Damien Germain

Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda)

Radial cross‐sections of 49 species of extant and two species of extinct amniotes of known lifestyle have been studied in order to assess the relationship between lifestyle (aquatic, amphibious or terrestrial) and bone microanatomy. Most compactness profile and body size parameters exhibit a phylogenetic signal; therefore, classical statistical tests should not be used. Permutational multiple linear regressions show an ecological signal in most compactness profile parameters and in the cross‐section maximal diameter. A linear discriminant analysis is performed with these parameters to distinguish the various lifestyles. The discriminant function based on taxa of known lifestyle is used to infer the lifestyle of three extinct amniotes: the early nothosaur Pachypleurosaurus (amphibious), the therapsid Lystrosaurus (amphibious) and the synapsid Ophiacodon (aquatic). These predictions are congruent with classical palaeoecological interpretations. This model may be very useful when attempting to infer the ancestral lifestyle of amniotes and other early limbed vertebrates.

Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference.

Bone microanatomy appears to track changes in various physiological or ecological properties of the individual or the taxon. Analyses of sections of the tibia of 99 taxa show a highly significant (P ≤ 0.005) relationship between long‐bone microanatomy and habitat. Randomization tests reveal a highly significant (P ≤ 0.005) phylogenetic signal on several compactness profile parameters and lifestyle. Discriminant analyses yield an inference model which has a success rate of 63% when lifestyle is coded into three states (aquatic, amphibious and terrestrial) or 83% for a binary model (aquatic vs. amphibious to terrestrial). Lifestyle is inferred to have been terrestrial for the stem‐tetrapod Discosauriscus (Early Permian), the basal synapsid Dimetrodon (Early Permian), the dicynodont therapsid Dicynodon (Late Permian), an unindentified gorgonopsian (Late Permian); the parareptile Pareiasaurus (Middle or Late Permian) is modelled as being aquatic, but was more likely amphibious.

Evolution of ossification sequences in salamanders and urodele origins assessed through event‐pairing and new methods

SUMMARY Ossification sequences of the skull in extant Urodela and in Permo‐Carboniferous Branchiosauridae have already been used to study the origin of lissamphibians. But most of these studies did not consider some recent methods developed to analyze the developmental sequences within a phylogenetic framework. Here, we analyze the ossification sequences of 24 cranial bones of 23 extant species of salamanders using the event‐pairing method. This reveals new developmental synapomorphies for several extant salamander taxa and ancestral sequences for Urodela under four alternative reference phylogenies. An analysis with the 12 bones for which ossification sequence data are available in urodeles and in the branchiosaurid Apateon is also performed in order to compare the ancestral condition of the crown‐group of Urodela to the sequence of Apateon. This reveals far more incompatibilities than previously suggested. The similarities observed between some extant salamanders and branchiosaurids may result from extensive homoplasy, as the extreme variation observed in extant Urodela suggests, or be plesiomorphic, as the conservation of some ossification patterns observed in other remotely related vertebrates like actinopterygians suggests. We propose a new, simpler method based on squared‐change optimization to estimate the relative timing of ossification of various bones of hypothetical ancestors, and use independent‐contrasts analysis to estimate the confidence intervals around these times. Our results show that the uncertainty of the ancestral ossification sequence of Urodela is much greater than event‐pairing suggests. The developmental data do not allow to conclude that branchiosaurids are closely related to salamanders and their limited taxonomic distribution in Paleozoic taxa precludes testing hypotheses about lissamphibian origins. This is true regardless of the analytical method used (event‐pairing or our new method based on squared‐change parsimony). Simulations show that the new analytical method is generally more powerful to detect evolutionary shifts in developmental timing, and has lower Type I error rate than event‐pairing. It also makes fewer errors in ancestral character value or state assignment than event‐pairing.

Developmental Characters in Phylogenetic Inference and Their Absolute Timing Information

Despite the recent surge of interest in studying the evolution of development, surprisingly little work has been done to investigate the phylogenetic signal in developmental characters. Yet, both the potential usefulness of developmental characters in phylogenetic reconstruction and the validity of inferences on the evolution of developmental characters depend on the presence of such a phylogenetic signal and on the ability of our coding scheme to capture it. In a recent study, we showed, using simulations, that a new method (called the continuous analysis) using standardized time or ontogenetic sequence data and squared-change parsimony outperformed event pairing and event cracking in analyzing developmental data on a reference phylogeny. Using the same simulated data, we demonstrate that all these coding methods (event pairing and standardized time or ontogenetic sequence data) can be used to produce phylogenetically informative data. Despite some dependence between characters (the position of an event in an ontogenetic sequence is not independent of the position of other events in the same sequence), parsimony analysis of such characters converges on the correct phylogeny as the amount of data increases. In this context, the new coding method (developed for the continuous analysis) outperforms event pairing; it recovers a lower proportion of incorrect clades. This study thus validates the use of ontogenetic data in phylogenetic inference and presents a simple coding scheme that can extract a reliable phylogenetic signal from these data.

