Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast
Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia Sta...
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Published in | Molecular ecology Vol. 21; no. 17; pp. 4300 - 4312 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Oxford, UK
Blackwell Publishing Ltd
01.09.2012
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Subjects | |
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Abstract | Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ∼40 years. |
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AbstractList | Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ∼40 years. Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ~40 years.Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ~40 years. Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea×E. imbricata and L. olivacea×C. caretta are F1 hybrids, whereas C. caretta×E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta×E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta×E. imbricata×Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or 40years. [PUBLICATION ABSTRACT] Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ∼40 years. Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea E. imbricata and L. olivacea C. caretta are F1 hybrids, whereas C. caretta E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. carettaE. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta E. imbricata Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or similar to 40 years. Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (E. imbricata), loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ~40 years. Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as Eretmochelys imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, because most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analysed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill ( E. imbricata ), loggerhead ( Caretta caretta ) and olive ridley ( Lepidochelys olivacea ). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas . The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ∼40 years. |
Author | VARGAS, SARAH M. SANTOS, FABRÍCIO R. SOARES, LUCIANO S. LARA-RUIZ, PAULA REIS, ESTÉFANE C. LÔBO-HAJDU, GISELE VILAÇA, SIBELLE T. MOLFETTI, ÉRICA |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22780882$$D View this record in MEDLINE/PubMed |
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References | Bowen BW, Grant WS, Hillis-Starr Z et al. (2007) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Molecular Ecology, 16, 49-60. Spinks PQ, Shaffer HB (2007) Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conservation Genetics, 8, 641-657. Lee PLM (2008) Molecular ecology of marine turtles: new approaches and future directions. Journal of Experimental Marine Biology and Ecology, 356, 25-42. Kamezaki N (1983) The possibility of hybridization between the loggerhead turtle, Caretta caretta, and the hawksbill turtle, Eretmochelys imbricata, in specimens hatched from eggs collected in Chita Peninsula. Japanese Journal of Herpetology, 10, 52-53. Le M, Raxworthy CJ, McCord WP, Mertz L (2006) A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517-531. Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198-207. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27, 83-109. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Molecular Ecology, 16, 4886-4907. Fritz U, Ayaz D, Buschbom J et al. (2007) Go east: phylogeographies of Mauremys caspica and M. rivulata- discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology, 21, 527-540. Conceição MB, Levy JA, Marins LF, Marcovaldi MA (1990) Electrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 97, 275-278. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361. DOI: 10.1007/s12686-011-9548-7 Wirtz P (1999) Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour, 58, 1-12. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. The American Journal of Human Genetics, 73, 1162-1169. