The physiological and genetic differences between flycatchers (Ficedula albicollis vs. Ficedula hypoleuca)
DOI:
https://doi.org/10.2478/foecol-2018-0012Keywords:
flycatchers, ISSR inter-microsatellite analysis, leukogram, micronucleiAbstract
The paper studies interspecies physiological and genetic differences between the white-collared flycatcher and the pied flycatcher of the genus Ficedula. The fact that the flycatchers are capable of interspecies hybridization is one more reason for particular interest to these species. Using our own-developed method of taking venous blood from the eye’s sinus, we took blood samples from birds in the protected area of Homilshanski Forests, Kharkiv, Ukraine, to study their leukogram patterns. The bird feathers were also collected for genetic analysis -- to identify interspecies differences with application of the ISSR technique. It was revealed that the percentage of heterophiles in the nestlings of the pied flycatcher was lower than in the nestlings of the white-collared flycatcher. The micronucleus test did not reveal any significant difference in the interspecies groups. The spectra of amplification products obtained with the primer (AGC)6 G showed that the white-collared flycatchers had a more heterogeneous structure. The study of the leukogram, micronucleus test, and the ISSR analysis can be especially effective in the study of intra-species genetic differentiation.
References
Almazov, V.А., Ryabov, S.I., 1963. Metody funktsionalnogo issledovaniya krovi [Techniques of functional blood testing]. Leningrad: Leningrad Press. 132 p.
Animal genome databases. [cit. 2017-11-05]. http://www.animalgenome.org/QTLdb/chicken.html
Animal genome size database. [cit. 2017-11-05]. http://www.genomesize.com
Baratti, M., Alberti, A., Groenen, M., Veenendaal, T., Fulgheri, F.D., 2001. Polymorphic microsatellites developed by cross-species amplifications in common pheasant breeds. Animal Genetics, 32: 222–225. https://doi.org/10.1046/j.1365-2052.2001.00767.x
Bessarabov, B., 2009. Zashchitnye mekhanizmy ptitsy v postembrionalnom razvitii [Defensive mechanisms of birds in the post-embryonic development]. Ptitsevodstvo, 10: 46–47.
Brown, W.R., Hubbard, S.J., Tickle, C., Wilson, S.A., 2003. The chicken as a model for large-scale analysis of vertebrate gene function. Nature Reviews Genetics, 4: 87–98. https://doi.org/10.1038/nrg998
Caccio, S., Jabbari, K., Matassi, G., Guermonprez, F.,Desgres, J., Bernardi, G., 1997. Methylation patterns in the isochores of vertebrate genomes. Gene, 205: 119–124. https://doi.org/10.1016/S0378-1119(97)00560-X
Cea, G.F., Etcheberry, K.F., Dulout, F.N., 1983. Induction of micronuclei in mouse bone-marrow cells by the flavonoid 5,3’,4’-trihydroxy-3,6,7,8-tetramethoxy-flavone (THTMF). Mutation Research, 119 (3): 339–42 https://doi.org/10.1016/0165-7992(83)90182-3
Chaplygina, A.B., Lezhenina, I.P., Gramma, V.N., Savinskaya, N.A., 2011. Foodration of nestlings of white-collared flycatcher (Ficedula albicollis (Temminck, 1815)) in the plane oak forests in Kharkiv region. The Kharkov Entomological Society, 19 (1): 39–46.
Chaplygina, A.B., Gramma, V.N., Bondarets, D.I., Savynska, N.O., 2015. Arthropods In trophic-cenosis structure of collared flycatcher consortium in conditions of forest ecosystems of North-Eastern Ukraine. Visnyk of Dnipropetrovsk University. Biology, Ecology, 23 (1): 74–85. https://doi.org/10.15421/011511
Chaplygina A.B., Yuzyk D.I., Savynska N.O., 2016. The robin, erithacus rubecula (passeriformes, turdidae), as a component of heterotrophic consortia of forest cenoses, northeast ukraine. Part 2. Vestnik Zoologii, 50 (6): 493–502. https://doi.org/10.1515/vzoo-2016-0056
Chernyavsky, S.D., Fedorova, M.Z., Than, V.V., Kuet, D.H., 2012. Perestroika aktinovogo tsitoskeleta yadernykh eritrotsitov i leikotsitov u ryb, lyagushek i ptits pri migratsii [Rearrangement of the actin cytoskeleton of nucleus erythrocytes and leukocytes in fish, frogs and birds during migration]. Tsitologiya, 5 (5): 412–416.
