Abstract
This study aims to test the potential of allelic frequency distributions of plasma proteins analysed by starch gel electrophoresis for identifying Amazon turtle (Podocnemis expansa Schweigger, 1812) stocks. Three proteins: transferrin (Tf), albumin (Alb) and general protein (GP), and four enzymes: esterase (EST), phosphoglucomutase (PGM), malate dehydrogenase (MDH) and superoxide dismutase (SOD) from three geographical areas in the Amazon region, totalizing three population samples: 1) Maracarana, Rio Uatumã-AM, 2) Trombetas, Rio Trombetas-PA and 3) Monte Cristo, Rio Tapajós-PA, were tested. Out of 11 presumptive loci detected, seven were monomorphic (GP-1, GP-2, EST-1, EST-2, PGM-1, SOD-1 and SOD-2) and four polymorphic (Tf, Alb, MDH and PGM-2). The chi-square (X2) analysis for testing the hypothesis of independent segregation between pairs of polymorphic loci in the population samples, revealed no statistically significant differences. Based on Wright’s F-statistics (FIS, FIT and FST) the detected average value of FIS = 0.1347, indicates a moderate inbreeding within the population samples, whereas the average value of FIT = 0.1912, indicates a moderately great inbreeding in the total population sample.The detected average value of FST = 0.0652, indicates a moderate genetic differentiation among the population samples. The pairwise comparisons of FST point to a moderate differentiation between all comparisons made with the Monte Cristo population sample (FST ranging from 0.061 to 0.066); but very little differentiation was detected between Maracarana and Trombetas samples (FST = 0.0035). A limited gene flow among the population samples was detected (Nm = 3.58). The UPGMA dendrogram showed the lowest genetic distance between population samples of Maracarana and Trombetas, whereas, the highest genetic distances were detected when these two samples were compared to that of Monte Cristo. Exact test for population differentiation revealed high levels of statistically significant differences in all pairwise comparisons made with the Monte Cristo sample. The data point out a possible existence of distinct subpopulations “stocks” of P. expansa in the sampled area, where Monte Cristo sample was always genetically different compared to the other two population samples examined.
References
Alfinito J. 1975. A preservação da tartaruga amazônica. Brasil Florestal 6(21):20-23.
Alfinito J, Vianna CM, Silva MMF and Rodrigues H. 1976. Transferência de tartarugas do rio Trombetas para o rio Tapajós. Brasil Florestal 7(26):49-53.
Alho CJR. 1985. Conservation and management strategies for commonly exploited Amazonian turtles. Biol Conserv 32:291-298.
Alho CJR and Pádua LFM. 1982. Reproductive parameters and nesting behavior of the Amazon turtle Podocnemis expansa (Testudinata, Pelomedusidae) in Brazil. Can J Zool 60:97-103.
Allendorf FW and Luikart G. 2007. Conservation and the genetics of populations. Blackwell Publishing. Malden, MA, Oxford.
Allendorf FW, Mitchell N, Ryman N and Ståhl G. 1977. Isozyme loci in brown trout (Salmo trutla L.): detection and interpretation from population data. Hereditas 86:179-190.
Alves RRN and Santana GG. 2008. Use and commercialization of Podocnemis expansa (Schweiger 1812) (Testudines: Podocnemididae) for medicinal purposes in two communities in North of Brazil. J Ethnobiol Ethnomed 4:1-6.
Anderson NL and Anderson NG. 2002. The human plasma proteome history, character and diagnostic prospects. Mol Cell Proteomics 1:845-867.
Ayala FJ and Kiger Jr. JA. 1980. Modern Genetics. The Benjamins/Cummings Publishing Company, Inc., Menlo Park, California.
Bates HW. 1863. The naturalist on the river Amazons. Murray, London.
Batista RP and Solé-Cava AM. 2005. Baixa diferenciação genética entre populações de peixe-batata (Lopholatilus villarii Miranda-Ribeiro, 1915) ao norte e sul do Banco dos Abrolhos, Brasil. In: Costa, P.A.S., Martins, A.S., Olavo, G. (Eds.). Pesca e potenciais de exploração de recursos vivos na região central da Zona Exclusiva brasileira. Museu Nacional, Rio de Janeiro. 241-247.
Beiguelman B. 2008. Genética de populações humanas. Sociedade Brasileira de Genética, Ribeirão Preto.
Bickham JW, Iverson JB, Parham JF, Philippen HD, Rhodin AGJ, Shaffer HB, Spinks PQ and Dijk PP. 2007. An annotated list of modern turtle terminal taxa with comments on areas of taxonomic instability and recent change Turtle taxonomy working group. Chelonian Research Monographs 4: 173-199.
Billington N. 1996. Genetic markers and stock identification. In: Summerfelt, R.C (Ed.). The walleye culture manual. NCRAC Culture Series 101. North Central Regional Aquaculture Center Publications Office. Iowa State University, Ames. 323 330.