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Molecular Ecology, 17, 2566-2580. Stuart BL, Parham JF (2007) Recent hybrid origin of three rare Chinese turtles. Conservation Genetics, 8, 169-175. Mallet J (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229-237. Naro-Maciel E, Le M, FitzSimmons NN, Amato G (2008) Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 49, 659-662. Lee PLM, Hays GC, Avise JC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proceedings of the National Academy of Sciences of the USA, 101, 6530-6535. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48. Marcovaldi MA, Vieitas CF, Godfrey MH (1999) Nesting and conservation management of hawksbill turtles (Eretmochelys imbricata) in northern Bahia, Brazil. Chelonian Conservation and Biology, 3, 301-307. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138. Reis EC, Soares LS, Lobo-Hajdu G (2010a) Evidence of olive ridley mitochondrial genome introgression into loggerhead turtle rookeries of Sergipe, Brazil. Conservation Genetics, 11, 1587-1591. Matsuzawa Y, Sato K, Sakamoto W, Bjorndal KA (2002) Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead sea turtle (Caretta caretta) pre-emergent hatchlings in Minabe, Japan. Marine Biology, 140, 639-646. Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. Journal of Heredity, 92, 206-211. Zbinden JA, Largiader AR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Molecular Ecology, 16, 3703-3711. Nielsen EEG, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Molecular Ecology Notes, 6, 971-973. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620. Karl SA, Avise JC (1993) PCR-based assays of mendelian polymorphisms from anonymous single-copy nuclear-DNA - techniques and applications for population-genetics. Molecular Biology and Evolution, 10, 342-361. Wood JR, Wood FE, Critchley K (1983) Hybridization of Chelonia mydas and Eretmochelys imbricata. Copeia, 3, 839-842. Reis EC, Soares LS, Vargas SM et al. (2010b) Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries. Conservation Genetics, 11, 1467-1477. Buskirk JR, Parham JF, Feldman CR (2005) On the hybridisation between two distantly related Asian turtles (Testudines: Sacalia Mauremys). Salamandra, 41, 21-26. Meylan AB, Donnelly M (1999) Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN Red List of threatened animals. Chelonian Conservation and Biology, 3, 200-224. Vianna JA, Bonde RK, Caballero S et al. (2006) Phylogeography, phylogeny and hybridization in trichechid sirenians: implications for manatee conservation. Molecular Ecology, 15, 433-447. Marcovaldi MA, Lopez GG, Soares LS, López-Mendilaharsu M (2012) Satellite tracking of hawksbill turtles Eretmochelys imbricata nesting in northern Bahia, Brazil: insights on movements and foraging destinations. Endangered Species Research, 17, 123-132. DOI: 10.3354/esr00421 Karl SA, Bowen BW, Avise JC (1995) Hybridization among the ancient mariners - characterization of marine turtle hybrids with molecular-genetic assays. Journal of Heredity, 86, 262-268. Shamblin BM, Faircloth BC, Dodd M et al. (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Molecular Ecology Notes, 7, 784-787. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. Frazier J (1988) Sea turtles in the land of the dragon. Sanctuary, 8, 15-23. Lara-Ruiz P, Lopez GG, Santos FR, Soares LS (2006) Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conservation Genetics, 7, 773-781. Krenz JG, Naylor GJP, Shaffer HB, Janzen FJ (2005) Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution, 37, 178-191. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution, 16, 613-622. Heppel SS (1998) Applicaton of life-history theory and population model analysis to turtle conservation. Copeia, 2, 367-375. Seminoff JA, Karl SA, Schwartz T, Resendiz A (2003) Hybridization of the green turtle (Chelonia mydas) and hawksbill turtle (Eretmochelys imbricata) in the Pacific Ocean: indication of an absence of gender bias in the directionality of crosses. Bulletin of Marine Science, 73, 643-652. Aggarwal RK, Velavan TP, Udaykumar D et al. (2004) Development and characterization of novel microsatellite markers from the olive ridley sea turtle (Lepidochelys olivacea). Molecular Ecology Notes, 4, 77-79. Casale P, Mazaris AD, Freggi D (2011) Estimation of age at maturity of loggerhead sea turtles Caretta caretta in the Mediterranean using length-frequency data. Endangered Species Research, 13, 123-129. Bass AL, Good DA, Bjorndal KA et al. (1996) Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Molecular Ecology, 5, 321-328. Farias IP, Jerozolimski A, Melo A et al. (2007) Population genetics of the Amazonian tortoises, Chelonoidis denticulata and C-carbonaria, (Cryptodira : Testudinidae) in an area of sympatry. Amphibia-Reptilia, 28, 357-365. 