Timing of organogenesis support basal position of turtles in the amniote tree of life

Background  

The phylogenetic position of turtles is the most disputed aspect in the reconstruction of the land vertebrate tree of life. This controversy has arisen after many different kinds and revisions of investigations of molecular and morphological data. Three main hypotheses of living sister-groups of turtles have resulted from them: all reptiles, crocodiles + birds or squamates + tuatara. Although embryology has played a major role in morphological studies of vertebrate phylogeny, data on developmental timing have never been examined to explore and test the alternative phylogenetic hypotheses. We conducted a comprehensive study of published and new embryological data comprising 15 turtle and eight tetrapod species belonging to other taxa, integrating for the first time data on the side-necked turtle clade.     

Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle <Emphasis Type="Italic">Myuchelys bellii</Emphasis> of eastern Australia

Freshwater turtles have an extraordinary physiological ability to endure dive times that can range from days to months using aquatic respiration. In cryptodires (e.g., white-lipped mud turtle Kinosternon leucostomum) aquatic respiration is via buccal or cutaneous routes whereas in pleurodires (e.g., Fitzroy River turtle Rheodytes leukops), it is achieved primarily via specialized cloacal bursae. This study records the voluntary diving performance of the western sawshelled turtle Myuchelys bellii in Bald Rock Creek from the temperate zone of the Murray–Darling Basin of Australia. Myuchelys bellii has a moderately specialized cloacal bursae morphology compared to other pleurodiran turtles and displays impressive dive durations spanning more than 15 days during the winter months. This is attributed to its ability to maintain aerobic dives via its cloacal bursae and low water temperatures in winter. Myuchelys bellii seasonal and diel diving performance, including its crepuscular habit, is comparable to R. leukops and Elseya albagula. This study also recorded the first aquatic hibernation at depth (>3 m) for any freshwater turtle; and only the second pleurodire to demonstrate aquatic hibernation as an overwintering strategy. Observed thermoregulation behavior in M. bellii is believed to provide multiple life history benefits.     

The leaf turtle population of Phnom Kulen National Park (northwestern Cambodia) has genetic and morphological signatures of hybridization

Cambodia is known to harbour three distinct species of Southeast Asian leaf turtles (Cyclemys spp.), which are heavily traded and common in seizures of wildlife. Confiscated leaf turtles are often released to natural habitats. Thus, an exact knowledge of the distribution of the individual species is of great importance to avoid the introduction of non‐native turtles, posing the risk of competition and hybridization. In this study, we examine a recently discovered leaf turtle population from Phnom Kulen National Park using external morphology, 17 unlinked microsatellite loci and the mitochondrial cytochrome b gene. Leaf turtles from the Phnom Kulen National Park morphologically resemble C. oldhamii, but harbour mitochondrial haplotypes of C. atripons. With respect to microsatellite loci, the turtles are distinct from C. atripons. Unfortunately no material of C. oldhamii was available from Cambodia. We propose that the Phnom Kulen population represents either a natural hybrid swarm of C. atripons and C. oldhamii or a distinct undescribed species with introgressed mitochondria of C. atripons. This underlines that genetic differentiation of wild leaf turtle populations in Cambodia is complex and suggests that this differentiation pattern becomes increasingly threatened by translocations of confiscated individuals. For drawing a definite conclusion about the taxonomic status of the Phnom Kulen population, denser sampling of other Cambodian leaf turtle populations would be required, in particular of C. oldhamii.     

Distinct patterns of mitochondrial genome diversity in bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) and humans

Background  

We have analyzed the complete mitochondrial genomes of 22 Pan paniscus (bonobo, pygmy chimpanzee) individuals to assess the detailed mitochondrial DNA (mtDNA) phylogeny of this close relative of Homo sapiens.     

The western painted turtle genome,a model for the evolution of extreme physiological adaptations in a slowly evolving lineage

Background

We describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species'' physiological capacities to withstand extreme anoxia and tissue freezing.

Results

Our phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented.

Conclusions

Our comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle''s extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.     

