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Laryngeal echolocation in bats could have evolved following two scenarios: a single origin from a common ancestor or an independent acquisition inside the two clades Yinpterochiroptera and Yangochiroptera. Later, some members of Yinpterochiroptera possibly lost their ability to echolocate. In bats, the larynx produces vocalizations for communication and, in most species, for echolocation. Here, we describe how comparative chiropteran laryngeal morphology is a novel area of research that could improve the understanding of echolocation and may help resolve the evolutionary history of bats. This review provides morphological descriptions and comparisons of the bat larynx and bioacoustics interpretations. We discuss the importance of understanding: (1) laryngeal sound production so it may be linked with the evolution of the chiropteran auditory system; and (2) the evolution of laryngeal morphology to understand the ecological and behavioural aspects of bat biology. We find that a strong phylogenetic signal is potentially the main source explaining macroevolutionary variation in laryngeal form among bats. We predict that the three parameters of sound production in echolocation (frequency, intensity, and rate of calls) are independently modulated by different laryngeal components, but this hypothesis remains understudied in terms of species diversity.

In the last decade, studies integrating palaeontology, embryology and experimental developmental biology have markedly altered our homological understanding of the mammalian skull. Indeed, new evidence suggests that we should revisit and restructure the conventional anatomical terminology applied to the components of the mammalian skull. Notably, these are classical problems that have remained unresolved since the ninteenth century. In this review, I offer perspectives on the overlooked problems associated with the homology, development, and conservatism of the mammalian skull, aiming to encourage future studies in these areas. I emphasise that ossification patterns, bone fusion, cranial sutures and taxon-specific neomorphic bones in the skull are virtually unexplored, and further studies would improve our homological understanding of the mammalian skull. Lastly, I highlight that overlooked bones may exist in the skull that are not yet known to science and suggest that further search is needed. This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

Bats have undergone one of the most drastic limb innovations in vertebrate history, associated with the evolution of powered flight. Knowledge of the genetic basis of limb organogenesis in bats has increased but little has been documented regarding the differences between limb organogenesis in bats and that of other vertebrates. We conducted embryological comparisons of the timelines of limb organogenesis in 24 bat species and 72 non-bat amniotes. In bats, the time invested for forelimb organogenesis has been considerably extended and the appearance timing of the forelimb ridge has been significantly accelerated, whereas the timing of the finger and first appearance of the claw development has been delayed, facilitating the enlargement of the manus. Furthermore, we discovered that bats initiate the development of their hindlimbs earlier than their forelimbs compared with other placentals. Bat neonates are known to be able to cling continuously with their well-developed foot to the maternal bodies or habitat substrates soon after birth. We suggest that this unique life history of neonates, which possibly coevolved with powered flight, has driven the accelerated development of the hindlimb and precocious foot.

Syndromic craniosynostosis (CS) patients exhibit early, bony fusion of calvarial sutures and cranial synchondroses, resulting in craniofacial dysmorphology. In this study, we chronologically evaluated skull morphology change after abnormal fusion of the sutures and synchondroses in mouse models of syndromic CS for further understanding of the disease. We found fusion of the inter-sphenoid synchondrosis (ISS) in Apert syndrome model mice (Fgfr2

The anatomical framework of the jawbones is highly conserved among most of the Osteichthyes, including the tetrapods. However, our recent study suggested that the premaxilla, the rostralmost upper jaw bone, was rearranged during the evolution of therian mammals, being replaced by the septomaxilla at least in the lateral part. In the present study, to understand more about the process of evolution from the ancestral upper jaw to the therian face, we re-examined the development of the therian premaxilla (incisive bone). By comparing mouse, bat, goat, and cattle fetuses, we confirmed that the therian premaxilla has dual developmental origins, the lateral body and the palatine process. This dual development is widely conserved among the therian mammals. Cell-lineage-tracing experiments using Dlx1-CreER

