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While brain size in primates and their relatives within Euarchontoglires is well-studied, less research has examined brain shape, or the allometric trajectories that underlie the relationship between size and shape. Defining these patterns is key to understanding evolutionary trends. 3D geometric morphometric analyses of endocranial shape were performed on 140 species of extant euarchontoglirans using digital cranial endocasts. Principal component analyses on Procrustes shape variables show a clear phylogenetic pattern in endocranial shape, supported by an ANOVA which identified significant differences in shape among several groups (e.g., Platyrrhini, Strepsirrhini, Scandentia, Rodentia, and Lagomorpha). ANOVAs of shape and size also indicate that allometry has a small but significant impact on endocranial shape across Euarchontoglires, with homogeneity of slopes tests finding significant differences in the scaling relationship between shape and size among these same groups. While most of these clades possess a distinct endocranial morphotype, the highly derived platyrrhines display the strongest relationship between size and shape. Rodents show the most diversity in endocranial shape, potentially attributed to their comparatively weak relationship between shape and size. These results suggest fundamental differences in how shape and size covary among Euarchontoglires, which may have facilitated the adaptive radiations that characterize members of this group., (© 2024. The Author(s).)

Landmark-based geometric morphometrics is widely used to study the morphology of the endocast, or internal mold of the braincase, and the diversity associated with this structure across vertebrates. Landmarks, as the basic unit of such methods, are intended to be points of correspondence, selected depending on the question at hand, whose proper definition is essential to guarantee robustness and reproducibility of results. In this study, 20 landmarks are defined to provide a framework to analyze the morphological variability in squamate endocasts. Ten species representing a cross-section of the diversity of Squamata from both phylogenetic and ecological (i.e., habitat) perspectives were considered, to select landmarks replicable throughout the entire clade, regardless of the degree of neuroanatomical resolution of the endocast. To assess the precision, accuracy, and repeatability of these newly defined landmarks, both intraobserver and interobserver error were investigated. Estimates of measurement error show that most of the landmarks established here are highly replicable, and preliminary results suggest that they capture aspects of endocast shape related to both phylogenetic and ecologic signals. This study provides a basis for further examinations of squamate endocast disparity using landmark-based geometric morphometrics., (© 2023 American Association for Anatomy.)

The relatively high level of morphological diversity in Australasian marsupials compared to that observed among American marsupials remains poorly understood. We undertake a comprehensive macroevolutionary analysis of ontogenetic allometry of American and Australasian marsupials to examine whether the contrasting levels of morphological diversity in these groups are reflected in their patterns of allometric evolution. We collate ontogenetic series for 62 species and 18 families of marsupials (n = 2091 specimens), spanning across extant marsupial diversity. Our results demonstrate significant lability of ontogenetic allometric trajectories among American and Australasian marsupials, yet a phylogenetically structured pattern of allometric evolution is preserved. Here we show that species diverging more than 65 million years ago converge in their patterns of ontogenetic allometry under animalivorous and herbivorous diets, and that Australasian marsupials do not show significantly greater variation in patterns of ontogenetic allometry than their American counterparts, despite displaying greater magnitudes of extant ecomorphological diversity., (© 2023. The Author(s).)

The evolution of the remarkably complex primate brain has been a topic of great interest for decades. Multiple factors have been proposed to explain the comparatively larger primate brain (relative to body mass), with recent studies indicating diet has the greatest explanatory power. Dietary specialisations also correlate with dental adaptations, providing a potential evolutionary link between brain and dental morphological evolution. However, unambiguous evidence of association between brain and dental phenotypes in primates remains elusive. Here we investigate the effect of diet on variation in primate brain and dental morphology and test whether the two anatomical systems coevolved. We focused on the primate suborder Strepsirrhini, a living primate group that occupies a very wide range of dietary niches. By making use of both geometric morphometrics and dental topographic analysis, we extend the study of brain-dental ecomorphological evolution beyond measures of size. After controlling for allometry and evolutionary relatedness, differences in brain and dental morphology were found between dietary groups, and brain and dental morphologies were found to covary. Historical trajectories of morphological diversification revealed a strong integration in the rates of brain and dental evolution and similarities in their modes of evolution. Combined, our results reveal an interplay between brain and dental ecomorphological adaptations throughout strepsirrhine evolution that can be linked to diet., Competing Interests: The authors have declared that no competing interests exist.

Bats use their forelimbs in different ways, but flight is the most notable example of morphological adaptation. Foraging and roosting specializations beyond flight have also been described in several bat lineages. Understanding postcranial evolution during the locomotory and foraging diversification of bats is fundamental to understanding bat evolution. We investigated whether different foraging and roosting behaviors influenced humeral cross-sectional shape and biomechanical variation, following Wolff's law of bone remodeling. The effect of body size and phylogenetic relatedness was also tested, in order to evaluate multiple sources of variation. Our results suggest strong ecological signal and no phylogenetic structuring in shape and biomechanical variation in humeral phenotypes. Decoupled modes of scaling of shape and biomechanical variation were consistently indicated across foraging and roosting behaviors, suggesting divergent allometric trajectories. Terrestrial locomoting and upstand roosting species showed unique patterns of shape and biomechanical variation across all our analyses, suggesting that these rare behaviors among bats place unique functional demands on the humerus, canalizing phenotypes. Our results suggest that complex and multiple adaptive pathways interplay in the postcranium, leading to the decoupling of different features and regions of skeletal elements optimized for different functional demands. Moreover, our results shed further light on the phenotypical diversification of the wing in bats and how adaptations besides flight could have shaped the evolution of the bat postcranium., (© 2021 American Association for Anatomy.)