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.

Limb-bone histology of temnospondyls: implications for understanding the diversification of palaeoecologies and patterns of locomotion of Permo-Triassic tetrapods

The locomotion of early tetrapods has long been a subject of great interest in the evolutionary history of vertebrates. However, we still do not have a precise understanding of the evolutionary radiation of their locomotory strategies. We present here the first palaeohistological study based on theoretical biomechanical considerations among a highly diversified group of early tetrapods, the temnospondyls. Based on the quantification of microanatomical and histological parameters in the humerus and femur of nine genera, this multivariate analysis provides new insights concerning the adaptations of temnospondyls to their palaeoenvironments during the Early Permian, and clearly after the Permo‐Triassic crisis. This study therefore presents a methodology that, if based on a bigger sample, could contribute towards a characterization of the behaviour of species during great evolutionary events.

The inner ear of Megatherium and the evolution of the vestibular system in sloths.

Extant tree sloths are uniquely slow mammals with a very specialized suspensory behavior. To improve our understanding of their peculiar evolution, we investigated the inner ear morphology of one of the largest and most popular fossil ground sloths, Megatherium americanum. We first address the predicted agility of this animal from the scaling of its semicircular canals (SC) relative to body mass, based on recent work that provided evidence that the size of the SC in mammals correlates with body mass and levels of agility. Our analyses predict intermediate levels of agility for Megatherium, contrasting with the extreme slowness of extant sloths. Secondly, we focus on the morphology of the SC at the inner ear scale and investigate the shape and proportions of these structures in Megatherium and in a large diversity of extant xenarthrans represented in our database. Our morphometric analyses demonstrate that the giant ground sloth clearly departs from the SC morphology of both extant sloth genera (Choloepus, Bradypus) and is in some aspects closer to that of armadillos and anteaters. Given the close phylogenetic relationships of Megatherium with the extant genus Choloepus, these results are evidence of substantial homoplasy of the SC anatomy in sloths. This homoplasy most likely corresponds to an outstanding convergent evolution between extant suspensory sloth genera.

A MICROANATOMICAL AND HISTOLOGICAL STUDY OF THE PAIRED FIN SKELETON OF THE DEVONIAN SARCOPTERYGIAN EUSTHENOPTERON FOORDI

Abstract Sections of fore- and hindlimbs of a Paleozoic sarcopterygian (Eusthenopteron foordi from the Devonian) possess a thin cortical compacta and an extensive and relatively loose medullary spongiosa. Most long bones have no free medullary cavity. The smallest bones appear to have a proportionately thicker cortical compacta (although the trend is not statistically significant) and a free medullary cavity. The morphological synapomorphies of panderichthyids and stegocephalians that could be interpreted as suggesting a life in shallow water and possibly occasional excursions on dry land are absent in E. foordi. Thus, recent data on sarcopterygian morphology are congruent with recent paleoecological interpretations that E. foordi lived in a marginal marine or estuarine environment and had an aquatic lifestyle.

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.

Earliest evidence of mammalian social behaviour in the basal Tertiary of Bolivia

The vast majority of Mesozoic and early Cenozoic metatherian mammals (extinct relatives of modern marsupials) are known only from partial jaws or isolated teeth, which give insight into their probable diets and phylogenetic relationships but little else. The few skulls known are generally crushed, incomplete or both, and associated postcranial material is extremely rare. Here we report the discovery of an exceptionally large number of almost undistorted, nearly complete skulls and skeletons of a stem-metatherian, Pucadelphys andinus, in the early Palaeocene epoch of Tiupampa in Bolivia. These give an unprecedented glimpse into early metatherian morphology, evolutionary relationships and, especially, ecology. The remains of 35 individuals have been collected, with 22 of these represented by nearly complete skulls and associated postcrania. These individuals were probably buried in a single catastrophic event, and so almost certainly belong to the same population. The preservation of multiple adult, sub-adult and juvenile individuals in close proximity (<1 m2) is indicative of gregarious social behaviour or at least a high degree of social tolerance and frequent interaction. Such behaviour is unknown in living didelphids, which are highly solitary and have been regarded, perhaps wrongly, as the most generalized living marsupials. The Tiupampan P. andinus population also exhibits strong sexual dimorphism, which, in combination with gregariousness, suggests strong male–male competition and polygyny. Our study shows that social interactions occurred in metatherians as early as the basal Palaeocene and that solitary behaviour may not be plesiomorphic for Metatheria as a whole.