2004; 101 2001; 92 1990; 97 1983; 3 2010a; 11 2008; 17 2006; 15 2004; 4 2006; 7 2005; 41 1983; 10 2005; 20 2006; 6 2011; 13 1999; 3 2012; 17 2000; 155 2010b; 11 2003; 73 2007; 16 2007; 28 1995; 86 2002; 160 2006; 40 2004; 19 2002; 140 1999; 16 1993; 10 1988; 8 2008; 49 1999; 58 2007; 8 2007; 7 1983 2001; 16 1998; 2 19962004 2008; 356 2005; 37 1996; 5 2007; 21 2012; 4 1996; 27 2005; 14 e_1_2_6_51_1 e_1_2_6_30_1 Kamezaki N (e_1_2_6_20_1) 1983; 10 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_34_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_43_1 Karl SA (e_1_2_6_21_1) 1993; 10 Seminoff JA (e_1_2_6_42_1) 2003; 73 e_1_2_6_41_1 e_1_2_6_9_1 Buskirk JR (e_1_2_6_10_1) 2005; 41 Carr AF (e_1_2_6_11_1) 1983 e_1_2_6_5_1 e_1_2_6_7_1 e_1_2_6_24_1 Meylan AB (e_1_2_6_32_1) 1999; 3 e_1_2_6_49_1 e_1_2_6_3_1 e_1_2_6_22_1 Frazier J (e_1_2_6_17_1) 1988; 8 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_26_1 e_1_2_6_47_1 e_1_2_6_31_1 e_1_2_6_50_1 Marcovaldi MA (e_1_2_6_29_1) 1999; 3 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_40_1 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_44_1 e_1_2_6_27_1 e_1_2_6_46_1 |
References_xml | – reference: Vianna JA, Bonde RK, Caballero S et al. (2006) Phylogeography, phylogeny and hybridization in trichechid sirenians: implications for manatee conservation. Molecular Ecology, 15, 433-447. – reference: Frazier J (1988) Sea turtles in the land of the dragon. Sanctuary, 8, 15-23. – reference: Marcovaldi MA, Vieitas CF, Godfrey MH (1999) Nesting and conservation management of hawksbill turtles (Eretmochelys imbricata) in northern Bahia, Brazil. Chelonian Conservation and Biology, 3, 301-307. – reference: Reis EC, Soares LS, Lobo-Hajdu G (2010a) Evidence of olive ridley mitochondrial genome introgression into loggerhead turtle rookeries of Sergipe, Brazil. Conservation Genetics, 11, 1587-1591. – reference: Farias IP, Jerozolimski A, Melo A et al. (2007) Population genetics of the Amazonian tortoises, Chelonoidis denticulata and C-carbonaria, (Cryptodira : Testudinidae) in an area of sympatry. Amphibia-Reptilia, 28, 357-365. – reference: Heppel SS (1998) Applicaton of life-history theory and population model analysis to turtle conservation. Copeia, 2, 367-375. – reference: Mallet J (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229-237. – reference: Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27, 83-109. – reference: Meylan AB, Donnelly M (1999) Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN Red List of threatened animals. Chelonian Conservation and Biology, 3, 200-224. – reference: Seminoff JA, Karl SA, Schwartz T, Resendiz A (2003) Hybridization of the green turtle (Chelonia mydas) and hawksbill turtle (Eretmochelys imbricata) in the Pacific Ocean: indication of an absence of gender bias in the directionality of crosses. Bulletin of Marine Science, 73, 643-652. – reference: Lara-Ruiz P, Lopez GG, Santos FR, Soares LS (2006) Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conservation Genetics, 7, 773-781. – reference: Stuart BL, Parham JF (2007) Recent hybrid origin of three rare Chinese turtles. Conservation Genetics, 8, 169-175. – reference: Kamezaki N (1983) The possibility of hybridization between the loggerhead turtle, Caretta caretta, and the hawksbill turtle, Eretmochelys imbricata, in specimens hatched from eggs collected in Chita Peninsula. Japanese Journal of Herpetology, 10, 52-53. – reference: Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48. – reference: Wirtz P (1999) Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour, 58, 1-12. – reference: Karl SA, Avise JC (1993) PCR-based assays of mendelian polymorphisms from anonymous single-copy nuclear-DNA - techniques and applications for population-genetics. Molecular Biology and Evolution, 10, 342-361. – reference: Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. – reference: Wood JR, Wood FE, Critchley K (1983) Hybridization of Chelonia mydas and