Bock BC, Páez VP and White MM. 2001. Genetic population structure of two threatened South American river turtle species, Podocnemis expansa and Podocnemis unifilis. Chelonian Conserv Bi 4:47-52.
Boettcher EW, Kistler P and Nitschmann HS. 1958. Method of isolating the β1 metal-combining globulin from human blood plasma. Nature 181:490-491.
Chakraborty R, Fuerst PA and Nei M. 1980. Statistical studies on protein polymorphism in natural populations. III. Distribution of allele frequencies and the number of alleles per locus. Genetics 94:1039-1063.
Cisneros-Heredia DF. 2006. Turtles of the Tiputini Biodiversity Station with remarks on the diversity and distribution of the Testudines from Ecuador. Biota Neotrop 6(1):11-23.
Dias LAS. 1998. Variância de frequências alélicas. In: Alfenas, A.C. (Ed.). Eletroforese de isoenzimas e proteínas afins fundamentos e aplicações em plantas e microrganismos. UFV, Viçosa. 381-404.
Durand P, Michalakis Y, Cestier S, Oury B, Leclerc MC, Tibayrenc M and Renaud F. 2003. Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of the Congo) highly endemic for malaria. Am J Trop Med Hyg 68(3):345-349.
Erdoğan M and Özbeyaz C. 2004. Investigation of Blood Protein Polymorphism and Estimation of Genetic Distances in Some Dog Breeds in Turkey. Turk J Vet Anim Sci 28:583-590.
Ferguson A. 1980. Biochemical systematics and evolution. Blackie, Glasgow and London.
Ferguson A, Taggart JB, Prodhöhl PA, McMeel O, Thompson C, Stone C, McGinnity P and Hynes RA. 1995. The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo. J Fish Biol (Suppplement A) 47:103-126.
Ferrarini SA. 1980. Quelônios: Animais em Extinção. Falangola, Manaus.
Ferreira Júnior PD. 2003. Influência dos processos sedimentológicos e geomorfológicos na escolha das áreas de nidificação de Podocnemis expansa (tartaruga-da-amazônia) e Podocnemis unifilis (tracajá), na bacia do rio Araguaia. Ph.D. Thesis, Universidade Federal de Ouro Preto, Escola de Minas, Ouro Preto, MG, Brazil.
Ferreira Júnior PD and Castro PTA. 2003. Geological control of Podocnemis expansa and Podocnemis unifilis nesting Areas in Rio Javaés, Bananal Island, Brazil. Acta Amazonica 33(3):445-468.
Frankham R, Ballou JD and Briscoe DA. 2002. Introduction to conservation genetics. Cambridge Univerity Press, Cambridge, UK.
Frankham R, Ballou JD and Briscoe DA. 2008. Fundamentos da genética da conservação. Editora da Sociedade Brasileira de Genética, Ribeirão Preto.
Futuyma DJ. 1997. Biologia evolutiva. Sociedade Brasileira de Genética, 3ª Ed., Ribeirão Preto.
Gillespie JH. 1998. Population Genetics. The Johns Hopkine University Press, Baltimore.
Gilmore RM. 1986. Fauna e etnozoologia da América do Sul tropical. In: Ribeiro, B.G. (Ed). Suma Etnológica Brasileira.Vozes, Petrópolis. 189-233.
Hartl DL. 2008. Princípios de genética de população. Third Edition. Editora FUNPEC, Ribeirão Preto, SP.
IBAMA. 1989. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis. Projetos Quelônios da Amazônia 10 Anos. IBAMA, Brasília.
Iverson JB. 1992. A revised checklist with distribution maps of the turtles of the world. Earlham College, Richmond, Indiana.
Jamieson A and Turner RJ. 1978. The extended series of Tf alleles in Atlantic cod, Gadus morhua. In: Battaglia B., Beardmore J.A. (Eds). Marine Organisms: genetics ecology and evolution, NATO Conference Series IV: Marine Sciences, No. 2. Plenum Press, New York & London. 699-729.
Kuz’min EV and Kuz’mina OY. 2005. Population analysis of electrophoretic variation in blood serum albumins of European (Acipencer ruthensis L.) and Siberian (A. ruthensis marsiglii Brandt) sterlet. Russ J Genet 41(2):246-253.
Manwell C and Baker C.M. 1970. Molecular Biology and the origin of species. Sidgwick & Jackson, London.
Miller MP. 1997. Tools for Population Genetic Analyses (TFPGA) 1.3: A Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author.
Mittermeier RA. 1978. South America’s river turtles: saving them by use. Oryx 14(3):222-230.
Mittermeier RA, Medem F and Rhodin AGJ. 1980. Vernacular names of South American turtles. Society for Study of Amphibians and Reptiles. Herpetological Circular 9:12.
