and Ivnitsky, S.B., Evolutionary role of phenotypic plasticity, Moscow Univ. Biol. Sci. Bull., 2016, vol. 71, no. 4, pp. 185–192.

    Google Scholar 

  83. McPhee, M.V., Utter, F., Stanford, J.A., Kuzishchin, K.V., Savvaitova, K.A., Pavlov, D.S., and Allendorf, F.W., Population structure and partial anadromy in Oncorhynchus mykiss from Kamchatka: relevance for conservation strategies around the Pacific Rim, Ecol. Freshwater Fish., 2007, vol. 16, pp. 539–547.

    Google Scholar 

  84. McPhee, M.V., Noakes, D.L.G., and Allendorf, F.W., Developmental rate: a unifying mechanism for sympatric divergence in postglacial fishes? Curr. Zool., 2012, vol. 58, pp. 21–34.

    Google Scholar 

  85. Mednikov, B.M., Ecological forms of fishes and sympatric speciation, Zool Zh., 1963, vol. 42, no. 1, pp. 70–77.

    Google Scholar 

  86. Mednikov, B.M., Genome divergence and evolutionary theory, Doctoral (Biol.) Dissertation, Moscow, 1977.

  87. Mednikov, B.M., Speciation and adaptive norms, Zh. Obshch. Biol., 1987, vol. 48, no. 1, pp. 15–26.

    CAS  PubMed  Google Scholar 

  88. Merilä, J., Nine-spined stickleback (Pungitius pungitius): an emerging model for evolutionary biology research, Ann. N. Y. Acad. Sci., 2013, vol. 1289, pp. 18–35.

    PubMed  Google Scholar 

  89. Mezhzherin, S.V., Kokodii, S.V., Kulish, A.V., and Fedorenko, L.V., The structure of hybrids Carassius auratus s. lato × C. carassius (Cyprinidae) in the habitats of crucian carp in the Dnieper and Severskii Donets river basin, Dopov. Nats. Akad. Nauk Ukr., 2009, no. 6, pp. 191–197.

  90. Mina, M.V., Mikroevolyutsiya ryb. Evolyutsionnye aspekty feneticheskogo raznoobraziya (Microevolution of Fishes: Evolutionary Aspects of Phenetic Diversity), Moscow: Nauka, 1986.

  91. Mina, M.V., Reshetnikov, Yu.S., and Dgebuadze, Yu.Yu., Taxonomic novelties and problems for users, J. Ichthyol., 2006, vol. 46, pp. 476–480.

    Google Scholar 

  92. Mina, M.V., Shkil, F.N., Dzerzhinskii, K.F., Abdissa Belay, Mironovsky, A.N., and Kapitanova, D.V., Morphological diversity and age dependent transformations in progeny of the large barbs (Barbus intermedius complex sensu Banister) of several morphotypes from Lake Tana (Ethiopia). Results of a long-time experiment, J. Ichthyol., 2012, vol. 52, pp. 821–837.

    Google Scholar 

  93. Mitton, J.B., Selection in Natural Populations, Oxford: Oxford Univ. Press, 1997.

    Google Scholar 

  94. Nagelkerke, L.A.J., Leon-Kloosterziel, K.M., Megens, H.-J., De Graaf, M., Diekmann, O.E., and Sibbing, F.A., Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana, Ethiopia, J. Fish Biol., 2015, vol. 87, pp. 1191–1208.

    CAS  PubMed  Google Scholar 

  95. Neiman, M. and Linksvayer, T.A., The conversion of variance and the evolutionary potential of restricted recombination, Heredity, 2006, vol. 96, pp. 111–121.

    CAS  PubMed  Google Scholar 

  96. Nikol’skii, G.V., Struktura vida i zakonomernosti izmenchivosti ryb (Structure of a Species and Variability Pattern of Fishes), Moscow: Pishchevaya Prom-st’, 1980.

  97. O’Malley, K.G., Vaux, F., and Black, A.N., Characterizing neutral and adaptive genomic differentiation in a changing climate: the most northerly freshwater fish as a model, Ecol. Evol., 2019, vol. 9, pp. 2004–2017.

