Integrating morphological, molecular and cytogenetic data for F2 sea turtle hybrids diagnosis revealed balanced chromosomal sets.
Cheloniidae
Cryptodira
diagnostics chromosomes
endangered species
introgression
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
19
06
2023
received:
06
03
2023
accepted:
10
07
2023
medline:
20
11
2023
pubmed:
27
10
2023
entrez:
27
10
2023
Statut:
ppublish
Résumé
Hybridization could be considered part of the evolutionary history of many species. The hybridization among sea turtle species on the Brazilian coast is atypical and occurs where nesting areas and reproductive seasons overlap. Integrated analysis of morphology and genetics is still scarce, and there is no evidence of the parental chromosome set distribution in sea turtle interspecific hybrids. In this study, chromosome markers previously established for pure sea turtle species were combined with morphological and molecular analyses aiming to recognize genetic composition and chromosome sets in possible interspecific hybrids initially identified by mixed morphology. The data showed that one hybrid could be an F2 individual among Caretta caretta × Eretmochelys imbricata × Chelonia mydas, and another is resulting from backcross between C. caretta × Lepidochelys olivacea. Native alleles of different parental lineages were reported in the hybrids, and, despite this, it was verified that the hybrid chromosome sets were still balanced. Thus, how sea turtle hybridism can affect genetic features in the long term is a concern, as the implications of the crossing-over in hybrid chromosomal sets and the effects on genetic function are still unpredictable.
Banques de données
RefSeq
['OR529472', 'OR529475', 'OR533309', 'OR533314', 'OP661360']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1595-1608Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 305142/2019-4
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
ID : Financial code 001
Informations de copyright
© 2023 European Society for Evolutionary Biology.
Références
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., … Zinner, D. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
Arantes, L. S., Ferreira, L. C. L., Driller, M., Repinaldo Filho, F. P. M., Mazzoni, C. J., & Santos, F. R. (2020). Genomic evidence of recent hybridization between sea turtles at Abrolhos archipelago and its association to low reproductive output. Scientific Reports, 10, 1-13.
Arantes, L. S., Vilaça, S. T., Mazzoni, C. J., & Santos, F. R. (2020). New genetic insights about hybridization and population structure of hawksbill and loggerhead turtles from Brazil. The Journal of Heredity, 111, 444-456.
Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
Barbosa, P., Pucci, M. B., Nogaroto, V., Almeida, M. C., Artoni, R. F., & Vicari, M. R. (2017). Karyotype analysis of three species of Corydoras (Siluriformes: Callichthyidae) from southern Brazil: Rearranged karyotypes and cytotaxonomy. Neotropical Ichthyology, 15, e160056.
Bérubé, M., & Palsbøll, P. J. (2018). Hybridism. In B. Würsig, J. G. M. Thewissen, & K. M. Kovacs (Eds.), Encyclopedia of marine mammals (3rd ed., pp. 496-501). Academic Press.
Bickham, J. W. (1981). Two-hundred-million-year-old chromosomes: Deceleration of the rate of karyotypic evolution in turtles. Science, 212, 1291-1293.
Bickham, J. W., Bjorndal, K. A., Haiduk, M. W., & Rainey, W. E. (1980). The karyotype and chromosomal banding patterns of the green turtle (Chelonia mydas). Copeia, 1980, 540-543.
Conceição, M. B., Sabaj, J. A. L., Marins, L. F. F., & Marcovaldi, M. A. A. G. D. (1990). Eletrophoretic characterization of a hybrid between Eretmochelys imbricata and Caretta caretta (Cheloniidae). Comparative Biochemistry and Physiology, 97B, 275-278.
Dobigny, G., Britton-Davidian, J., & Robinson, T. J. (2017). Chromosomal polymorphism in mammals: An evolutionary perspective. Biological Reviews of the Cambridge Philosophical Society, 92, 1-21.
Driller, M., Arantes, L. S., Vilaça, S. T., Carrasco-Valenzuela, T., Heeger, F., Mbedi, S., Chevallier, D., De Thoisy, B., & Mazzoni, C. J. (2021). Achieving high-quality ddRAD-like reference catalogs for non-model species: The power of overlapping paired-end reads. BioRxiv. https://doi.org/10.1101/2020.04.03.024331
Faria, R., & Navarro, A. (2010). Chromosomal speciation revisited: Rearranging theory with pieces of evidence. Trends in Ecology & Evolution, 25, 660-669.
