A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell

A new, thin-shelled fossil from the Upper Triassic (Revueltian: Norian) Chinle Group of New Mexico, Chinlechelys tenertesta, is one of the most primitive known unambiguous members of the turtle stem lineage. The thin-shelled nature of the new turtle combined with its likely terrestrial habitat preference hint at taphonomic filters that basal turtles had to overcome before entering the fossil record. Chinlechelys tenertesta possesses neck spines formed by multiple osteoderms, indicating that the earliest known turtles were covered with rows of dermal armour. More importantly, the primitive, vertically oriented dorsal ribs of the new turtle are only poorly associated with the overlying costal bones, indicating that these two structures are independent ossifications in basal turtles. These novel observations lend support to the hypothesis that the turtle shell was originally a complex composite in which dermal armour fused with the endoskeletal ribs and vertebrae of an ancestral lineage instead of forming de novo. The critical shell elements (i.e. costals and neurals) are thus not simple outgrowths of the bone of the endoskeletal elements as has been hypothesized from some embryological observations.     

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.     

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

The turtle shell and the relationship of the shoulder girdle inside or ‘deep’ to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.     

Caught in the act: the first record of copulating fossil vertebrates

The behaviour of fossil organisms can typically be inferred only indirectly, but rare fossil finds can provide surprising insights. Here, we report from the Eocene Messel Pit Fossil Site between Darmstadt and Frankfurt, Germany numerous pairs of the fossil carettochelyid turtle Allaeochelys crassesculpta that represent for the first time among fossil vertebrates couples that perished during copulation. Females of this taxon can be distinguished from males by their relatively shorter tails and development of plastral kinesis. The preservation of mating pairs has important taphonomic implications for the Messel Pit Fossil Site, as it is unlikely that the turtles would mate in poisonous surface waters. Instead, the turtles initiated copulation in habitable surface waters, but perished when their skin absorbed poisons while sinking into toxic layers. The mating pairs from Messel are therefore more consistent with a stratified, volcanic maar lake with inhabitable surface waters and a deadly abyss.     

Natural beaches confer fitness benefits to nesting marine turtles

Coastal ecosystems provide vital linkages between aquatic and terrestrial habitats and thus support extremely high levels of biodiversity. However, coastlines also contain the highest densities of human development anywhere on the planet and are favoured destinations for tourists, creating a situation where the potential for negative effects on coastal species is extremely high. I gathered data on marine turtle reproductive output from the literature to determine whether coastal development negatively influences offspring production. Female loggerhead (Caretta caretta) and green turtles (Chelonia mydas) nesting on natural beaches (as opposed to beaches with permanent development) produce significantly more hatchling turtles per nest; all else being equal, females that successfully produce more offspring will have higher fitness than conspecifics producing fewer offspring. Thus, female marine turtles nesting on natural beaches probably have higher fitness than turtles nesting on developed beaches. Consequently, populations nesting on natural beaches may be able to recover more quickly from the historic population declines that have plagued marine turtles, and some species may recover more quickly than others.     

A new, nearly complete stem turtle from the Jurassic of South America with implications for turtle evolution

Turtles have been known since the Upper Triassic (210Myr old); however, fossils recording the first steps of turtle evolution are scarce and often fragmentary. As a consequence, one of the main questions is whether living turtles (Testudines) originated during the Late Triassic (210Myr old) or during the Middle to Late Jurassic (ca 160Myr old). The discovery of the new fossil turtle, Condorchelys antiqua gen. et sp. nov. from the Middle to Upper Jurassic (ca 160-146Myr old) of South America (Patagonia, Argentina), presented here sheds new light on early turtle evolution. An updated cladistic analysis of turtles shows that C. antiqua and other fossil turtles are not crown turtles, but stem turtles. This cladistic analysis also shows that stem turtles were more diverse than previously thought, and that until the Middle to Upper Jurassic there were turtles without the modern jaw closure mechanism.     