Until recently, bat phylogeny separated megabats (laryngeally non-echolocators) and microbats (all laryngeal echolocators) into two distinct clades. This segregation was consistent with the assumption that laryngeal echolocation was acquired by a common ancestor and inherited by all microchiropterans. Thus, laryngeal echolocation was regarded to have evolved once. Recent advances in bat genome sequencing have added insights regarding the origin of bats and their phylogenetic relationships. The megabats previously thought to be phylogenetically isolated are now sharing a common ancestor with the superfamily Rhinolophoidea, which is constituted of laryngeal echolocators. This new relationship brings a counterpoint regarding the hypothesis of single origin of echolocation, which could have appeared several times independently. Concomitantly, recent studies in bat evolutionary developmental biology have illuminated the importance of characters from embryonic development to discussions of how and when echolocation evolved. Here, we describe how comparative chiropteran laryngeal morphology is a novel area of research that could improve the understanding of echolocation and may help resolve the evolutionary history of bats. This review provides morphological descriptions and comparisons of the larynx, bioacoustics interpretations, and newly developed visualisation approaches (i.e., contrast-enhanced computed tomography). We discuss the importance of understanding (1) laryngeal sound production so it may be linked with the evolution of the Chiropteran auditory system and (2) the evolution of laryngeal morphology to understand the ecological and behavioural aspects of bat biology.

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.

Anatomy of bat genital organs has been conventionally studied by gross and microscopic observations to date. Here, we employ both histological observation and diceCT (diffusible iodine-based contrast-enhanced computed tomography) to study the detailed three-dimensional morphological structure of the male genital organs in bats, using the greater horseshoe bat, Rhinolophus ferrumequinum. This is the first study to three-dimensionally describe the whole reproductive organs of bats in detail. Our highly resolved three-dimensional reconstruction reveals that the male organs of R. ferrumequinum consist of paired testes, epididymides, deferent ducts, and five accessory genital glands. The boundary between the ampullary and vesicular glands has been difficult to identify in previous observations, but our diceCT imaging allowed us to clearly differentiate the two. We found that the ampullary gland is located at the terminal part of the deferent ducts, and the vesicular gland lies distal to the ampullary glands. This species possesses a single and carrot-shaped urethral gland, which is not found in most chiropteran families. The presence of the urethral gland in this species and its secretions suggest that after copulation this species is capable of forming a vaginal plug, which can seal the female’s vaginal orifice to block the entrance of spermatozoa from other males. The presence of the urethral gland and elongated epididymal tail and the fact that some individuals can terminate their hibernation and reactivate imply forced copulation on hibernating females can occur in R. ferrumequinum.

During development, the embryonic cartilaginous skull in most vertebrates is partially replaced by bones with endochondral and perichondral ossifications. Muscle attachments are thought to influence the patterns of ossification and, hence, the differentiation of the skull. To investigate the association between muscle attachments and early ossifications of reptilian embryos, we conducted digital 3D reconstructions of the cranium, the head, and the neck musculature from a histological section series of a late term embryonic tuatara, Sphenodon punctatus, with a total body length of 52 mm. As the sole living rhynchocephalian species, it is an important outgroup in comparative studies of squamate evolution. We found that head and neck muscles are largely associated with early ossification of the basal plate and the palatoquadrate, and with three other ossifications in an older specimen with a total body length of 72 mm. These results suggest that tensile forces resulting from embryonic muscle contraction are largely, but not exclusively, correlated with the area of endochondral ossification in the chondrocranium and palatoquadrate in tuatara. Beyond little-known genetic factors, the complexity of chondrocranial architecture, the progress of its development, and the effect of multiple muscle transmitting forces in the chondrocranium must be considered to provide a more comprehensive discussion of the mechanical properties of the embryonic skull.

Shape analysis of biological data is crucial for investigating the morphological variations during development or evolution. However, conventional approaches for quantifying shapes are difficult as exemplified by the ambiguity in the landmark-based method in which anatomically prominent “landmarks” are manually annotated. In this study, a morphological regulated variational autoencoder (Morpho-VAE) is proposed that conducts image-based shape analysis using imaging processing through a deep-learning framework, thereby removing the need for defining landmarks. The proposed architecture comprises a VAE combined with a classifier module. This integration of unsupervised and supervised learning models (i.e., VAE and classifier modules) is designed to reduce dimensionality by focusing on the morphological features in which the differences between data with different labels are best distinguished. The proposed method is applied to the image dataset of the primate mandible to extract morphological features, which allow us to distinguish different families in a low dimensional latent space. Furthermore, the visualization analysis of decision-making of Morpho-VAE clarifies the area of the mandibular joint that is important for family-level classification. The generative nature of the proposed model is also demonstrated to complement a missing image segment based on the remaining structure. Therefore, the proposed method, which flexibly performs landmark-free feature extraction from complete and incomplete image data is a promising tool for analyzing morphological datasets in biology.AUTHOR SUMMARYShape is the most intuitive visual characteristic; however, shape is generally difficult to measure using a small number of variables. Specifically, for biological data, shape is sometimes highly diverse as it has been acquired through a long evolutionary process, adaptation to environmental factors, etc., which limits the straightforward approach to shape measurement. Therefore, a systematic method for quantifying such a variety of shapes using a low-dimensional quantity is needed. To this end, we propose a novel method that extracts low-dimensional features to describe shapes from image data using machine learning. The proposed method is applied to the primate mandible image data to extract morphological features that reflect the characteristics of the groups to which the organisms belong and then those features are visualized. This method also reconstructs a missing image segment from an incomplete image based on the remaining structure. To summarize, this method is applicable to the shape analysis of various organisms and is a useful tool for analyzing a wide variety of image data, even those with a missing segment.

