Combined use of mitochondrial and nuclear genetic markers further reveal immature marine turtle hybrids along the South Western Atlantic

Brito, Cíntia; Vilaça, Sibelle Torres; Lacerda, Ana Luzia; Maggioni, Rodrigo; Marcovaldi, Maria Ângela; Vélez-Rubio, Gabriela; Proietti, Maíra Carneiro

doi:10.1590/1678-4685-GMB-2019-0098

Cíntia Brito

Universidade Federal do Rio Grande (FURG), Instituto de Oceanografia (IO), Laboratório de Ecologia Molecular Marinha, Rio Grande, RS, Brazil.

* These authors contributed equally as first authors.

http://orcid.org/0000-0001-5828-3400

Sibelle Torres Vilaça

Trent University, Environmental and Life Sciences Graduate Program, Peterborough, Canada.

Department of Evolutionary Genetics, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany.

* These authors contributed equally as first authors.

http://orcid.org/0000-0002-6887-4703

Ana Luzia Lacerda

Universidade Federal do Rio Grande (FURG), Instituto de Oceanografia (IO), Laboratório de Ecologia Molecular Marinha, Rio Grande, RS, Brazil.

http://orcid.org/0000-0001-6654-5597

Rodrigo Maggioni

Universidade Federal do Ceará (UFC), Instituto de Ciências do Mar (LABOMAR), Fortaleza, CE, Brazil.

http://orcid.org/0000-0002-1119-1020

Maria Ângela Marcovaldi

Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Projeto TAMAR, Salvador, BA, Brazil.

Fundação Pró-TAMAR, Salvador, BA, Brazil.

Gabriela Vélez-Rubio

Asociación Civil Karumbé, Montevideo, Uruguay.

Universidade de la República, Centro Universitario Regional del Este (CURE), Rocha, Uruguay.

http://orcid.org/0000-0002-6033-0920

Maíra Carneiro Proietti

Universidade Federal do Rio Grande (FURG), Instituto de Oceanografia (IO), Laboratório de Ecologia Molecular Marinha, Rio Grande, RS, Brazil.

http://orcid.org/0000-0002-5504-5770

Send correspondence to Cíntia Brito Universidade Federal do Rio Grande (FURG), Instituto de Oceanografia (IO), Laboratório de Ecologia Molecular Marinha, Av. Itália, s/n Km 8 Carreiros, CEP: 96203-900, Rio Grande, RS, Brazil. E-mail: cintiabrito@gmail.com. #Present address: University of Ferrara, Department of Life Sciences and Biotechnology, Ferrara, Italy.

*
These authors contributed equally as first authors.

Conflict of Interest The authors declare that there is no conflict of interest that could be perceived as prejudicial to the impartiality of the reported research.

Author Contributions MCP and CB conceived the study, ALL, RM, AMA and GVR contributed with samples, CB conducted the experiments, CB and STV analyzed the data. CB, MCP and STV wrote the manuscript. All authors read, revised and approved the final version of the manuscript.

Associate Editor: Antonio Solé-Cava

Figures (5)
Tables (2)

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Figure 1
Sampling sites in the South Western Atlantic, indicating the number of individuals analyzed for mtDNA/nDNA. ASP São Pedro and São Paulo Archipelago; AB Abrolhos Archipelago; AL Alagoas; CA Cassino; CE Ceará, BA Bahia; ES Espírito Santo; RJ Rio de Janeiro; SC Santa Catarina; SE Sergipe; UY Uruguay.

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Figure 2
mtDNA (D-Loop) haplotype network constructed based on the Median-Joining method. Circles represent each of the identified haplotypes, size corresponds to the frequency of occurrence of the haplotype, and color represents the sampling location. Dashes between haplotypes represent the number of distinct bases between them.

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Figure 3
Geographic distribution of D-Loop haplotypes found in the mtDNA analysis along the South Western Atlantic. ASP São Pedro and São Paulo Archipelago; (n = 12); AB Abrolhos Archipelago (n = 75); AL - Alagoas (n = 6); CA - Cassino (n = 33); CE - Ceará (n = 56), BA - Bahia (n = 61); ES - Espírito Santo (n = 11); RJ Rio de Janeiro (n = 2); SC Santa Catarina (n = 6); SE - Sergipe (n = 1); UY - Uruguay (n = 7).

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Figure 4
Cluster analysis performed in STRUCTURE for three nDNA markers (RAG1, RAG2 and CMOS). X-axis represents each of the individuals analysed, y-axis is the estimated mixture ratio of each of the parent species in the composition of these individuals. Species abbreviation and colors: blue, E. imbricata (Ei); orange, C. caretta (Cc); purple, L. olivacea (Lo); green, C. mydas (Cm).

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Figure 5
Assignment probability model for the 12 E. imbricata x C. caretta hybrids identified by mtDNA analysis (AP56 UY05) and two additional hybrids identified only through nDNA (CA23 and PF06). The y-axis represents the probability that each individual belongs to each of the six categories presented (Ei, Cc, F1, F2, F1xEi e F1xCc).

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Table 1
Hybridization events reported between Cheloniidae marine turtles, the respective species, number of observed hybrids and country.

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Table 2
Immature sea turtle hybridsImmature sea turtle hybrids identified at the South Western Atlantic, with sampling area, mtDNA haplotype, species involved, and inference on hybrid classes. AL - Alagoas, BA - Bahia, CA - Cassino, CE - Ceará, ES - Espirito Santo, UY - Uruguay.

