Search for: All records

Abstract This special issue of The Anatomical Record is inspired by and dedicated to Professor Kunwar P. Bhatnagar, whose lifelong interests in biology, and long career studying bats, inspired many and advanced our knowledge of the world's only flying mammals. The 15 articles included here represent a broad range of investigators, treading topics familiar to Prof. Bhatnagar, who was interested in seemingly every aspect of bat biology. Key topics include broad themes of bat development, sensory systems, and specializations related to flight and diet. These articles paint a complex picture of the fascinating adaptations of bats, such as rapid fore limb development, ear morphologies relating to echolocation, and other enhanced senses that allow bats to exploit niches in virtually every part of the world. In this introduction, we integrate and contextualize these articles within the broader story of bat ecomorphology, providing an overview of each of the key themes noted above. This special issue will serve as a springboard for future studies both in bat biology and in the broader world of mammalian comparative anatomy and ecomorphology. 

Adaptive radiations are bursts in biodiversity that generate new evolutionary lineages and phenotypes. However, because they typically occur over millions of years, it is unclear how their macroevolutionary dynamics vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets-from insects to vertebrates, fruit, nectar, and blood-and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; phyllostomids' initial, higher-level diversification involved an "early burst" in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified within broad adaptive zones, likely reflecting finer-scale niche partitioning. Importantly, the observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the value of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic levels, with early bursts being more common at higher levels. 

Nasal turbinals, scrolled thin bones of the nasal cavity, increase surface area for conditioning inspired air or for olfaction in mammals. To assess function in Eptesicus fuscus (Big Brown Bat), we quantify surface area of respiratory and olfactory turbinals from birth to adult size, using data from microCT scans before and after iodine staining. Surface area of each turbinal is significantly correlated with postnatal age and cranial length. The surface area of the maxilloturbinal and first ethmoturbinal (ET I) grows faster, relative to skull size, than surface area of caudal ethmoturbinals or the frontoturbinal. Histological examination of selected specimens reveals ET I grows disproportionately more presumptive respiratory mucosa than olfactory mucosa, supporting the hypothesis that ET I has a dual function. Lastly, we find that distribution of olfactory mucosa in the caudal nasal cavity diminishes with age. Our findings suggest a reduction in olfactory function in E. fuscus, perhaps due to a diminished role in food acquisition by this aerial insectivore. 

Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size ( i.e. , body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels. 

Abstract Tooth classes are an innovation that has contributed to the evolutionary success of mammals. However, our understanding of the mechanisms by which tooth classes diversified remain limited. We use the evolutionary radiation of noctilionoid bats to show how the tooth developmental program evolved during the adaptation to new diet types. Combining morphological, developmental and mathematical modeling approaches, we demonstrate that tooth classes develop through independent developmental cascades that deviate from classical models. We show that the diversification of tooth number and size is driven by jaw growth rate modulation, explaining the rapid gain/loss of teeth in this clade. Finally, we mathematically model the successive appearance of tooth buds, supporting the hypothesis that growth acts as a key driver of the evolution of tooth number and size. Our work reveal how growth, by tinkering with reaction/diffusion processes, drives the diversification of tooth classes and other repeated structure during adaptive radiations. 

Conventionally, the size, shape, and biomechanics of cartilages are determined by their voluminous extracellular matrix. By contrast, we found that multiple murine cartilages consist of lipid-filled cells called lipochondrocytes. Despite resembling adipocytes, lipochondrocytes were molecularly distinct and produced lipids exclusively through de novo lipogenesis. Consequently, lipochondrocytes grew uniform lipid droplets that resisted systemic lipid surges and did not enlarge upon obesity. Lipochondrocytes also lacked lipid mobilization factors, which enabled exceptional vacuole stability and protected cartilage from shrinking upon starvation. Lipid droplets modulated lipocartilage biomechanics by decreasing the tissue’s stiffness, strength, and resilience. Lipochondrocytes were found in multiple mammals, including humans, but not in nonmammalian tetrapods. Thus, analogous to bubble wrap, superstable lipid vacuoles confer skeletal tissue with cartilage-like properties without “packing foam–like” extracellular matrix. 

Abstract The evolution of complex dentitions in mammals was a major innovation that facilitated the expansion into new dietary niches, which imposed selection for tight form–function relationships. Teeth allow mammals to ingest and process food items by applying forces produced by a third-class lever system composed by the jaw adductors, the cranium, and the mandible. Physical laws determine changes in jaw adductor (biting) forces at different bite point locations along the mandible (outlever), thus, individual teeth are expected to experience different mechanical regimes during feeding. If the mammal dentition exhibits functional adaptations to mandible feeding biomechanics, then teeth are expected to have evolved to develop mechanically advantageous sizes, shapes, and positions. Here, we present bats as a model system to test this hypothesis and, more generally, for integrative studies of mammal dental diversity. We combine a field-collected dataset of bite forces along the tooth row with data on dental and mandible morphology across 30 bat species. We (1) describe, for the first time, bite force trends along the tooth row of bats; (2) use phylogenetic comparative methods to investigate relationships among bite force patterns, tooth, and mandible morphology; and (3) hypothesize how these biting mechanics patterns may relate to the developmental processes controlling tooth formation. We find that bite force variation along the tooth row is consistent with predictions from lever mechanics models, with most species having the greatest bite force at the first lower molar. The cross-sectional shape of the mandible body is strongly associated with the position of maximum bite force along the tooth row, likely reflecting mandibular adaptations to varying stress patterns among species. Further, dental dietary adaptations seem to be related to bite force variation along molariform teeth, with insectivorous species exhibiting greater bite force more anteriorly, narrower teeth and mandibles, and frugivores/omnivores showing greater bite force more posteriorly, wider teeth and mandibles. As these craniodental traits are linked through development, dietary specialization appears to have shaped intrinsic mechanisms controlling traits relevant to feeding performance.