Johan Lindgren

Mesozoic marine tetrapod diversity: mass extinctions and temporal heterogeneity in geological megabiases affecting vertebrates

The fossil record is our only direct means for evaluating shifts in biodiversity through Earths history. However, analyses of fossil marine invertebrates have demonstrated that geological megabiases profoundly influence fossil preservation and discovery, obscuring true diversity signals. Comparable studies of vertebrate palaeodiversity patterns remain in their infancy. A new species-level dataset of Mesozoic marine tetrapod occurrences was compared with a proxy for temporal variation in the volume and facies diversity of fossiliferous rock (number of marine fossiliferous formations: FMF). A strong correlation between taxic diversity and FMF is present during the Cretaceous. Weak or no correlation of Jurassic data suggests a qualitatively different sampling regime resulting from five apparent peaks in Triassic–Jurassic diversity. These correspond to a small number of European formations that have been the subject of intensive collecting, and represent ‘Lagerstätten effects’. Consideration of sampling biases allows re-evaluation of proposed mass extinction events. Marine tetrapod diversity declined during the Carnian or Norian. However, the proposed end-Triassic extinction event cannot be recognized with confidence. Some evidence supports an extinction event near the Jurassic/Cretaceous boundary, but the proposed end-Cenomanian extinction is probably an artefact of poor sampling. Marine tetrapod diversity underwent a long-term decline prior to the Cretaceous–Palaeogene extinction.

Molecular preservation of the pigment melanin in fossil melanosomes

Fossil feathers, hairs and eyes are regularly preserved as carbonized traces comprised of masses of micrometre-sized bodies that are spherical, oblate or elongate in shape. For a long time, these minute structures were regarded as the remains of biofilms of keratinophilic bacteria, but recently they have been reinterpreted as melanosomes; that is, colour-bearing organelles. Resolving this fundamental difference in interpretation is crucial: if endogenous then the fossil microbodies would represent a significant advancement in the fields of palaeontology and evolutionary biology given, for example, the possibility to reconstruct integumentary colours and plumage colour patterns. It has previously been shown that certain trace elements occur in fossils as organometallic compounds, and hence may be used as biomarkers for melanin pigments. Here we expand this knowledge by demonstrating the presence of molecularly preserved melanin in intimate association with melanosome-like microbodies isolated from an argentinoid fish eye from the early Eocene of Denmark.

Skin pigmentation provides evidence of convergent melanism in extinct marine reptiles

Throughout the animal kingdom, adaptive colouration serves critical functions ranging from inconspicuous camouflage to ostentatious sexual display, and can provide important information about the environment and biology of a particular organism. The most ubiquitous and abundant pigment, melanin, also has a diverse range of non-visual roles, including thermoregulation in ectotherms. However, little is known about the functional evolution of this important biochrome through deep time, owing to our limited ability to unambiguously identify traces of it in the fossil record. Here we present direct chemical evidence of pigmentation in fossilized skin, from three distantly related marine reptiles: a leatherback turtle, a mosasaur and an ichthyosaur. We demonstrate that dark traces of soft tissue in these fossils are dominated by molecularly preserved eumelanin, in intimate association with fossilized melanosomes. In addition, we suggest that contrary to the countershading of many pelagic animals, at least some ichthyosaurs were uniformly dark-coloured in life. Our analyses expand current knowledge of pigmentation in fossil integument beyond that of feathers, allowing for the reconstruction of colour over much greater ranges of extinct taxa and anatomy. In turn, our results provide evidence of convergent melanism in three disparate lineages of secondarily aquatic tetrapods. Based on extant marine analogues, we propose that the benefits of thermoregulation and/or crypsis are likely to have contributed to this melanisation, with the former having implications for the ability of each group to exploit cold environments.

Convergent evolution in aquatic tetrapods: insights from an exceptional fossil mosasaur.

Mosasaurs (family Mosasauridae) are a diverse group of secondarily aquatic lizards that radiated into marine environments during the Late Cretaceous (98–65 million years ago). For the most part, they have been considered to be simple anguilliform swimmers – i.e., their propulsive force was generated by means of lateral undulations incorporating the greater part of the body – with unremarkable, dorsoventrally narrow tails and long, lizard-like bodies. Convergence with the specialized fusiform body shape and inferred carangiform locomotory style (in which only a portion of the posterior body participates in the thrust-producing flexure) of ichthyosaurs and metriorhynchid crocodyliform reptiles, along with cetaceans, has so far only been recognized in Plotosaurus, the most highly derived member of the Mosasauridae. Here we report on an exceptionally complete specimen (LACM 128319) of the moderately derived genus Platecarpus that preserves soft tissues and anatomical details (e.g., large portions of integument, a partial body outline, putative skin color markings, a downturned tail, branching bronchial tubes, and probable visceral traces) to an extent that has never been seen previously in any mosasaur. Our study demonstrates that a streamlined body plan and crescent-shaped caudal fin were already well established in Platecarpus, a taxon that preceded Plotosaurus by 20 million years. These new data expand our understanding of convergent evolution among marine reptiles, and provide insights into their evolutions tempo and mode.

Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia, Squamata) - Implications for Aquatic Adaptation and Growth Rates

Background During their evolution in the Late Cretaceous, mosasauroids attained a worldwide distribution, accompanied by a marked increase in body size and open ocean adaptations. This transition from land-dwellers to highly marine-adapted forms is readily apparent not only at the gross anatomic level but also in their inner bone architecture, which underwent profound modifications. Methodology/Principal Findings The present contribution describes, both qualitatively and quantitatively, the internal organization (microanatomy) and tissue types and characteristics (histology) of propodial and epipodial bones in one lineage of mosasauroids; i.e., the subfamily Mosasaurinae. By using microanatomical and histological data from limb bones in combination with recently acquired knowledge on the inner structure of ribs and vertebrae, and through comparisons with extant squamates and semi-aquatic to fully marine amniotes, we infer possible implications on mosasaurine evolution, aquatic adaptation, growth rates, and basal metabolic rates. Notably, we observe the occurrence of an unusual type of parallel-fibered bone, with large and randomly shaped osteocyte lacunae (otherwise typical of fibrous bone) and particular microanatomical features in Dallasaurus, which displays, rather than a spongious inner organization, bone mass increase in its humeri and a tubular organization in its femora and ribs. Conclusions/Significance The dominance of an unusual type of parallel-fibered bone suggests growth rates and, by extension, basal metabolic rates intermediate between that of the extant leatherback turtle, Dermochelys, and those suggested for plesiosaur and ichthyosaur reptiles. Moreover, the microanatomical features of the relatively primitive genus Dallasaurus differ from those of more derived mosasaurines, indicating an intermediate stage of adaptation for a marine existence. The more complete image of the various microanatomical trends observed in mosasaurine skeletal elements supports the evolutionary convergence between this lineage of secondarily aquatically adapted squamates and cetaceans in the ecological transition from a coastal to a pelagic lifestyle.

Microspectroscopic evidence of cretaceous bone proteins.

Low concentrations of the structural protein collagen have recently been reported in dinosaur fossils based primarily on mass spectrometric analyses of whole bone extracts. However, direct spectroscopic characterization of isolated fibrous bone tissues, a crucial test of hypotheses of biomolecular preservation over deep time, has not been performed. Here, we demonstrate that endogenous proteinaceous molecules are retained in a humerus from a Late Cretaceous mosasaur (an extinct giant marine lizard). In situ immunofluorescence of demineralized bone extracts shows reactivity to antibodies raised against type I collagen, and amino acid analyses of soluble proteins extracted from the bone exhibit a composition indicative of structural proteins or their breakdown products. These data are corroborated by synchrotron radiation-based infrared microspectroscopic studies demonstrating that amino acid containing matter is located in bone matrix fibrils that express imprints of the characteristic 67 nm D-periodicity typical of collagen. Moreover, the fibrils differ significantly in spectral signature from those of potential modern bacterial contaminants, such as biofilms and collagen-like proteins. Thus, the preservation of primary soft tissues and biomolecules is not limited to large-sized bones buried in fluvial sandstone environments, but also occurs in relatively small-sized skeletal elements deposited in marine sediments.

Landlubbers to leviathans: evolution of swimming in mosasaurine mosasaurs

Abstract Incremental stages of major evolutionary transitions within a single animal lineage are rarely observed in the fossil record. However, the extraordinarily complete sequence of well preserved material spanning the 27-Myr existence of the marine squamate subfamily Mosasaurinae provides a unique exception. By comparison with extant and extinct analogs, the tail morphology of four mosasaurine genera is examined, revealing a pattern of evolution that begins with the generalized varanoid anatomy and culminates in a high-aspect-ratio fin, similar to that of sharks. However, unlike the epicercal caudal fluke of selachians in which the tail bends dorsocaudally, derived mosasaurs develop a hypocercal tail with a ventrocaudal bend. Progressive caudal regionalization, reduced intervertebral mobility, increased tail depth due to a marked downturn of the posterior caudal segment, and the development of finlike paired appendages reveal a pattern of adaptation toward an optimized marine existence. This change in morphology reflects a transition from anguilliform or sub-carangiform locomotion to carangiform locomotion, and indicates a progressive shift from nearshore dwellers to pelagic cruisers—a change in foraging habitat independently corroborated by paleobiogeographic, stable isotope, osteohistological, and paleopathological data. Evolutionary patterns similar to those observed in mosasaurine mosasaurs are seen in other secondarily aquatically adapted amniotes, notably metriorhynchid crocodyliforms, cetaceans, and ichthyosaurs, and may be explained by developmental modularity governing the observed phenotypic expression.

