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Locations and sample sizes of genetically-described immature hawksbill areas (dots) and the Bahia rookery (red star) in Brazil. Red dots indicate detection of hawksbill × loggerhead sea turtle hybrids from the Bahia rookery.
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Hybridization between hawksbill (Eretmochelys imbricata) and loggerhead (Caretta caretta) breeding groups is unusually common in Bahia state, Brazil. Such hybridization is possible because hawksbill and loggerhead nesting activities overlap temporally and spatially along the coast of this state. Nevertheless, the destinations of their offspring are...
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... National Marine Park (n = 65, CCL = 24.5-63.0 cm, mean 37.9 cm); as well as from three areas with sporadic occurrence of this species: (1) Arvoredo Biological Marine Biological Reserve (n = 6, CCL = 30-59.5 cm, mean 41.3 cm); (2) Ceará coast (n = 23, CCL = 22.4-57.5 cm, mean 37.8 cm); and (3) Cassino Beach (n = 25, CCL = 30-60 cm, mean 41 cm; Fig. 1). Loggerheads are not commonly observed at most of these areas (Reisser et al., 2008;, but occur at Ceará (Marcovaldi et al., 2012) and are frequently found at Cassino Beach (Bugoni, Krause & Petry, 2001;Monteiro, Bugoni & Estima, 2006). Samples were collected using disposable scalpels from the flippers of turtles hand-captured in ...
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... Most of these hybrids presented the morphology of pure hawksbill turtles (Fig. 2) and were identified as such, but their mtDNA haplotype was characteristic of nesting loggerheads of the Bahia rookery (BR3). This haplotype was present in one of 23 samples from Ceará (northeast Brazil), and in three of 19 samples from Cassino in the far South ( Fig. 1). At Ceará, the hybrid was sampled after being incidentally caught in fisheries, and at Cassino all three hybrids were found dead on the beach. At Cassino one hybrid displayed carapace with overlapping scutes and serrated edges like hawksbills, but a short and thick neck typical of loggerheads ( Fig. 2A). This mixed morphology brings ...
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... hybrids from the Bahia rookery remain highly undetected relative to the considerable number that is generated, reporting their occurrence at loggerhead feeding grounds (Cassino Beach and Ceará) and their absence at important hawksbill feeding grounds (e.g., Abrolhos, SPSP) is an important step towards better understanding this phenomenon (see Fig. 1). Our modeling approach also highlights the importance of sea turtle nesting season on shaping the spatial distribution of post-hatchlings, with differences observed between hawksbill, loggerhead and hybrid dispersal (see Fig. 3). While immature hybrids were observed at areas uncommon for hawksbills, they were absent at recognized ...
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We report here a dataset comprising nine nuclear markers for the Brazilian population of Cheloniidae turtles: hawksbills (Eretmochelys imbricata), loggerheads (Caretta caretta), olive ridleys (Lepidochelys olivacea), and green turtles (Chelonia mydas). Because hybridization is a common phenomenon between the four Cheloniidae species nesting on the...
Citations
... However, it can also compromise small populations by limiting their growth rate through the production of inviable offspring (Todesco et al. 2016). The consequences of these processes in sea turtles are not yet completely understood, but a few studies have observed some differences in behavior and reproductive success between hybrids and parental species (Proietti et al. 2014b;Soares et al. 2017;Arantes et al. 2020a). For instance, while the clutch size of loggerhead and hawksbill hybrids has been reported as intermediate, emergence success was lower in hybrids (Soares et al. 2017;Arantes et al. 2020a). ...
... Likewise, post-emergence behavior can also be slightly divergent. Some hybrids, morphologically identified as one parental species, may adopt the migration patterns of the other (Proietti et al. 2014b). Furthermore, these hybrids are not likely to be completely inviable since genetic studies using mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) have detected crosses between F1 hybrids and parental species (e.g., Vilaça et al. 2012;Brito et al. 2020;Arantes et al. 2020c). ...