Evidence of olive ridley mitochondrial genome introgression into loggerhead turtle rookeries of Sergipe, Brazil

The coastline of Sergipe state hosts the main Brazilian nesting sites of Lepidochelys olivacea (Eschscholtz, 1829). The second most abundant species of turtles in Sergipe is Caretta caretta (Linnaeus, 1758). Both sea turtle species, respectively known as olive ridley and loggerhead, are currently listed as endangered by the International Union for the Conservation of Nature and Natural Resources. The genetic diversity of the Sergipe loggerhead population (N = 51) was assayed by analyzing 627 bp from the control region of mitochondrial DNA in nesting females. Three haplotypes were identified: CC-A4, CC-A24 and CC × LO. The last one was recorded for specimens considered hybrids because they represent L. olivacea’s mtDNA, but had the external morphology of C. caretta or of a mixture of both species. Based on the two types of hybrids, it was hypothesized that at least two hybridization events had occurred: a more ancient hybridization event, accompanied by introgression (F2 or later backcrosses), and a recent one (F1), both of which involving the same L. olivacea haplotype. The incidence of L. olivacea mitochondrial genome introgression into the C. caretta rookeries was only observed in Sergipe, which could be related to the large numbers of L. olivacea in this region and an overlap of reproduction periods and distribution areas of both species. This may also be associated to global warming since it might alter the sex ratio of sea turtles, thus facilitating interspecific mating. Awareness of gene flow between these species will significantly influence the development and implementation of adequate management strategies.     

The cranial morphology of Kayentachelys,an Early Jurassic cryptodire,and the early history of turtles

Gaffney, E.S. and Jenkins, F.A., Jr. 2010. The cranial morphology of Kayentachelys, an Early Jurassic cryptodire, and the early history of turtles. — Acta Zoologica (Stockholm) 91 : 335–368 The skull morphology of Kayentachelys aprix Gaffney et al., 1987 , a turtle from the Early Jurassic Kayenta Fm of northern Arizona, demonstrates the presence of cryptodiran synapomorphies in agreement with Gaffney et al. (1987, 1991, 2007) , and contrary to the conclusions of Sterli and Joyce (2007) , Joyce (2007) , Sterli (2008) , and Anquetin et al. (2008) . Specific characters found in Kayentachelys and diagnostic of cryptodires include the processus trochlearis oticum, the curved processus pterygoideus externus with a vertical plate, and the prefrontal–vomer contact, which are confirmed as absent in the outgroups, specifically the Late Triassic Proganochelys. The Joyce (2007) analysis suffers from the reduction of the signal from skull characters, with a consequently greater reliance on shell characters, resulting in pleurodires being resolved at various positions within the cryptodires. Kayentachelys reveals what a primitive cryptodire would be expected to look like: a combination of primitive and derived characters, with the fewer derived characters providing the best test of its relationships to other turtles. Although incompletely known, the Mid‐Late Jurassic Condorchelys, Heckeremys, and Eileanchelys may be early cryptodires close to Kayentachelys. We confirm the Late Triassic Proterochersis as a pleurodire, dating the pleurodire–cryptodire split as Late Triassic or earlier.     

Turtle origins: insights from phylogenetic retrofitting and molecular scaffolds

Adding new taxa to morphological phylogenetic analyses without substantially revising the set of included characters is a common practice, with drawbacks (undersampling of relevant characters) and potential benefits (character selection is not biased by preconceptions over the affinities of the ‘retrofitted’ taxon). Retrofitting turtles (Testudines) and other taxa to recent reptile phylogenies consistently places turtles with anapsid‐grade parareptiles (especially Eunotosaurus and/or pareiasauromorphs), under both Bayesian and parsimony analyses. This morphological evidence for turtle–parareptile affinities appears to contradict the robust genomic evidence that extant (living) turtles are nested within diapsids as sister to extant archosaurs (birds and crocodilians). However, the morphological data are almost equally consistent with a turtle–archosaur clade: enforcing this molecular scaffold onto the morphological data does not greatly increase tree length (parsimony) or reduce likelihood (Bayesian inference). Moreover, under certain analytic conditions, Eunotosaurus groups with turtles and thus also falls within the turtle–archosaur clade. This result raises the possibility that turtles could simultaneously be most closely related to a taxon traditionally considered a parareptile (Eunotosaurus) and still have archosaurs as their closest extant sister group.     

