The aim of the study is a comparative investigation of changes that certain genome parts undergo during speciation. The research was focused on divergence of coding and noncoding sequences in different groups of salmonid fishes of the Salmonidae (Salmo, Parasalmo, Oncorhynchus, and Salvelinus genera) and the Coregonidae families under different levels of reproductive isolation. Two basic approaches were used: (1) PCR-RAPD with a 20–22？nt primer design with subsequent cloning and sequencing of the products and (2) a modified endonuclease restriction analysis. The restriction fragments were shown with sequencing to represent satellite DNA. Effects of speciation are found in repetitive sequences. The revelation of expressed sequences in the majority of the employed anonymous loci allows for assuming the adaptive selection during allopatric speciation in isolated char forms. 1. Introduction In view of the biological concept of Mayr [1] the process of speciation in the organisms with the sexual reproduction involves accumulation of differences sufficient to set the barrier of partial or complete incompatibility. According to Dobzhansky [2] it implies for the process of unlimited genetic recombinations within the species and the lack of gene flow between the species. Meanwhile, as repeatedly noted by many researches, for example, Mallet, Garside and Christie, Svardson, Wolf et al., Gross et al., and Scribner et al. ([3–7], review [8]), hybridization between species is known to occur both in the wild and under artificial conditions, and the hybrid forms exist along with the parental species. The fate of such interspecific hybrids sporadically occurring in the wild and their contribution in the genetic structure of populations are still under question, as Coyne and Orr and Hudson et al. [9, 10] showed. Repetitive DNA sequences are convenient for the studies of the genome evolution [11–13]. According to Ohno [14], this fraction originates in the process of gene duplications and has a potential for large-scale rearrangements, because they are not subjected to the pressing of the natural selection. From the directly obtained experimental data, phylogenetic reconstructions for the lower taxa on the basis of the repetitive DNA sequences yield better results than the other nuclear sequences for both animals and plants as Chase et al., Thompson et al., and Warburton and Willard [15–17] wrote. As mentioned by Ohta, [18], the factors of intragenomic homogenization counteract intragenomic differentiation of the fraction of repeats. These sequences become peculiar
References
[1]
E. Mayr, Animal Species and Evolution, Harvard University Press, Cambridge, Mass, USA, 1963.
[2]
T. Dobzhansky, Genetics and the Origin of Species, Columbia University Press, New York, NY, USA, 1937.
[3]
J. Mallet, “Perspectives Poulton, Wallace and Jordan: how discoveries in Papilio butterflies led to a new species concept 100 years ago,” Systematics and Biodiversity, vol. 1, no. 4, pp. 441–452, 2004.
[4]
E. T. Garside and W. J. Christie, “Experimental hybridization among three coregonine fishes,” Transaction of the American Fishery Society, vol. 9, no. 2, pp. 196–200, 1962.
[5]
G. Svardson, “The Coregonid problem. VII. The isolation mechanism in sympatric species,” Reports of the Institute of Freshwater Research, vol. 46, pp. 95–123, 1965.
[6]
J. B. W. Wolf, J. Lindell, and N. Backstr？m, “Speciation genetics: current status and evolving approaches,” Philosophical Transactions of the Royal Society B, vol. 365, no. 1547, pp. 1717–1733, 2010.
[7]
R. Gross, B. Gum, R. Reiter, and R. Kühn, “Genetic introgression between Arctic charr (Salvelinus alpinus) and brook trout (Salvelinus fontinalis) in Bavarian hatchery stocks inferred from nuclear and mitochondrial DNA markers,” Aquaculture International, vol. 12, no. 1, pp. 19–32, 2004.
[8]
K. T. Scribner, K. S. Page, and M. L. Bartron, “Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference,” Reviews in Fish Biology and Fisheries, vol. 10, no. 3, pp. 293–323, 2000.
[9]
J. A. Coyne and H. A. Orr, “The evolutionary genetics of speciation,” Philosophical Transactions of the Royal Society B, vol. 353, no. 1366, pp. 287–305, 1998.
[10]
A. G. Hudson, P. Vonlanthen, R. Müller, and O. Seehausen, “Review: the geography of speciation and adaptive radiation in coregonines. Biology and management of coregonid fishes,” Archives of Hydrobiology Special Issue Advances in Limnology, vol. 60, no. 2, pp. 111–146, 2007.