    PubMed  PubMed Central  Google Scholar 

  98. Osinov, A.G., Senchukova, A.L., Mugue, N.S., Pavlov, S.D., and Chereshnev, I.A., Speciation and genetic divergence of three species of charr from ancient Lake El’gygytgyn (Chukotka) and their phylogenetic relationships with other representatives of the genus Salvelinus,Biol. J. Linn. Soc., 2015, vol. 116, pp. 63–85.

    Google Scholar 

  99. Ovidii. Metamorfozy (Ovid. Metamorphoses), St. Petersburg: Azbuka, 2017.

  100. Park, I.-S., Im, J.H., Ryu, D.K., Nam, Y.K., and Kim, D.S., Effect of starvation on morphometric changes in Rhynchocypris oxycephalus (Sauvage and Dabry), J. Appl. Ichthyol., 2001, vol. 17, pp. 277–281.

    Google Scholar 

  101. Perreault-Payette, A., Muir, A.M., Goetz, F., Perrier, C., Normandeau, E., Sirois, P., and Bernatchez, L., Investigating the extent of parallelism in morphological and genomic divergence among lake trout ecotypes in Lake Superior, Mol. Ecol., 2017, vol. 26, pp. 1477–1497.

    CAS  PubMed  Google Scholar 

  102. Pigliucci, M., Phenotypic Plasticity: Beyond Nature and Nurture, London: John Hopkins Univ. Press, 2001.

    Google Scholar 

  103. Pollard, S.M., Danzmann, R.G., and Claytor, R.R., Association between the regulatory locus PGM-1r* and life-history types of juvenile Atlantic salmon (Salmo salar), Can. J. Fish. Aquat. Sci., 1994, vol. 51, pp. 1322–1329.

    Google Scholar 

  104. Polyakov, G.D., Ekologicheskie zakonomernosti populyatsionnoi izmenchivosti ryb (Ecological Pattern of Population Variability of Fishes), Moscow: Nauka, 1975.

  105. Popov, A.V., Morphofunctional adaptation of Schizopygopsis stoliczkai Steind. in the Yashilkul Lake, Vopr. Ikhtiol., 1968, vol. 8, no. 1, pp. 15–30.

    Google Scholar 

  106. Reshetnikov, A.N., The current range of Amur sleeper Perccottus glenii Dybowski, 1877 (Odontobutidae, Pisces) in Eurasia, Russ. J. Biol. Invasions, 2010, vol. 1, no. 2, pp. 119–126.

    Google Scholar 

  107. Robinson, B.W. and Parsons, K.J., Changing time, space, and faces: test and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes, Can. J. Fish. Aquat. Sci., 2002, vol. 59, pp. 1819–1833.

    Google Scholar 

  108. Robinson, B.W. and Schluter, D., Natural selection and the evolution of adaptive genetic variation in northern freshwater fishes, in Adaptive Genetic Variation in the Wild, Mousseau, T.A., Sinervo, B., and Endler, J., Eds., Oxford: Oxford Univ. Press, 2000, pp. 65–94.

    Google Scholar 

  109. Savvaitova, K.A., Sympatric formation and speciation in fishes, Biol. Nauki, 1985, no. 11, pp. 18-31.

  110. Savvaitova, K.A., Arkticheskie gol’tsy (Arctic Chars), Moscow: Agropromizdat, 1989.

  111. Savvaitova, K.A., Shanin, A.Yu., and Maksimov, V.A., Intraspecific differentiation of Schizopygopsis stoliczkai Steindaechner, 1866 from the Pamirs, Vestn. Mosk. Univ., Ser. 16: Biol., 1987, no. 2, pp. 9–17.

  112. Schluter, D., Ecological speciation in postglacial fishes, Philos. Trans. R. Soc., B, 1996, vol. 351, pp. 807–814.

  113. Schmalhausen, I.I., Factors of Evolution. The Theory of Stabilizing Selection, Philadelphia: Blakiston, 1949.

    Google Scholar 

  114. Schulz, M., Freyhof, J., Saint-Laurent, R., Ǿstbye, K., Mehner, T., and Bernatchez, L., Evidence for independent origin of two spring-spawning ciscoes (Salmoniformes: Coregonidae) in Germany, J. Fish Biol., 2006, vol. 68, pp. 119–135.