Bats show a remarkable ecological diversity that is reflected both in dietary and foraging guilds (FGs). Cranial ecomorphological adaptations linked to diet have been widely studied in bats, using a variety of anatomical, computational and mathematical approaches. However, foraging-related ecomorphological adaptations and the concordance between cranial and postcranial morphological adaptations remain unexamined in bats and limited to the interpretation of traditional aerodynamic properties of the wing (e.g. wing loading [WL] and aspect ratio [AR]). For this reason, the postcranial ecomorphological diversity in bats and its drivers remain understudied. Using 3D virtual modelling and geometric morphometrics (GMM), we explored the phylogenetic, ecological and biological drivers of humeral morphology in bats, evaluating the presence and magnitude of modularity and integration. To explore decoupled patterns of variation across the bone, we analysed whole-bone shape, diaphyseal and epiphyseal shape. We also tested whether traditional aerodynamic wing traits correlate with humeral shape. By studying 37 species from 20 families (covering all FGs and 85% of dietary guilds), we found similar patterns of variation in whole-bone and diaphyseal shape and unique variation patterns in epiphyseal shape. Phylogeny, diet and FG significantly correlated with shape variation at all levels, whereas size only had a significant effect on epiphyseal morphology. We found a significant phylogenetic signal in all levels of humeral shape. Epiphyseal shape significantly correlated with wing AR. Statistical support for a diaphyseal-epiphyseal modular partition of the humerus suggests a functional partition of shape variability. Our study is the first to show within-structure modular morphological variation in the appendicular skeleton of any living tetrapod. Our results suggest that diaphyseal shape correlates more with phylogeny, whereas epiphyseal shape correlates with diet and FG., (© 2020 Anatomical Society.)

Fluctuating asymmetry (random fluctuations between the left and right sides of the body) has been interpreted as an index to quantify both the developmental instabilities and homeostatic capabilities of organisms, linking the phenotypic and genotypic aspects of morphogenesis. However, studying the ontogenesis of fluctuating asymmetry has been limited to mostly model organisms in postnatal stages, missing prenatal trajectories of asymmetry that could better elucidate decoupled developmental pathways controlling symmetric bone elongation and thickening. In this study, we quantified the presence and magnitude of asymmetry during the prenatal development of bats, focusing on the humerus, a highly specialized bone adapted in bats to perform under multiple functional demands. We deconstructed levels of asymmetry by measuring the longitudinal and cross-sectional asymmetry of the humerus using a combination of linear measurements and geometric morphometrics. We tested the presence of different types of asymmetry and calculated the magnitude of size-controlled fluctuating asymmetry to assess developmental instability. Statistical support for the presence of fluctuating asymmetry was found for both longitudinal and cross-sectional asymmetry, explaining on average 16% of asymmetric variation. Significant directional asymmetry accounted for less than 6.6% of asymmetric variation. Both measures of fluctuating asymmetry remained relatively stable throughout ontogeny, but cross-sectional asymmetry was significantly different across developmental stages. Finally, we did not find a correspondence between developmental patterns of longitudinal and cross-sectional asymmetry, indicating that processes promoting symmetrical bone elongation and thickening work independently. We suggest various functional pressures linked to newborn bats' ecology associated with longitudinal (altricial flight capabilities) and cross-sectional (precocial clinging ability) developmental asymmetry differentially. We hypothesize that stable magnitudes of fluctuating asymmetry across development could indicate the presence of developmental mechanisms buffering developmental instability., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2021 López-Aguirre, Hand, Koyabu, Tu and Wilson.)

Bats are the second-most speciose group of mammals, comprising 20% of species diversity today. Their global explosion, representing one of the greatest adaptive radiations in mammalian history, is largely attributed to their ability of laryngeal echolocation and powered flight, which enabled them to conquer the night sky, a vast and hitherto unoccupied ecological niche. While there is consensus that powered flight evolved only once in the lineage, whether laryngeal echolocation has a single origin in bats or evolved multiple times independently remains disputed. Here, we present developmental evidence in support of laryngeal echolocation having multiple origins in bats. This is consistent with a non-echolocating bat ancestor and independent gain of echolocation in Yinpterochiroptera and Yangochiroptera, as well as the gain of primitive echolocation in the bat ancestor, followed by convergent evolution of laryngeal echolocation in Yinpterochiroptera and Yangochiroptera, with loss of primitive echolocation in pteropodids. Our comparative embryological investigations found that there is no developmental difference in the hearing apparatus between non-laryngeal echolocating bats (pteropodids) and terrestrial non-bat mammals. In contrast, the echolocation system is developed heterotopically and heterochronically in the two phylogenetically distant laryngeal echolocating bats (rhinolophoids and yangochiropterans), providing the first embryological evidence that the echolocation system evolved independently in these bats., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.)