Sea turtles are migratory species with wide geographical distributions, usually spanning multiple countries. This characteristic , along with their complex life cycle, makes sea turtle conservation challenging. In Brazil, continued monitoring and recent studies have advanced the knowledge of sea turtle genetic composition and population structure. Some of these studies have shown that hybridization is highly frequent in certain regions along the Brazilian coast, despite being relatively rare globally. Here, we investigate the hybridization and genetic diversity of sea turtles in nesting and feeding grounds in the state of Alagoas, northeastern Brazil, using the control region of mitochondrial DNA and three nuclear loci. We were able to identify hybrids between four sea turtle species, but mainly between Caretta caretta and Eretmochelys imbricata and C. caretta and Lepidochelys olivacea. Most hybrids were readily identified using morphology and mitochondrial DNA, but some were only detected with nuclear DNA. Apart from hybrids, the genetic profile of each species was congruent with previous studies in Brazil. However, one stranded E. imbricata had a haplotype (Ei-IP17) and nuclear allele typically found in the Indo-Pacific, suggesting long distance migration for this species. Our results indicate that hybridization events might be even more geographically spread along the coast of Brazil and provide evidence of the connection between E. imbricata from the Atlantic and Indo-Pacific Ocean basins.
... Other less common hybrids in Bahia include those between loggerheads x olive ridleys, hawksbills x olive ridleys (Soares et al., 2018(Soares et al., , 2021(Soares et al., , 2017Vilaça et al., 2012), and greens x loggerheads (Karl et al., 1995). Interestingly, most molecular studies involving morphologicallyidentified hawksbills found hybrids with loggerhead mitochondrial DNA (mtDNA), and very few hybrid individuals displayed hawksbill mtDNA (Bass et al., 1996;Brito et al., 2020;Lara-Ruiz et al., 2006;Proietti et al., 2014;Soares et al., 2018Soares et al., , 2017. ...
... Genetic studies in the Praia do Forte population have been done since the 1980s and the presence of hybrids has been reported in all studies of this rookery Bass et al., 1996;Brito et al., 2020;Conceição, Levy, Marins, & Marcovaldi, 1990;Karl et al., 1995;Lara-Ruiz et al., 2006;Proietti et al., 2014;Soares et al., 2018Soares et al., , 2017Vilaça et al., 2013Vilaça et al., , 2012. However, no adult backcross has been reported yet, indicating that there is evidence of strong hybrid breakdown in the second generation. ...
... Previous studies have found hybrid juveniles in hawksbills' feeding areas in southern Brazil, and dispersal simulations showed that hybrids can potentially migrate following both species patterns (Brito et al., 2020;Proietti et al., 2014). Sea turtles are one of the classical examples of species that navigate long distances by sensing Earth's geomagnetic field (Lohmann, Goforth, Mackiewicz, Lim, & Lohmann, 2022;Lohmann et al., 2008). ...
Hybridization is known to be part of many species' evolutionary history. Sea turtles have a fascinating hybridization system in which species separated by as much as 43 million years are still capable of hybridizing. Indeed, the largest nesting populations in Brazil of loggerheads (Caretta caretta) and hawksbills (Eretmochelys imbricata) have a high incidence of hybrids between these two species. A third species, olive ridleys (Lepidochelys olivacea), is also known to hybridize although at a smaller scale. Here we used restriction site-associated DNA sequencing (RAD-Seq) markers, mitogenomes, and satellite-telemetry to investigate the patterns of hybridization and introgression in the Brazilian sea turtle population and their relationship with the migratory behaviors between feeding and nesting aggregations. We also explicitly test if the mixing of two divergent genomes in sea turtle hybrids causes mitochondrial paternal leakage. We developed a new species-specific PCR-assay capable of detecting mitochondrial DNA (mtDNA) inheritance from both parental species and performed ultra-deep sequencing to estimate the abundance of each mtDNA type. Our results show that all adult hybrids are first generation (F1) and most display a loggerhead migratory behavior. We detected paternal leakage in F1 hybrids and different proportions of mitochondria from maternal and paternal species. Although previous studies showed no significant fitness decrease in hatchlings, our results support genetically-related hybrid breakdown possibly caused by cytonuclear incompatibility. Further research on hybrids from other populations besides Brazil and between different species will show if backcross inviability and mitochondrial paternal leakage is observed across sea turtle species.
... Considering C. caretta reproductively more isolated than E. imbricata, which is probably why there is no contribution of genetic variation from other subpopulations (Wallace et al., 2010), this study reinforces the importance of secondary nesting areas, which can contribute genetically by producing more male hatchlings. The former has been demonstrated in sea turtle populations laying eggs in Brazil that are characterized by a high incidence of hybrids, in addition to a significant genetic differentiation from other turtle populations (Vilaça et al., 2013;Proietti et al., 2014) highlighted that the spatial and temporal overlap in nesting sites of C. caretta and E. imbricata can result in hybrid individuals. Furthermore, in Brazil the nesting groups of C. caretta and E. imbricata have exceptionally high hybridization rates (Lara-Ruiz et al., 2006). ...