Fujita, M. K., Engstrom, T. N., Starkey, D. E., & Shaffer, H. B. (2004). Turtle phylogeny: Insights from a novel nuclear intron. Molecular Phylogenetics and Evolution, 31, 1031-1040.
Galindo, D. J., Martins, G. S., Vozdova, M., Cernohorska, H., Kubickova, S., Bernegossi, A. M., Kadlcikova, D., Rubes, J., & Duarte, J. M. B. (2021). Chromosomal polymorphism and speciation: The case of the genus Mazama (Cetartiodactyla; Cervidae). Genes, 12, 165.
Garofalo, L., Zaccaroni, A., Scaravelli, D., Insacco, G., Zangrilli, M. P., Novelletto, A., & Lorenzini, R. (2012). Morphology vs genetics: The hybrid origin of a sea turtle disproved by DNA. Mediterranean Marine Science, 13, 239-242.
Haddad, C. F., Pombal, J. P., Jr., & Batistic, R. F. (1994). Natural hybridization between diploid and tetraploid species of leaf-frogs, genus Phyllomedusa (amphibia). Journal of Herpetology, 28, 425-430.
Harrison, R. G., & Larson, E. L. (2014). Hybridization, introgression, and the nature of species boundaries. The Journal of Heredity, 105, 795-809.
Hart, C. E., Ley-Quñonez, C. P., Abreu-Grobois, F. A., Plata-Rosas, L. J., Llamas-Gonzalez, I., & Oceguera-Camacho, D. K. E. (2019). Possible hybridization between east Pacific green Chelonia mydas and olive ridley Lepidochelys olivacea sea turtles in Northwest Mexico. Amphibian & Reptile Conservation, 13, 174-180.
IUCN. (2021). The IUCN red list of threatened species. Version 2021-1. https://www.iucnredlist.org
James, M. C., Martin, K., & Dutton, P. H. (2004). Hybridization between a green turtle, Chelonia mydas, and loggerhead turtle, Caretta caretta, and the first record of a green turtle in Atlantic Canada. Canadian Field-Naturalist, 118, 579-582.
Káldy, J., Mozsár, A., Fazekas, G., Farkas, M., Fazekas, D. L., Fazekas, G. L., Goda, K., Gyöngy, Z., Kovács, B., Semmens, K., Bercsényi, M., Molnár, M., & Patakiné Várkonyi, E. (2020). Hybridization of Russian sturgeon (Acipenser gueldenstaedtii, Brandt and Ratzeberg, 1833) and American paddlefish (Polyodon spathula, Walbaum 1792) and evaluation of their progeny. Genes, 11, 753.
Kalvari, I., Nawrocki, E. P., Ontiveros-Palacios, N., Argasinska, J., Lamkiewicz, K., Marz, M., Griffiths-Jones, S., Toffano-Nioche, C., Gautheret, D., Weinberg, Z., & Rivas, E. (2020). Rfam 14: Expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Research, 49, D192-D200.
Karl, S. A., Bowen, B. W., & Avise, J. C. (1995). Hybridization among the ancient mariners: Characterization of marine turtle hybrids with molecular genetic assays. The Journal of Heredity, 86, 262-268.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.
Kelez, S., Velez-Zuazo, X., & Pacheco, A. S. (2016). First record of hybridization between green Chelonia mydas and hawksbill Eretmochelys imbricata sea turtles in the Southeast Pacific. PeerJ, 4, e1712.
King, M. (1995). Species evolution: The role of chromosome change. Cambridge University Press.
Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Pääbo, S., Villablanca, F. X., & Wilson, A. C. (1989). Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196-6200.
Lara-Ruiz, P., Lopez, G. G., Santos, F. R., & Soares, L. S. (2006). Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conservation Genetics, 7, 773-781.
Le, M., Raxworthy, C. J., McCord, W. P., & Mertz, L. (2006). A molecular phylogeny of tortoises (testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517-531.
Leigh, J. W., & Bryant, D. (2015). popart: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110-1116.
Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
Machado, C. R. D., Domit, C., Pucci, M. B., Gazolla, C. B., Glugoski, L., Nogaroto, V., & Vicari, M. R. (2020). Heterochromatin and microsatellites detection in karyotypes of four sea turtle species: Interspecific chromosomal differences. Genetics and Molecular Biology, 43, e20200213.
