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"Dutton, Peter"
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Breeding Sex Ratios in Adult Leatherback Turtles (Dermochelys coriacea) May Compensate for Female-Biased Hatchling Sex Ratios
For vertebrates with temperature-dependent sex determination, primary (or hatchling) sex ratios are often skewed, an issue of particular relevance to concerns over effects of climate change on populations. However, the ratio of breeding males to females, or the operational sex ratio (OSR), is important to understand because it has consequences for population demographics and determines the capacity of a species to persist. The OSR also affects mating behaviors and mate choice, depending on the more abundant sex. For sea turtles, hatchling and juvenile sex ratios are generally female-biased, and with warming nesting beach temperatures, there is concern that populations may become feminized. Our purpose was to evaluate the breeding sex ratio for leatherback turtles at a nesting beach in St. Croix, USVI. In 2010, we sampled nesting females and later sampled their hatchlings as they emerged from nests. Total genomic DNA was extracted and all individuals were genotyped using 6 polymorphic microsatellite markers. We genotyped 662 hatchlings from 58 females, matching 55 females conclusively to their nests. Of the 55, 42 females mated with one male each, 9 mated with 2 males each and 4 mated with at least 3 males each, for a multiple paternity rate of 23.6%. Using GERUD1.0, we reconstructed parental genotypes, identifying 47 different males and 46 females for an estimated breeding sex ratio of 1.02 males for every female. Thus we demonstrate that there are as many actively breeding males as females in this population. Concerns about female-biased adult sex ratios may be premature, and mate choice or competition may play more of a role in sea turtle reproduction than previously thought. We recommend monitoring breeding sex ratios in the future to allow the integration of this demographic parameter in population models.
Journal Article
The evolutionary history and global phylogeography of the green turtle ( Chelonia mydas )
AimTo examine the genetic structure and global phylogeography of the endangered green sea turtle, Chelonia mydas, in light of past climatic events and current conservation needs.LocationTropical and subtropical beaches around the world.MethodsWe analysed 386 base pairs of the mitochondrial (mt)DNA control region of 4,878 individual nesting green turtle samples from 127 rookeries globally. We used phylogeographic analysis to assess how demographic history, dispersal and barriers to gene flow have led to the current distribution of mtDNA lineages.ResultsWe identified 11 divergent lineages that were tied to specific biogeographical regions. The phylogenetic analyses revealed an ancient origin for the species centred in the Indo‐Pacific and more recent colonization of the Central/Eastern Pacific as well as the Atlantic Basin. Overall the phylogeographic structure was strong but with a clear pattern of regional connectivity among rookeries. A Large genetic separation was found where there were obvious barriers to dispersal such as between the Atlantic and Pacific oceans and across the Pacific Ocean, as well as less obvious barriers to dispersal. Admixture of mtDNA haplotype lineages was detected at latitudinal extremes across the Indian Ocean and western Pacific Ocean resulting in these areas being nucleotide diversity hotspots. The highest regional genetic diversity and high endemic richness was observed in the SW Pacific, NW Pacific, SW Indian and NW Indian oceans.Main conclusionsPast climatic fluctuations greatly affected the distribution of genetic diversity in the highly migratory green turtle. Our data suggest that past climatic events influenced local populations in different ways and the species appears to have survived the last glaciations in multiple glacial refugia.
Journal Article
Geographic patterns of genetic variation in a broadly distributed marine vertebrate: new insights into loggerhead turtle stock structure from expanded mitochondrial DNA sequences
Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (~800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology.
Journal Article
Genetic analysis and satellite tracking reveal origin of the green turtles in San Diego Bay
Understanding population structure and migration patterns is critical for conservation of marine species that undertake seasonal migrations, often spanning entire oceans, between breeding grounds and distant feeding areas. To examine the stock origin of the green turtle foraging aggregation in San Diego Bay, California, USA (32.6°N, 117.1°W) and evaluate current life history hypotheses, 770 bp sequences of the mitochondrial DNA control region from 121 green turtles captured in San Diego Bay were compared to potential source (nesting) populations across the Pacific. Mixed stock analysis indicated that the San Diego Bay foraging population originates from eastern Pacific nesting sites, primarily the Revillagigedo Archipelago and the coast of Michoacán, Mexico. To further understand migratory pathways and breeding destinations, three mature female turtles were satellite tracked from the San Diego Bay foraging ground (FG), including one turtle tracked for 364 days that nested at Socorro Island in Revillagigedo and returned to San Diego Bay (total distance approx. 3200 km), one of the first continuous satellite tracks of a sea turtle from a FG to its nesting site and back. Tracks from another turtle indicated possible nesting at Tres Marias Islands, approximately 100 km off the Mexican mainland coast. All three turtles have subsequently been recaptured in San Diego Bay, indicating a high degree of FG philopatry. These results rule out previous speculation that Hawaiian green turtles were also using San Diego Bay, provide insights into the distribution of the Revillagigedo Islands and Michoacán breeding populations and draw attention to the Tres Marias Islands as a potential source of green turtles in the temperate North Pacific.