Cichoń, M., Dubiec, A., Chadzińska M., 2001. The effect of elevated reproductive effort on humoral immune function in collared flycatcher females. Acta Oecologica, 22 (1): 71–76. https://doi.org/10.1016/S1146-609X(00)01094-8
Derjusheva, S, Kurganova, A, Habermann, F, Gaginskaya, E., 2004. High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Research, 12: 715–723. https://doi.org/10.1023/B:CHRO.0000045779.50641.00
Donnik, I. Derkho, M., Kharlap, S., 2015. Kletki krovi kak indikator aktivnosti stress-reaktsii v organizme tsyplyat [Blood cells as an indicator of the stress response activity in the chicken organisms]. Agrarnyi Vestnik Urala. Ptitsevodstvo, 5 (135): 68–71.
Drahulian, M., Chaplygina, A., Kostenko, S., Savynska, N., Sopot, V., Gritsenko, Yu., 2018a. Neobkhodimost razrabotki novogo metoda vzyatiya gematologicheskogo materiala u ptits dlya monitoringa zoonozov [The need to develop a new method of taking haematological material from birds to monitor zoonoses]. Journal of National Academy of Medical Sciences of Ukraine, Special iss., Scientific and practical conference of junior scientists dedicated to the 25th anniversary of National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine, March 23, 2018: 112.
Drahulian, M., Chaplygina, A., Savynska, N., Kostenko, S., Buchek, P., 2018b. Clinical blood analysis of the Great Tit Parus Major. ScienceRise, 44 (3): 11–14. https://doi.org/10.15587/2313-8416.2018.127387
Edwards, S.V., Gasper, J, March, M., 1998. Genomics and polymorphism of Agph-DAB1, an Mhc class II B gene in Red-winged Blackbirds (Agelaius phoeniceus). Molecular Biology and Evolution, 15: 236–250.9501491 https://doi.org/10.1093/oxfordjournals.molbev.a025921
Glazko, V., Glazko, T., 2015. Reproductive “success” and population-genetic consequences of environmental stress on the example of accidents in Chernobyl and Fukushima. Biogeosystem Technique, 6 (4): 316–326. https://doi.org/10.13187/bgt.2015.6.316
Glazko, V.I, Kosovsky, G.Yu., 2013. Struktura genov, kodiruyushchikh obolochechnye belki retrovirusa ptichego grippa i retrovirusa bychego leikoza [The structure of genes encoding envelope proteins of retroviruses of the avian influenza and bovine leukosis]. Reports of the Russian Academy of Agricultural Sciences, 5: 56–60.