Significance The anatomical framework of the jaw has traditionally been thought to be highly conserved among vertebrates. However, here we show that the therian-unique face (muzzle) evolved via a drastic alteration of the common pattern of the tetrapod jaw. Through comparative morphological and developmental analyses, we demonstrated that the therian mammal’s premaxilla (rostral-most upper jawbone) is derived from the maxillary prominence of the mandibular arch. The developmental primordium that produces the premaxilla in nonmammalian tetrapods rarely contributes to the upper jaw in therian mammals but rather forms a motile nose. We propose that these previously unrecognized rearrangements allowed key innovations such as the highly sensitive tactile perception and olfactory function in mammalian evolution., The anterior end of the mammalian face is characteristically composed of a semimotile nose, not the upper jaw as in other tetrapods. Thus, the therian nose is covered ventrolaterally by the “premaxilla,” and the osteocranium possesses only a single nasal aperture because of the absence of medial bony elements. This stands in contrast to those in other tetrapods in whom the premaxilla covers the rostral terminus of the snout, providing a key to understanding the evolution of the mammalian face. Here, we show that the premaxilla in therian mammals (placentals and marsupials) is not entirely homologous to those in other amniotes; the therian premaxilla is a composite of the septomaxilla and the palatine remnant of the premaxilla of nontherian amniotes (including monotremes). By comparing topographical relationships of craniofacial primordia and nerve supplies in various tetrapod embryos, we found that the therian premaxilla is predominantly of the maxillary prominence origin and associated with mandibular arch. The rostral-most part of the upper jaw in nonmammalian tetrapods corresponds to the motile nose in therian mammals. During development, experimental inhibition of primordial growth demonstrated that the entire mammalian upper jaw mostly originates from the maxillary prominence, unlike other amniotes. Consistently, cell lineage tracing in transgenic mice revealed a mammalian-specific rostral growth of the maxillary prominence. We conclude that the mammalian-specific face, the muzzle, is an evolutionary novelty obtained by overriding ancestral developmental constraints to establish a novel topographical framework in craniofacial mesenchyme.

Background How bats deviate heterochronically from other mammals remains largely unresolved, reflecting the lack of a quantitative staging framework allowing comparison among species. The standard event system (SES) is an embryonic staging system allowing quantitative detection of interspecific developmental variations. Here, the first SES-based staging system for bats, using Asian parti-colored bat (Vespertilio sinensis) is introduced. General aspects of normal embryonic development and the three-dimensional development of the bat cochlea were described for the first time. Recoding the embryonic staging tables of 18 previously reported bat species and Mus musculus into the SES system, quantitative developmental comparisons were performed. Results It was found that limb bud development of V. sinensis is relatively late among 19 bat species and late limb development is a shared trait of vespertilionid bats. The inner ear cochlear canal forms before the semicircular canal in V. sinensis while the cochlear canal forms after the semicircular canal in non-volant mammals. Conclusions The present approach using the SES system provides a powerful framework to detect the peculiarities of bat development. Incorporating the timing of gene expression patterns into the SES framework will further contribute to the understanding of the evolution of specialized features in bats.