This study evaluates the reproductive and ecological similarity between loggerhead sea turtle (Caretta caretta) and Hawksbill sea turtle (Eretmochelys imbricata) two species of sea turtles on the southern coast of Bahia (Brazil) during two breeding seasons (October to April 2013 to 2015). The study covers a 10-km area composed of three beaches, Pompilho, Itacarezinho and Patizeiro beach, which are 5, 3, and 2 km long, respectively. Daily field surveys were performed for 102 days to assess patterns between the studied species, using the non-metric multidimensional scaling order and the Spearman correlation analysis to obtain the oviposition pattern of the two species. Moreover, Kruskall-Wallys tests were performed to review the differences in the number of hatchlings on the three beaches. The NMDS proved the species are very similar from an ecological perspective since as there were three clear groupings in terms of the number of hatchlings on the three beaches. With reference to the number of nests, a negative correlation was observed in the two species. Regarding the hatching activity of both species on the three beaches studied, a larger amount of C. caretta and E. imbricata hatchlings was found on Pompilho beach, followed by Patizeiro and Itacarézinho. These findings influence management strategies to reduce anthropogenic impact and contribute to the conservation of these two endangered sea turtle species.
... Segundo Arantes (2019), os prováveis fatores que contribuem para este evento único no Brasil incluem: (i) a sobreposição espaço-temporal das desovas de diferentes espécies, que dão oportunidade para que o cruzamento interespecífico ocorra. Isto é corroborado pela observação de que o período de maior ocorrência de híbridos é intermediário ao pico reprodutivo das tartarugas de pente e cabeçuda na Bahia (SOARES et al., 2017), (ii) a recente diminuição do tamanho populacional das tartarugas marinhas, o que torna mais raros os encontros de indivíduos de cada sexo da mesma espécie (VILAÇA et al., 2012), (iii) os tamanhos populacionais diferentes para as espécies envolvidas na hibridização, visto que a tartaruga-cabeçuda é mais abundante no país e a grande maioria dos casos de hibridização na costa brasileira envolvem fêmeas de tartaruga-cabeçuda (VILAÇA et al., 2012;PROIETTI et al., 2014), e (iv) a taxa sexual altamente desproporcional, uma vez que estima-se que aproximadamente 90% dos filhotes nascidos na Bahia sejam fêmeas (MARCOVALDI; GODFREY; MROSOVSKY, 1997, MARCOVALDI et al., 2014. ...
The described work presents a bibliographic review about the hybridization process being described in the literature between animal and plant species, intensified in the last decades through anthropic actions. In sea turtles it can occur naturally, since many
species have overlapping spawning areas and reproductive seasons of two or more species. Molecular studies were used in addition to morphological observations to accurately identify hybrid individuals, with the application of techniques with molecular markers through mitochondrial DNA and nuclear markers, verifying haplotypes and loci of these individuals in relation to their parental species.
... Particle tracking software (Ichthyop v.3.2) has been used extensively to model dispersal patterns of sea turtles (Proietti et al., 2014;Putman et al., 2016) and other marine creatures (Pagán et al., 2003;Condie et al., 2011). To estimate the dispersal route of green turtle hatchlings in the South China Sea, this study used particle tracking software (Ichthyop v.3.2,www.ichthyop.org) ...
High-resolution ocean circulation models have increased our understanding of the movement and distribution of worldwide ocean currents, which were previously unknown and difficult to study. The metabolic expenditure data obtained through open-flow respirometric analysis was put into an energy budget context by comparing it to their available reserved energy in the body upon entering the swimming life phase. We modeled the dispersal range of green turtle hatchling from Chagar Hutang in various monsoon season using the particle-tracking program Ichthyop v3.2 and ocean surface current output from HYCOM (Hybrid Coordinate Ocean Model). The prediction distribution suggests that ocean current variability determines their movements into different dispersal areas. The simulated hatchlings are distributed north into the Gulf of Thailand during the Southwest monsoon, while during the Northeast monsoon, the simulated hatchlings travel south into the Java Sea. By quantifying hatchlings potential energy, they can swim a distance of 116 km and can last up to 7 days. Green turtle hatchlings from Chagar Hutang reached offshore water of Kelantan State and Terengganu waters near Tenggol Island on Day 7. These findings highlight areas of high priority for conservation, as habitat crucial for an endangered sea turtle species during a critical period of early development.