Hale, M.L., Petrie, M., Wolff, K., 2004. Polymorphic microsatellite loci in peafowl (Pavocristatus). Molecular Ecology Notes, 4: 528–530. https://doi.org/10.1111/j.1471-8286.2004.00714.x
Hanotte, O., Burke, T., Armour, J. A. L., Jeffreys, A.J., 1991. Hypervariable minisatellite DNA sequences in the Indian peafowl Pavo cristatus. Genomics, 9: 587–597. https://doi.org/10.1016/0888-7543(91)90351-E
Hansson, B., Akesson, M., Slate, J., Pemberton, J.M., 2005. Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proceedings of the Royal Society B. Biological Sciences, 272: 2289–2298. https://doi.org/10.1098/rspb.2005.3228
Huang, Y., Tu, J., Cheng, X., Tang, B., Hu, X., Liu, Z., Feng, J., Lou, Y., Lin, L., Xu, K., Zhao, Y., Li, N., 2005. Characterization of 35 novel microsatellite DNA markers from the duck (Anas platyrhynchos) genome and cross-amplification in other birds. Genetics Selection Evolution, 37: 455–472. https://doi.org/10.1186/1297-9686-37-5-455
Huang, Y., Zhao, Y., Haley, C.S., Hu, S., Hao, J., Wu, C., Li, N., 2006. A genetic and cytogenetic map for the duck (Anas platyrhynchos). Genetics, 173: 287–296. https://doi.org/10.1534/genetics.105.053256
Imangulov, Sh.A., Egorov, I.A., Okolelova, T.M., Tishenkov, A.N., Lenkova, T.N., Pankov, P.N., Ezerskaya, A.V., Ignatov, G.V., Dogadaeva, I.V., Avdonin, B.F., Petrina, Z.A., Borisova, T.V., Gromova, T.I, 2004. Metodika provedeniya nauchnykh i proizvodstvennykh issledovanii po kormleniyu selskokhozyaistvennoi ptitsy: rekomendatsii [Technique of carrying out scientific and industrial studies on the feeding of agricultural poultry: recommendations]. Sergiev Posad: VNITIP. 43 p.
Irisov, E.A. Kamaeva, S.I., Andryushina, O.A., Toporov, K.V., Denisova, E.G., Karmanova, O.V., 1980. Morfologicheskie i biokhimicheskie pokazateli krovi ptits plato Putorana [Morphological and biochemical blood indices of birds from Putorana Plateau]. Tomsk. 143 p.
Ivanov, A.E., 2004. Ekologiya blizkorodstvennykh vidov mukholovok roda Ficedula v mestakh ikh simbiotopii [Ecology of closely related species of flycatchers of the genus Ficedula in the areas of their symbiotopia]. Russkii Ornitologicheskii Zhurnal, 13 (251): 87–94.
Ivanov, A.E., 2005. Pitanie ptentsov mukholovki-belosheiki Ficedula albicollis i mukholovki-pestrushki F. Hypoleuca v usloviyakh simbiotopii [The nestling diet of the white collared flycatcher and the pied flycatcher in the conditions of symbiotopia]. Russkii Ornitologicheskii Zhurnal, 14 (287): 418–421.
Kadi, F., Mouchiroud, D., Sabeur, G., Bernardi, G., 1993. The compositional patterns of the avian genomes and their evolutionary implications. Journal of Molecular Evolution, 37: 544–551. https://doi.org/10.1007/BF00160434
Kamara, D., Geng, T., Xu, J., Guynn, S., Hopwood, K., Smith, E.J., 2007. Isolation and characterization of microsatellite markers from the budgerigar, Melopsittacus undulates. Molecular Ecology Notes, 7: 507–509. https://doi.org/10.1111/j.1471-8286.2006.01636.x
Kameda, K. Goodridge, A.G., 1991. Isolation and partial characterization of the gene for goose fatty acid synthase. Journal of Biological Chemistry, 266: 419–426. https://doi.org/10.1016/S0021-9258(18)52451-0
Kayang, B.B., Inoue-Murayama, M., Hoshi, T., Matsuo, K., Takahashi, H., Minezawa, M., Mizutani, M., Ito, S., 2002. Microsatellite loci in Japanese quail and cross-species amplification in chicken and guinea fowl. Genetics Selection Evolution, 34: 233–253.270543012081810 https://doi.org/10.1186/1297-9686-34-2-233
Kellner, W.A., Sullivan, R.T., Carlson, B.H., Thomas, J.W., 2005. Uprobe: a genome-wide universal probe resource for comparative physical mapping in vertebrates. Genome Research, 15: 166–173. https://doi.org/10.1101/gr.3066805
Khmeleva, E.V. Beskrovnaya, N.I., Smetanin, V.T., Sidorov, N.A., 2009. DNK-markirovanie kanalnogo soma [DNA-marking of the channel catfish]. Visnyk Dnipropetrovskogo Derzhavnogo Universytetu, 1: 126–130.