Machado, C. R. D., Glugoski, L., Domit, C., Pucci, M. B., Goldberg, D. W., Marinho, L. A., da Costa, G. W. W. F., Nogaroto, V., & Vicari, M. R. (2020). Comparative cytogenetics of four sea turtle species (Cheloniidae): G-banding pattern and in situ localization of repetitive DNA units. Cytogenetic and Genome Research, 160, 531-538.
MacPherson, N., Champion, C. P., Weir, L. K., & Dalziel, A. C. (2023). Reproductive isolating mechanisms contributing to asymmetric hybridization in killifishes (Fundulus spp.). Journal of Evolutionary Biology, 36, 605-621.
Mallet, J. (2005). Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229-237.
Mast, R. B., & Carr, J. L. (1989). Carapacial scute variation in Kemp's Ridley Sea turtle (Lepidochelys kempi) hatchlings and juveniles. Conservation and Management, 89, 202-219.
Mayr, E. (1963). Animal species and evolution. Harvard University Press.
Moritz, C. (1994). Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology & Evolution, 9, 373-375.
Naro-Maciel, E., Le, M., FitzSimmon, N. N., & Amato, G. (2008). Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 49, 659-662.
Noonan, B. P., & Chippindale, P. T. (2006). Dispersal and vicariance: The complex evolutionary history of boid snakes. Molecular Phylogenetics and Evolution, 40, 347-358.
Noronha, R. C. R., Almeida, B. R. R., Chagas, M. C. S., Tavares, F. S., Cardoso, A. L., Bastos, C. E. M. C., Silva, N. K. N., Klautau, A. G. C. M., Luna, F. O., Attademo, F. L. N., Lima, D. S., Sabioni, L. A., Sampaio, M. I. C., Oliveira, J. M., Nascimento, L. A. S., Martins, C., Vicari, M. R., Nagamachi, C. Y., & Pieczarka, J. C. (2022). Karyotypes of manatees: New insights into hybrid formation (Trichechus inunguis × Trichechus m. manatus) in the Amazon estuary. Genes, 13, 1263.
Olave, M., Avila, L. J., Sites, J. W., Jr., & Morando, M. (2018). Hybridization could be a common phenomenon within the highly diverse lizard genus Liolaemus. Journal of Evolutionary Biology, 31, 893-903.
Ozdemir, B., & Turkozan, O. (2006). Carapacial scute variation in green turtle, Chelonia mydas hatchlings in Northern Cyprus. Turkish Journal of Zoology, 30, 141-146.
Pekkala, N., Knott, K. E., Kotiaho, J. S., Nissinen, K., & Puurtinen, M. (2012). The benefits of interpopulation hybridization diminish with increasing divergence of small populations. Journal of Evolutionary Biology, 25, 2181-2193.
Piett, S., Hager, H. A., & Gerrard, C. (2015). Characteristics for evaluating the conservation value of species hybrids. Biodiversity and Conservation, 24, 1931-1955.
Pinkel, D., Straume, T., & Gray, J. W. (1986). Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proceedings of the National Academy of Sciences of the United States of America, 83, 2934-2938.
Pomianowski, K., & Ocalewicz, K. (2021). Cytogenetic investigation of Arctic char × brook trout F1, F2 and backcross hybrids revealed remnants of the chromosomal rearrangements. Journal of Applied Genetics, 62, 151-164.
Pritchard, P. C. H., & Mortimer, J. A. (1999). Taxonomy, external morphology, and species identification. In K. L. Eckert, K. A. Bjorndal, F. A. Abreu-Grobois, & M. Donnelly (Eds.), Research and management techniques for the conservation of sea turtles (4th ed., pp. 31-48). IUCN/Species Survival Commission Marine Turtles Specialist Group Publication.
Proietti, M. C., Reisser, J., Marins, L. F., Marcovaldi, M. A., Soares, L. S., Monteiro, D. S., Wijeratne, S., Pattiaratchi, C., & Secchi, E. R. (2014). Hawksbill × loggerhead sea turtle hybrids at Bahia, Brazil: Where do their offspring go? PeerJ, 2, e255.
Purves, W. K., Sadava, D., Orians, G. H., & Heller, H. C. (2001). Life: The science of biology. W H Freeman & Co.
Reis, E. C., Soares, L. S., & Lôbo-Hajdu, G. (2010). Evidence of olive ridley mitochondrial genome introgression into loggerhead turtle rookeries of Sergipe, Brazil. Conservation Genetics, 11, 1587-1591.