Distribution of mitochondrial haplotypes (cytb) in Polish populations of Emys orbicularis (L., 1758)

The European pond turtle, Emys orbicularis, inhabits a wide distribution area in the western Palaearctic. Polish populations of pond turtle represent the nominotypical subspecies Emys orbicularis orbicularis. The mitochondrial DNA haplotype (cytb gene) variation among 131 turtles from 26 locations in five regions of Poland was investigated. Five haplotypes belonging to three distinct lineages were identified. Two clades (I and II) were represented by two haplotypes each, while the other clade (IV) was represented by one haplotype. Three haplotypes were reported for the first time in E. orbicularis. The eastern part of Poland is inhabited exclusively by turtles bearing haplotype Ia. The remaining four sequence variants were recorded in western Poland where only the IIb haplotype is considered endemic. The distribution of the other haplotypes in western Poland could thus reflect past introductions or accidental releases. The authors regarded the two locations (Drzeczkowo and Karpicko) that were first included in the western Poland populations as autochthonous catchment areas of haplotype Ia.     

Relationship between tropical cyclones and the distribution of sea turtle nesting grounds

Aim This study examines the relationship between the distribution of existing sea turtle nesting sites and historical patterns of tropical cyclone events to investigate whether cyclones influence the current distribution of sea turtle nesting sites. The results, together with information on predicted cyclone activity and other key environmental variables, will help in the identification and prediction of future nesting sites for sea turtles as changes to the coastal environment continue. Location Queensland, Australia. Methods We used data on the nesting distribution of seven populations of four species of sea turtles [green (Chelonia mydas), flatback (Natator depressus), hawksbill (Eretmochelys imbricata) and loggerhead (Caretta caretta)] from the eastern Queensland coast, and tropical cyclone track data from 1969 to 2007 to explore the relationship between (1) sea turtle nesting phenology and cyclone season, and (2) sea turtle nesting sites and cyclone distribution. Furthermore, using two green turtle populations as a case study, we investigated the relationship between cyclone disturbance and sea turtle reproductive output, nesting site and season. Bootstrapping was used to explore if current sea turtle nesting sites are located in areas with lower or higher cyclone frequency than areas where turtles are currently not nesting. Results All populations of sea turtles studied here were disturbed by cyclone activity during the study period. The exposure (frequency) of tropical cyclones that crossed each nesting site varied greatly among and within the various sea turtle populations. This was mainly a result of the spatial distribution of each population’s nesting sites. Bootstrapping indicated that nesting sites generally have experienced lower cyclone activity than other areas that are available for nesting. Main conclusions Tropical cyclones might have been sufficiently detrimental to sea turtle hatching success on the eastern Queensland coast that through a natural selection process turtles in this region are now nesting in areas with lower cyclone activity. Therefore, it is important that future studies that predict climate or range shifts for sea turtle nesting distributions consider future cyclone activity as one of the variables in their model.     

Atlantic leatherback migratory paths and temporary residence areas

Background

Sea turtles are long-distance migrants with considerable behavioural plasticity in terms of migratory patterns, habitat use and foraging sites within and among populations. However, for the most widely migrating turtle, the leatherback turtle Dermochelys coriacea, studies combining data from individuals of different populations are uncommon. Such studies are however critical to better understand intra- and inter-population variability and take it into account in the implementation of conservation strategies of this critically endangered species. Here, we investigated the movements and diving behaviour of 16 Atlantic leatherback turtles from three different nesting sites and one foraging site during their post-breeding migration to assess the potential determinants of intra- and inter-population variability in migratory patterns.