THE FIRST RECORD OF HAINOSAURUS (REPTILIA: MOSASAURIDAE) FROM SWEDEN

Abstract Isolated marginal tooth crowns of the early Campanian mosasaur Hainosaurus Dollo, 1885, from the Kristianstad Basin and the Vomb Trough, southern Sweden, are described and illustrated. The teeth have been collected from a narrow stratigraphic interval corresponding to the highest belemnite zone in the lower part of the European two-fold division of the Campanian stage. A reexamination of dental and skeletal characters in two alleged species of Hainosaurus, ‘H.’ pembinensis Nicholls, 1988 and ‘H.’ gaudryi (Thévenin, 1896), and detailed comparisons with the corresponding elements in H. bernardi Dollo, 1885 and Tylosaurus proriger (Cope, 1869a), strongly indicate that ‘H.’ pembinensis and ‘H.’ gaudryi are both Tylosaurus Marsh, 1872. Diagnostic features of Hainosaurus include a very small infrastapedial process on the quadrate (conspicuous protuberance in Tylosaurus), flattened, symmetrically bicarinate marginal teeth (asymmetric and conical in Tylosaurus), short and wide pygal centra, and anteriorly situated intermediate caudal vertebral centra with dorsoventrally thin transverse processes (markedly triangular centra and thick processes in Tylosaurus).

New Data on the Postcranial Anatomy of the California Mosasaur Plotosaurus bennisoni (Camp, 1942) (Upper Cretaceous: Maastrichtian), and the Taxonomic Status of P. tuckeri (Camp, 1942)

Abstract New axial and appendicular material permits a detailed re-description of the postcranial skeleton of the derived mid-Maastrichtian California mosasaur genus Plotosaurus. Centrum morphology, vertebral process shape, and extreme hyperphalangy provide compelling evidence to demonstrate that Plotosaurus achieved the highest level of aquatic adaptation among mosasaurs. A re-examination of the type material of P. bennisoni and of P. tuckeri indicates that only one taxon, P. bennisoni, is present, of which P. tuckeri is a junior synonym.

Cenomanian—Campanian (Late Cretaceous) Mid-Palaeolatitude Sharks of Cretalamna appendiculata Type

The type species of the extinct lamniform genus Cretalamna, C. appendiculata, has been assigned a 50 Ma range (Albian—Ypresian) by a majority of previous authors. Analysis of a partly articulated dentition of a Cretalamna from the Smoky Hill Chalk, Kansas, USA (LACM 128126) and isolated teeth of the genus from Cenomanian to Campanian strata of Western Australia, France, Sweden, and the Western Interior of North America, indicates that the name of the type species, as applied to fossil material over the last 50 years, represents a large species complex. The middle Cenomanian part of the Gearle Siltstone, Western Australia, yielded C. catoxodon sp. nov. and “Cretalamna” gunsoni. The latter, reassigned to the new genus Kenolamna, shares several dental features with the Paleocene Palaeocarcharodon. Early Turonian strata in France produced the type species C. appendiculata, C. deschutteri sp. nov., and C. gertericorum sp. nov. Cretalamna teeth from the late Coniacian part of the Smoky Hill Chalk in Kansas are assigned to C. ewelli sp. nov., whereas LACM 128126, of latest Santonian or earliest Campanian age, is designated as holotype of C. hattini sp. nov. Early Campanian deposits in Sweden yielded C. borealis and C. sarcoportheta sp. nov. A previous reconstruction of the dentition of LACM 128126 includes a posteriorly situated upper lateroposterior tooth, with a distally curved cusp, demonstrably misplaced as a reduced upper “intermediate” tooth. As originally reconstructed, the dentition resembled that of cretoxyrhinids (sensu stricto) and lamnids. Tooth morphology, however, indicates an otodontid affinity for Cretalamna. The root is typically the most diagnostic feature on an isolated Cretalamna tooth. This porous structure is commonly abraded and/or corroded and, consequently, many collected Cretalamna teeth are indeterminable at species level.