Klipper, E., Sklan, D., Friedman, A., 2000. Immune response of chickens to dietary protein antigens. Veterinary Immunology and Immunopathology, 74: 209–223. https://doi.org/10.1016/S0165-2427(00)00172-0
Kurilenko, Yu.F., Suprun, I.A., 2015. Ispolzovanie ISSR-markernykh sistem v konevodstve [Use of ISSR-marker systems in horse breeding] Zootekhnicheskaya Nauka Belarusi, 50 (1): 101–108.
Kursa, M.A., Afanasyeva, E.S., Rushkovsky, S.R., Barchuk, R.A., Varenyuk, I.N., Bluma, O.V., Bezrukov, V.F., 2005. Tsitogeneticheskie parametry nestabilnosti genoma ptits v ekologo-geneticheskom monitoringe [Cytogenetic parameters of the instability of the bird genome in environmental-genetic monitoring]. Problemy Bezpeky Atomnykh Elektrostantsii i Chornobylya, 3 (2): 92–98.
Longmire, J.L, Hahn, C.C., Roach, J.L., 1999. Low abundance of microsatellite repeats in the genome of the brown-headed cowbird (Molothrus ater). The Journal of Heredity, 90: 574–578. https://doi.org/10.1093/jhered/90.5.574
Lugaskova, N.V., Karfidova, A.A., Belsky, E.A., 2005. Gematologicheskie kharakteristiki mukholovki-pestrushki (Ficedula hypoleuca Pall.) v usloviyakh promyshlennogo zagryazneniya [Haematological characteristics of the pied flycatcher under industrial pollution]. Sibirskii Ekologicheskii Zhurnal, 3: 507–514.
Maak, S., Wimmers, K., Weigend, S., Neumann, K., 2003. Isolation and characterization of 18 microsatellites in the Peking duck (Anas platyrhynchos) and their application in other waterfowl species. Molecular Ecology Notes, 3: 224–227. https://doi.org/10.1046/j.1471-8286.2003.00405.x
Miklyaeva, M., Okolnicheva, A. Popenko, N., Miklyaeva, Yu., Antipova, M., 2017. Izuchenie vliyaniya fosfoorganicheskikh pestitsidov na ptentsov bolshoi sinitsy obitayushchikh v promyshlennykh sadakh [Studying the influence of organophosphorus pesticides on chicks of the great tits inhabiting industrial gardens]. In Vostretsov, A.I. (ed.). Inovacionnye podchody k sovremennoi nauke (Innovatice approaches to modern science. Ufa: Naučnoissledovatel’skii centr Mir nauki, p. 34–39. [cit. 2018-12-29], http://science-peace.ru/files/IPvSN_2017.pdf
Moon, D.A., Magor, K.E., 2004. Construction and characterization of a fosmid library for comparative analysis of the duck genome. Animal Genetics, 35: 417–418. https://doi.org/10.1111/j.1365-2052.2004.01177.x
Pang, S.W., Ritland, C., Carlson, J.E, Cheng, K.M., 1999. Japanese quail microsatellite loci amplified with chicken-specific primers. Animal Genetics, 30: 195–199. https://doi.org/10.1046/j.1365-2052.1999.00464.x
Paulke, E., Haase, E., 1978. A comparison of seasonal changers in the concentrations of androgens in the peripheral blood of wild and domestic ducks. General and Comparative Endocrinology, 34 (4): 381–390. https://doi.org/10.1016/0016-6480(78)90278-2
Plokhinsky, I.A., 1969. Rukovodstvo po biometrii dlya zootekhnikov [Practical guide on biometrics for livestock experts]. Moscow: Kolos, 256 p.