[11]
J. M. Wright, “Nucleotide sequence, genomic organization and evolution of a major repetitive DNA family in tilapia (Oreochromis mossambicuslhomorum),” Nucleic Acids Research, vol. 17, no. 13, pp. 5071–5079, 1989.
[12]
J. A. Shapiro and R. von Sternberg, “Why repetitive DNA is essential to genome function,” Biological Reviews of the Cambridge Philosophical Society, vol. 80, no. 2, pp. 227–250, 2005.
[13]
M. A. Biscotti, A. Canapa, E. Olmo et al., “Repetitive DNA, molecular cytogenetics and genome organization in the King scallop (Pecten maximus),” Gene, vol. 406, no. 1-2, pp. 91–98, 2007.
[14]
S. Ohno, Evolution By Gene Duplication, Springer, New York, NY, USA, 1970.
[15]
W. Chase, A. V. Cox, D. E. Soltis, et al., “Large DNA sequences matrices phylogenetic signal and feasibility: an empirical approach,” in Proceedings of the American Society of Plant Taxonomists Annual Meetings, Montreal, Canada, August 1997.
[16]
J. D. Thompson, J. E. Sylvester, I. Laudien Gonzalez, C. C. Constanzi, and D. Gillespie, “Definition of a second dimeric subfamily of human α satellite DNA,” Nucleic Acids Research, vol. 17, no. 7, pp. 2769–2782, 1989.
[17]
P. Warburton and H. Willard, “Evolution of centromeric alpha satellite DNA: molecular organization within and between human and primate chromosomes,” in Human Genome Evolution, M. S. T. Jackson and G. Dover, Eds., pp. 121–145, BIOS Scientific Publishers, 1996.
[18]
T. Ohta, “On the evolution of multigene families,” Theoretical Population Biology, vol. 23, no. 2, pp. 216–240, 1983.
[19]
E. A. Zimmer, S. L. Martin, and S. M. Beverley, “Rapid duplication and loss of genes coding for the α chains of hemoglobin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 4, pp. 2158–2162, 1980.
[20]
A. J. Jeffreys, V. Wilson, and S. L. Thein, “Hypervariable “minisatellite” regions in human DNA,” Nature, vol. 314, no. 6006, pp. 67–73, 1985.
[21]
K. M. Gray, J. W. White, C. Costanzi et al., “Recent amplification of an alpha satellite DNA in humans,” Nucleic Acids Research, vol. 13, no. 2, pp. 521–535, 1985.
[22]
J. F. Elder Jr. and B. J. Turner, “Concerted evolution at the population level: pupfish HindIII satellite DNA sequences,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 3, pp. 994–998, 1994.
[23]
A. N. Fedorov, L. V. Fedorova, V. V. Grechko et al., “Variable and invariable DNA repeat characters revealed by taxonprint approach are useful for molecular systematics,” Journal of Molecular Evolution, vol. 48, no. 1, pp. 69–76, 1999.
[24]
W. M. Brown, “Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 6, pp. 3605–3609, 1980.
[25]
V. V. Grechko, L. V. Fedorova, A. N. Fedorov et al., “Restriction endonuclease analysis of highly repetitive DNA as a phylogenetic tool,” Journal of Molecular Evolution, vol. 45, no. 3, pp. 332–336, 1997.
[26]
I. A. Roudykh, V. V. Grechko, D. G. Ciobanu, D. A. Kramerov, and I. S. Darevsky, “Variability of restriction sites in satellite DNA as a molecular basis of taxonoprint method: evidence from the study of Caucasian rock lizards,” Russian Journal of Genetics, vol. 38, no. 8, pp. 937–941, 2002.
[27]
B. M. Mednikov, E. A. Shubina, M. N. Mel’nikova, et al., “The problem of the generic status of Pacific salmon and trout (Genetic Taxonomic Analysis),” Journal of Ichthyology, vol. 39, no. 1, pp. 10–17, 1999.
[28]
L. Bernatchez and J. J. Dodson, “Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis,” Evolution, vol. 44, no. 5, pp. 1263–1271, 1990.
