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 inMolecular ecology Vol. 21; no. 17; pp. 4300 - 4312
Main Authors VILAÇA, SIBELLE T., VARGAS, SARAH M., LARA-RUIZ, PAULA, MOLFETTI, ÉRICA, REIS, ESTÉFANE C., LÔBO-HAJDU, GISELE, SOARES, LUCIANO S., SANTOS, FABRÍCIO R.
Format Journal Article
LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.09.2012
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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.
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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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.
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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
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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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https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1365-294X.2012.05685.x
https://www.ncbi.nlm.nih.gov/pubmed/22780882
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Volume 21
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