... Particle tracking software (Ichthyop v.3.2) has been used extensively to model dispersal patterns of sea turtles (Proietti et al., 2014;Putman et al., 2016) and other marine creatures (Pagán, 2003;Condie et al., 2011). In order to estimate the dispersal route of green turtle hatchlings in the South China Sea, this study used particle tracking software (Ichthyop v.3.2, www.ichthyop.org) ...
... The study of genetic variability and sea turtle evolution are crucial for monitoring population stocks and management areas and for assessing biological and behavioral patterns, in addition to addressing aspects of animal conservation [Wallace et al., 2011]. Although interspecific hybridization in chelonian species has been reported from the last 3 decades [Lara-Ruiz et al., 2006;Proietti et al., 2014;Arantes et al., 2020], the chromosomal mechanisms involved in hybrid formation in sea turtles are poorly understood. ...
Sea turtles are considered flagship species for marine biodiversity conservation and are considered to be at varying risk of extinction globally. Cases of hybridism have been reported in sea turtles, but chromosomal analyses are limited to classical karyotype descriptions and a few molecular cyto-genetic studies. In order to compare karyotypes and understand evolutive mechanisms related to chromosome differentiation in this group, Chelonia mydas, Caretta caretta, Eretmochelys imbricata, and Lepidochelys olivacea were cy-togenetically characterized in the present study. When the obtained cytogenetic data were compared with the puta-tive ancestral Cryptodira karyotype, the studied species showed the same diploid number (2n) of 56 chromosomes, with some variations in chromosomal morphology (karyo-typic formula) and minor changes in longitudinal band locations. In situ localization using a 18S ribosomal DNA probe indicated a homeologous microchromosome pair bearing a 45S ribosomal DNA locus and size heteromorphism in all 4 species. Interstitial telomeric sites were identified in a micro-chromosome pair in C. mydas and C. caretta. The data showed that interspecific variations occurred in chromo-somal sets among the Cheloniidae species, in addition to other Cryptodira karyotypes. These variations generated lineage-specific karyotypic diversification in sea turtles, which will have considerable implications for hybrid recognition and for the study, the biology, ecology, and evolutionary history of regional and global populations. Furthermore , we demonstrated that some chromosome rearrangements occurred in sea turtle species, which is in conflict with the hypothesis of conserved karyotypes in this group.
... All sea turtle species show different levels of threat of extinction and are considered flag species for the conservation of biodiversity (IUCN, 2020) since numerous threats affect the populations maintenance (Lara-Ruiz et al., 2006;Proietti et al., 2014;Arantes et al., 2020). In addition, chromosomal studies in turtles demonstrated great karyotypic diversification among evolutionary lineages, making the cytogenetic knowledge important for recognition of species diversity and conservation (Valenzuela and Adams, 2011;Montiel et al., 2016;Rovatsos et al., 2017;Cavalcante et al., 2018;Lee et al., 2019;Deakin and Ezaz, 2019;Clemente et al., 2020;Viana et al., 2020). ...
The wide variation in size and content of eukaryotic genomes is mainly attributed to the accumulation of repetitive DNA sequences, like microsatellites, which are tandemly repeated DNA sequences. Sea turtles share a diploid number (2n) of 56, however recent molecular cytogenetic data have shown that karyotype conservatism is not a rule in the group. In this study, the heterochromatin distribution and the chromosomal location of microsatellites (CA) n , (GA) n , (CAG) n , (GATA) n , (GAA) n , (CGC) n and (GACA) n in Chelonia mydas, Caretta caretta, Eretmochelys imbricata and Lepidochelys olivacea were comparatively investigated. The obtained data showed that just the (CA) n , (GA) n , (CAG) n and (GATA) n microsatellites were located on sea turtle chromosomes, preferentially in heterochromatic regions of the microchromosomes (mc). Variations in the location of heterochromatin and microsatellites sites, especially in some pericentromeric regions of macrochromosomes, corroborate to proposal of centromere repositioning occurrence in Cheloniidae species. Furthermore, the results obtained with the location of microsatellites corroborate with the temperature sex determination mechanism proposal and the absence of heteromorphic sex chromosomes in sea turtles. The findings are useful for understanding part of the karyotypic diversification observed in sea turtles, especially those that explain the diversification of Carettini from Chelonini species.