Haeckel's recapitulation theory has been a controversial topic in evolutionary biology. However, we have seen some recent cases applying Haeckel's view to interpret the interspecific variation of prenatal ontogeny. To revisit the validity of Haeckel's recapitulation theory, we take bats that have undergone drastic morphological changes and possess a characteristic ecology as a case study. All members of Rhinolophoidea and Yangochiroptera can generate an ultrasonic pulse from the larynx to interpret surrounding objects (laryngeal echolocation) whereas Pteropodidae lacks such ability. It is known that the petrosal bone is particularly derived in shape and expanded in laryngeal echolocators. If Haeckel's recapitulation theory holds, the formation of this derived trait should occur later than those of other bones. Therefore, we compared the prenatal ossification timing of the petrosal in 15 bat species and five outgroup species. We found that the ossification of the petrosal is accelerated in laryngeal echolocators while it is the last bone to ossify in non-laryngeal echolocating bats and non-volant mammals, which runs counter to the prediction generated by Haeckel's recapitulation theory. We point out the evolutionarily labile nature of trait developmental timing and emphasize that Haeckel's recapitulation theory does not hold in many cases. We caution that generating predictions on ancestral conditions and evolutionary history leading from Haeckel's recapitulation theory is not well supported.

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.

International audience; Yellow house bats (Scotophilus) have been known for centuries as a widespread genus of vesper bats in the Indomalayan Region. Despite this, their taxonomic status and phylogeographical patterns remain unclear due to differing criteria employed by early taxonomists and inconsistencies between morphological and molecular assessments. To address these issues, we undertook a comparative phylogeographic analysis of Asian Scotophilus spp. using integrated genetic and morphological analyses of samples collected across the region. These demonstrate that yellow house bats in Asia can be classified into just two widespread species, namely the smaller S. kuhlii (e.g., FA ≤ 53.1 mm, GLS ≤ 20.18 mm) and the larger S. heathii (e.g., FA ≥ 53.4 mm, GLS ≥ 20.85 mm), which occur in sympatry in different parts of the Indomalayan Region. Although these two sympatric species share similar eco‐ethological preferences, they differ considerably in their geographic distributions and intraspecific variation in mtDNA sequences and morphological traits. These disparities were likely misinterpreted as indicating potential cryptic diversity in previous studies, whereas we suggest they are related to interspecific differences in sex‐biased gene flow and phenotypic plasticity to adapt to varying environments. Our study highlights the importance of using multiple datasets to resolve taxonomic uncertainties and reconstruct demographic and phylogeographic histories of sympatric species.

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.

In the past decade, the early Acheulean before 1 Mya has been a focus of active research. Acheulean lithic assemblages have been shown to extend back to ∼1.75 Mya, and considerable advances in core reduction technologies are seen by 1.5 to 1.4 Mya. Here we report a bifacially flaked bone fragment (maximum dimension ∼13 cm) of a hippopotamus femur from the ∼1.4 Mya sediments of the Konso Formation in southern Ethiopia. The large number of flake scars and their distribution pattern, together with the high frequency of cone fractures, indicate anthropogenic flaking into handaxe-like form. Use-wear analyses show quasi-continuous alternate microflake scars, wear polish, edge rounding, and striae patches along an ∼5-cm-long edge toward the handaxe tip. The striae run predominantly oblique to the edge, with some perpendicular, on both the cortical and inner faces. The combined evidence is consistent with the use of this bone artifact in longitudinal motions, such as in cutting and/or sawing. This bone handaxe is the oldest known extensively flaked example from the Early Pleistocene. Despite scarcity of well-shaped bone tools, its presence at Konso shows that sophisticated flaking was practiced by ∼1.4 Mya, not only on a range of lithic materials, but also occasionally on bone, thus expanding the documented technological repertoire of African Early Pleistocene Homo.

Leaf-eating monkeys (colobines) are a highly diversified subfamily with 61 species in ten genera, in which patterns and constraints of morphological evolution are still poorly resolved. In the present study, we measured the skulls of 452 specimens collected from different museums worldwide. Using one of the most extensive samples ever employed, and geometric morphometric techniques, we aimed to elucidate the evolutionary processes that have led to the craniofacial diversification of colobines. Our comprehensive analyses of the colobine cranium demonstrated that phylogeny is the first order signal to emerge, with clear interspecific patterns of differentiation. Allometric trend constrains shape variation for most colobine taxa, but to a lesser degree than phylogeny. We also confirmed that diet is significantly associated with the variation in cranial shape among colobines. In particular, the mechanical advantage of the masseter for biting at the anterior dentition is linked to seed intake. We postulate that such ecomorphological patterns explain, in part, the non-phylogenetic and non-allometric variations in the colobine skull, and indicate the importance of diet in interspecific resource partitioning, allowing for species coexistence.