[29]
T. N. Todd and G. R. Smith, “A review of differentiation in Great Lakes ciscoes,” Polskie Archiwum Hydrobiologii, vol. 39, no. 3-4, pp. 261–267, 1992.
[30]
J. Turgeon and L. Bernatchez, “Reticulate evolution and phenotypic diversity in North American ciscoes, Coregonus ssp. (Teleostei: Salmonidae): implications for the conservation of an evolutionary legacy,” Conservation Genetics, vol. 4, no. 1, pp. 67–81, 2003.
[31]
G. R. Smith and R. F. Stearley, “The classification and scientific names of rainbow and cutthroat trouts,” Fisheries, vol. 14, no. 1, pp. 4–10, 1989.
[32]
J. Welsh and M. McClelland, “Genomic fingerprinting using arbitrarily primed PCR and a matrix of pairwise combinations of primers,” Nucleic Acids Research, vol. 19, no. 19, pp. 5275–5279, 1991.
[33]
J. G. K. Williams, M. K. Hanafey, J. A. Rafalski, and S. V. Tingey, “Genetic analysis using random amplified polymorphic DNA markers,” Methods in Enzymology, vol. 218, pp. 704–740, 1993.
[34]
F. E. Arrighi, J. Bergendahl, and M. Mandel, “Isolation and characterization of DNA from fixed cells and tissues,” Experimental Cell Research, vol. 50, no. 1, pp. 40–47, 1968.
[35]
S. E. Saunders and J. F. Burke, “Rapid isolation of miniprep DNA for double strand sequencing,” Nucleic Acids Research, vol. 18, no. 16, pp. 4948–4950, 1990.
[36]
M. G. Murray and W. F. Thompson, “Rapid isolation of high molecular weight plant DNA,” Nucleic Acid Research, vol. 8, no. 19, pp. 4321–4325, 1980.
[37]
R. Boom, C. J. A. Sol, M. M. M. Salimans, C. L. Jansen, P. M. E. Wertheim-Van Dillen, and J. Van Der Noordaa, “Rapid and simple method for purification of nucleic acids,” Journal of Clinical Microbiology, vol. 28, no. 3, pp. 495–503, 1990.
[38]
J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Publishing, New York, NY, USA, 2nd edition, 1989.
[39]
T. Maniatis, E. E. Fritch, and J. Sambrook, Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory, 1982.
[40]
N. Saitou and M. Nei, “The neighbor-joining method: a new method for reconstructing phylogenetic trees,” Molecular Biology and Evolution, vol. 4, no. 4, pp. 406–425, 1987.
[41]
M. Nei and W. H. Li, “Mathematical model for studying genetic variation in terms of restriction endonucleases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 10, pp. 5269–5273, 1979.
[42]
M. Nei, “Genetic distance between populations,” American Naturalist, vol. 106, no. 949, pp. 283–292, 1972.
[43]
Y. Van De Peer and R. De Wachter, “Treecon for windows: a software package for the construction and drawing of evolutionary trees for the microsoft windows environment,” Bioinformatics, vol. 10, no. 5, pp. 569–570, 1994.
[44]
J. Felsenstein, “Confidence limits on phylogenies: an approach using the bootstrap,” Evolution, vol. 39, no. 4, pp. 783–791, 1985.
[45]
V. A. Maksimov, K. A. Savvaitova, B. M. Mednikov, et al., “Alpine char-a new form of Arctic char (Salvelinus) from Taimyr,” Journal of Ichthyology, vol. 35, no. 7, pp. 1–9, 1995.
[46]
R. J. Behnke, Native Trout of Western North America, vol. 6, American Fisheries Society Monograph, Bethesda, Md, USA, 1992.
[47]
A. G. Osinov and V. S. Lebedev, “Salmonid fishes (Salmonidae, Salmoniformes): the systematic position in the superorder Protacanthopterygii -the main stages of evolution, and molecular dating,” Journal of Ichthyology, vol. 44, no. 9, pp. 690–715, 2004.
[48]
I. A. Chereshnev and M. B. Skopets, “Salvethymus svetovidovi gen. at sp. nova, a new endemic fish from subfamily Salmonidae from Lake El’gygytgyn (the Central Chukotka),” Journal of Ichthyology, vol. 30, no. 2, pp. 201–213, 1990.
