Ontogenetic growth and the development of a unique fibrocartilage entheses in Macropus fuliginosus

The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed NMRs are known for their long lifespans among rodents and for having low metabolic rates We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70) Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (ie, slow bone turnover), thus most likely reflecting the low metabolic rates of this species Secondary osteons occurred regardless of reproductive status However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (ie, mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling

Bone remodeling in the longest living rodent, the naked mole‐rat: Interelement variation and the effects of reproduction

Convergent evolution is a major topic in evolutionary biology. Low bone cortical compactness (CC, a measure of porosity of cortical bone) in the extant genera of "tree sloths," has been linked to their convergent slow arboreal ecology. This proposed relationship of low CC with a slow arboreal lifestyle suggests potential convergent evolution of this trait in other slow arboreal mammals. Femoral and humeral CC were analyzed in "tree sloths," lorisids, koala, and extinct palaeopropithecids and Megaladapis, in comparison to closely related but ecologically distinct taxa, in a phylogenetic framework. Low CC in "tree sloths" is unparalleled by any analyzed clade and the high CC in extinct sloths suggests the recent convergence of low CC in "tree sloths." A tendency for low CC was found in Palaeopropithecus and Megaladapis. However, lorisids and the koala yielded unexpected CC patterns, preventing the recognition of a straightforward convergence of low CC in slow arboreal mammals. This study uncovers a complex relationship between CC and convergent evolution of slow arboreality, highlighting the multifactorial specificity of bone microstructure.

Evolution of bone cortical compactness in slow arboreal mammals

We present a detailed histological study of long bones from an ontogenetic series of Mussaurus patagonicus, an early sauropodomorph from the Lower Jurassic of Argentina. Twenty long bones, including humeri, femora and fibulae, obtained from 13 individuals of different body sizes were sampled for histological analysis. In general terms, the cortical bone is formed by a well vascularized fibrolamellar and parallel fibred bone. Except for the smaller individuals, cyclical growth marks (CGMs) are well recorded in all the specimens but their number and relative position is highly variable. Mussaurus exhibits marked variation regarding relative growth rate, with some individuals growing much faster than others. Such variation affects the size of the adult individuals, which results in a poor correlation between the body size and the age/ontogenetic stage for this taxon. These discrepancies may be related to sexual dimorphism and/or developmental plasticity. Intraspecific variation is also recorded with regard to the growth strategies, which can vary from cyclical, as in other early sauropodomorphs, to continuous, as reported in sauropods. Sexual maturity appears to have been reached between 23 and 31 years, which is delayed in comparison to other early sauropodomorphs but more comparable with derived sauropods. The attainment of somatic maturity appears to have been reached at about 14 years after onset of sexual maturity. Mussaurus is a sauropodiform, phylogenetically closer to sauropods than most other Early Jurassic sauropodomorphs, and therefore provides critical information for understanding palaeobiological aspects of the origin of sauropods and the onset of gigantism in this lineage.

Palaeobiology of the early sauropodomorph Mussaurus patagonicus inferred from its long bone histology

Lifestyle convergences and related phenotypes are a major topic in evolutionary biology. Low bone cortical compactness (CC), shared by the two genera of ′tree sloths′, has been linked to their convergently evolved slow arboreal ecology. The proposed relationship of low CC with ′tree sloths′ lifestyle suggests a potential convergent acquisition of this trait in other slow arboreal mammals. ′Tree sloths′, ′Lorisidae′, Palaeopropithecidae, Megaladapis and koalas were included in a phylogenetically informed CC analysis of the humerus and femur, as well as closely related but ecologically distinct taxa. We found that ′tree sloths′ are unparalleled by any analysed clade, in featuring an extremely low CC. A tendency for low CC was however found in palaeopropithecids (especially Palaeopropithecus) and Megaladapis. On the other hand, low CC was not found in ′Lorisidae′. Koalas, although deviating from the compact structure generally observed in mammals, are not clearly distinct from their sister taxon (wombats) and show humeral CC that is higher than femoral CC. Multiple factors seem to influence CC, preventing the recognition of a simple relationship between slow arborealism and low CC. Highly compact cortical bone in extinct sloths confirms that low CC in ′tree sloths′ likely represents a recent convergence.

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\n Given that the biology of the recently extinct aepyornithids is poorly understood, we undertook a histological study of 29 skeletal elements of adult and juvenile specimens of Aepyornithidae, i.e. Aepyornis maximus, Aepyornis hildebrandti and Vorombe titan, in addition to a group of taxonomically unidentifiable juvenile Aepyornithiformes. Comparative analysis of the histology of the different skeletal elements showed that although the femur retained a good record of growth during early ontogeny, the tibiotarsus provided the best record of growth. Our data showed that, like other insular birds and their extant relative, the kiwi, Aepyornithidae experienced protracted growth. We also found that intracortical remodelling began early in ontogeny and continued throughout their lives, becoming more extensive throughout the compacta with age, albeit more restricted to the perimedullary region in the femora. We also deduced that the different skeletal elements experienced variable amounts of intracortical remodelling, which was most likely to be related to biomechanical constraints, size of the element and ontogenetic age. Additionally, we documented the occurrence of an unusual endosteal tissue within the large perimedullary erosional spaces of a femur of A. maximus. Overall, our study provided a lot of new information about the life history of these giant, recently extinct ratites.

Ursula B Göhlich

Papers

Bone histology yields insights into the biology of the extinct elephant birds (Aepyornithidae) from Madagascar