Methodology/Principal Findings

Using satellite-derived behavioural and oceanographic data, we show that turtles used Temporary Residence Areas (TRAs) distributed all around the Atlantic Ocean: 9 in the neritic domain and 13 in the oceanic domain. These TRAs did not share a common oceanographic determinant but on the contrary were associated with mesoscale surface oceanographic features of different types (i.e., altimetric features and/or surface chlorophyll a concentration). Conversely, turtles exhibited relatively similar horizontal and vertical behaviours when in TRAs (i.e., slow swimming velocity/sinuous path/shallow dives) suggesting foraging activity in these productive regions. Migratory paths and TRAs distribution showed interesting similarities with the trajectories of passive satellite-tracked drifters, suggesting that the general dispersion pattern of adults from the nesting sites may reflect the extent of passive dispersion initially experienced by hatchlings.

Conclusions/Significance

Intra- and inter-population behavioural variability may therefore be linked with initial hatchling drift scenarios and be highly influenced by environmental conditions. This high degree of behavioural plasticity in Atlantic leatherback turtles makes species-targeted conservation strategies challenging and stresses the need for a larger dataset (>100 individuals) for providing general recommendations in terms of conservation.     

The complete mitochondrial genome sequences of <Emphasis Type="Italic">Chelodina rugosa</Emphasis> and <Emphasis Type="Italic">Chelus fimbriata</Emphasis> (Pleurodira: Chelidae): implications of a common absence of initiation sites (O<Subscript>L</Subscript>) in pleurodiran turtles

Within the order Testudines, while phylogenetic analyses have been performed on the suborder Cryptodira with complete mitochondrial genomes (mitogenomes), mitogenomic information from another important suborder Pleurodira has been inadequate. In the present study, complete mitochondrial DNA (mtDNA) sequences of two chelid turtles Chelodina rugosa and Chelus fimbriata were firstly determined, the lengths of which were 16,582 and 16,661 bp respectively. As the typical vertebrate mitogenome, both mtDNAs consist of 13 protein coding genes, 2 ribosomal RNAs (rRNAs), 22 transfer RNAs (tRNAs), and a long noncoding region (control region, CR). However, the initiation sites for light-strand replication (O_L), which has been identified in all reported Cryptodire mitogenomes, were not found in the putative position of the two chelid turtles and African helmeted turtle Pelomedusa subrufa. The results suggested that the absence of mitogenomic initiation sites (O_L) could be a characteristic of Pleurodira. Phylogenetic relationships of chelid turtles and other turtles were reconstructed using the reported mitogenomes. Both maximum likelihood (ML) and Bayesian inference (BI) analyses suggested the monophyly of Pleurodira and Cryptodira as well as a sister group relationship between the two chelid turtles with strong statistical support. This phylogenetic framework was also utilized to estimate divergence dates among lineages using relaxed-clock methods combined with fossil evidence. Divergence estimates revealed that genus Chelodina diverged from genus Chelus in Late Cretaceous (~83 million years ago (mya)), and the time is consistent with the vicariance of the fragments which was caused by Gondwana split.     

Triassic turtle tracks and the origin of turtles

Turtle (Testudines) tracks, Chelonipus torquatus, reported from the early Middle Triassic (Anisian) of Germany, and Chelonipus isp. from the late Early Triassic (Spathian) of Wyoming and Utah, are the oldest fossil evidence of turtles, but have been omitted in recent discussions of turtle origins. These tracks provide significant clues as to how early the turtle Bauplan originated. Turtle trackways are quite distinctive: the manus and pes form tracks nearly parallel to the midline and indicate an unusually wide gait in which the trackway width is nearly equal to the stride length. These tracks do not fit what would be expected to be made by Triassic Pappochelys or Odontochelys, a supposed prototurtle and an early turtle, respectively. In contrast, these tracks are consistent with what would be expected from the Triassic turtles Proganochelys and Palaeochersis. The features inferred to be present in Triassic turtle tracks support the notion that Odontochelys is a derived aquatic branch of the turtle stem lineage rather than the ancestral state of all turtles. Chelonipus also resembles the Permian track Pachypes dolomiticus, generally assigned to a pareiasaur trackmaker. These revelations highlight the need to consider all available evidence regarding turtle origins, rather than just the body fossils.     

