ANNUAL DIFFERENCES IN FEMALE REPRODUCTIVE SUCCESS AFFECT SPATIAL AND COHORT-SPECIFIC GENOTYPIC HETEROGENEITY IN PAINTED TURTLES

Long-term ecological data were used to evaluate the relative importance of movements, breeding structure, and reproductive ecological factors to the degree of spatial and age-specific variation in genetic characteristics of painted turtles (Chrysemys picta) on the E. S. George Reserve in southeastern Michigan. Estimates of the degree of spatial genetic structuring were based on the proportion of total genotypic variance partitioned within and between subpopulations (inferred from hierarchical F-statistics based on variation at 18 protein loci), and in terms of gene correlations (co-ancestry among individuals derived from reproductive data on full-sib families of females nesting at specific nesting areas). Little variation in allele frequency was observed among turtles from different marshes (F_mt = 0.003), though significant variation was observed among turtles from different nesting areas associated with each marsh (F_nm = 0.046). Gene correlations among individuals within nesting areas varied greatly over years (0.032-0.171; mean = 0.069) and were negatively correlated to the proportion of females that successfully nested during each year. General concordance between independent estimates of genotypic correlations (i.e., F_nm derived from protein electrophoretic variation vs. mean co-ancestry) suggests that allozyme data, when collected over spatial scales consistent with species behavioral characteristics and reproductive ecology, may accurately reflect the apportionment of gene diversity within and among subpopulations. The magnitude and patterning of allelic variation among nesting areas and individuals appears to be primarily a function of gametic correlations among members of full-sib families, irrespective of the degree of gene flow or female nesting-site fidelity. Comparisons of genetic characteristics among 11 cohorts (1974-1984) revealed that heterozygosity (H) and inbreeding coefficients (F) varied greatly. Cohort estimates of H and F were correlated to female nesting success and to estimates of co-ancestry for the same years. Results clearly reflect the concomitant importance of ecological factors (principally the proportion of the female population that successfully produce offspring during each year) in determining the magnitude and patterning of gene correlations within and among groups, and to the genotypic composition of offspring born during each year.     

Putting the heat on sex determination

Sex determination and differentiation are inherently fascinating to both layperson and geneticist. Major advances have accelerated interest in the molecular genetic events mediating these processes in nematodes, flies, mice and humans. Far less attention has been paid to those organisms, particularly reptiles, where sex is determined by environmental cues. However, recent experimental evidence suggests that the two modes of sex determination may not only share common genetic elements, but may also be regulated by similar mechanisms. We argue that the ability to manipulate sex by temperature provides a particularly suitable model for exploring the molecular basis of this fundamental biological process.     

Quantifying impacts of plastic debris on marine wildlife identifies ecological breakpoints

Quantifying sublethal effects of plastics ingestion on marine wildlife is difficult, but key to understanding the ontogeny and population dynamics of affected species. We developed a method that overcomes the difficulties by modelling individual ontogeny under reduced energy intake and expenditure caused by debris ingestion. The predicted ontogeny is combined with a population dynamics model to identify ecological breakpoints: cessation of reproduction or negative population growth. Exemplifying this approach on loggerhead turtles, we find that between 3% and 25% of plastics in digestive contents causes a 2.5–20% reduction in perceived food abundance and total available energy, resulting in a 10–15% lower condition index and 10% to 88% lower total seasonal reproductive output compared to unaffected turtles. The reported plastics ingestion is insufficient to impede sexual maturation, but population declines are possible. The method is readily applicable to other species impacted by debris ingestion.     