First fossil gravid turtle provides insight into the evolution of reproductive traits in turtles

Here we report on the first discovery of shelled eggs inside the body cavity of a fossil turtle and on an isolated egg clutch, both referable to the Cretaceous turtle Adocus. These discoveries provide a unique opportunity to gain insight into the reproductive traits of an extinct turtle and to understand the evolution of such traits among living turtles. The gravid adult and egg clutch indicate that Adocus laid large clutches of rigid-shelled spherical eggs and established their nests near rivers, traits that are shared by its closest living relatives, the soft-shelled turtles. Adocus eggshell, however, was probably more rigid than that of living turtles, based on its great thickness and structure, features that may represent unique adaptations to intense predation or to arid nest environments. In light of the reproductive traits observed in Adocus, the distribution of reproductive traits among turtles reveals that large clutches of rigid-shelled eggs are primitive for hidden-necked turtles (cryptodirans) and that spherical eggs may have evolved independently within this group.     

A new phylogenetic hypothesis of turtles with implications for the timing and number of evolutionary transitions to marine lifestyles in the group

Evolutionary transitions to marine habitats occurred frequently among Mesozoic reptiles. Only one such clade survives to the present: sea turtles (Chelonioidea). Other marine turtles originated during the Mesozoic, but uncertain affinities of key fossils have obscured the number of transitions to marine life, and the timing of the origin of marine adaptation in chelonioids. Phylogenetic studies support either a highly‐inclusive chelonioid total‐group including fossil marine clades from the Jurassic and Cretaceous (e.g. protostegids, thalassochelydians, sandownids) or a less inclusive chelonioid total‐group excluding those clades. Under this paradigm, these clades belong outside Cryptodira, and represent at least one additional evolutionary transition to marine life in turtles. We present a new phylogenetic hypothesis informed by high resolution computed tomographic data of living and fossil taxa. Besides a well‐supported Chelonioidea, which includes protostegids, we recover a previously unknown clade of stem‐group turtles, Angolachelonia, which includes the Late Jurassic thalassochelydians, and the Cretaceous–Palaeogene sandownids. Accounting for the Triassic Odontochelys, our results indicate three independent evolutionary transitions to marine life in non‐pleurodiran turtles (plus an additional two‐three in pleurodires). Among all independent origins of marine habits, a pelagic ecology only evolved once, among chelonioids. All turtle groups that independently invaded marine habitats in the Jurassic–Cretaceous (chelonioids, angolachelonians, bothremydid pleurodires) survived the Cretaceous–Palaeogene mass extinction event. This highlights extensive survival of marine turtles compared to other marine reptiles. Furthermore, deeply‐nested clades such as chelonioids are found by the middle Early Cretaceous, suggesting a rapid diversification of crown‐group turtles during the Early Cretaceous.     

Palaeoecology of triassic stem turtles sheds new light on turtle origins

Competing hypotheses of early turtle evolution contrast sharply in implying very different ecological settings-aquatic versus terrestrial-for the origin of turtles. We investigate the palaeoecology of extinct turtles by first demonstrating that the forelimbs of extant turtles faithfully reflect habitat preferences, with short-handed turtles being terrestrial and long-handed turtles being aquatic. We apply this metric to the two successive outgroups to all living turtles with forelimbs preserved, Proganochelys quenstedti and Palaeochersis talampayensis, to discover that these earliest turtle outgroups were decidedly terrestrial. We then plot the observed distribution of aquatic versus terrestrial habits among living turtles onto their hypothesized phylogenies. Both lines of evidence indicate that although the common ancestor of all living turtles was aquatic, the earliest turtles clearly lived in a terrestrial environment. Additional anatomical and sedimentological evidence favours these conclusions. The freshwater aquatic habitat preference so characteristic of living turtles cannot, consequently, be taken as positive evidence for an aquatic origin of turtles, but must rather be considered a convergence relative to other aquatic amniotes, including the marine sauropterygians to which turtles have sometimes been allied.     

Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

Incubation temperature affects developmental rates and defines many phenotypes and fitness characteristics of reptilian embryos. In turtles, eggs are deposited in layers within the nest, such that thermal gradients create independent developmental conditions for each egg. Despite differences in developmental rate, several studies have revealed unexpected synchronicity in hatching, however, the mechanisms through which synchrony are achieved may be different between species. Here, we examine the phenomenon of synchronous hatching in turtles by assessing proximate mechanisms in an Australian freshwater turtle (Emydura macquarii). We tested whether embryos hatch prematurely or developmentally compensate in response to more advanced embryos in a clutch. We established developmental asynchrony within a clutch of turtle eggs and assessed both metabolic and heart rates throughout incubation in constant and fluctuating temperatures. Turtles appeared to hatch at similar developmental stages, with less-developed embryos in experimental groups responding to the presence of more developed eggs in a clutch by increasing both metabolic and heart rates. Early hatching did not appear to reduce neuromuscular ability at hatching. These results support developmental adjustment mechanisms of the 'catch-up hypothesis' for synchronous hatching in E. macquarii and implies some level of embryo-embryo communication. The group environment of a nest strongly supports the development of adaptive communication mechanisms between siblings and the evolution of environmentally cued hatching.     

First satellite tracks of neonate sea turtles redefine the ‘lost years’ oceanic niche

Few at-sea behavioural data exist for oceanic-stage neonate sea turtles, a life-stage commonly referred to as the sea turtle ‘lost years’. Historically, the long-term tracking of small, fast-growing organisms in the open ocean was logistically or technologically impossible. Here, we provide the first long-term satellite tracks of neonate sea turtles. Loggerheads (Caretta caretta) were remotely tracked in the Atlantic Ocean using small solar-powered satellite transmitters. We show that oceanic-stage turtles (i) rarely travel in Continental Shelf waters, (ii) frequently depart the currents associated with the North Atlantic Subtropical Gyre, (iii) travel quickly when in Gyre currents, and (iv) select sea surface habitats that are likely to provide a thermal benefit or refuge to young sea turtles, supporting growth, foraging and survival. Our satellite tracks help define Atlantic loggerhead nursery grounds and early loggerhead habitat use, allowing us to re-examine sea turtle ‘lost years’ paradigms.     

Biomechanics on the half shell: functional performance influences patterns of morphological variation in the emydid turtle carapace

This study uses the carapace of emydid turtles to address hypothesized differences between terrestrial and aquatic species. Geometric morphometrics are used to quantify shell shape, and performance is estimated for two shell functions: shell strength and hydrodynamics. Aquatic turtle shells differ in shape from terrestrial turtle shells and are characterized by lower frontal areas and presumably lower drag. Terrestrial turtle shells are stronger than those of aquatic turtles; many-to-one mapping of morphology to function does not entirely mitigate a functional trade-off between mechanical strength and hydrodynamic performance. Furthermore, areas of morphospace characterized by exceptionally poor performance in either of the functions are not occupied by any emydid species. Though aquatic and terrestrial species show no significant differences in the rate of morphological evolution, aquatic species show a higher lineage density, indicative of a greater amount of convergence in their evolutionary history. The techniques employed in this study, including the modeling of theoretical shapes to assess performance in unoccupied areas of morphospace, suggest a framework for future studies of morphological variation.     

Limb-size proportions in Australopithecus afarensis and Australopithecus africanus