Establishing physiological blood parameters in the loggerhead sea turtle (Caretta caretta)

The loggerhead sea turtle (Caretta caretta), one of the three sea turtle species inhabiting the Mediterranean Sea, is an endangered species. However, although frequently treated in marine animal rescue centers, and the subject of several studies in literature, as yet, few studies have been conducted on large numbers of loggerhead sea turtles in order to establish physiological reference ranges that enable the identification of pathological values. The lack of studies on reference parameters probably depends on the fact that marine turtles treated in wildlife rescue centers are usually in a critical conditions, thus precluding the collection of data on healthy animals and compromising the reliability of any data obtained from them. The present biological study was therefore conducted in order to obtain a database from healthy animals in natural conditions. Serum biochemistry and serum protein electrophoresis were performed on blood samples obtained from 65 healthy adult loggerhead sea turtles captured and delivered to the Sea Turtle Rescue Center of Linosa (Italy); the blood samples were collected during the clinical examination of rescued animals. Laboratory analyses of serum samples were made in order to establish reference parameters, commonly required for laboratory diagnoses in mammals and diseased animals.

(Not) far from home: No sex bias in dispersal,but limited genetic patch size,in an endangered species,the Spotted Turtle (Clemmys guttata)

Sex-biased dispersal is common in many animals, with male-biased dispersal often found in studies of mammals and reptiles, including interpretations of spatial genetic structure, ostensibly as a result of male–male competition and a lack of male parental care. Few studies of sex-biased dispersal have been conducted in turtles, but a handful of studies, in saltwater turtles and in terrestrial turtles, have detected male-biased dispersal as expected. We tested for sex-biased dispersal in the endangered freshwater turtle, the spotted turtle (Clemmys guttata) by investigating fine-scale genetic spatial structure of males and females. We found significant spatial genetic structure in both sexes, but the patterns mimicked each other. Both males and females typically had higher than expected relatedness at distances <25 km, and in many distance classes greater than 25 km, less than expected relatedness. Similar patterns were apparent whether we used only loci in Hardy–Weinberg equilibrium (n = 7) or also included loci with potential null alleles (n = 5). We conclude that, contrary to expectations, sex-biased dispersal is not occurring in this species, possibly related to the reverse sexual dimorphism in this species, with females having brighter colors. We did, however, detect significant spatial genetic structure in males and females, separate and combined, showing philopatry within a genetic patch size of <25 km in C. guttata, which is concerning for an endangered species whose populations are often separated by distances greater than the genetic patch size.     

A Giant Chelonioid Turtle from the Late Cretaceous of Morocco with a Suction Feeding Apparatus Unique among Tetrapods

Background

Secondary adaptation to aquatic life occurred independently in several amniote lineages, including reptiles during the Mesozoic and mammals during the Cenozoic. These evolutionary shifts to aquatic environments imply major morphological modifications, especially of the feeding apparatus. Mesozoic (250–65 Myr) marine reptiles, such as ichthyosaurs, plesiosaurs, mosasaurid squamates, crocodiles, and turtles, exhibit a wide range of adaptations to aquatic feeding and a broad overlap of their tooth morphospaces with those of Cenozoic marine mammals. However, despite these multiple feeding behavior convergences, suction feeding, though being a common feeding strategy in aquatic vertebrates and in marine mammals in particular, has been extremely rarely reported for Mesozoic marine reptiles.

Principal Findings

A relative of fossil protostegid and dermochelyoid sea turtles, Ocepechelon bouyai gen. et sp. nov. is a new giant chelonioid from the Late Maastrichtian (67 Myr) of Morocco exhibiting remarkable adaptations to marine life (among others, very dorsally and posteriorly located nostrils). The 70-cm-long skull of Ocepechelon not only makes it one of the largest marine turtles ever described, but also deviates significantly from typical turtle cranial morphology. It shares unique convergences with both syngnathid fishes (unique long tubular bony snout ending in a rounded and anteriorly directed mouth) and beaked whales (large size and elongated edentulous jaws). This striking anatomy suggests extreme adaptation for suction feeding unmatched among known turtles.

