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Trabecular bone is modelled throughout an animal’s life in response to its mechanical environment, but like other skeletal anatomy, it is also subject to evolutionary influences. Yet the relative strengths of factors that affect trabecular bone architecture are little studied. We investigated these influences across the Philippine endemic murine rodent clade Chrotomyini. These mammals have robustly established phylogenetic relationships, exhibit a range of well-documented substrate-use types, and have a body size range spanning several hundred grammes, making them ideal for a tractable study of extrinsic and intrinsic influences on trabecular bone morphology. We found slight differences in vertebral trabecular bone among different substrate-use categories, with more divergent characteristics in more ecologically specialized taxa. This suggests that the mechanical environment must be relatively extreme to affect trabecular bone morphology in small mammals. We also recovered allometric patterns that imply that selective pressures on bone may differ between small and large mammals. Finally, we found high intrataxonomic variation in trabecular bone morphology, but it is not clearly related to any variable we measured, and may represent a normal degree of variation in these animals rather than a functional trait. Future studies should address how this plasticity affects biomechanical properties and performance of the skeleton.

 

Photosynthetic carbon (C) fixation by phytoplankton in the Southern Ocean (SO) plays a critical role in regulating air–sea exchange of carbon dioxide and thus global climate. In the SO, photosynthesis (PS) is often constrained by low iron, low temperatures, and low but highly variable light intensities. Recently, proton-pumping rhodopsins (PPRs) were identified in marine phytoplankton, providing an alternate iron-free, light-driven source of cellular energy. These proteins pump protons across cellular membranes through light absorption by the chromophore retinal, and the resulting pH energy gradient can then be used for active membrane transport or for synthesis of adenosine triphosphate. Here, we show that PPR is pervasive in Antarctic phytoplankton, especially in iron-limited regions. In a model SO diatom, we found that it was localized to the vacuolar membrane, making the vacuole a putative alternative phototrophic organelle for light-driven production of cellular energy. Unlike photosynthetic C fixation, which decreases substantially at colder temperatures, the proton transport activity of PPR was unaffected by decreasing temperature. Cellular PPR levels in cultured SO diatoms increased with decreasing iron concentrations and energy production from PPR photochemistry could substantially augment that of PS, especially under high light intensities, where PS is often photoinhibited. PPR gene expression and high retinal concentrations in phytoplankton in SO waters support its widespread use in polar environments. PPRs are an important adaptation of SO phytoplankton to growth and survival in their cold, iron-limited, and variable light environment.

 

Southern Ocean (SO) diatoms play an important role in global carbon flux, and their influence on carbon export is directly linked to interactions with epiphytic bacteria. Bacterial symbionts that increase diatom growth promote atmospheric carbon uptake, while bacterial degraders divert diatom biomass into the microbial loop where it can then be released as carbon dioxide through respiration. To further explore SO diatom-bacterial associations, a natural model system is needed that is representative of these diverse and important interactions. Here, we use concurrent cultivation to isolate a species of the ecologically-important SO diatom, Pseudo-nitzschia subcurvata, and its co-occurring bacteria. Although vitamin-depleted, axenic Pseudo-nitzschia grew poorly in culture, addition of a co-isolated Roseobacter promoted diatom growth, while addition of a co-isolated Flavobacterium negatively impacted diatom growth. Microscopy revealed both bacterial isolates are physically associated with diatom cells and genome sequencing identified important predicted functions including vitamin synthesis, motility, cell attachment mechanisms, and diverse antimicrobial weapons that could be used for interbacterial competition. These findings revealed the natural coexistence of competing symbiotic strategies of diatom-associated bacteria in the SO, and the utility of this tripartite system, composed of a diatom and two bacterial strains, as a co-culture model to probe ecological-relevant interactions between diatoms and the bacteria that compete for access to the phycosphere.

 

Captive specimens in museum collections facilitate study of rare taxa, but the lifestyles, diets, and lifespans of captive animals differ from their wild counterparts. Trabecular bone architecture adapts to in vivo forces, and may reflect interspecific variation in ecology and behavior as well as intraspecific variation between captive and wild specimens. We compared trunk vertebrae bone microstructure in captive and wild xenarthran mammals to test the effects of ecology and captivity. We collected μCT scans of the last six presacral vertebrae in 13 fossorial, terrestrial, and suspensorial xenarthran species (body mass: 120 g to 35 kg). For each vertebra, we measured centrum length; bone volume fraction (BV.TV); trabecular number and mean thickness (Tb.Th); global compactness (GC); cross-sectional area; mean intercept length; star length distribution; and connectivity and connectivity density. Wild specimens have more robust trabeculae, but this varies with species, ecology, and pathology. Wild specimens of fossorial taxa (Dasypus) have more robust trabeculae than captives, but there is no clear difference in bone microstructure between wild and captive specimens of suspensorial taxa (Bradypus, Choloepus), suggesting that locomotor ecology influences the degree to which captivity affects bone microstructure. Captive Tamandua and Myrmecophaga have higher BV.TV, Tb.Th, and GC than their wild counterparts due to captivity-caused bone pathologies. Our results add to the understanding of variation in mammalian bone microstructure, suggest caution when including captive specimens in bone microstructure research, and indicate the need to better replicate the habitats, diets, and behavior of animals in captivity. 

