Fossil insect eyes shed light on trilobite optics and the arthropod pigment screen.

Fossilized eyes permit inferences of the visual capacity of extinct arthropods1-3. However, structural and/or chemical modifications as a result of taphonomic and diagenetic processes can alter the original features, thereby necessitating comparisons with modern species. Here we report the detailed molecular composition and microanatomy of the eyes of 54-million-year-old crane-flies, which together provide a proxy for the interpretation of optical systems in some other ancient arthropods. These well-preserved visual organs comprise calcified corneal lenses that are separated by intervening spaces containing eumelanin pigment. We also show that eumelanin is present in the facet walls of living crane-flies, in which it forms the outermost ommatidial pigment shield in compound eyes incorporating a chitinous cornea. To our knowledge, this is the first record of melanic screening pigments in arthropods, and reveals a fossilization mode in insect eyes that involves a decay-resistant biochrome coupled with early diagenetic mineralization of the ommatidial lenses. The demonstrable secondary calcification of lens cuticle that was initially chitinous has implications for the proposed calcitic corneas of trilobites, which we posit are artefacts of preservation rather than a product of in vivo biomineralization4-7. Although trilobite eyes might have been partly mineralized for mechanical strength, a (more likely) organic composition would have enhanced function via gradient-index optics and increased control of lens shape.

Tooth morphology elucidates shark evolution across the end-Cretaceous mass extinction.

Sharks (Selachimorpha) are iconic marine predators that have survived multiple mass extinctions over geologic time. Their prolific fossil record is represented mainly by isolated shed teeth, which provide the basis for reconstructing deep time diversity changes affecting different selachimorph clades. By contrast, corresponding shifts in shark ecology, as measured through morphological disparity, have received comparatively limited analytical attention. Here, we use a geometric morphometric approach to comprehensively examine tooth morphologies in multiple shark lineages traversing the catastrophic end-Cretaceous mass extinction-this event terminated the Mesozoic Era 66 million years ago. Our results show that selachimorphs maintained virtually static levels of dental disparity in most of their constituent clades across the Cretaceous-Paleogene interval. Nevertheless, selective extinctions did impact apex predator species characterized by triangular blade-like teeth. This is particularly evident among lamniforms, which included the dominant Cretaceous anacoracids. Conversely, other groups, such as carcharhiniforms and orectolobiforms, experienced disparity modifications, while heterodontiforms, hexanchiforms, squaliforms, squatiniforms, and †synechodontiforms were not overtly affected. Finally, while some lamniform lineages disappeared, others underwent postextinction disparity increases, especially odontaspidids, which are typified by narrow-cusped teeth adapted for feeding on fishes. Notably, this increase coincides with the early Paleogene radiation of teleosts as a possible prey source, and the geographic relocation of disparity sampling "hotspots," perhaps indicating a regionally disjunct extinction recovery. Ultimately, our study reveals a complex morphological response to the end-Cretaceous mass extinction and highlights an event that influenced the evolution of modern sharks.

Soft-tissue evidence for homeothermy and crypsis in a Jurassic ichthyosaur.

Ichthyosaurs are extinct marine reptiles that display a notable external similarity to modern toothed whales. Here we show that this resemblance is more than skin deep. We apply a multidisciplinary experimental approach to characterize the cellular and molecular composition of integumental tissues in an exceptionally preserved specimen of the Early Jurassic ichthyosaur Stenopterygius. Our analyses recovered still-flexible remnants of the original scaleless skin, which comprises morphologically distinct epidermal and dermal layers. These are underlain by insulating blubber that would have augmented streamlining, buoyancy and homeothermy. Additionally, we identify endogenous proteinaceous and lipid constituents, together with keratinocytes and branched melanophores that contain eumelanin pigment. Distributional variation of melanophores across the body suggests countershading, possibly enhanced by physiological adjustments of colour to enable photoprotection, concealment and/or thermoregulation. Convergence of ichthyosaurs with extant marine amniotes thus extends to the ultrastructural and molecular levels, reflecting the omnipresent constraints of their shared adaptation to pelagic life.

Interpreting melanin-based coloration through deep time: a critical review.