Species A	Species B	No. identified hybrids	Country	References
Caretta caretta	Lepidochelys kempii	1	USA	Karl et al., 1995Karl SA, Bowen BW and Avise JC (1995) Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J Hered 86:262-268.
Caretta caretta	Chelonia mydas	4	Brazil	Karl et al., 1995Karl SA, Bowen BW and Avise JC (1995) Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J Hered 86:262-268.
		1	Canada	James et al., 2004
		3	USA	Komoroske et al., 2019
Caretta caretta	Lepidochelys olivacea	14	Brazil	Reis et al., 2010Reis EC, Soares LS, Vargas SM, Santos FR, Young RJ, Bjorndal KA, Bolten AB and Lôbo-Hajdu G (2010) Genetic composition, population structure and phylogeography of the loggerhead sea turtle: Colonization hypothesis for the Brazilian rookeries. Conserv Genet 11:1467-1477.
Eretmochelys imbricata	Caretta caretta	2	USA	Karl et al., 1995Karl SA, Bowen BW and Avise JC (1995) Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J Hered 86:262-268.
		50	Brazil	Lara-Ruiz et al., 2006Lara-Ruiz P, Lopez GG, Santos FR and Soares LS (2006) Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conserv Genet 7:773-781.
		1	Brazil	Conceição et al., 1990Conceição MB, Levy JA, Marins LF and Marcovaldi MA (1990) Electrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comp Biochem Physiol 97:275-278.
		4	Brazil	Proietti et al., 2012
		34	Brazil	Soares et al., 2017Soares LS, Bolten AB, Wayne ML, Vilaça ST, Santos FR, Marcovaldi MAG and Bjorndal KA (2017) Comparison of reproductive output of hybrid sea turtles and parental species. Mar Biol 164:9.
		10	Brazil	Bass et al., 1996
		1	USA	Komoroske et al., 2019
		2	Argentina	Prosdocimi et al., 2014Prosdocimi L, Bruno I, Diaz L, Carman VG, Albareda DA and Remis MI (2014) Southernmost reports of the hawksbill sea turtle, Eretmochelys imbricata, in temperate waters of Argentina and evidence of a hybrid origin supported by mitochondrial DNA analysis. Herpetol Rev 45:1-5.
Eretmochelys imbricata	Chelonia mydas	1	Suriname	Karl et al., 1995Karl SA, Bowen BW and Avise JC (1995) Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J Hered 86:262-268.
		1	Mexico	Seminoff et al., 2003Seminoff JA, Karl SA, Schwartz TS and 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. Bull Mar Sci 73:643-652.
		1	Peru	Kelez et al., 2016
Eretmochelys imbricata	Lepidochelys olivacea	2	Brazil	Lara-Ruiz et al., 2006Lara-Ruiz P, Lopez GG, Santos FR and Soares LS (2006) Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conserv Genet 7:773-781.

Sample	Area	Haplotype	mtDNA	nDNA	F - M*	Classes
AL02	AL	CCA4.2	EixCc	-	Cc - Ei	-
AP56	BA	CCA4.2	EixCc	EixCc	Cc - Ei	F1
PF06	BA	EiA01	Ei	EixCc	Ei - Cc or Ei - EixCc	F1 or F1xEi
SA10	BA	CCA4.2	EixCc	-	Cc - Ei	-
CA04	CA	CCA4.2	EixCc	-	Cc - Ei	-
CA12	CA	CCA4.2	EixCc	Ei	EixCc - Ei	F1xEi
CA14	CA	CCA4.2	EixCc	Ei	EixCc - Ei	F1xEi
CA22	CA	CCA4.2	EixCc	Ei	EixCc - Ei	F1xEi
CA23	CA	EiA01	Ei	EixCc	Ei - Cc or Ei - EixCc	F1 or F1xEi
CA24	CA	CCA4.2	EixCc	EixCc	Cc - Ei	F1
CA25	CA	CCA4.2	EixCc	EixCc	Cc - Ei	F1
CA31	CA	CCA4.2	EixCc	EixCc	Cc - Ei	F1
CA32	CA	CCA24.1	EixCc	-	Cc - Ei	-
CA33	CA	CCA4.1	EixCc	-	Cc - Ei	-
CA36	CA	CCA4.1	EixCc	EixCc	Cc - Ei	F1
CE04	CE	CCA4.2	EixCc	EixCc	Cc - Ei	F1
CE32	CE	Hap F	EixLo	Ei/Lo	Lo - Ei	-
CE43	CE	Hap F	EixLo	Ei/Lo	Lo - Ei	-
CE51	CE	CCA4.2	EixCc	EixCc	Cc - Ei	F1
ES05	ES	Hap F	EixLo	-	Lo - Ei	-
UY01	UY	CCA4.2	EixCc	Ei	EixCc - Ei	F1xEi
UY05	UY	CCA4.2	EixCc	Ei	EixCc - Ei	F1xEi
*F: female – M: male.

[1] Send correspondence to Cíntia Brito Universidade Federal do Rio Grande (FURG), Instituto de Oceanografia (IO), Laboratório de Ecologia Molecular Marinha, Av. Itália, s/n Km 8 Carreiros, CEP: 96203-900, Rio Grande, RS, Brazil. E-mail: cintiabrito@gmail.com. #Present address: University of Ferrara, Department of Life Sciences and Biotechnology, Ferrara, Italy.

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Combined use of mitochondrial and nuclear genetic markers further reveal immature marine turtle hybrids along the South Western Atlantic

Abstract