Moura AS, Oliveira PHG, Klein GN, Tancredi NS, Silva CA and Teixeira AS. 2011. Temporal distribution of the transferrin alleles (Tfa and Tfb) in Amazon turtle (Podocnemis expansa Schweigger, 1812). J Res Biol., 5:346-351.
NC-IUBMB. 2009. Nomenclature Committee of the International Union of Biochemistry and Molecular Biology. Available in
Nei M. 1973. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321-3323.
Nei M. 1975. Molecular population genetics and evolution. North-Halland, Amsterdam and New York.
Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-590.
Nevo E, Ben-Shlomo R, and Lavie B. 1984. Mercury selection of allozymes in marine organisms: Prediction and verification in nature. Proc Natl Acad Sci USA 81:1258-1259.
Nikiforov SM and Zvyagintsev AY. 2008. Allozyme diversity among local populations of the pacific Mussel Mytilus trossulus (Bivalvia: Mytilidae) from polluted areas of Peter the Great bay (Sea of Japan). Russ J Mar Biol., 34(1):45-50.
Pantoja-Lima J. 2007. Aspectos da Biologia Reprodutiva de Podocnemis expansa Schweigger, 1812, Podocnemis sextuberculata Cornalia, 1849 e Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae) na Reserva Biológica do Abufari, Amazonas, Brasil. Master Thesis, Instituto Nacional de Pesquisa da Amazônia/Universidade Federal do Amazonas, Manaus, AM, Brazil.
Pearse DE, Arndt AD, Valenzuela N, Miller BA, Cantarelli V and Sites Jr. JW. 2006. Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon river turtle, Podocnemis expansa (Chelonia: Podocnemididae). Mol Ecol., 15:985-1006.
Pritchard PCH and Trebbau P. 1984. The Turtles of Venezuela. Society for the study of Amphibians and Reptiles, Contributions in Herpetology 2. Fundación de Internados Rurales, Caracas, Venezuela.
Raymond M and Rousset F. 1995. An exact test for population differentiation. Evolution 49:1280-1283.
Redford KH and Robinson JG. 1991. Subsistence and commercial uses of wildlife. In: Robinson, J.G., Redford, K.H. (Eds). Neotropical wildlife use and conservation. Chicago, University of Chicago Press. 7-23.
Ridgway GJ, Sherbune SW and Lewis RD. 1970. Polymorphism in the esterases of Atlantic herring. T Am Fish Soc., 99:147-151.
Ridgway T. 2005. Allozyme electrophoresis still represents a powerful technique in the management of coral reefs. Biodivers Conserv., 14:135-149.
Robinson IP. 1998. Aloenzimas na genética de populações de plantas. In: Alfenas, A.C. (Ed.). Eletroforese de isoenzimas e proteínas afins fundamentos e aplicações em plantas e microrganismos. UFV, Viçosa. 329-380.
Rogers JS. 1972. Measures of genetic similarity and genetic distance. In: Studies in Genetics VII, University of Texas, Austin,TX, USA. Publication 7213:145-154.
Santos JMM, Maia JF, Tadei WP and Rodriguez GAD. 2003. Isoenzymatic variability among five Anopheles species belonging to the Nyssorhynchus and Anopheles Subgenera of the Amazon Region, Brazil. Mem I Oswaldo Cruz 98(2):247-253.
Scaltsoyiannes A. 1999. Allozyme differentiation and phylogeny of Cedar species. Silvae Genet 48 (2):61-68.
Scarpassa VM and Tadei WP. 2000. Enzymatic analysis in Anopheles nuneztovari Gabaldón (Diptera, Culicidae). Rev Bras Biol., 60(4):539-550.
Scribner KT, Evans EJ, Morreale SJ, Smith MH, and Gibbons JW. 1986. Genetic divergence among Populations of the Yellow-bellied Slider turtle (Pseudemys scripta) separated by aquatic and terrestrial habitats. Copeia 3:691-700.
Shaw CR and Prasad R. 1970. Strarch gel electrophoresis of enzymes – A compilation of recipes. Biochem Genet., 4:297-320.
Simon JC and Hebert PN. 1995. Patterns of genetic variation among Canadian populations of the bird cherry-oat aphid, Rhopalosiphum padi L. (Homoptera: Aphididae). Heredity 74:46-35.
Sites Jr. JW, Fritzsimmons NN, da Silva Jr. NJ and Cantarelli VH. 1999. Conservation genetics of the giant Amazon river turtle (Podocnemis expansa: Pelomedusidae) - Inferences from two classes of molecular markers. Chelonian Conserv Bi 3:454-463.
Smith NJH. 1974. Destructive exploitation of the South American river turtle. APCG Yearbook 36:85-102.
Smith NJH. 1979. Aquatic turtles of Amazonia: an endangered resource. Biol Conserv., 16:165-176.