Colour, derived primarily from melanin and/or carotenoid pigments, is integral to many aspects of behaviour in living vertebrates, including social signalling, sexual display and crypsis. Thus, identifying biochromes in extinct animals can shed light on the acquisition and evolution of these biological traits. Both eumelanin and melanin-containing cellular organelles (melanosomes) are preserved in fossils, but recognizing traces of ancient melanin-based coloration is fraught with interpretative ambiguity, especially when observations are based on morphological evidence alone. Assigning microbodies (or, more often reported, their 'mouldic impressions') as melanosome traces without adequately excluding a bacterial origin is also problematic because microbes are pervasive and intimately involved in organismal degradation. Additionally, some forms synthesize melanin. In this review, we survey both vertebrate and microbial melanization, and explore the conflicts influencing assessment of microbodies preserved in association with ancient animal soft tissues. We discuss the types of data used to interpret fossil melanosomes and evaluate whether these are sufficient for definitive diagnosis. Finally, we outline an integrated morphological and geochemical approach for detecting endogenous pigment remains and associated microstructures in multimillion-year-old fossils.

Oldest southern sauropterygian reveals early marine reptile globalization.

Sauropterygians were the stratigraphically longest-ranging clade of Mesozoic marine reptiles with a global fossil record spanning ∼180 million years1. However, their early evolution has only been known from what is now the Northern Hemisphere, extending across the northern and trans-equatorial western margins of the Tethys paleo-ocean1 after the late-Early Triassic (late Olenekian, ∼248.8 million years [Ma] ago2), and via possible trans-Arctic migration1 to the Eastern Panthalassa super-ocean prior to the earliest Middle Triassic (Olenekian-earliest Anisian3,4, ∼247 Ma). Here, we describe the geologically oldest sea-going reptile from the Southern Hemisphere - a nothosaur (basal sauropterygian5) from the Middle Triassic (Anisian, after ∼246 Ma6) of New Zealand. Time-scaled ancestral range estimations thus reveal an unexpected circum-Gondwanan high-paleolatitude (>60° S7) dispersal from a northern Tethyan origination center. This coincides with the adaptive diversification of sauropterygians after the end-Permian mass extinction8 and suggests that rapid globalization accompanied their initial radiation in the earliest Mesozoic.

The rise of macropredatory pliosaurids near the Early-Middle Jurassic transition.

The emergence of gigantic pliosaurid plesiosaurs reshaped the trophic structure of Mesozoic marine ecosystems, and established an ~ 80 million-year (Ma) dynasty of macropredatory marine reptiles. However, the timescale of their 'defining' trait evolution is incompletely understood because the fossil record of gigantic pliosaurids is scarce prior to the late-Middle Jurassic (Callovian), ~ 165.3 Ma. Here, we pinpoint the appearance of large body size and robust dentitions to early-Middle Jurassic (Bajocian) pliosaurids from northeastern France and Switzerland. These specimens include a new genus that sheds light on the nascent diversification of macropredatory pliosaurids occurring shortly after the Early-Middle Jurassic transition, around ~ 171 Ma. Furthermore, our multivariate assessment of dental character states shows that the first gigantic pliosaurids occupied different morphospace from coeval large-bodied rhomaleosaurid plesiosaurs, which were dominant in the Early Jurassic but declined during the mid-Jurassic, possibly facilitating the radiation and subsequent ecomorph acme of pliosaurids. Finally, we posit that while the emergence of macropredatory pliosaurids was apparently coordinated with regional faunal turnover in the epeiric basins of Europe, it paralleled a globally protracted extinction of other higher trophic-level marine reptiles that was not completed until after the earliest-Late Jurassic, ~ 161.5 Ma.

Earliest Triassic ichthyosaur fossils push back oceanic reptile origins.

Reptiles first radiated into oceanic environments after the cataclysmic end-Permian mass extinction (EPME)1, 251.9 million years (Ma) ago. The geologically oldest fossils evincing this adaptive transition have been recovered from upper-Lower Triassic (lower Spathian) strata, ∼248.8 Ma2, and postdate a landmark turnover of amphibian-dominated to reptile-dominated marine ecosystems spanning the late Smithian crisis (LSC)3, ∼249.6 Ma4 -less than ∼2.3 Ma after the EPME. Here, we report ichthyopterygian (the group including 'fish-shaped' ichthyosaurians1) remains from the Arctic island of Spitsbergen that predate the LSC in later-middle to early-late Smithian5 deposits up to ∼250 Ma. Unexpectedly, however, their large size and spongy internal bone structure indicate a fully pelagic ichthyopterygian1,6. Given this unambiguous occurrence ∼2 Ma after the EPME, these pioneering seagoing tetrapods can now be feasibly recast as mass extinction survivors instead of ecological successors2,3 within the earliest Mesozoic marine predator communities.