Eretmochelys imbricata. Copeia, 3, 839-842. – reference: Casale P, Mazaris AD, Freggi D (2011) Estimation of age at maturity of loggerhead sea turtles Caretta caretta in the Mediterranean using length-frequency data. Endangered Species Research, 13, 123-129. – reference: Marcovaldi MA, Lopez GG, Soares LS, López-Mendilaharsu M (2012) Satellite tracking of hawksbill turtles Eretmochelys imbricata nesting in northern Bahia, Brazil: insights on movements and foraging destinations. Endangered Species Research, 17, 123-132. DOI: 10.3354/esr00421 – reference: Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Molecular Ecology, 16, 4886-4907. – reference: Conceição MB, Levy JA, Marins LF, Marcovaldi MA (1990) Electrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 97, 275-278. – reference: Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. Journal of Heredity, 92, 206-211. – reference: Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138. – reference: Bowen BW, Grant WS, Hillis-Starr Z et al. (2007) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Molecular Ecology, 16, 49-60. – reference: Fritz U, Ayaz D, Buschbom J et al. (2007) Go east: phylogeographies of Mauremys caspica and M. rivulata- discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology, 21, 527-540. – reference: Nielsen EEG, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Molecular Ecology Notes, 6, 971-973. – reference: Buskirk JR, Parham JF, Feldman CR (2005) On the hybridisation between two distantly related Asian turtles (Testudines: Sacalia Mauremys). Salamandra, 41, 21-26. – reference: Matsuzawa Y, Sato K, Sakamoto W, Bjorndal KA (2002) Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead sea turtle (Caretta caretta) pre-emergent hatchlings in Minabe, Japan. Marine Biology, 140, 639-646. – reference: Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution, 16, 613-622. – reference: Lee PLM, Hays GC, Avise JC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proceedings of the National Academy of Sciences of the USA, 101, 6530-6535. – reference: Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. The American Journal of Human Genetics, 73, 1162-1169. – reference: Krenz JG, Naylor GJP, Shaffer HB, Janzen FJ (2005) Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution, 37, 178-191. – reference: Aggarwal RK, Velavan TP, Udaykumar D et al. (2004) Development and characterization of novel microsatellite markers from the olive ridley sea turtle (Lepidochelys olivacea). Molecular Ecology Notes, 4, 77-79. – reference: Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198-207. – reference: Le M, Raxworthy CJ, McCord WP, Mertz L (2006) A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517-531. – reference: Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361. DOI: 10.1007/s12686-011-9548-7 – reference: Lee PLM (2008) Molecular ecology of marine turtles: new approaches and future directions. Journal of Experimental Marine Biology and Ecology, 356, 25-42. – reference: Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620. – reference: Bass AL, Good DA, Bjorndal KA et al. (1996) Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Molecular Ecology, 5, 321-328. – reference: Naro-Maciel E, Le M, FitzSimmons NN, Amato G (2008) Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 49, 659-662. – reference: Karl SA, Bowen BW, Avise JC (1995) Hybridization among the ancient mariners - characterization of marine turtle hybrids with molecular-genetic assays. Journal of Heredity, 86, 262-268. – reference: Shamblin BM, Faircloth BC, Dodd M et al. (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Molecular Ecology Notes, 7, 784-787. – reference: Zbinden JA, Largiader AR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Molecular Ecology, 16, 3703-3711. – reference: Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229. – reference: Spinks PQ, Shaffer HB (2007) Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conservation Genetics, 8, 641-657. – reference: Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Molecular Ecology, 17, 2566-2580. – reference: Reis EC, Soares LS, Vargas SM et al. (2010b) Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries. Conservation Genetics, 11, 1467-1477. – volume: 