Background: Self-powered flight is one of the most energy-intensive types of locomotion found in vertebrates. It is also associated with a range of extreme morpho-physiological adaptations that evolved independently in three different vertebrate groups. Considering that development acts as a bridge between the genotype and phenotype on which selection acts, studying the ossification of the postcranium can potentially illuminate our understanding of bat flight evolution. However, the ontogenetic basis of vertebrate flight remains largely understudied. Advances in quantitative analysis of sequence heterochrony and morphogenetic growth have created novel approaches to study the developmental basis of diversification and the evolvability of skeletal morphogenesis. Assessing the presence of ontogenetic disparity, integration and modularity from an evolutionary approach allows assessing whether flight may have resulted in evolutionary differences in the magnitude and mode of development in bats., Results: We quantitatively compared the prenatal ossification of the postcranium (24 bones) between bats (14 species), non-volant mammals (11 species) and birds (14 species), combining for the first time prenatal sequence heterochrony and developmental growth data. Sequence heterochrony was found across groups, showing that bat postcranial development shares patterns found in other flying vertebrates but also those in non-volant mammals. In bats, modularity was found as an axial-appendicular partition, resembling a mammalian pattern of developmental modularity and suggesting flight did not repattern prenatal postcranial covariance in bats., Conclusions: Combining prenatal data from 14 bat species, this study represents the most comprehensive quantitative analysis of chiropteran ossification to date. Heterochrony between the wing and leg in bats could reflect functional needs of the newborn, rather than ecological aspects of the adult. Bats share similarities with birds in the development of structures involved in flight (i.e. handwing and sternum), suggesting that flight altriciality and early ossification of pedal phalanges and sternum are common across flying vertebrates. These results indicate that the developmental modularity found in bats facilitates intramodular phenotypic diversification of the skeleton. Integration and disparity increased across developmental time in bats. We also found a delay in the ossification of highly adaptable and evolvable regions (e.g. handwing and sternum) that are directly associated with flight performance.

Most morphological and physiological adaptations associated with bat flight are concentrated in the postcranium, reflecting strong functional demands for flight performance. Despite an association between locomotory diversity and trophic differentiation, postcranial morphological diversity in bats remains largely unexplored. Evolutionary developmental biology is a novel approach providing a link between the analysis of genotypic and phenotypic variation resulting from selective pressures. To quantify the morphological diversity of the postcranium in bats and to explore its developmental basis, we reconstructed the postcranial allometric trajectories of nine bat species from different prenatal developmental series, representing five families and both suborders. We tested for allometric growth in Chiroptera and also quantified levels of allometric disparity and inter-trajectory distances. Using a phylogenetic scaffold, we assessed whether ontogenetic differences reflect evolutionary relationships. We found significant allometric growth trajectories in almost all species. Interspecific trajectory distances showed lower variance within Yinpterochiroptera than within Yangochiroptera and between suborders. Each suborder occupied nonoverlapping sections of allometric space, showing changes in the growth rates of specific bones for each suborder. The allometry-corrected disparity was significantly higher in larger species. Statistically significant phylogenetic signal in our results suggests that there is an ontogenetic basis for the postcranial morphological diversity in modern bats. Ancestral state reconstruction also showed an increase in the amount of change in shape with size in the larger species studied. We hypothesize that differences in allometric patterns among bat taxa may reflect a size-dependent evolutionary constraint, whereby variability in body size and allometric patterns are associated., (© 2019 Wiley Periodicals, Inc.)

Neotropical bats of the genus Carollia are widely studied due to their abundance, distribution and relevance for ecosystems. However, the ecomorphological boundaries of these species are poorly differentiated, and consequently correspondence between their geographic distribution, ecological plasticity and morphological variation remains unclear. In this study, patterns of cranial and mandibular morphological variation were assessed for Carollia brevicauda, C. castanea and C. perspicillata from Colombia. Using geometric morphometrics, morphological variation was examined with respect to: differences in intraspecific variation, morphological modularity and integration, and biogeographic patterns. Patterns of intraspecific variation were different for each species in both cranial and mandibular morphology, with functional differences apparent according to diet. Cranial modularity varied between species whereas mandibular modularity did not. High cranial and mandibular correlation reflects Cranium-Mandible integration as a functional unit. Similarity between the biogeographic patterns in C. brevicauda and C. perspicillata indicates that the Andes do not act as a barrier but rather as an independent region, isolating the morphology of Andean populations of larger-bodied species. The biogeographic pattern for C. castanea was not associated with the physiography of the Andes, suggesting that large body size does not benefit C. brevicauda and C. perspicillata in maintaining homogeneous morphologies among populations.