Mitogenome of the extinct Desert 'rat-kangaroo' times the adaptation to aridity in macropodoids.

The evolution of Australia's distinctive marsupial fauna has long been linked to the onset of continent-wide aridity. However, how this profound climate change event affected the diversification of extant lineages is still hotly debated. Here, we assemble a DNA sequence dataset of Macropodoidea-the clade comprising kangaroos and their relatives-that incorporates a complete mitogenome for the Desert 'rat-kangaroo', Caloprymnus campestris. This enigmatic species went extinct nearly 90 years ago and is known from a handful of museum specimens. Caloprymnus is significant because it was the only macropodoid restricted to extreme desert environments, and therefore calibrates the group's specialisation for increasingly arid conditions. Our robustly supported phylogenies nest Caloprymnus amongst the bettongs Aepyprymnus and Bettongia. Dated ancestral range estimations further reveal that the Caloprymnus-Bettongia lineage originated in nascent xeric settings during the middle to late Miocene, ~ 12 million years ago (Ma), but subsequently radiated into fragmenting mesic habitats after the Pliocene to mid-Pleistocene. This timeframe parallels the ancestral divergences of kangaroos in woodlands and forests, but predates their adaptive dispersal into proliferating dry shrublands and grasslands from the late Miocene to mid-Pleistocene, after ~ 7 Ma. We thus demonstrate that protracted changes in both climate and vegetation likely staged the emergence of modern arid zone macropodoids.

Feeding ecology has shaped the evolution of modern sharks.

Sharks are iconic predators in today's oceans, yet their modern diversity has ancient origins. In particular, present hypotheses suggest that a combination of mass extinction, global climate change, and competition has regulated the community structure of dominant mackerel (Lamniformes) and ground (Carcharhiniformes) sharks over the last 66 million years. However, while these scenarios advocate an interplay of major abiotic and biotic events, the precise drivers remain obscure. Here, we focus on the role of feeding ecology using a geometric morphometric analysis of 3,837 fossil and extant shark teeth. Our results reveal that morphological segregation rather than competition has characterized lamniform and carcharhiniform evolution. Moreover, although lamniforms suffered a long-term disparity decline potentially linked to dietary "specialization," their recent disparity rivals that of "generalist" carcharhiniforms. We further confirm that low eustatic sea levels impacted lamniform disparity across the end-Cretaceous mass extinction. Adaptations to changing prey availability and the proliferation of coral reef habitats during the Paleogene also likely facilitated carcharhiniform dispersals and cladogenesis, underpinning their current taxonomic dominance. Ultimately, we posit that trophic partitioning and resource utilization shaped past shark ecology and represent critical determinants for their future species survivorship.

Skeletal pathologies track body plan evolution in ichthyosaurs.

Changing predator-prey interactions during the Mesozoic Marine Revolution (MMR) profoundly altered the trajectory of marine tetrapod evolution. Here, we assess potential signatures of this landmark transition through the fossil record of skeletal pathologies in ichthyosaurs - iconic marine reptiles that developed increasingly 'fish-like' body plans over time. We surveyed a stratigraphically constrained sample of 200 Middle Triassic ichthyosaur specimens and compared the type, distribution and prevalence of pathologies with an approximately equivalent assemblage of Early Jurassic age. Overall, skeletal pathologies were equally prevalent in these groups, and most often manifested in species >4 m long. However, pathological bones were found to be concentrated in the hind limbs and tail of Triassic ichthyosaurs, whereas the jaws, forelimbs, and ribcage were preferentially affected in Jurassic taxa. We posit that the occurrence of ankylosed zygapophyses in the caudal peak of Triassic ichthyosaurs could represent a functional by-product of their primitive 'eel-like' swimming. Conversely, increased instances of broken ribs in Jurassic ichthyosaurs may infer ramming or tail strike behaviours that characterise morphologically 'fish-like' marine tetrapods, such as modern toothed whales. Different categories of skeletal pathologies thus evidently reflect structural modifications in the ichthyosaur body plan, and indirectly coincide with ecological turnover during the MMR.