19 start-page: 198 year: 2004 end-page: 207 article-title: Hybridization and adaptive radiation publication-title: Trends in Ecology & Evolution – volume: 41 start-page: 21 year: 2005 end-page: 26 article-title: On the hybridisation between two distantly related Asian turtles (Testudines: Sacalia Mauremys) publication-title: Salamandra – volume: 4 start-page: 77 year: 2004 end-page: 79 article-title: Development and characterization of novel microsatellite markers from the olive ridley sea turtle ( ) publication-title: Molecular Ecology Notes – volume: 16 start-page: 4886 year: 2007 end-page: 4907 article-title: Population genetics and phylogeography of sea turtles publication-title: Molecular Ecology – volume: 17 start-page: 2566 year: 2008 end-page: 2580 article-title: Multiple paternity in reptiles: patterns and processes publication-title: Molecular Ecology – volume: 13 start-page: 123 year: 2011 end-page: 129 article-title: Estimation of age at maturity of loggerhead sea turtles in the Mediterranean using length‐frequency data publication-title: Endangered Species Research – volume: 8 start-page: 169 year: 2007 end-page: 175 article-title: Recent hybrid origin of three rare Chinese turtles publication-title: Conservation Genetics – volume: 140 start-page: 639 year: 2002 end-page: 646 article-title: Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead sea turtle ( ) pre‐emergent hatchlings in Minabe, Japan publication-title: Marine Biology – volume: 49 start-page: 659 year: 2008 end-page: 662 article-title: Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes publication-title: Molecular Phylogenetics and Evolution – volume: 73 start-page: 1162 year: 2003 end-page: 1169 article-title: A comparison of bayesian methods for haplotype reconstruction from population genotype data publication-title: The American Journal of Human Genetics – volume: 58 start-page: 1 year: 1999 end-page: 12 article-title: Mother species‐father species: unidirectional hybridization in animals with female choice publication-title: Animal Behaviour – volume: 101 start-page: 6530 year: 2004 end-page: 6535 article-title: Polyandry in a marine turtle: females make the best of a bad job publication-title: Proceedings of the National Academy of Sciences of the USA – volume: 8 start-page: 15 year: 1988 end-page: 23 article-title: Sea turtles in the land of the dragon publication-title: Sanctuary – volume: 92 start-page: 206 year: 2001 end-page: 211 article-title: Turtle mating systems: behavior, sperm storage, and genetic paternity publication-title: Journal of Heredity – volume: 16 start-page: 613 year: 2001 end-page: 622 article-title: The problems with hybrids: setting conservation guidelines publication-title: Trends in Ecology & Evolution – volume: 4 start-page: 137 year: 2004 end-page: 138 article-title: Distruct: a program for the graphical display of population structure publication-title: Molecular Ecology Notes – volume: 3 start-page: 200 year: 1999 end-page: 224 article-title: Status justification for listing the hawksbill turtle ( ) as critically endangered on the 1996 IUCN Red List of threatened animals publication-title: Chelonian Conservation and Biology – volume: 16 start-page: 3703 year: 2007 end-page: 3711 article-title: High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles publication-title: Molecular Ecology – volume: 27 start-page: 83 year: 1996 end-page: 109 article-title: Extinction by hybridization and introgression publication-title: Annual Review of Ecology and Systematics – volume: 3 start-page: 839 year: 1983 end-page: 842 article-title: Hybridization of and publication-title: Copeia – volume: 3 start-page: 301 year: 1999 end-page: 307 article-title: Nesting and conservation management of hawksbill turtles ( ) in northern Bahia, Brazil publication-title: Chelonian Conservation and Biology – volume: 356 start-page: 25 year: 2008 end-page: 42 article-title: Molecular ecology of marine turtles: new approaches and future directions publication-title: Journal of Experimental Marine Biology and Ecology – year: 19962004 – volume: 5 start-page: 321 year: 1996 end-page: 328 article-title: Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, , with mtDNA sequences publication-title: Molecular