Previous analyses have suggested that Australopithecus africanus possessed more apelike limb proportions than Australopithecus afarensis. However, due to the errors involved in estimating limb length and body size, support for this conclusion has been limited. In this study, we use a new Monte Carlo method to (1) test the hypothesis that A. africanus had greater upper:lower limb-size proportions than A. afarensis and (2) assess the statistical significance of interspecific differences among these taxa, extant apes, and humans. Our Monte Carlo method imposes sampling constraints that reduce extant ape and human postcranial measurements to sample sizes comparable to the fossil samples. Next, composite ratios of fore- and hindlimb geometric means are calculated for resampled measurements from the fossils and comparative taxa. Mean composite ratios are statistically indistinguishable (alpha=0.05) from the actual ratios of extant individuals, indicating that this method conserves each sample's central tendency. When applied to the fossil samples, upper:lower limb-size proportions in A. afarensis are similar to those of humans (p=0.878) and are significantly different from all great ape proportions (p< or =0.034), while Australopithecus africanus is more similar to the apes (p> or =0.180) and significantly different from humans and A. afarensis (p< or =0.031). These results strongly support the hypothesis that A. africanus possessed more apelike limb-size proportions than A. afarensis, suggesting that A. africanus either evolved from a more postcranially primitive ancestor than A. afarensis or that the more apelike limb-size proportions of A. africanus were secondarily derived from an A. afarensis-like ancestor. Among the extant taxa, limb-size proportions correspond with observed levels of forelimb- and hindlimb-dominated positional behaviors. In conjunction with detailed anatomical features linked to arboreality, these results suggest that arboreal posture and locomotion may have been more important components of the A. africanus behavioral repertoire relative to that of A. afarensis.     

DNA barcoding of Brazilian sea turtles (Testudines)

Five out of the seven recognized species of sea turtles (Testudines) occur on the Brazilian coast. The Barcode Initiative is an effort to undertake a molecular inventory of Earth biodiversity. Cytochrome Oxidase c subunit I (COI) molecular tags for sea turtle species have not yet been described. In this study, COI sequences for the five species of sea turtles that occur in Brazil were generated. These presented widely divergent haplotypes. All observed values were on the same range as those already described for other animal groups: the overall mean distance was 8.2%, the mean distance between families (Dermochelyidae and Cheloniidae) 11.7%, the mean intraspecific divergence 0.34%, and the mean distance within Cheloniidae 6.4%, this being 19-fold higher than the mean divergence observed within species. We obtained species-specific COI barcode tags that can be used for identifying each of the marine turtle species studied.     

The origin of the turtle body plan: evidence from fossils and embryos

The origin of the unique body plan of turtles has long been one of the most intriguing mysteries in evolutionary morphology. Discoveries of several new stem-turtles, together with insights from recent studies on the development of the shell in extant turtles, have provided crucial new information concerning this subject. It is now possible to develop a comprehensive scenario for the sequence of evolutionary changes leading to the formation of the turtle body plan within a phylogenetic framework and evaluate it in light of the ontogenetic development of the shell in extant turtles. The fossil record demonstrates that the evolution of the turtle shell took place over millions of years and involved a number of steps.     

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.     

Morphogenetic and constructional differences of the carapace of aquatic and terrestrial turtles and their evolutionary significance

The postembryonic development of the turtle carapace was studied in the aquatic Еmys orbicularis and the terrestrial Тestudo graeca. Differences in the structure of the bony shell in aquatic and terrestrial turtles were shown to be associated with varying degrees of development of epidermal derivatives, namely, the thickness of the scutes and the depth of horny furrows. Sinking of the horny furrows into the dermis causes local changes in the structure of the collagen matrix, which might precondition the acceleration of the ossification. Aquatic turtles possess a relatively thin horny cover, whose derivatives are either weakly developed or altogether absent and thus make no noticeable impact on the growth dynamics of bony plates. Carapace plates of these turtles outgrow more or less evenly around the periphery, which results in uniform costals, relatively narrow and partly reduced neurals, and broad peripherals extending beyond the marginal scutes. In terrestrial turtles (Testudinidae), horny structures are much more developed and exert a considerable impact on the growth of bony elements. As a result, bony plates outgrow unevenly in the dermis, expanding fast in the zones under the horny furrows and slowly outside these zones. This determines the basic features of the testudinid carapace: alternately cuneate shape of costals, an alternation of broad octagonal and narrow tetragonal neurals, and the limitation of the growth of peripherals by pleuro-marginal furrows. The evolutionary significance of morphogenetic and constructional differences in the turtle carapace, and the association of these differences with the turtle habitats are discussed.