Smith PJ, Francis RICC and Jamieson A. 1981. An excess of homozygotes at a serum esterase locus in the Atlantic mackerel Scomber scombrus. Anim Blood Groups Biochem Genet 12:171-180.
Solferini VN and Selivon D. 2001. Polimorfismos de isozimas. In: Matioli, S.R. (Ed.). Biologia Molecular e Evolução. Holos, Editora, Ribeirão Preto, SP. 137-142.
Sujatha, K, Iswarya Deepti, VA and Shrikanya, KVL. 2011. Allozyme electrophoretic studies in four species of groupers (Pisces: Serranidae) represented in the commercial fishery of Visakhapatnam – India. Indian Journal of Geo-Marine Sciences (IJMS) 40 (3):365-371.
Swofford DL, Selander RB and Black W.C. 1997. BIOSYS-2: A computer program for the analysis of allelic variation in populations genetics and biochemical systematics. Illinois Natural History Survey, IL, USA.
Tao J, Qin Z-Q, Tao Y, Wen L, Shu X-S, Wang Z-C, Liu X-W, Li W-J and Hu W-X. 2007. Genetic relationships among Chinese pigs and other pig populations from Hunan Province, China. Anim Genet 38:417-420.
Teixeira AS, Jamieson A, Raposo JCP and Vieira AA. 1996. Transferrin polymorphism in Amazon Turtle (Podocnemis expansa) stocks. Braz J Genet 19:559-564.
Valenzuela N. 2001. Genetic differentiation among nesting beaches in the highly migratory giant river turtle (Podocnemis expansa) from Colombia. Herpetologica 57:48-57.
Veasey EA, Cardin D, Silva RM, Bressan EA and Vencovsky R. 2008. Assessing the genetic structure of Oryza glumaepatula populations with isozyme markers. Braz Arch Biol Tech., 51(5):873-882.
Verspoor E, Beardmore JA, Consuegra S, García de Leániz C, Hindar K, Jordan WC, Koljonen M-L, Mahkrov AA, Paaver T, Sánchez JA, Skaala Ø, Titov S and Cross TF (2005). Population structure in the Atlantic salmon: insights from 40 years of research into genetic protein variation. J Fish Biol., 67:3-54.
Vogt RC. 2008. Tartarugas da Amazônia. Gráfica Biblos, Lima, Peru.
Wetterberg GB, Ferreira M, Brito WLS and Araujo VC. 1976. Espécies da fauna amazônica potencialmente preferidas para consumo nos restaurantes de Manaus. Brasil Florestal 7(25):59-68.
Workman PL and Niswander JD. 1970. Population studies on southwestern Indian tribes. II. Local genetic differentiation in the Papago. Am J Hum Genet., 22:24-49.
Wright S. 1921. Systems of mating. II. The effects of inbreeding on the genetic composition of a population. Genetics 6:111-123.
Wright S. 1951. The genetical structure of populations. Annals of Eugenic 15:395-420.
Wright S. 1978. Evolution and the genetics of populations, vol.4. Variability within and among natural populations. Universty of Chicago Press, Chicago.
Yeh FC, Yang RC and Boyle T. 1999. Popgene version 1.32. Microsoft Windows-based Freeware for Population Genetic Analysis. Quick User Guide. Center for International Forestry Research, University of Alberta.
Yiğit N, Kankiliç T, Çolak R, Çolak E, Gattermann R, Neumann K, Özkurt Ş and Gharkheloo M.M. 2007. Allozyme variations and genetic differentiation in Mesocricetus brandti Nehring, 1898 and Masocricetus auratus (Waterhouse, 1839) (Mammalia: Rodentia). Turk J Zool., 31:219-227.
Zawadzki CH, Renesto E, Peres MD and Paiva S. 2008. Allozyme variation among three populations of the armored catfish Hypostomus regani (Ihering, 1905) (Siluriformes, Loricariidae) from the Paraná and Paraguay river basins, Brazil. Genet Mol Biol., 31(3):767-771.
Zeidler M. 2000. Electrophoretic analysis of plant isozymes. Acta Univ Palacki Olomuc Fac R Nat 38:7 -16.
Copyright license for the research articles published in Journal of Research in Biology are as per the license given below
Creative Commons License
Journal of Research in Ecology is licensed under a Creative Commons Attribution 4.0 International (CC BY 4.0). (www.creativecommons.org)
Based on a work at www.jresearchbiology.com
What this License explains us?
You are free to:
Share — copy and redistribute the material in any medium or format
Adapt — remix, transform, and build upon the material
for any purpose, even commercially.
This license is acceptable for Free Cultural Works. The licensor cannot revoke these freedoms as long as you follow the license terms.
[As given in the www.creativecommons.org website]
Under the following terms:
Attribution — You must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.
No additional restrictions — You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.