Ecology – volume: 7 start-page: 773 year: 2006 end-page: 781 article-title: Extensive hybridization in hawksbill turtles ( ) nesting in Brazil revealed by mtDNA analyses publication-title: Conservation Genetics – volume: 16 start-page: 37 year: 1999 end-page: 48 article-title: Median‐joining networks for inferring intraspecific phylogenies publication-title: Molecular Biology and Evolution – volume: 11 start-page: 1467 year: 2010b end-page: 1477 article-title: Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries publication-title: Conservation Genetics – volume: 86 start-page: 262 year: 1995 end-page: 268 article-title: Hybridization among the ancient mariners – characterization of marine turtle hybrids with molecular‐genetic assays publication-title: Journal of Heredity – volume: 20 start-page: 229 year: 2005 end-page: 237 article-title: Hybridization as an invasion of the genome publication-title: Trends in Ecology and Evolution – volume: 17 start-page: 123 year: 2012 end-page: 132 article-title: Satellite tracking of hawksbill turtles nesting in northern Bahia, Brazil: insights on movements and foraging destinations publication-title: Endangered Species Research – volume: 7 start-page: 784 year: 2007 end-page: 787 article-title: Tetranucleotide microsatellites from the loggerhead sea turtle ( ) publication-title: Molecular Ecology Notes – volume: 97 start-page: 275 year: 1990 end-page: 278 article-title: Electrophoretic characterization of a hybrid between and (Cheloniidae) publication-title: Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology – volume: 73 start-page: 643 year: 2003 end-page: 652 article-title: Hybridization of the green turtle ( ) and hawksbill turtle ( ) in the Pacific Ocean: indication of an absence of gender bias in the directionality of crosses publication-title: Bulletin of Marine Science – volume: 28 start-page: 357 year: 2007 end-page: 365 article-title: Population genetics of the Amazonian tortoises, Chelonoidis denticulata and C‐carbonaria, (Cryptodira : Testudinidae) in an area of sympatry publication-title: Amphibia-Reptilia – start-page: 277 year: 1983 end-page: 287 – volume: 14 start-page: 2611 year: 2005 end-page: 2620 article-title: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study publication-title: Molecular Ecology – volume: 40 start-page: 517 year: 2006 end-page: 531 article-title: A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes publication-title: Molecular Phylogenetics and Evolution – volume: 155 start-page: 945 year: 2000 end-page: 959 article-title: Inference of population structure using multilocus genotype data publication-title: Genetics – volume: 160 start-page: 1217 year: 2002 end-page: 1229 article-title: A model‐based method for identifying species hybrids using multilocus genetic data publication-title: Genetics – volume: 2 start-page: 367 year: 1998 end-page: 375 article-title: Applicaton of life‐history theory and population model analysis to turtle conservation publication-title: Copeia – volume: 4 start-page: 359 year: 2012 end-page: 361 article-title: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method publication-title: Conservation Genetics Resources – 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Snippet | Surprisingly, a high frequency of interspecific sea turtle hybrids has been previously recorded in a nesting site along a short stretch of the Brazilian coast.... |
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SubjectTerms | Animals Anthropogenic factors Aquatic reptiles backcrossing Bayes Theorem Biological Evolution Brazil Caretta caretta Cell Nucleus Cell Nucleus - genetics Chelonia mydas Cluster Analysis coasts DNA, Mitochondrial DNA, Mitochondrial - genetics Eretmochelys imbricata Female females genetics Genotype Haplotypes Hybridization Hybridization, Genetic Hybrids introgression Lepidochelys olivacea Male Microsatellite Repeats Mitochondrial DNA Molecular Sequence Data Mydas Nesting nesting sites Polymorphism, Restriction Fragment Length Population genetics Reptiles & amphibians sea turtles Sequence Analysis, DNA Turtles Turtles - genetics Wildlife conservation |
Title | Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast |
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