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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

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.

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.

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.

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.

The water deer (Hydropotes inermis) is the only species in the genus Hydropotes, subfamily Hydropotinae, family Cervidae. Two subspecies of water deer have traditionally been recognized. One is the Chinese water deer (H. i. inermis) [26], distributed in the lower Yangtze Basin, west to Hupeh in China [6]. The other is the Korean water deer (H. i. argyropus) [13], distributed throughout the whole of the Korean peninsula [1, 5]. The subspecies classification has been based solely on the pelage color differences between the two populations. The Korean subspecies is reported to have darker pelage, with more reddish coloring in the head region compared to the Chinese subspecies [28]. Otherwise, the 2 subspecies are very similar [28]. A recent molecular study has raised questions about this subspecies classification [17]. The authors studied the mitochondrial DNA (mtDNA) control region (927 bp) and cytochrome b gene (1,140 bp) sequences of both populations. A total of 30 samples from 3 sites in China and 45 samples from 5 sites in Korea were used. The authors demonstrated 2 sympatric mtDNA clades (a major clade from China and Korea and a minor clade from Korea) with an average genetic distance of 2.1% in the control region and 1.3% in the cytochrome b gene, respectively. A total of 35 haplotypes from the control region were detected with more than 50% bootstrap values; a major clade consisted of 27 haplotypes from China and Korea, and a minor clade had 8 haplotypes from Korea. Based on the cytochrome-b gene, 25 haplotypes were identified. A major clade had 17 haplotypes from China and Korea, and a minor clade had 8 haplotypes from Korea. From this finding, the authors concluded that the current subspecific classification based on pelage color cannot be supported and pointed out the need to morphologically reexamine the validity of the conventional subspecies classification. In many cases, morphological variation related to adaptations to local climate is found between “subspecies” (i.e., Bergmann’s rule) [4]. Bergmann’s rule predicts that the average body size of a population in colder areas is generally larger than that in warmer regions due to physiological adaptations to colder environments. Numerous studies have tested Bergmann’s rule, and the results have been equivocal, with some observations being consistent and others being inconsistent with the rule. According to Meiri and Dayan [23], 97 of 149 mammal species from 12 orders (65.1%) follow Bergmann’s rule. They reported that the validity of Bergmann’s rule differed depending on the taxon. For example, Artiodactyla (7 species), Carnivora (43 species), Cetacea (1 species), Chiroptera (13 species), Didelphimorphia (1 species), Diprotodontia (6 species), Hyracoidea (1 species), Insectivora (10 species), Primates (6 species) and Proboscidea (1 species) generally comply with the rule, whereas Rodentia (51 species) does not. Of the orders that do, some include fewer than 10 species or even only one species, which can be problematic for statistical analysis. That study included the order Artiodactyla, which includes the genus Hydropotes. The ranges of the two subspecies of water deer are at notably different latitudes (Chinese population: 30°N and Korean population: 35–38°N; Fig. 1), and the average lowest temperature differs considerably (about 2–8°C in January in the Zhoushan archipelago and about −10°C in January in Korea). In this study, we used skull size as an indicator of Bergmann’s rule, instead of body mass, because skull size and body mass have high correlation [16]. If Bergmann’s rule holds, we would expect to find larger individuals in the Korean population. Fig. 1. Range map of water deer. Gray: original range map, black: distribution map of individuals used in this research. A: Chinese population, B: Korean population (redrawn from Whitehead, 1993). Here, we report the first detailed morphological study of water deer. We examined geographical variation in the skull using 36 measurements and tested the validity of the conventional classification. The difference in sexual dimorphic patterns between the 2 populations was also examined. Based on the results, we suggest the need to reconsider the subspecies classification of water deer.

The sequence of cranial suture closure among cervids is reported to be generally species-specific and highly conservative within species. On the other hand, it is known that intraspecific variation often exists to some extent in other mammalian taxa. Here we studied the cranial suture closures of Capreolus pygargus from Jeju Island and compared it with other cervid species. We found that the timing of the interparietal suture closure is highly variable within C. pygargus. Capreolus capreolus similarly shows intraspecific variation of the interparietal suture closure, whereas other cervid species studied to date do not show any intraspecific variation in the sequence of cranial suture closure. Such high intraspecific variation of the interparietal suture may be a derived character for Capreolus.