Cochlear morphology has been regarded as one of the key traits to understand the origin and evolution of echolocation in bats, given its functionality and performance for receiving echolocation sonar. While numerous researchers have compared adult-stage morphology, few have studied the prenatal development of the cochlea. Here, we provide the first detailed three-dimensional description of the prenatal cranial development in bats, using Rhinolophus thomasi as a model, with particular interest to the petrosal which houses the cochlea. Results revealed that among all cranial bones the onset of the ossification of the petrosal is earlier in R. thomasi when compared to other reported mammals. Generally, the cochlea reaches adult size and shape before or around birth in placental mammals including bats, but we found that its shape and size growths continue until maturity in Rhinolophus species. The relationship of cochlear size and skull size is maintained constant throughout the postnatal ontogeny to adulthood in Rhinolophus, a pattern previously reported neither in any other bats nor other mammals. The peculiar developmental pattern in Rhinolophus possibly allows them to form their characteristically large cochlea and facilitate their distinctive echolocation behavior. A recent study reported that non-echolocating Pteropodidae shares a similar prenatal cochlear size to laryngeal echolocating bats. The apparent resemblance of fetal cochlear size was proposed to be a vestigial signal of large cochlear size in the last common ancestor of bats and thus as supporting evidence for the single origin of laryngeal echolocation. However, results from the present observations suggest that limited aspects of the cochlear development were captured in this previous investigation and that the resulting interpretations may be questionable. We point out that diversity and patterns of cochlear development among bats are still not resolved, and the controversy on the origins of laryngeal echolocation is still open to discussion.

Interspecific diversity exists in cranial suture closure patterns among mammalian species. Suture closure patterns partly reflect phylogenesis, but it has also been claimed that it is influenced by biomechanical factors. Here we provide the first report on the cranial suture closure pattern in water deer. Among cervids, the water deer is an exceptional species, as it is the only one without antlers. Instead, the male water deer possess prominent canines, which are utilized during male-male combats. This unique morphological setting allowed us to examine whether the presence of prominent canines affects cranial suture closure. We found that the only sexual difference in cranial suture closure pattern is the closure of the interfrontal suture in males, which is found in some other cervid species as well. Except for the interfrontal suture closure, timing and sequence of cranial suture closure were comparable between both sexes, suggesting that the presence of prominent canines in males has no influence on cranial suture closure pattern. Our results indicate that interfrontal suture closure in males is a phylogenetic pattern, i.e. an apomorphy for Capreolini, Hydropotini and Alceini.

The mastication system of the southern tamandua (Tamandua tetradactyla) was examined by means of gross anatomy and three dimensional image analysis. Three-dimensional computed tomography image analysis revealed that the mandibles medio-laterally rotated during the mastication. The temporal muscle dorso-medially pull the dorsal part of the mandubular bones, and the masseter muscle latero-rostrally operates the ventro-lateral part of the mandibles. The two muscles may contribute to the opening of the mandibles to enlarge the oral cavity and to house the contractile tongue. In contrast the medial and lateral pterygoid muscles may act as a closer of the mandible to medially pulling the ventro-medial part of the mandibles. The extraordinarily specialized mastication mechanism is functionally similar to that of the giant anteater. Although the muscles of the giant anteater show a more complicated structure in the temporal and masseter muscles than those of the southern tamandua, the weight distributio...

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. Electronic supplementary material The online version of this article (10.1186/s12862-019-1396-1) contains supplementary material, which is available to authorized users.

Habitats of two closely related Japanese field mice, Apodemus argenteus and A. speciosus, broadly overlap in many Japanese forests. A. argenteus being more arboreal and A. speciosus being more terrestrial, it is thought that such ecological segregation allows their sympatric distribution. Comparing these two congeners, whether ecological difference is reflected in postcranial development was examined. Although overall ossification sequences were virtually identical, development of the caudal vertebrae was remarkably earlier in A. argenteus. One of the clearest morphological differences between the two species is the relative length of the tail, which is arguably related to the degree of arboreality. I suggest that accelerated ossification of the caudal vertebrae found in A. argenteus is related to its elongation of the tail.

