Bone microstructure and the evolution of growth patterns in Permo-Triassic therocephalians (Amniota, Therapsida) of South Africa

Therocephalians were a speciose clade of nonmammalian therapsids whose ecological diversity and survivorship of the end-Permian mass extinction offer the potential to investigate the evolution of growth patterns across the clade and their underlying influences on post-extinction body size reductions, or ‘Lilliput effects’. We present a phylogenetic survey of limb bone histology and growth patterns in therocephalians from the Middle Permian through Middle Triassic of the Karoo Basin, South Africa. Histologic sections were prepared from 80 limb bones representing 11 genera of therocephalians. Histologic indicators of skeletal growth, including cortical vascularity (%CV) and mean primary osteon diameters (POD), were evaluated in a phylogenetic framework and assessed for correlations with other biologically significant variables (e.g., size and robusticity). Changes in %CV and POD correlated strongly with evolutionary changes in body size (i.e., smaller-bodied descendants tended to have lower %CV than their larger-bodied ancestors across the tree). Bone wall thickness tended to be high in early therocephalians and lower in the gracile-limbed baurioids, but showed no general correlation with cross-sectional area or degree of vascularity (and, thus, growth). Clade-level patterns, however, deviated from previously studied within-lineage patterns. For example, Moschorhinus, one of few therapsid genera to have survived the extinction boundary, demonstrated higher %CV in the Triassic than in the Permian despite its smaller size in the extinction aftermath. Results support a synergistic model of size reductions for Triassic therocephalians, influenced both by within-lineage heterochronic shifts in survivor taxa (as reported in Moschorhinus and the dicynodont Lystrosaurus) and phylogenetically inferred survival of small-bodied taxa that had evolved short growth durations (e.g., baurioids). These findings mirror the multi-causal Lilliput patterns described in marine faunas, but contrast with skeletochronologic studies that suggest slow, prolonged shell secretion over several years in marine benthos. Applications of phylogenetic comparative methods to new histologic data will continue to improve our understanding of the evolutionary dynamics of growth and body size shifts during mass extinctions and recoveries

Digging the compromise: investigating the link between limb bone histology and fossoriality in the aardvark (Orycteropus afer)

Bone microstructure has long been known as a powerful tool to investigate lifestyle-related biomechanical constraints, and many studies have focused on identifying such constraints in the limb bones of aquatic or arboreal mammals in recent years. The limb bone microstructure of fossorial mammals, however, has not been extensively described. Furthermore, so far, studies on this subject have always focused on the bone histology of small burrowers, such as subterranean rodents or true moles. Physiological constraints associated with digging, however, are known to be strongly influenced by body size, and larger burrowers are likely to exhibit a histological profile more conspicuously influenced by fossorial activity. Here, we describe for the first time the limb bone histology of the aardvark (Orycteropus afer), the largest extant burrowing mammal. The general pattern is very similar for all six sampled limb bones (i.e., humerus, radius, ulna, femur, tibia, and fibula). Most of the cortex at midshaft is comprised of compacted coarse cancellous bone (CCCB), an endosteal tissue formed in the metaphyses through the compaction of bony trabeculae. Conversely, the periosteal bone is highly resorbed in all sections, and is reduced to a thin outer layer, suggesting a pattern of strong cortical drift. This pattern contrasts with that of most large mammals, in which cortical bone is of mostly periosteal origin, and CCCB, being a very compliant bone tissue type, is usually resorbed or remodeled during ontogeny. The link between histology and muscle attachment sites, as well as the influence of the semi-arid environment and ant-eating habits of the aardvark on its bone microstructure, are discussed. We hypothesize that the unusual histological profile of the aardvark is likely the outcome of physiological constraints due to both extensive digging behavior and strong metabolic restrictions. Adaptations to fossoriality are thus the result of a physiological compromise between limited food availability, an environment with high temperature variability, and the need for biomechanical resistance during digging. These results highlight the difficulties of deciphering all factors potentially involved in bone formation in fossorial mammals. Even though the formation and maintaining of CCCB through ontogeny in the aardvark cannot be unambiguously linked with its fossorial habits, a high amount of CCCB has been observed in the limb bones of other large burrowing mammals. The inclusion of such large burrowers in future histological studies is thus likely to improve our understanding of the functional link between bone growth and fossorial lifestyle in an evolutionary context

Burrowing in <i>Lystrosaurus</i>: preadaptation to a postextinction environment?