... Our temporal nesting distribution, although not systematically sampled, corroborates data from Soares et al. 14 indicating that loggerhead females nest earlier than both hybrids and hawksbills, and that hybrids have a temporal nesting distribution that overlaps with both parental species. Hawksbill males arrive in the reproductive area of Bahia (Praia do Forte) around the loggerhead nesting peak (November and December), thus having the opportunity to mate with conspecific females as well as loggerhead females, which is the most abundant species on the Brazilian coast and in Abrolhos 10,23 . The timing of reproductive seasons of both species and the abundance of loggerheads along the Brazilian coast appear to favor interspecific crossings in Bahia 14 . ...
Hybridization between sea turtle species occurs with particularly high frequency at two adjacent nesting areas in northeastern Brazil. To understand the outcomes of hybridization and their consequences for sea turtle conservation, we need to evaluate the extent of hybridization occurrence and possible deleterious effects in the hybrid progeny. Thus, we investigated the hypothesis of the existence of a new hybrid spot offshore of Brazil’s northeastern coast. The Abrolhos Archipelago is surrounded by the largest and richest coral reefs in the South Atlantic and is known to be a nesting site for loggerhead turtles (Carettacaretta). In this study, we performed a multidisciplinary investigation into levels of hybridization in sea turtles and their reproductive output in the Abrolhos beaches. Genetic data from mitochondrial DNA (mtDNA) and six autosomal markers showed that there are first-generation hybrid females nesting in Abrolhos, resulting from crossings between hawksbill males (Eretmochelysimbricata) and loggerhead females, and backcrossed hatchlings from both parental species. The type and extent of hybridization were characterized using genomic data obtained with the 3RAD method, which confirmed backcrossing between F1 hybrids and loggerhead turtles. The reproductive output data of Abrolhos nests suggests a disadvantage of hybrids when compared to loggerheads. For the first time, we have shown the association between hybridization and low reproductive success, which may represent a threat to sea turtle conservation.
... Other genetic studies including Brazilian sea turtles have investigated their demographic history (Bjorndal et al. 2006;Vargas et al. 2008;Molfetti et al. 2013), population structure (Reis et al. 2010a;Vilaça et al. 2013;Shamblin et al. 2014;Arantes et al. 2020), mixed stocks at foraging aggregations (Proietti et al. 2009(Proietti et al. , 2014bReis et al. 2010a;Vilaça et al. 2013) and interspecific hybridization (Lara-Ruiz et al. 2006;Reis et al. 2010b;Vilaça et al. 2012;Proietti et al. 2014a;Soares et al. 2017Soares et al. , 2018. For example, phylogeographic analyses using mtDNA showed significant genetic divergence among 3 Brazilian rookeries of C. caretta, suggesting the recognition of 3 different management units (Shamblin et al. 2014), while 2 separate demographic units were recognized for E. imbricata in Brazilian nesting areas . ...
... This is probably associated with the prevalence of C. caretta along the Brazilian coast and the partial overlapping of reproductive season with E. imbricata (Vilaça et al. 2012). The beginning of the nesting season for E. imbricata overlaps with the nesting peak of C. caretta (November and December), when E. imbricata males encounter a higher number of C. caretta females to mate (Proietti et al. 2014a). Conversely, the encounter between C. caretta males and E. imbricata females may happen less frequently, since C. caretta males leave the mating areas before a large number of E. imbricata females arrive at nesting beaches (Vilaça et al. 2012). ...
An extremely high incidence of hybridization among sea turtles is found along the Brazilian coast. To understand this atypical phenomenon and its impact on sea turtle conservation, research focused in the evolutionary history of sea turtles is fundamental. We assessed high quality multilocus haplotypes of 143 samples of the five species of sea turtles that occur along the Brazilian coast to investigate the hybridization process and the population structure of hawksbill (Eretmochelys imbricata) and loggerhead turtles (Caretta caretta). The multilocus data were initially used to characterize interspecific hybrids. Introgression (F2 hybrids) was only confirmed in hatchlings of F1 hybrid females (hawksbill x loggerhead), indicating that introgression was either previously overestimated and F2 hybrids may not survive to adulthood, or the first-generation hybrid females nesting in Brazil were born as recent as few decades ago. Phylogenetic analyses using nuclear markers recovered the mtDNA-based Indo-Pacific and Atlantic lineages for hawksbill turtles, demonstrating a deep genetic divergence dating from the early Pliocene. In addition, loggerhead turtles that share a common feeding area and belong to distinct Indo-Pacific and Atlantic mtDNA clades present no clear genetic differentiation at the nuclear level. Finally, our results indicate that hawksbill and loggerhead rookeries along the Brazilian coast are likely connected by male-mediated gene flow.