Conclusion/Significance

The feeding apparatus of Ocepechelon, a bony pipette-like snout, is unique among tetrapods. This new taxon exemplifies the successful systematic and ecological diversification of chelonioid turtles during the Late Cretaceous. This new evidence for a unique trophic specialization in turtles, along with the abundant marine vertebrate faunas associated to Ocepechelon in the Late Maastrichtian phosphatic beds of Morocco, further supports the hypothesis that marine life was, at least locally, very diversified just prior to the Cretaceous/Palaeogene (K/Pg) biotic crisis.     

On Sea Turtle‐associated Craspedostauros (Bacillariophyta), with Description of Three Novel Species

The current study focuses on four species from the primarily marine diatom genus Craspedostauros that were observed growing attached to numerous sea turtles and sea turtle‐associated barnacles from Croatia and South Africa. Three of the examined taxa, C. danayanus sp. nov., C. legouvelloanus sp. nov., and C. macewanii sp. nov., are described based on morphological and, whenever possible, molecular characteristics. The new taxa exhibit characters not previously observed in other members of the genus, such as the presence of more than two rows of cribrate areolae on the girdle bands, shallow perforated septa, and a complete reduction of the stauros. The fourth species, C. alatus, itself recently described from museum sea turtle specimens, is reported for the first time from loggerhead sea turtles rescued in Europe. A 3‐gene phylogenetic analysis including DNA sequence data for three sea turtle‐associated Craspedostauros species and other marine and epizoic diatom taxa indicated that Craspedostauros is monophyletic and sister to Achnanthes. This study, being based on a large number of samples and animal specimens analyzed and using different preservation and processing methods, provides new insights into the ecology and biogeography of the genus and sheds light on the level of intimacy and permanency in the host–epibiont interaction within the epizoic Craspedostauros species.     

Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales

Background

Resolving threats to widely distributed marine megafauna requires definition of the geographic distributions of both the threats as well as the population unit(s) of interest. In turn, because individual threats can operate on varying spatial scales, their impacts can affect different segments of a population of the same species. Therefore, integration of multiple tools and techniques — including site-based monitoring, genetic analyses, mark-recapture studies and telemetry — can facilitate robust definitions of population segments at multiple biological and spatial scales to address different management and research challenges.

Methodology/Principal Findings

To address these issues for marine turtles, we collated all available studies on marine turtle biogeography, including nesting sites, population abundances and trends, population genetics, and satellite telemetry. We georeferenced this information to generate separate layers for nesting sites, genetic stocks, and core distributions of population segments of all marine turtle species. We then spatially integrated this information from fine- to coarse-spatial scales to develop nested envelope models, or Regional Management Units (RMUs), for marine turtles globally.

Conclusions/Significance

The RMU framework is a solution to the challenge of how to organize marine turtles into units of protection above the level of nesting populations, but below the level of species, within regional entities that might be on independent evolutionary trajectories. Among many potential applications, RMUs provide a framework for identifying data gaps, assessing high diversity areas for multiple species and genetic stocks, and evaluating conservation status of marine turtles. Furthermore, RMUs allow for identification of geographic barriers to gene flow, and can provide valuable guidance to marine spatial planning initiatives that integrate spatial distributions of protected species and human activities. In addition, the RMU framework — including maps and supporting metadata — will be an iterative, user-driven tool made publicly available in an online application for comments, improvements, download and analysis.     

Major genomic mitochondrial lineages delineate early human expansions

Background  

The phylogeographic distribution of human mitochondrial DNA variations allows a genetic approach to the study of modern Homo sapiens dispersals throughout the world from a female perspective. As a new contribution to this study we have phylogenetically analysed complete mitochondrial DNA(mtDNA) sequences from 42 human lineages, representing major clades with known geographic assignation.