[49]
T. M. Cavender, “Review of the fossil history of North American freshwater fishes,” in The Zoogeography of North American Freshwater Fishes, C. H. Hocutt and E. O. Wiley, Eds., pp. 700–724, John Wiley & Sons, NewYork, NY, USA, 1986.
[50]
Yu. S. Reshetnikov, Ecology and Systematics of Coregonine Fishes, Nauka, Moscow, Russia, 1980.
[51]
R. J. Behnke, “The systematics of salmonid fishes of recently glaciated lakes,” Journal of Fisheries Research Board of Canada, vol. 29, no. 5, pp. 639–671, 1972.
[52]
R. A. Bodaly, J. Vuorinen, R. D. Ward, M. Luczynski, and J. D. Reist, “Genetic comparisons of New and Old World coregonid fishes,” Journal of Fish Biology, vol. 38, no. 1, pp. 37–51, 1991.
[53]
G. Kh. Shaposhnikova, “On the taxonomy of whitefishes from the USSR,” in Biology of Coregonid Fishes, C. C. Lindsey and C. S. Woods, Eds., pp. 195–208, University Manitoba Press, Winnipeg, Manitoba, Canada, 1970.
[54]
K. A. Savvaitova, “Patterns of diversity and processes of speciation in Arctic charr,” Nordic Journal of Freshwater Research, vol. 71, no. 1, pp. 81–91, 1995.
[55]
Yu. S. Reshetnikov, Ed., Atlas of Russian Freshwater Fishes, vol. 1, Nauka, Moscow, Russia, 2002.
[56]
V. V. Barsukov, “About systematic of the Chukotka charr of the genus Salvelinus,” Journal of Ichtiology, vol. 14, no. 1, pp. 3–17, 1960.
[57]
A. G. Osinov and S. D. Pavlov, “Allozyme variation and genetic divergence between populations of Arctic char and Dolly Varden (Salvelinus alpinus-Salvelinus malma complex),” Journal of Ichthyology, vol. 38, no. 1, pp. 42–55, 1998.
[58]
A. G. Osinov, “Evolutionary relationships between the main taxa of the Salvelinus alpinus-Salvelinus malma complex: results of a comparative analysis of allozyme data from different authors,” Journal of Ichthyology, vol. 41, no. 3, pp. 192–208, 2001.
[59]
L. S. Berg, “Fishes of the Amur River basin,” Memoires de l'Academie Imperial des Sciences Classe Physico-Math, vol. 24, no. 9, pp. 1–270, 1909.
[60]
S. S. Alekseev and M. Y. Pichugin, “A new form of charr Salvelinus alpinus (Salmonidae) from Lake Davatchan in Transbaikalia and its morphological differences from sympatric forms,” Journal of Ichthyology, vol. 38, no. 4, pp. 292–302, 1998.
[61]
B. F. Koop, K. R. von Schalburg, J. L. N. Walker, et al., “A salmonid EST genomic study: genes, duplications, phylogeny and microarrays,” BMC Genomics, vol. 9, p. 545, 2008.
[62]
A. G. Osinov and V. S. Lebedev, “Genetic divergence and phylogeny of the Salmoninae based on allozyme data,” Journal of Fish Biology, vol. 57, no. 2, pp. 354–381, 2000.
[63]
P. A. Crane, L. W. Seeb, and J. E. Seeb, “Genetic relationships among Salvelinus species inferred from allozyme data,” Canadian Journal of Fisheries and Aquatic Science, vol. 51, supplement 1, pp. 182–197, 1994.
[64]
S. Kumar and S. B. Hedges, “A molecular timescale for vertebrate evolution,” Nature, vol. 392, no. 6679, pp. 917–920, 1998.
[65]
J. P. Thorpe, “The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics,” Annual Review of Ecology, Evolution, and Systematic, vol. 13, pp. 139–168, 1982.
[66]
A. H. Berst, A. R. Emery, and G. R. Spangler, “Reproductive behavior of hybrid charr (Salvelinus fontinalis x S namaycush),” Canadian Journal of Fisheries and Aquatic Science, vol. 38, no. 4, pp. 432–440, 1981.