Climbing adaptations, locomotory disparity and ecological convergence in ancient stem 'kangaroos'.

Living kangaroos, wallabies and rat-kangaroos (Macropodoidea) constitute the most ecologically diverse radiation of Australasian marsupials. Indeed, even their hallmark bipedal hopping gait has been variously modified for bounding, walking and climbing. However, the origins of this locomotory adaptability are uncertain because skeletons of the most ancient macropodoids are exceptionally rare. Some of the stratigraphically oldest fossils have been attributed to Balbaridae-a clade of potentially quadrupedal stem macropodoids that became extinct during the late Miocene. Here we undertake the first assessment of balbarid locomotion using two-dimensional geometric morphometrics and a correlative multivariate analysis of linear measurements. We selected the astragalus and pedal digit IV ungual as proxies for primary gait because these elements are preserved in the only articulated balbarid skeleton, as well as some unusual early Miocene balbarid-like remains that resemble the bones of modern tree-kangaroos. Our results show that these fossils manifest character states indicative of contrasting locomotory capabilities. Furthermore, predictive modelling reveals similarities with extant macropodoids that employ either bipedal saltation and/or climbing. We interpret this as evidence for archetypal gait versatility, which probably integrated higher-speed hopping with slower-speed quadrupedal progression and varying degrees of scansoriality as independent specializations for life in forest and woodland settings.

Elasmosaur (Reptilia: Sauropterygia) neck flexibility: implications for feeding strategies.

Elasmosaurs were extremely long-necked, aquatic reptiles that used four flippers for locomotion. Their distinctive long neck distinguishes them from all other Mesozoic forms, yet the potential uses and constraints of this structure are poorly understood, particularly with regard to feeding. Several associated series of elasmosaurian cervical vertebrae were used to measure ranges of potential flexion. Two-dimensional models, based on a complete specimen of the Late Cretaceous elasmosaur Aphrosaurus furlongi, were created to measure mobility in both vertical and horizontal planes. Accuracy of the models was assessed through comparative analyses with currently extant vertebrate analogues (e.g. snake, turtle, seal). Results suggest that the elasmosaurian neck was capable of a 75-177 degrees ventral, 87-155 degrees dorsal, and 94-176 degrees lateral range of movement depending upon the thickness of cartilage reconstructed between each vertebra. Neck postures such as a 'swan-like' S-shape are shown to be implausible because they require >360 degrees vertical flexion. However, maintenance of a straight neck while swimming, together with considerable lateral and/or ventral movement during prey capture and feeding are feasible.

Static Dental Disparity and Morphological Turnover in Sharks across the End-Cretaceous Mass Extinction.

The Cretaceous-Palaeogene (K-Pg) mass extinction profoundly altered vertebrate ecosystems and prompted the radiation of many extant clades [1, 2]. Sharks (Selachimorpha) were one of the few larger-bodied marine predators that survived the K-Pg event and are represented by an almost-continuous dental fossil record. However, the precise dynamics of their transition through this interval remain uncertain [3]. Here, we apply 2D geometric morphometrics to reconstruct global and regional dental morphospace variation among Lamniformes (Mackerel sharks) and Carcharhiniformes (Ground sharks). These clades are prevalent predators in today's oceans, and were geographically widespread during the late Cretaceous-early Palaeogene. Our results reveal a decoupling of morphological disparity and taxonomic richness. Indeed, shark disparity was nearly static across the K-Pg extinction, in contrast to abrupt declines among other higher-trophic-level marine predators [4, 5]. Nevertheless, specific patterns indicate that an asymmetric extinction occurred among lamniforms possessing low-crowned/triangular teeth and that a subsequent proliferation of carcharhiniforms with similar tooth morphologies took place during the early Paleocene. This compositional shift in post-Mesozoic shark lineages hints at a profound and persistent K-Pg signature evident in the heterogeneity of modern shark communities. Moreover, such wholesale lineage turnover coincided with the loss of many cephalopod [6] and pelagic amniote [5] groups, as well as the explosive radiation of middle trophic-level teleost fishes [1]. We hypothesize that a combination of prey availability and post-extinction trophic cascades favored extant shark antecedents and laid the foundation for their extensive diversification later in the Cenozoic [7-10].