Evolution of the middle ear ossicles was a key innovation for mammals, enhancing the transmission of airborne sound. Radiation into various habitats from a terrestrial environment resulted in diversification of the auditory mechanisms among mammals. However, due to the paucity of phylogenetically controlled investigations, how middle ear traits have diversified with functional specialization remains unclear. In order to identify the respective patterns for various lifestyles and to gain insights into fossil forms, we employed a high-resolution tomography technique and compared the middle ear morphology of eulipotyphlan species (moles, shrews and hedgehogs), a group that has radiated into various environments, such as terrestrial, aquatic and subterranean habitats. Three-dimensional geometric morphometric analysis was conducted within a phylogenetically controlled framework. Quantitative shapes were found to strongly reflect the degree of subterranean lifestyle and weakly involve phylogeny. Our analyses demonstrate that subterranean adaptation should include a relatively shorter anterior process of the malleus, an enlarged incus, an enlarged stapes footplate and a reduction of the orbicular apophysis. These traits arguably allow improving low-frequency sound transmission at low frequencies and inhibiting the low-frequency noise which disturbs the subterranean animals in hearing airborne sounds.

The multiple skeletal components of the skull originate asynchronously and their developmental schedule varies across amniotes. Here we present the embryonic ossification sequence of 134 species, covering all major groups of mammals and their close relatives. This comprehensive data set allows reconstruction of the heterochronic and modular evolution of the skull and the condition of the last common ancestor of mammals. We show that the mode of ossification (dermal or endochondral) unites bones into integrated evolutionary modules of heterochronic changes and imposes evolutionary constraints on cranial heterochrony. However, some skull-roof bones, such as the supraoccipital, exhibit evolutionary degrees of freedom in these constraints. Ossification timing of the neurocranium was considerably accelerated during the origin of mammals. Furthermore, association between developmental timing of the supraoccipital and brain size was identified among amniotes. We argue that cranial heterochrony in mammals has occurred in concert with encephalization but within a conserved modular organization., The skeletal components of the skull develop at different times in mammals. Here, Koyabu et al. show that the mode of bone ossification constrains the timing of bone formation and find an association between the developmental timing of the supraoccipital bone and brain size.

Sexual dimorphism in the craniomandibular traits in the Korean water deer Hydropotes inermis argyropus was examined for the first time. Multivariate analyses using only cranial traits showed a clear separation between sexes. However, the separation was not obvious in the discriminant analysis using only mandibular traits. The most clearly dimorphic trait was in the incisive bone breadth, which was about 12% larger in males. The incisive bone width reflects the characteristically large canines in male. In contrast to this, most of the cranial measurements, except for the incisive breadth, were larger in female, indicating a larger overall skull size. Given that males are generally larger than females, this sexually dimorphic pattern is unique among mammals. We propose that factors, for example, a unique parental care, have influenced the larger skull size in the females of this species.

We examined sexual dimorphism in the craniodental traits of the raccoon dog Nyctereutes procyonoides from South Korea. Univariate comparisons of skull (cranium and mandible) and dental measurements revealed a small extent of sexual dimorphism in some measurements. The most indicative dimorphic measurements were the breadths of the upper and lower canines which were around 8% larger in male specimens on average. On the other hand, multivariate analyses using only skull traits showed slightly a clearer separation between sexes than those using only dental ones. This discrepancy may be derived from a higher variability in dental traits than in those of the skull. In conclusion, sexual dimorphism within N. procyonoides of South Korea is present, but was not so pronounced as for other local populations. However, measurements showing significant sexual dimorphism varied between different localities. This suggests that the selective forces acting upon craniodental morphology of each sex vary between populations of the species.

Background Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development. Results An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification). Conclusions The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.

The tympanic ring, malleus and incus of the mammalian middle ear (MME) derive from the ancestral primary jaw joint of land vertebrates. In Mesozoic mammals, evolutionary detachment of the MME from the lower jaw occurred when Meckel’s cartilage - the last connection between MME and dentary – disappeared. This disappearance is famously recapitulated in early mammalian development. Further developmental recapitulation of Mesozoic MME detachment is thought to occur in the form of negative allometry and posterior/medial replacement of MME bones relative to the jaw joint. However, despite being widely accepted, such detailed recapitulation scenarios have never been quantified. Here we show, based on µCT scans of developmental series of several marsupials and monotremes, that negative allometry of MME bones relative to the skull occurs only after MME detachment, ruling it out as a developmental detachment trigger; additionally, there is no positional change of ectotympanic or malleus relative to the dentary. Differential positioning of MME bones in the two monotreme species is also not developmentally recapitulated. Our results challenge the developmental prerequisites of widely accepted evolutionary scenarios regarding MME detachment. Rather, we observe an association of MME detachment and dental eruption, suggesting a detachment trigger relating to the onset of dentary function.