    CAS  Google Scholar 

  115. Shink, K.G., Sutton, T.M., Murphy, J.M., and López, J.A., Genetic variation and populations structure among larval Lethenteron spp. within the Yukon River drainage, Alaska, J. Fish Biol., 2018, vol. 93, pp. 1130–1140.

    PubMed  Google Scholar 

  116. Shkil, F.N., Lazebnyi, O.E., Kapitanova, D.V., Belay Abdissa, Borisov, V.B., and Smirnov, S.V., Ontogenetic mechanisms of explosive morphological divergence in the Lake Tana (Ethiopia) species flock of large African barbs (Labeobarbus; Cyprinidae; Teleostei), Russ. J. Dev. Biol., 2015, vol. 46, no. 5, pp. 294–306.

    Google Scholar 

  117. Smith, T.B. and Skúlason, S., Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds, Annu. Rev. Ecol. Syst., 1996, vol. 27, pp. 111–133.

    Google Scholar 

  118. Stärner, H., Påhlsson, C., and Lindén, M., Tandem repeat polymorphism and heteroplasmy in the mitochondrial DNA control region of threespine stickleback (Gasterosteus aculeatus), Behaviour, 2004, vol. 141, pp. 1357–1369.

    Google Scholar 

  119. Svärdson, G., The Coregonid problem. VI. The Palearctic species and their intergrades, Rep.-Inst. Freshwater Res.,Drottningholm, 1957, vol. 38, pp. 267–356.

    Google Scholar 

  120. Symonová, R., Majtánová, Z., Sember, A., Staaks, G.B.O., Bohlen, J., Freyhof, J., Rábová, M., and Ráb, P., Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications, BMC Evol. Biol., 2013, vol. 13, p. 42.

    PubMed  PubMed Central  Google Scholar 

  121. Szulkin, M., Bierne, N., and David, P., Heterozygosity-fitness correlation: a time for reappraisal, Evolution, 2010, vol. 64, pp. 1202–1217.

    PubMed  Google Scholar 

  122. Taylor, E.B., Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation, Rev. Fish Biol. Fish., 1999, vol. 9, pp. 299–324.

    Google Scholar 

  123. Taylor, J.S. and Breden, F., The inheritance of heteroplasmy in guppies, J. Fish Biol., 2002, vol. 60, pp. 1346–1350.

    CAS  Google Scholar 

  124. Terekhanova, N.V., Logacheva, M.D., Penin, A.A., Neretina, T.V., Barmintseva, A.E., Bazykin, G.A., Kondrashov, A.S., and Mugue, N.S., Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus,PLoS Genet., 2014, vol. 10, p. e1004696.

    PubMed  PubMed Central  Google Scholar 

  125. Thrower, F.P., Hard, J.J., and Joyce, J.E., Genetic architecture of growth and early life-history transitions in anadromous and derived freshwater populations of steelhead, J. Fish Biol., 2004, vol. 65, suppl. A, pp. 286–307.

  126. Timirkhanov, S.R., Lomov, A.A., and Mednikov, B.M., Degree of DNA divergence of Schizopygopsis stolichkai Steindaechner from the Yashilkul Lake by molecular hybridization, Dokl. Akad. Nauk SSSR, 1990, vol. 313, no. 6, pp. 1509–1511.

    CAS  Google Scholar 

  127. Trubenová, B., Krejca, M.S., Lehre, P.K., and Kötzing, T., Surfing on the seascape: adaptation in a changing environment, Evolution, 2019, vol. 73, pp. 1356–1374.

    PubMed  PubMed Central  Google Scholar 

  128. 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 

  129. Turner, G.F., Parallel speciation, despeciation and respeciation: implications for species definition, Fish Fish., 2002, vol. 3, pp. 225–229.

    Google Scholar 

  130. Valen van, L.M., A new evolutionary low, Evol. Theory, 1973, vol. 1, pp. 1–30.

    Google Scholar 

  131. Verspoor, E., Coulson, M.W., Greer, R.B., and Knox, D., Unique sympatric quartet of limnetic, benthic, profundal and piscivorous brown trout populations resolved by 3D sampling and focused molecular marker selection, Freshwater Biol., 2019, vol. 64, pp. 121–137.