Pathological survey on Temnodontosaurus from the Early Jurassic of southern Germany.

Paleopathologies document skeletal damage in extinct organisms and can be used to infer the causes of injury, as well as aspects of related biology, ecology and behavior. To date, few studies have been undertaken on Jurassic marine reptiles, while ichthyosaur pathologies in particular have never been systematically evaluated. Here we survey 41 specimens of the apex predator ichthyosaur Temnodontosaurus from the Early Jurassic of southern Germany in order to document the range and absolute frequency of pathologies observed in this taxon as a function of the number of specimens examined. According to our analysis, most observed pathologies in Temnodontosaurus are force-induced traumas with signs of healing, possibly inflicted during aggressive interactions with conspecifics. When the material is preserved, broken ribs are correlated in most of the cases with traumas elsewhere in the skeleton such as cranial injuries. The range of cranial pathologies in Temnodontosaurus is similar to those reported for extinct cetaceans and mosasaurs, which were interpreted as traces of aggressive encounters. Nevertheless, Temnodontosaurus differs from these other marine amniotes in the absence of pathologies in the vertebral column, consistent with the pattern previously documented in ichthyosaurs. We did not detect any instances of avascular necrosis in Temnodontosaurus from southern Germany, which may reflect a shallow diving life style. This study is intended to provide baseline data for the various types of observed pathologies in large ichthyosaurs occupying the 'apex predator' niche, and potentially clarifies aspects of species-specific behavior relative to other ichthyosaurs and marine amniotes.

Exceptionally prolonged tooth formation in elasmosaurid plesiosaurians.

Elasmosaurid plesiosaurians were globally prolific marine reptiles that dominated the Mesozoic seas for over 70 million years. Their iconic body-plan incorporated an exceedingly long neck and small skull equipped with prominent intermeshing 'fangs'. How this bizarre dental apparatus was employed in feeding is uncertain, but fossilized gut contents indicate a diverse diet of small pelagic vertebrates, cephalopods and epifaunal benthos. Here we report the first plesiosaurian tooth formation rates as a mechanism for servicing the functional dentition. Multiple dentine thin sections were taken through isolated elasmosaurid teeth from the Upper Cretaceous of Sweden. These specimens revealed an average of 950 daily incremental lines of von Ebner, and infer a remarkably protracted tooth formation cycle of about 2-3 years-other polyphyodont amniotes normally take ~1-2 years to form their teeth. Such delayed odontogenesis might reflect differences in crown length and function within an originally uneven tooth array. Indeed, slower replacement periodicity has been found to distinguish larger caniniform teeth in macrophagous pliosaurid plesiosaurians. However, the archetypal sauropterygian dental replacement system likely also imposed constraints via segregation of the developing tooth germs within discrete bony crypts; these partly resorbed to allow maturation of the replacement teeth within the primary alveoli after displacement of the functional crowns. Prolonged dental formation has otherwise been linked to tooth robustness and adaption for vigorous food processing. Conversely, elasmosaurids possessed narrow crowns with an elongate profile that denotes structural fragility. Their apparent predilection for easily subdued prey could thus have minimized this potential for damage, and was perhaps coupled with selective feeding strategies that ecologically optimized elasmosaurids towards more delicate middle trophic level aquatic predation.

Reappraisal of Europe's most complete Early Cretaceous plesiosaurian: Brancasaurus brancai Wegner, 1914 from the "Wealden facies" of Germany.