[67]
K. M. Westrich, N. R. Konkol, M. P. Matsuoka, and R. B. Phillips, “Interspecific relationships among charrs based on phylogenetic analysis of nuclear growth hormone intron sequences,” Environmental Biology of Fishes, vol. 64, no. 1–3, pp. 217–222, 2002.
[68]
S. U. Qadri, “Morphological comparisons of three populations of the lake charr, Cristivomer namaykush, from Ontario and Manitoba,” Journal of the Fisheries Research Board of Canada, vol. 24, pp. 1407–1411, 1967.
[69]
B. J. Crespi and M. J. Fulton, “Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny,” Molecular Phylogenetics and Evolution, vol. 31, no. 2, pp. 658–679, 2004.
[70]
L. N. Ermolenko, “Genetic divergence in the family Coregonidae,” Polskie Archiwum Hydrobiologii, vol. 39, no. 3-4, pp. 533–539, 1992.
[71]
D. V. Politov, N. Y. Gordon, and A. A. Makhrov, “Genetic identification and taxonomic relationships of six Siberian species of Coregonus,” Advances in Limnology, vol. 57, pp. 21–34, 2002.
[72]
L. Bernatchez, F. Colombani, and J. J. Dodson, “Phylogenetic relationships among the subfamily Coregoninae as revealed by mitochondrial DNA restriction analysis,” Journal of Fish Biology, vol. 39, supplement, pp. 283–290, 1991.
[73]
G. R. Smith and T. N. Todd, “Morphological cladistic study of Coregonine fishes,” Polskie Archiwum Hydrobiologii, vol. 39, no. 3-4, pp. 479–490, 1992.
[74]
S. V. Frolov, “Some aspects of kariotype evolution in the Coregoninae,” Polskie Archiwum Hydrobiologii, vol. 39, no. 3-4, pp. 509–515, 1992.
[75]
G. Sv？rdson, “Significance of introgression in coregonid evolution,” in Biology of Coregonid Fishes, C. C. Lindsey and C. S. Woods, Eds., pp. 33–59, University of Manitoba Press, Winnipeg, Manitoba, Canada, 1970.
[76]
L. Bernatchez, S. Renaut, A. R. Whiteley et al., “On the origin of species: insights from the ecological genomics of lake whitefish,” Philosophical Transactions of the Royal Society B, vol. 365, no. 1547, pp. 1783–1800, 2010.
[77]
Yu. Kartavtsev, “Genetic variability and differentiation in Salmonid fish,” Nordic Journal of Freshwater Research, vol. 67, pp. 96–117, 1992.
[78]
G. Svardson, “The Coregonid problem. VI. The palearctic species and their intergrades,” Reports of the Institute of Freshwater Research Drottningholm, vol. 38, pp. 267–356, 1975.
[79]
G. Svardson, “Postglacial dispersal and reticulate evolution of Nordic Coregonids,” Nordic Journal of Freshwater Research Drottningholm, vol. 74, pp. 3–32, 1998.
[80]
V. Grant, Plant Speciation, Columbia University Press, New York, NY, USA, 2nd edition, 1981.
[81]
S. Renaut and L. Bernatchez, “Transcriptome-wide signature of hybrid breakdown associated with intrinsic reproductive isolation in lake whitefish species pairs (Coregonus spp. Salmonidae),” Heredity, vol. 106, no. 6, pp. 1003–1011, 2011.
[82]
K. Johannesson, “Parallel speciation: a key to sympatric divergence,” Trends in Ecology and Evolution, vol. 16, no. 3, pp. 148–153, 2001.
[83]
N. Osada and C.-I. Wu, “Inferring the mode of speciation from genomic data: a study of the great apes,” Genetics, vol. 169, no. 1, pp. 259–264, 2005.
[84]
A. L. Schmidt and L. M. Anderson, “Repetitive DNA elements as mediators of genomic change in response to environmental cues,” Biological Reviews of the Cambridge Philosophical Society, vol. 81, no. 4, pp. 531–543, 2006.
[85]
P. M. Ferree and D. A. Barbash, “Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila,” PLoS Biology, vol. 7, no. 10, Article ID e1000234, 2009.