Mammals feature not only great phenotypic disparity, but also diverse growth and life history patterns, especially in maturity level at birth, ranging from altriciality to precocity. Gestation length, morphology at birth, and other markers of life history are fundamental to our understanding of mammalian evolution. Based on the first synthesis of embryological data and the study of new ontogenetic series, we reconstructed estimates of the ancestral chronology of organogenesis and life-history modes in placental mammals. We found that the ancestor of marsupial and placental mammals was placental-like at birth but had a long, marsupial-like infancy. We hypothesize that mammalian viviparity might have evolved in association with the extension of growth after birth, enabled through lactation, and that mammalian altriciality is inherited from the earliest amniotes. The precocial lifestyle of extant sauropsids and that of many placental mammals were acquired secondarily. We base our conclusions on the best estimates and provide a comprehensive discussion on the methods used and the limitations of our dataset. We provide the most comprehensive embryological dataset ever published, "rescue" old literature sources, and apply available methods and illustrate thus an approach on how to investigate comparatively organogenesis in macroevolution.

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.

Although the sea otter (Enhydra lutris) is a complete aquatic species, spending its entire life in the ocean, it has been considered morphologically to be a semi-aquatic animal. This study aimed to clarify the unique hindlimb morphology and functional adaptations of E. lutris in comparison to other Mustelidae species. We compared muscle mass and bone measurements of five Mustelidae species: the sea otter, Eurasian river otter (Lutra lutra), American mink (Neovison vison), Japanese weasel (Mustela itatsi) and Siberian weasel (M. sibirica). In comparison with the other 4 species, E. lutris possessed significantly larger gluteus, popliteus and peroneus muscles, but smaller adductor and ischiopubic muscles. The popliteus muscle may act as a medial rotator of the crus, and the peroneus muscle may act as an abductor of the fifth toe and/or the pronator of the foot. The bundles of the gluteus superficialis muscle of E. lutris were fused with those of the tensor fasciae latae muscle and gluteofemoralis muscles, and they may play a role in femur abduction. These results suggest that E. lutris uses the abducted femur, medially rotated crus, eversion of the ankle and abducted fifth digit or extended interdigital web as a powerful propulsion generator. Therefore, we conclude that E. lutris is a complete aquatic animal, possessing differences in the proportions of the hindlimb muscles compared with those in other semi-aquatic and terrestrial mustelids.

We investigated ontogenetic changes in the trunk muscles of the Japanese black salamander (Hynobius nigrescens) before, during and after metamorphosis. Given that amphibians change their locomotive patterns with metamorphosis, we hypothesized that they may also change the structure of their trunk muscles. The trunk muscles were macroscopically observed, and the weight ratios of each trunk muscle group were quantified at six different developmental stages. Immediately after hatching, we found that the lateral hypaxial muscle was composed of one thick M. ventralis, from ventral edge of which M. transversus abdominis arose later, followed by M. obliquus externus and M. rectus abdominis. The weight ratios of the dorsal and abdominal muscles to the trunk muscles increased with growth. We suggest that a single thick and large lateral hypaxial muscle facilitates swimming during early developmental stages. The increase in the weight ratios of the dorsal and abdominal muscles with growth possibly assists with gravity resistance necessary for terrestrial life.

Clarification of the trunk structure in Urodela is important in understanding the locomotive evolution of basal tetrapods. The components of the muscular trunk wall among Urodela using different modes of locomotion were compared. Since the whole trunk may be used for swimming and the effect of limbs may be small in the more aquatic species, they showed smaller differences in the trunk muscles among anterior, middle and posterior sections of the trunk. By contrast, in the more terrestrial species, the dorsal and abdominal muscles are larger in the middle section than those in the anterior and posterior sections. High compressive stresses occur in the supporting limbs and their insertion at the trunk on the ventral side, and spread from the forelimbs along the back to the supporting hindlimbs on the dorsal side. Tensile stresses occur in the middle ventral part. The components of the trunk muscles among the three sections may reflect differences in stresses occurring in the trunk of the more terrestrial species. The findings also suggest that in the middle section, larger dorsal muscles for stiffening the back to maintain posture and larger abdominal muscles are responsible for balancing the body weight while it is supported by the limbs in the more terrestrial species.