The holotype of Brancasaurus brancai is one of the most historically famous and anatomically complete Early Cretaceous plesiosaurian fossils. It derived from the Gerdemann & Co. brickworks clay pit near Gronau (Westfalen) in North Rhine-Westphalia, northwestern Germany. Stratigraphically this locality formed part of the classic European "Wealden facies," but is now more formally attributed to the upper-most strata of the Bückeberg Group (upper Berriasian). Since its initial description in 1914, the type skeleton of B. brancai has suffered damage both during, and after WWII. Sadly, these mishaps have resulted in the loss of substantial information, in particular many structures of the cranium and limb girdles, which are today only evidenced from published text and/or illustrations. This non-confirmable data has, however, proven crucial for determining the relationships of B. brancai within Plesiosauria: either as an early long-necked elasmosaurid, or a member of the controversial Early Cretaceous leptocleidid radiation. To evaluate these competing hypotheses and compile an updated osteological compendium, we undertook a comprehensive examination of the holotype as it is now preserved, and also assessed other Bückeberg Group plesiosaurian fossils to establish a morphological hypodigm. Phylogenetic simulations using the most species-rich datasets of Early Cretaceous plesiosaurians incorporating revised scores for B. brancai, together with a second recently named Bückeberg Group plesiosaurian Gronausaurus wegneri (Hampe, 2013), demonstrated that referral of these taxa to Leptocleididae was not unanimous, and that the topological stability of this clade is tenuous. In addition, the trait combinations manifested by B. brancai and G. wegneri were virtually identical. We therefore conclude that these monotypic individuals are ontogenetic morphs and G. wegneri is a junior synonym of B. brancai. Finally, anomalies detected in the diagnostic features for other "Wealden" plesiosaurians have prompted reconsiderations of interspecies homology versus intraspecific variability. We therefore propose that the still unresolved taxonomy of B. brancai should emphasize only those character states evident in the examinable fossil material, and specifically accommodate for growth-related modifications delimited via osteologically mature referred specimens.

Boreal earliest Triassic biotas elucidate globally depauperate hard substrate communities after the end-Permian mass extinction.

The end-Permian mass extinction constituted the most devastating biotic crisis of the Phanerozoic. Its aftermath was characterized by harsh marine conditions incorporating volcanically induced oceanic warming, widespread anoxia and acidification. Bio-productivity accordingly experienced marked fluctuations. In particular, low palaeolatitude hard substrate communities from shallow seas fringing Western Pangaea and the Tethyan Realm were extremely impoverished, being dominated by monogeneric colonies of filter-feeding microconchid tubeworms. Here we present the first equivalent field data for Boreal hard substrate assemblages from the earliest Triassic (Induan) of East Greenland. This region bordered a discrete bio-realm situated at mid-high palaeolatitude (>30°N). Nevertheless, hard substrate biotas were compositionally identical to those from elsewhere, with microconchids encrusting Claraia bivalves and algal buildups on the sea floor. Biostratigraphical correlation further shows that Boreal microconchids underwent progressive tube modification and unique taxic diversification concordant with changing habitats over time. We interpret this as a post-extinction recovery and adaptive radiation sequence that mirrored coeval subequatorial faunas, and thus confirms hard substrate ecosystem depletion as a hallmark of the earliest Triassic interval globally.

Bandicoot fossils and DNA elucidate lineage antiquity amongst xeric-adapted Australasian marsupials.

Bandicoots (Peramelemorphia) are a unique order of Australasian marsupials whose sparse fossil record has been used as prima facie evidence for climate change coincident faunal turnover. In particular, the hypothesized replacement of ancient rainforest-dwelling extinct lineages by antecedents of xeric-tolerant extant taxa during the late Miocene (~10 Ma) has been advocated as a broader pattern evident amongst other marsupial clades. Problematically, however, this is in persistent conflict with DNA phylogenies. We therefore determine the pattern and timing of bandicoot evolution using the first combined morphological + DNA sequence dataset of Peramelemorphia. In addition, we document a remarkably archaic new fossil peramelemorphian taxon that inhabited a latest Quaternary mosaic savannah-riparian forest ecosystem on the Aru Islands of Eastern Indonesia. Our phylogenetic analyses reveal that unsuspected dental homoplasy and the detrimental effects of missing data collectively obscure stem bandicoot relationships. Nevertheless, recalibrated molecular clocks and multiple ancestral area optimizations unanimously infer an early diversification of modern xeric-adapted forms. These probably originated during the late Palaeogene (30-40 Ma) alongside progenitors of other desert marsupials, and thus occupied seasonally dry heterogenous habitats long before the onset of late Neogene aridity.