Reis, E. C., Soares, L. S., Vargas, S. M., Santos, F. R., Young, R. J., Bjorndal, K. A., Bolten, A. B., & Lôbo-Hajdu, G. (2010). Genetic composition, population structure and phylogeography of the loggerhead sea turtle: Colonization hypothesis for the Brazilian rookeries. Conservation Genetics, 11, 1467-1477.
Rhymer, J. M., & Simberloff, D. (1996). Extinction by hybridization and introgression. Annual Review of Ecology, Evolution, and Systematics, 27, 83-109.
Rodríguez, P. A., Ortiz, M. L., & Bueno, M. L. (2003). Agentes mitogénicos para cultivos de linfocitos en quelonios. Orinoquia, 7, 47-49.
Romano, S. L., & Palumbi, S. R. (1997). Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. Journal of Molecular Evolution, 45, 397-411.
Seabright, M. (1971). A rapid banding technique for human chromosomes. Lancet, 2, 971-972.
Seminoff, J. A., Karl, S. A., 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.
Sim, E. L., Booth, D. T., & Limpus, C. J. (2014). Non-modal Scute patterns, morphology, and locomotor performance of loggerhead (Caretta caretta) and flatback (Natator depressus) turtle hatchlings. Copeia, 2014, 63-69.
Soares, L., Bjorndal, K., Bolten, A., Wayne, M., Castilhos, J., Weber, M., López-Mendilaharsu, M., Marcovaldi, M. A., Vilaça, S. T., & Naro-Maciel, E. (2020). Reproductive output, foraging destinations, and isotopic niche of olive ridley and loggerhead sea turtles, and their hybrids, in Brazil. Endangered Species Research, 44, 237-251.
Soares, L. S., Bjorndal, K. A., Bolten, A. B., Marcovaldi, M. A., Luz, P. B., Machado, R., Lo, R., McDaniel, S. F., Payton, A. C., Waltzek, T. B., & Wayne, M. L. (2018). Effects of hybridization on sea turtle fitness. Conservation Genetics, 19, 1311-1322.
Soares, L. S., Bolten, A. B., Wayne, M. L., Vilaça, S. T., Santos, F. R., Marcovaldi, M. A., & Bjorndal, K. A. (2017). Comparison of reproductive output of hybrid sea turtles and parental species. Marine Biology, 164, 1-10.
Stephens, M., & Donnelly, P. (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162-1169.
Suárez, P., Pinto Barroso, I. C. G., Silva, D. D. S., Milhomem, S. S., Cabral-de-Mello, D. C., Martins, C., Pieczarka, J. C., & Nagamachi, C. Y. (2017). Highest diploid number among Gymnotiformes: First cytogenetic insights into Rhabdolichops (Sternopygidae). Zebrafish, 14, 272-279.
Sumner, A. T. (1972). A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research, 75, 304-306.
Vilaça, S. T., Maroso, F., Lara, P., de Thoisy, B., Chevallier, D., Arantes, L. S., Santos, F. R., Bertorelle, G., & Mazzoni, C. J. (2022). Evidence of backcross inviability and mitochondrial DNA paternal leakage in sea turtle hybrids. Molecular Ecology, 32, 628-643.
Vilaça, S. T., Piccinno, R., Rota-Stabelli, O., Gabrielli, M., Benazzo, A., Matschiner, M., Soares, L. S., Bolten, A. B., Bjorndal, K. A., & Bertorelle, G. (2021). Divergence and hybridization in sea turtles: Inferences from genome data show evidence of ancient gene flow between species. Molecular Ecology, 30, 6178-6192.
Vilaça, S. T., & Santos, F. R. D. (2013). Molecular data for the sea turtle population in Brazil. Dataset Papers in Science, 2013, 196492.
Vilaça, S. T., Vargas, S. M., Lara-Ruiz, P., Molfetti, E., Reis, E. C., Lôbo-Hajdu, G., Soares, L. S., & Santos, F. R. (2012). Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast. Molecular Ecology, 21, 4300-4312.
Wnuk, M., Kotylak, Z., Bugno, M., & Słota, E. (2005). Karyotype analysis in pigs-hybrids of European wild boar (Sus scrofa scrofa) and domestic pig (Sus scrofa domestica). Annals of Animal Science, 5, 11-19.
Wood, J. R., Wood, F. E., & Critchley, K. (1983). Hybridization of Chelonia mydas and Eretmochelys imbricata. Copeia, 1983, 839-842.
Wyneken, J. (2001). The anatomy of sea turtles. NOAA Technical Memorandum NMFS-SEFSC-470, 2001, 1-172.