    CAS  Google Scholar 

  132. West-Eberhard, M.J., Developmental Plasticity and Evolution, Oxford: Oxford Univ. Press, 2003.

    Google Scholar 

  133. Wetjen, M., Cortey, M., Vera, M., Schmidt, T., Schulz, R., and García-Marín, J.-L., Occurrence of length polymorphism and heteroplasmy in brown trout, Gene Rep., 2017, vol. 6, pp. 1–7.

    Google Scholar 

  134. Wilkens, H. and Strecker, U., Evolution in the Dark: Darwin’s Loss Without Selection, Berlin: Springer-Verlag, 2017.

    Google Scholar 

  135. Wimberger, P.H., Trophic polymorphisms, plasticity and speciation in vertebrates, in Theory and Application of Fish Feeding Ecology, Stouder, D.J., Fresh, K.L., and Feller, R.S., Eds., Columbia, SC: Univ. of South Carolina Press, 1994, pp. 19–43.

    Google Scholar 

  136. Wollebaek, J., Heggenes, J., and Roed, K.H., Life histories and ecotype conservation in an adaptive vertebrate: genetic constitution of piscivorous brown trout covaries with habitat stability, Ecol. Evol., 2018, vol. 8, pp. 2729–2745.

    PubMed  PubMed Central  Google Scholar 

  137. Yamazaki, Y., Yokoyama, R., Nagai, T., and Goto, A., Population structure and gene flow among anadromous arctic lamprey (Lethenteron camtschaticum) populations deduced from polymorphic microsatellite loci, Environ. Biol. Fish., 2014, vol. 97, pp. 43–52.

    Google Scholar 

  138. Yoshida, K., Makino, T., Yamaguchi, K., Shigenobu, S., Hasebe, M., Kawata, M., Kume, M., Mori, S., Peichel, C.L., Toyoda, A., Fujiyama, A., and Kitano, J., Sex chromosome turnover contributes to genomic divergence between incipient stickleback species, PLoS Genet., 2014, vol. 10, no. 3, p. e1004223.

    PubMed  PubMed Central  Google Scholar 

  139. Zimmerman, C.E., Kuzishchin, K.V., Gruzdeva, M.A., Pavlov, D.S., Stanford, J.A., and Savvaitova, K.A., Experimental determination of the life history strategy of the Kamchatka mykizha Parassalmo mykiss (Walb.) (Salmonidae, Salmoniformes) on the basis of analysis of the Sr/Ca ratio in otoliths, Dokl. Biol. Sci., 2003, vol. 389, nos. 1–6, pp. 138–142.

    CAS  PubMed  Google Scholar 

  140. Zimmerman, C.E., Edwards, G.W., and Perry, L., Maternal origin and migratory history of steelhead and rainbow trout captured in rivers of the Central Valley, California, Trans. Am. Fish. Soc., 2009, vol. 138, pp. 280–291.

    CAS  Google Scholar 

  141. Zyuganov, V.V., Fauna SSSR. Ryby. Tom 5. Vyp. 1. Semeistvo kolyushkovykh (Gasterosteidae) mirovoi fauny (Fauna of USSR. Fishes, Vol. 5, No. 1: Family Gasterosteidae in the World Fauna), Leningrad: Nauka, 1991.

Download references

ACKNOWLEDGMENTS

We are grateful to Yu.P. Altukhov, I.N. Bolotov, E.A. Borovikova, I.V. Vikhrev, Yu.Yu. Dgebuadze, E.Yu. Krysanov, K.V. Kuzishchin, B.M. Mednikov, M.V. Mina, V.M. Spitsyn, and V.S. Fridman for helpful discussions of the problems considered in the review. The work was supported by the Russian Science Foundation (project no. 16-14-10001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. A. Makhrov.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

“The face of Nature in a vast expanse was naught but Chaos uniformly waste. It was a rude and undeveloped mass, that nothing made except a ponderous weight; and all discordant elements confused, were there congested in a shapeless heap” (Ovidii, 2017)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makhrov, A.A., Artamonova, V.S. Instability Stabilized: Mechanisms of Evolutionary Stasis and Genetic Diversity Accumulation in Fishes and Lampreys from Environments with Unstable Abiotic Factors. Contemp. Probl. Ecol. 13, 370–381 (2020). https://doi.org/10.1134/S1995425520040083

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995425520040083

Keywords:

Navigation