<p><i>Lystrosaurus</i> is iconic for surviving the Permo-Triassic Mass Extinction and becoming the most abundant terrestrial vertebrate during the Early Triassic. Previous reports of skeletal remains of the Triassic species being found in fossilized burrows hint at a possible reason for its success, but unequivocal evidence showing that <i>Lystrosaurus</i> individuals were the burrow makers was lacking. I present here the first articulated skeleton of <i>Lystrosaurus</i> in a fossilized burrow from the Lower Triassic of the South African Karoo Basin, along with taphonomic evidence indicating that this individual was the burrow maker. The species is identified as <i>L. curvatus</i>, the only <i>Lystrosaurus</i> species recovered from above and below the inferred Permo-Triassic extinction horizon. It provides the first evidence of burrowing in a Permian species of <i>Lystrosaurus</i>, suggesting that this behavior was more prevalent than previously thought. Based on its size, the specimen is inferred to be a juvenile, showing that <i>Lystrosaurus</i> was capable of excavating burrows at young ontogenetic stages. The abundance of <i>Lystrosaurus</i> body fossils and similar-sized burrows from Lower Triassic strata suggests that burrowing played a pivotal role in the success of this genus in harsh, unpredictable postextinction conditions. Given the abundance of these burrows throughout the Lower Triassic <i>Lystrosaurus</i> Assemblage Zone, <i>Lystrosaurus</i> may have acted as an ecosystem engineer and refuge provider for other species, which may help to explain the high species diversity in the lowermost Triassic in the Karoo Basin.</p> <p>SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at <a href="http://www.tandfonline.com/UJVP" target="_blank">www.tandfonline.com/UJVP</a></p> <p>Citation for this article: J. Botha-Brink. 2017. Burrowing in <i>Lystrosaurus</i>: preadaptation to a postextinction environment?. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2017.1365080.</p

Postcranial morphology of the Early Triassic epicynodont Galesaurus planiceps (Owen) from the Karoo Basin, South Africa

The Early Triassic non-mammaliaform epicynodont Galesaurus planiceps formed an important part of ecosystems following the Permo-Triassic Mass Extinction, the greatest mass extinction in Phanerozoic history. Here, we re-examine the postcranial skeleton of Galesaurus and present data which sheds light on the biology, ecology and possible survival strategies of this species. We find evidence for two distinct morphotypes, a gracile and a robust morph, which we interpret as stages in an ontogenetic series. The primary differences between the morphs manifest in the girdles, with further subtle differences in the fore and hind limbs. Our study also reveals postcranial differences between Galesaurus and the contemporaneous taxon Thrinaxodon liorhinus, allowing these taxa to be distinguished in the absence of cranial material. We also report the first evidence of intraspecific variation in the presence and distribution of disc-like phalanges in a non-mammaliaform cynodont. Ananalysis of the osteohistology of Galesaurus reveals rapid growth to skeletal maturity within one year, thereafter transitioning to slow intermittent growth. This growth pattern is similar to that of Thrinaxodon, which also grew rapidly and continuously to skeletal, and possibly reproductive, maturity within its first year of life. Features such as a strong, reinforced pelvis, elongated ilium, thick, robust forelimbs and stout unguals indicate that Galesaurus was capable of actively excavating burrows. The combination of rapid maturation and fossoriality may have aided its survival in the harsh, unpredictable post-extinction Early Triassic environment.Fil: Butler, Elize. National Museum; SudáfricaFil: Abdala, Nestor Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Botha Brink, Jennifer. National Museum; Sudáfric