Polchaninova, N.Yu., Prishada, I.A., 1994. Pauki v pishchevom ratsione ptentsov mukholovki-belosheiki Ficedula albicollis Temm.) v nagornykh dubravakh Kharkovskoi oblasti [Spiders in the nestling diet of the white collared flycatcher in upland oak groves of Kharkov Region]. Izvestiya Kharkovskogo Entomologicheskogo Obshchestva, 2 (1): 146–149.
Rodionov A.V., 1996. Micro versus macro: a review of structure and function of avian micro- and macrochromosomes. Genetika, 32: 597–608.
Romanov, M.N, Price, J.A, Dodgson, J.B., 2004. First century of chicken gene study and mapping – a look back and forward. World’s Poultry Science Journal, 60: 19–41. https://doi.org/10.1079/WPS20032
Romanov, M.N., Dodgson, J.B., 2006. Cross-species overgo hybridization and comparative physical mapping within avian genomes. Animal Genetics, 37: 397–399.16879356 https://doi.org/10.1111/j.1365-2052.2006.01463.x
Roots, E.H., Baker, R.J., 2002. Distribution and characterization of microsatellites in the emu (Dromaius novaehollandiae) genome. The Journal of Heredity, 93: 100–106.12140269 https://doi.org/10.1093/jhered/93.2.100
Sazanov, A.A., Sazanova A.L., Kozyreva A.A., Smirnov A.F., Andreotszi L., Federico K., Motta C., Sakkone C., Bernardi G., 2003. Sravnitelnoe kompozitsionnoe kartirovanie khromosom kuritsy i perepela [Comparative composite mapping of chromosomes of the chicken and quail]. Genetika, 39: 819–825. https://doi.org/10.1023/A:1024414128325
Schmid, M., Nanda, I., Guttenbach, M., Steinlein, C., Hoehn, M., Schartl, M., Haaf, T., Weigend, S., Fries, R., Buerstedde, J.M., Wimmers, K., Burt, D.W., Smith, J., A’Hara, S., Law, A., Griffin, D.K., Bumstead, N., Kaufman, J., Thomson, P.A., Burke, T., Groenen, M.A., Crooijmans, R.P., Vignal, A., Fillon, V., Morisson, M., Pitel, F., Tixier-Boichard, M., Ladjali-Mohammedi, K., Hillel, J., Mäki-Tanila, A., Cheng, H.H., Delany, M.E., Burnside, J., Mizuno, S., 2000. First report on chicken genes and chromosomes 2000. Cytogenetetics and Cell Genetics, 90: 169–218.11124517 https://doi.org/10.1159/000056772
Schütz, K.E., Kerje, S., Carlborg, Ö., Jacobsson, L., Andersson, L., Jensen, P., 2002. QTL analysis of a red junglefowl × White Leghorn intercross reveals trade-off in resource allocation between behavior and production traits. Behavior Genetics, 32: 423–433. https://doi.org/10.1023/A:1020880211144
Shiina, T., Shimizu, C., Oka, A., Teraoka, Y., Imanishi, T., Gojobori, T., Hanzawa, K., Watanabe, S., Inoko, H., 1999. Gene organization of the quail major histocompatibility complex (MhcCoja) class I gene region. Immunogenetics, 49: 384–394.10199914 https://doi.org/10.1007/s002510050511
Stern, C.D., 2004. The chick embryo – past, present and future as a model system in developmental biology. Mechanisms of Development, 121: 1011–1013.15358007 https://doi.org/10.1016/j.mod.2004.06.009
Takahashi, R., Akahane, K., Arai, K., 2003. Nucleotide sequences of pigeon feather keratin genes. DNA Sequence, 14: 205–210.14509833 https://doi.org/10.1080/1042517031000095390
Tang, B., Huang, Y.H., Lin, L., Hu, X.X., Feng, J.D., Yao, P., Zhang, L., Li, N., 2003. Isolation and characterization of 70 novel microsatellite markers from ostrich (Struthio camelus) genome. Genome, 46: 833–840.14608400 https://doi.org/10.1139/g03-059