Towards the integration of animal‐borne instruments into global ocean observing systems

Marine animals are increasingly instrumented with environmental sensors that provide large volumes of oceanographic data. Here, we conduct an innovative and comprehensive global analysis to determine the potential contribution of animal‐borne instruments (ABI) into ocean observing systems (OOSs) and provide a foundation to establish future integrated ocean monitoring programmes. We analyse the current gaps of the long‐term Argo observing system (>1.5 million profiles) and assess its spatial overlap with the distribution of marine animals across eight major species groups (tuna and billfishes, sharks and rays, marine turtles, pinnipeds, cetaceans, sirenians, flying seabirds and penguins). We combine distribution ranges of 183 species and satellite tracking observations from >3,000 animals. Our analyses identify potential areas where ABI could complement OOS. Specifically, ABI have the potential to fill gaps in marginal seas, upwelling areas, the upper 10 m of the water column, shelf regions and polewards of 60° latitude. Our approach provides the global baseline required to plan the integration of ABI into global and regional OOS while integrating conservation and ocean monitoring priorities.     

Reconstructing paternal genotypes to infer patterns of sperm storage and sexual selection in the hawksbill turtle

Postcopulatory sperm storage can serve a range of functions, including ensuring fertility, allowing delayed fertilization and facilitating sexual selection. Sperm storage is likely to be particularly important in wide‐ranging animals with low population densities, but its prevalence and importance in such taxa, and its role in promoting sexual selection, are poorly known. Here, we use a powerful microsatellite array and paternal genotype reconstruction to assess the prevalence of sperm storage and test sexual selection hypotheses of genetic biases to paternity in one such species, the critically endangered hawksbill turtle, Eretmochelys imbricata. In the majority of females (90.7%, N = 43), all offspring were sired by a single male. In the few cases of multiple paternity (9.3%), two males fertilized each female. Importantly, the identity and proportional fertilization success of males were consistent across all sequential nests laid by individual females over the breeding season (up to five nests over 75 days). No males were identified as having fertilized more than one female, suggesting that a large number of males are available to females. No evidence for biases to paternity based on heterozygosity or relatedness was found. These results indicate that female hawksbill turtles are predominantly monogamous within a season, store sperm for the duration of the nesting season and do not re‐mate between nests. Furthermore, females do not appear to be using sperm storage to facilitate sexual selection. Consequently, the primary value of storing sperm in marine turtles may be to uncouple mating and fertilization in time and avoid costly re‐mating.     

New taxa described in Zoology in the Middle East

Abstract

The region between Mersin and ?skenderun was selected for studying marine turtles in the Turkish waters of the Mediterranean sea, as the most important nesting grounds of Green Turtles (Chelonia mydas) in the Mediterranean are situated there. In the 1995–96 fishing season, the 5 trawl boats taking part in the project reported that nets in the Eastern Mediterranean trapped 160 Green Turtles and 26 Loggerhead Turtles (Caretta caretta). In the following trawling season (1996/97), 306 Green Turtles, 116 Loggerhead Turtles (Caretta caretta) and 437 Nile Soft-shelled Turtles (Trionyx triunguis) were found to be trapped as a by-catch in the trawling nets. 87% of these turtles were captured by mid-trawling nets, the rest by bottom-trawling nets, mostly at depths of 11–30 m. 95% of all turtles were caught alive and healthy, and were usually released back into the sea immediately after capture by the fishermen. Training measures were given to local fishermen in order to raise their awareness of the threats to marine turtles.     

Natal homing in juvenile loggerhead turtles (Caretta caretta)

Juvenile loggerhead turtles (Caretta caretta) from West Atlantic nesting beaches occupy oceanic (pelagic) habitats in the eastern Atlantic and Mediterranean, whereas larger juvenile turtles occupy shallow (neritic) habitats along the continental coastline of North America. Hence the switch from oceanic to neritic stage can involve a trans-oceanic migration. Several researchers have suggested that at the end of the oceanic phase, juveniles are homing to feeding habitats in the vicinity of their natal rookery. To test the hypothesis of juvenile homing behaviour, we surveyed 10 juvenile feeding zones across the eastern USA with mitochondrial DNA control region sequences (N = 1437) and compared these samples to potential source (nesting) populations in the Atlantic Ocean and Mediterranean Sea (N = 465). The results indicated a shallow, but significant, population structure of neritic juveniles (PhiST = 0.0088, P = 0.016), and haplotype frequency differences were significantly correlated between coastal feeding populations and adjacent nesting populations (Mantel test R2 = 0.52, P = 0.001). Mixed stock analyses (using a Bayesian algorithm) indicated that juveniles occurred at elevated frequency in the vicinity of their natal rookery. Hence, all lines of evidence supported the hypothesis of juvenile homing in loggerhead turtles. While not as precise as the homing of breeding adults, this behaviour nonetheless places juvenile turtles in the vicinity of their natal nesting colonies. Some of the coastal hazards that affect declining nesting populations may also affect the next generation of turtles feeding in nearby habitats.     