Osteohistology of Late Triassic prozostrodontian cynodonts from Brazil

The Prozostrodontia includes a group of Late Triassic-Early Cretaceous eucynodonts plus the clade Mammaliaformes, in which Mammalia is nested. Analysing their growth patterns is thus important for understanding the evolution of mammalian life histories. Obtaining material for osteohistological analysis is difficult due to the rare and delicate nature of most of the prozostrodontian taxa, much of which comprises mostly of crania or sometimes even only teeth. Here we present a rare opportunity to observe the osteohistology of several postcranial elements of the basal prozostrodontid Prozostrodon brasiliensis, the tritheledontid Irajatherium hernandezi, and the brasilodontids Brasilodon quadrangularis and Brasilitherium riograndensis from the Late Triassic of Brazil (Santa Maria Supersequence). Prozostrodon and Irajatherium reveal similar growth patterns of rapid early growth with annual interruptions later in ontogeny. These interruptions are associated with wide zones of slow growing bone tissue. Brasilodon and Brasilitherium exhibit a mixture of woven-fibered bone tissue and slower growing parallel-fibered and lamellar bone. The slower growing bone tissues are present even during early ontogeny. The relatively slower growth in Brasilodon and Brasilitherium may be related to their small body size compared to Prozostrodon and Irajatherium. These brasilodontids also exhibit osteohistological similarities with the Late Triassic/Early Jurassic mammaliaform Morganucodon and the Late Cretaceous multituberculate mammals Kryptobaatar and Nemegtbaatar. This may be due to similar small body sizes, but may also reflect their close phylogenetic affinities as Brasilodon and Brasilitherium are the closest relatives to Mammaliaformes. However, when compared with similar-sized extant placental mammals, they may have grown more slowly to adult size as their osteohistology shows it took more than one year for growth to attenuate. Thus, although they exhibit rapid juvenile growth, the small derived, brasilodontid prozostrodontians still exhibit an extended growth period compared to similar-sized extant mammals

Data from: Palaeohistological evidence for ancestral high metabolic rate in archosaurs

Metabolic heat production in archosaurs has played an important role in their evolutionary radiation during the Mesozoic, and their ancestral metabolic condition has long been a matter of debate in systematics and palaeontology. The study of fossil bone histology provides crucial information on bone growth rate, which has been used to indirectly investigate the evolution of thermometabolism in archosaurs. However, no quantitative estimation of metabolic rate has ever been performed on fossils using bone histological features. Moreover, to date, no inference model has included phylogenetic information in the form of predictive variables. Here we performed statistical predictive modelling using the new method of phylogenetic eigenvector maps on a set of bone histological features for a sample of extant and extinct vertebrates, in order to estimate metabolic rates of fossil archosauromorphs. This modelling procedure serves as a case study for eigenvector-based predictive modelling in a phylogenetic context, as well as an investigation of the poorly known evolutionary patterns of metabolic rate in archosaurs. Our results show that Mesozoic theropod dinosaurs exhibit metabolic rates very close to those found in modern birds, that archosaurs share an higher ancestral metabolic rate than that of extant ectotherms, and that this derived high metabolic rate was acquired at a much more inclusive level of the phylogenetic tree, among non-archosaurian archosauromorphs. These results also highlight the difficulties of assigning a given heat production strategy (i.e. endothermy, ectothermy) to an estimated metabolic rate value, and confirm findings of previous studies that the definition of the endotherm/ectotherm dichotomy may be ambiguous

McPhee et al 2018 Current Biology

Ledumahadi Mafube dataset

Supplementary Table 3

Resting metabolic rate measured for extant species and osteohistological characters measured from all available tibiae in the sample

Trends of therapy diabetes mellitus 2 type

Phylogenetic tree of all species in our sample of tibiae, as a NEXUS file