The regionalized vertebral column is a hallmark of mammalian morphology and reflects functional differentiation of the vertebral regions. Mammalian vertebrae are serially homologous and morphologically patterened by Hox expression, but also vary in number and gross morphology across species. The trabecular bone inside vertebral centra is more plastic than gross vertebral bone, and structurally adapts to better withstand forces it experiences during life. However, the functional regionalization of vertebral trabecular bone is poorly examined. Are there trabecular "regions” reflecting the differing functions and in-vivo stress patterns of gross morphological vertebral regions? Or is trabecular morphology homogeneous throughout the spine, suggesting that differences in functional demands are borne exclusively by external characteristics? To address these questions, we collected μCT scans and linear measurements of cervical, thoracic, and lumbar vertebrae in four species of large shrews, including two species of the hero shrew Scutisorex, which has a highly modified vertebral column. We compared linear measurements and trabecular bone characteristics of the cranial and caudal ends of each centrum across species. To detect unique vertebral regions, we executed principal coordinates analysis and segmented regression on three versions of our data set: trabecular bone data only, external measurements only, and the two combined. We found that some regionalization is recovered using only trabecular bone data, but trabecular bone regions do not correspond exactly to gross vertebral regions. This reflects divergence between the functional signals of internal and external vertebral bone morphology, which should be further examined in a kinematic context. 

Captive specimens in natural history collections allow researchers to inspect the morphologies of rare taxa, but the lifestyles,diets, and lifespans of captive animals differ from those of their wild counterparts. To quantify these differences, we compared bone microstructure of trunk vertebrae in captive and wild xenarthran mammals (sloths, armadillos, anteaters). Because trabecular bone architecture (TBA) adapts to in vivo forces, bone microstructure reflects ecology and behavior, but this means that it may differ between captive and wild specimens of the same species. We collected μCT scans of the last six presacral vertebrae in 13 species of fossorial, terrestrial, and suspensorial xenarthrans ranging in body mass from 120g (Chlamyphorus) to 35kg (Myrmecophaga). For each vertebra, we measured bone volume fraction (BVF); trabecular number, mean thickness (TbTh), and orientation; global compactness; and cross sectional area. Wild specimens generally have more robust trabeculae, but this differs based on species, vertebral position, ecology, and pathology. The wild specimens of fossorial taxa (Dasypus) have more robust trabeculae than their captive counterparts, but there is no clear difference in TBA of wild and captive specimens in suspensorial and terrestrial taxa (Bradypus, Choloepus, Cyclopes). These data suggest that locomotor ecology affects the level to which captivity affects bone microstructure. The captive specimens of both Tamandua and Myrmecophaga have higher BVF and TbTh than their wild counterparts, indicating more brittle trabeculae due to bone pathologies caused by captivity. Our results add to the overall understanding of variation in mammalian bone microstructure and suggest caution when including captive specimens in research on TBA. 

The regionalization of the mammalian spinal column is an important evolutionary, developmental, and functional hallmark of the clade. Vertebral column regions are usually defined using transitions in external bone morphology, such as the presence of transverse foraminae or rib facets, or measurements of vertebral shape. Yet the internal structure of vertebrae, specifically the trabecular (spongy) bone, plays an important role in vertebral function, and is subject to the same variety of selective, functional, and developmental influences as external bone morphology. Here, we investigated regionalization of external and trabecular bone morphology in the vertebral column of a group of shrews (family Soricidae). The primary goals of this study were to: (1) determine if vertebral trabecular bone morphology is regionalized in large shrews, and if so, in what configuration relative to external morphology; (2) assess correlations between trabecular bone regionalization and functional or developmental influences; and (3) determine if external and trabecular bone regionalization patterns provide clues about the function of the highly modified spinal column of the hero shrew Scutisorex. Trabecular bone is regionalized along the soricid vertebral column, but the configuration of trabecular bone regions does not match that of the external vertebral morphology, and is less consistent across individuals and species. The cervical region has the most distinct and consistent trabecular bone morphology, with dense trabeculae indicative of the ability to withstand forces in a variety of directions. Scutisorex exhibits an additional external morphology region compared to unmodified shrews, but this region does not correspond to a change in trabecular architecture. Although trabecular bone architecture is regionalized along the soricid vertebral column, and this regionalization is potentially related to bone functional adaptation, there are likely aspects of vertebral functional regionalization that are not detectable using trabecular bone morphology. For example, the external morphology of the Scutisorex lumbar spine shows signs of an extra functional region that is not apparent in trabecular bone analyses. It is possible that body size and locomotor mode affect the degree to which function is manifest in trabecular bone, and broader study across mammalian size and ecology is warranted to understand the relationship between trabecular bone morphology and other measures of vertebral function such as intervertebral range of motion.

 

Biological structures with extreme morphologies are puzzling because they often lack obvious functions and stymie comparisons to homologous or analogous features with more typical shapes. An example of such an extreme morphotype is the uniquely modified vertebral column of the hero shrew Scutisorex , which features numerous accessory intervertebral articulations and massively expanded transverse processes. The function of these vertebral structures is unknown, and it is difficult to meaningfully compare them to vertebrae from animals with known behavioural patterns and spinal adaptations. Here, we use trabecular bone architecture of vertebral centra and quantitative external vertebral morphology to elucidate the forces that may act on the spine of Scutisorex and that of another large shrew with unmodified vertebrae ( Crocidura goliath ). X-ray micro-computed tomography (µCT) scans of thoracolumbar columns show that Scutisorex thori is structurally intermediate between C. goliath and S. somereni internally and externally, and both Scutisorex species exhibit trabecular bone characteristics indicative of higher in vivo axial compressive loads than C. goliath. Under compressive load, Scutisorex vertebral morphology is adapted to largely restrict bending to the sagittal plane (flexion). Although these findings do not solve the mystery of how Scutisorex uses its byzantine spine in vivo , our work suggests potentially fruitful new avenues of investigation for learning more about the function of this perplexing structure.