Journal Article
Multiple Distant Origins for Green Sea Turtles Aggregating off Gorgona Island in the Colombian Eastern Pacific
Mitochondrial DNA analyses have been useful for resolving maternal lineages and migratory behavior to foraging grounds (FG) in sea turtles. However, little is known about source rookeries and haplotype composition of foraging green turtle aggregations in the southeastern Pacific. We used mitochondrial DNA control region sequences to identify the haplotype composition of 55 green turtles, Chelonia mydas, captured in foraging grounds of Gorgona National Park in the Colombian Pacific. Amplified fragments of the control region (457 bp) revealed the presence of seven haplotypes, with haplotype (h) and nucleotide (π) diversities of h = 0.300±0.080 and π = 0.009±0.005 respectively. The most common haplotype was CMP4 observed in 83% of individuals, followed by CMP22 (5%). The genetic composition of the Gorgona foraging population primarily comprised haplotypes that have been found at eastern Pacific rookeries including Mexico and the Galapagos, as well as haplotypes of unknown stock origin that likely originated from more distant western Pacific rookeries. Mixed stock analysis suggests that the Gorgona FG population is comprised mostly of animals from the Galapagos rookery (80%). Lagrangian drifter data showed that movement of turtles along the eastern Pacific coast and eastward from distant western and central Pacific sites was possible through passive drift. Our results highlight the importance of this protected area for conservation management of green turtles recruited from distant sites along the eastern Pacific Ocean.
Journal Article
Mixed stock analysis of juvenile green turtles aggregating at two foraging grounds in Fiji reveals major contribution from the American Samoa Management Unit
In this study we assessed the breeding population, or Management Unit (MU), origin of green turtles (Chelonia mydas) present at Yadua Island and Makogai Island foraging grounds in Fiji, central South Pacific. Based on analysis of mitochondrial (mt) DNA sequences from 150 immature green turtles caught during surveys carried out in 2015–2016, we identified a total of 18 haplotypes, the most common being CmP22.1 (44%) which is a primary haplotype characterizing the American Samoa breeding population. Results of a Bayesian mixed-stock analysis reveals that the two foraging grounds are used by green turtles from the American Samoa MU (72%, Credible Interval (CI): 56–87%), New Caledonia MU (17%, CI: 6–26%) and French Polynesia MU (7%, CI: 0–23%). The prominence of the contribution we found from the American Samoa MU compared to that of French Polynesia, both which have historic telemetry and tagging data showing connectivity with Fijian foraging areas, may reflect the current relative abundance of these two nesting populations and draws attention to a need to update population surveys and identify any significant nesting in Fiji that may have been overlooked.
Journal Article
First Assessment of the Sex Ratio for an East Pacific Green Sea Turtle Foraging Aggregation: Validation and Application of a Testosterone ELISA
Determining sex ratios of endangered populations is important for wildlife management, particularly species subject to sex-specific threats or that exhibit temperature-dependent sex determination. Sea turtle sex is determined by incubation temperature and individuals lack external sex-based traits until sexual maturity. Previous research utilized serum/plasma testosterone radioimmunoassays (RIA) to determine sex in immature/juvenile sea turtles. However, there has been a growing application of enzyme-linked immunosorbent assay (ELISA) for wildlife endocrinology studies, but no study on sea turtles has compared the results of ELISA and RIA. This study provides the first sex ratio for a threatened East Pacific green sea turtle (Chelonia mydas) foraging aggregation, a critical step for future management of this species. Here, we validate a testosterone ELISA and compare results between RIA and ELISA of duplicate samples. The ELISA demonstrated excellent correspondence with the RIA for providing testosterone concentrations for sex determination. Neither assay proved reliable for predicting the sex of reproductively active females with increased testosterone production. We then applied ELISA to examine the sex ratio of 69 green turtles foraging in San Diego Bay, California. Of 45 immature turtles sampled, sex could not be determined for three turtles because testosterone concentrations fell between the ranges for either sex (females: 4.1-113.1 pg/mL, males: 198.4-2,613.0 pg/mL) and these turtles were not subsequently recaptured to enable sex determination; using a Bayesian model to predict probabilities of turtle sex we predicted all three 'unknowns' were female (> 0.86). Additionally, the model assigned all turtles with their correct sex (if determined at recapture) with 100% accuracy. Results indicated a female bias (2.83F:1M) among all turtles in the aggregation; when focusing only on putative immature turtles the sex ratio was 3.5F:1M. With appropriate validation, ELISA sexing could be applied to other sea turtle species, and serve as a crucial conservation tool.
Journal Article
Cumulative human impacts on marine predators
Stressors associated with human activities interact in complex ways to affect marine ecosystems, yet we lack spatially explicit assessments of cumulative impacts on ecologically and economically key components such as marine predators. Here we develop a metric of cumulative utilization and impact (CUI) on marine predators by combining electronic tracking data of eight protected predator species (
n
=685 individuals) in the California Current Ecosystem with data on 24 anthropogenic stressors. We show significant variation in CUI with some of the highest impacts within US National Marine Sanctuaries. High variation in underlying species and cumulative impact distributions means that neither alone is sufficient for effective spatial management. Instead, comprehensive management approaches accounting for both cumulative human impacts and trade-offs among multiple stressors must be applied in planning the use of marine resources.
Human activities affect marine predators in complex ways, yet we lack spatial understanding of cumulative impacts across key habitats. Here the authors analyse distribution and movements of eight marine predators, and find that species and human impacts vary across space and overlap within marine sanctuaries.
Journal Article
Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories
Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 Mya. The genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of noncollinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared with other reptiles, and harbor a higher genetic load compared with green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.
Journal Article