Taylor, E.L., Vercoe, P., Cockrem, J., Groth, D., Wetherall, J.D., Martin, G.B., 1999. Isolation and characterization of microsatellite loci in the emu, Dromaius novaehollandiae, and cross-species amplification within Ratitae. Molecular Ecology, 8: 1963–1964.10620242 https://doi.org/10.1046/j.1365-294x.1999.00778-4.x
Thomas, J.W., Prasad, A.B., Summers, T.J., Lee-Lin, S.Q., Maduro, V.V., Idol, J.R., Ryan, J.F., Thomas, P.J., Mc-Dowell, J.C., Green, E.D., 2002. Parallel construction of orthologous sequence-ready clone contig maps in multiple species. Genome Research, 12: 1277–1285.18664312176935 https://doi.org/10.1101/gr.283202
Тörök, J., Hargitai, R., Hegyi, G., Matus, Z., Michl, G., Péczely, P., Rosivall, B., Tóth, G., 2007. Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. Behavioural Ecology and Sociobiology, 61 (4): 541–550. https://doi.org/10.1007/s00265-006-0282-1
Traxler, B., Brem, G., Müller, M., Achmann, R., 2000. Polymorphic DNA microsatellites in the domestic pigeon, Columba livia var. domestica. Molecular Ecology, 9: 366–368. https://doi.org/10.1046/j.1365-294x.2000.00874-2.x
Turitsyna, E.G., Makarskaya, G.V., Tarskikh, S.V., Tsarev, P.Yu., 2013. Dinamika parametrov khemilyuminestsentcii kletok organov immunogeneza tsyplyat rannego vozrasta [Dynamics of chemiluminescence indices of immunogenesis cells of early age chickens]. Vestnik Kras GAU. Veterinariya i Zhivotnovodstvo, 9: 171–176.
Valkyunas, G., Ezhova, T., Mironov, S., 2001. Vysokie ekstensivnost zarazheniya i raznoobrazie kroveparazitov u vorobinykh ptits v Yuzhnom Turkmenistane [High extensity of infection and variety of blood parasites in passerine birds in South Turkmenistan]. Parazitologiya, 35 (2): 135–142.
Vartanyan, V., Karapetyan, S., 1959. Metod ischisleniya formennykh elementov krovi ptits, amfibii i reptilii [Method of calculating blood cells in birds, amphibians and reptiles]. DAN Armyanskoi SSR, 29 (2): 93–96. https://doi.org/10.2307/1440060
Visser, М.E., Lessells, C.M., 2001. The costs of egg production and incubation in great tits (Parus major). Proceedings of the Royal Society London B, 268: 1271–1277. [cit. 2018-15-02]. https://doi.org/10.1098/rspb.2001.1661
Yezdakova, I.Yu., Chuyko, O.M. Chadina, E.O., 2008. Dinamika rozetkoobrazuyushchikh kletok kur v ontogeneze [Dynamics of rosette-forming cells of chickens in ontogenesis]. Problemy Priklandnoy Nauki. Veterinarnaya Patologiya, 2: 62–64.
Zietkiewicze, Е., Rafalski, A., Labuda, D., 1994. Genome finger-printing by simple sequence repeat (SSR)-anchored polymerase chain reactiоn amplification. Genomics, 20: 176–183. https://doi.org/10.1006/geno.1994.1151
Zúñiga-González, G., Torres-Bugarín, O., Zamora-Pérez, A., Gómez-Meda, B.C., Ramos-Ibarra, M.L., Martínez-González, S., Gonzales-Rodriguez, A., Luna-Aquirre, J., Ramos-Mora, A., Ontiveros-Lira, D., Gallegos-Arreola, M.P., 2001. Differences in the number of micronucleated erythrocytes among young and adult animals including humans. Spontaneous micronuclei in 43 species. Mutation Research, 494: 161–167. https://doi.org/10.1016/S1383-5718(01)00180-2
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