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.

Mammals display a broad spectrum of limb specializations coupled with different locomotor strategies and habitat occupation. This anatomical diversity reflects different patterns of development and growth, including the timing of epiphyseal growth plate closure in the long bones of the skeleton. We investigated the sequence of union in 15 growth plates in the limbs of about 400 specimens, representing 58 mammalian species: 34 placentals, 23 marsupials and one monotreme. We found a common general pattern of growth plate closure sequence, but one that is universal neither between species nor in higher-order taxa. Locomotor habitat has no detectable correlation with the growth plate closure sequence, but observed patterns indicate that growth plate closure sequence is determined more strongly through phylogenetic factors. For example, the girdle elements (acetabulum and coracoid process) always ossify first in marsupials, whereas the distal humerus is fused before the girdle elements in some placentals. We also found that heterochronic shifts (changes in timing) in the growth plate closure sequence of marsupials occur with a higher rate than in placentals. This presents a contrast with the more limited variation in timing and morphospace occupation typical for marsupial development. Moreover, unlike placentals, marsupials maintain many epiphyses separated throughout life. However, as complete union of all epiphyseal growth plates is recorded in monotremes, the marsupial condition might represent the derived state.

Sexual dimorphism in the craniomandibular traits in the Korean water deer Hydropotes inermis argyropus was examined for the first time. Multivariate analyses using only cranial traits showed a clear separation between sexes. However, the separation was not obvious in the discriminant analysis using only mandibular traits. The most clearly dimorphic trait was in the incisive bone breadth, which was about 12% larger in males. The incisive bone width reflects the characteristically large canines in male. In contrast to this, most of the cranial measurements, except for the incisive breadth, were larger in female, indicating a larger overall skull size. Given that males are generally larger than females, this sexually dimorphic pattern is unique among mammals. We propose that factors, for example, a unique parental care, have influenced the larger skull size in the females of this species.

Background Talpids include forms with different degree of fossoriality, with major specializations in the humerus in the case of the fully fossorial moles. We studied the humeral microanatomy of eleven extant and eight extinct talpid taxa of different lifestyles and of two non-fossorial outgroups and examined the effects of size and phylogeny. We tested the hypothesis that bone microanatomy is different in highly derived humeri of fossorial taxa than in terrestrial and semi-aquatic ones, likely due to special mechanical strains to which they are exposed to during digging. This study is the first comprehensive examination of histological parameters in an ecologically diverse and small-sized mammalian clade. Results No pattern of global bone compactness was found in the humeri of talpids that could be related to biomechanical specialization, phylogeny or size. The transition zone from the medullary cavity to the cortical compacta was larger and the ellipse ratio smaller in fossorial talpids than in non-fossorial talpids. No differences were detected between the two distantly related fossorial clades, Talpini and Scalopini. Conclusions At this small size, the overall morphology of the humerus plays a predominant role in absorbing the load, and microanatomical features such as an increase in bone compactness are less important, perhaps due to insufficient gravitational effects. The ellipse ratio of bone compactness shows relatively high intraspecific variation, and therefore predictions from this ratio based on single specimens are invalid.

The homologies of mammalian skull elements are now fairly well established, except for the controversial interparietal bone. A previous experimental study reported an intriguing mixed origin of the interparietal: the medial portion being derived from the neural crest cells, whereas the lateral portion from the mesoderm. The evolutionary history of such mixed origin remains unresolved, and contradictory reports on the presence or absence and developmental patterns of the interparietal among mammals have complicated the question of its homology. Here we provide an alternative perspective on the evolutionary identity of the interparietal, based on a comprehensive study across more than 300 extinct and extant taxa, integrating embryological and paleontological data. Although the interparietal has been regarded as being lost in various lineages, our investigation on embryos demonstrates its presence in all extant mammalian "orders." The generally accepted paradigm has regarded the interparietal as consisting of two elements that are homologized to the postparietals of basal amniotes. The tabular bones have been postulated as being lost during the rise of modern mammals. However, our results demonstrate that the interparietal consists not of two but of four elements. We propose that the tabulars of basal amniotes are conserved as the lateral interparietal elements, which quickly fuse to the medial elements at the embryonic stage, and that the postparietals are homologous to the medial elements. Hence, the dual developmental origin of the mammalian interparietal can be explained as the evolutionary consequence of the fusion between the crest-derived "postparietals" and the mesoderm-derived "tabulars.", ヒトをはじめとする哺乳類の頭蓋骨の進化的起源を解明. 京都大学プレスリリース. 2012-08-14.