Population genetics and phylogeography of sea turtles

The seven species of sea turtles occupy a diversity of niches, and have a history tracing back over 100 million years, yet all share basic life-history features, including exceptional navigation skills and periodic migrations from feeding to breeding habitats. Here, we review the biogeographic, behavioural, and ecological factors that shape the distribution of genetic diversity in sea turtles. Natal homing, wherein turtles return to their region of origin for mating and nesting, has been demonstrated with mtDNA sequences. These maternally inherited markers show strong population structure among nesting colonies while nuclear loci reveal a contrasting pattern of male-mediated gene flow, a phenomenon termed 'complex population structure'. Mixed-stock analyses indicate that multiple nesting colonies can contribute to feeding aggregates, such that exploitation of turtles in these habitats can reduce breeding populations across the region. The mtDNA data also demonstrate migrations across entire ocean basins, some of the longest movements of marine vertebrates. Multiple paternity occurs at reported rates of 0-100%, and can vary by as much as 9-100% within species. Hybridization in almost every combination among members of the Cheloniidae has been documented but the frequency and ultimate ramifications of hybridization are not clear. The global phylogeography of sea turtles reveals a gradient based on habitat preference and thermal regime. The cold-tolerant leatherback turtle (Dermochelys coriacea) shows no evolutionary partitions between Indo-Pacific and Atlantic populations, while the tropical green (Chelonia mydas), hawksbill (Eretmochelys imbricata), and ridleys (Lepidochelys olivacea vs. L. kempi) have ancient separations between oceans. Ridleys and loggerhead (Caretta caretta) also show more recent colonization between ocean basins, probably mediated by warm-water gyres that occasionally traverse the frigid upwelling zone in southern Africa. These rare events may be sufficient to prevent allopatric speciation under contemporary geographic and climatic conditions. Genetic studies have advanced our understanding of marine turtle biology and evolution, but significant gaps persist and provide challenges for the next generation of sea turtle geneticists.     

Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea

Hawksbill turtles (Eretmochelys imbricata) migrate between nesting beaches and feeding habitats that are often associated with tropical reefs, but it is uncertain which nesting colonies supply which feeding habitats. To address this gap in hawksbill biology, we compile previously published and new mitochondrial DNA (mtDNA) haplotype data for 10 nesting colonies (N = 347) in the western Atlantic and compare these profiles to four feeding populations and four previously published feeding samples (N = 626). Nesting colonies differ significantly in mtDNA haplotype frequencies (Phi(ST) = 0.588, P < 0.001), corroborating earlier conclusions of nesting site fidelity and setting the stage for mixed-stock analysis. Feeding aggregations show lower but significant structure (Phi(ST) = 0.089, P < 0.001), indicating that foraging populations are not homogenous across the Caribbean Sea. Bayesian mixed-stock estimates of the origins of juveniles in foraging areas show a highly significant, but shallow, correlation with nesting population size (r = 0.378, P = 0.004), supporting the premise that larger rookeries contribute more juveniles to feeding areas. A significant correlation between the estimated contribution and geographical distance from nesting areas (r = -0.394, P = 0.003) demonstrates the influence of proximity on recruitment to feeding areas. The influence of oceanic currents is illustrated by pelagic stage juveniles stranded in Texas, which are assigned primarily (93%) to the upstream rookery in Yucatan. One juvenile had a haplotype previously identified only in the eastern Atlantic, invoking rare trans-oceanic migrations. The mixed-stock analysis demonstrates that harvests in feeding habitats will impact nesting colonies throughout the region, with the greatest detriment to nearby nesting populations.