Daisuke Koyabu

• Ph.D.
• Full Professor at Sun Yat-sen University

Key innovations play a crucial role in driving biodiversity and facilitating evolutionary success by enabling organisms to adapt to various ecological niches through the diversification of phenotypic traits. These innovations have been observed in different vertebrate clades, such as mammals evolving hypsodonty to graze on contemporary grasses and...

Sonic hedgehog ( Shh ) is expressed in the oropharyngeal epithelium, including the frontonasal ectodermal zone (FEZ), which is defined as the boundary between Shh and Fgf8 expression domains in the frontonasal epithelium. To investigate the role of SHH signaling from the oropharyngeal epithelium, we generated mice in which Shh expression is specifi...

Orofacial morphology in mammals plays a critical role in essential life functions such as feeding and communication, which are influenced by the shapes of these anatomical structures. Bats are known to exhibit highly diversified orofacial morphotypes within their clade, reflecting their varied diets and echolocation behaviors. The presence of bony...

Background Mutations in genes encoding spliceosome components result in craniofacial structural defects in humans, referred to as spliceosomopathies. The SF3b complex is a crucial unit of the spliceosome, but model organisms generated through genetic modification of the complex do not perfectly mimic the phenotype of spliceosomopathies. Since the p...

Craniofacial morphology is extremely diversified within bat phylogeny, however growth and development of the palate in bats remains unstudied. The formation of both midline and bilateral orofacial clefts in laryngeally echolocating bats, morphologically similar to the syndromic and non‐syndromic cleft palate in humans, are not well understood. Deve...

Background The hyolaryngeal apparatus generates biosonar pulses in the laryngeally echolocating bats. The cartilage and muscles comprising the hyolarynx of laryngeally echolocating bats are morphologically modified compared to those of non-bat mammals, as represented by the hypertrophied intrinsic laryngeal muscle. Despite its crucial contribution...

Most of over 1400 extant bat species produce high-frequency pulses with their larynx for echolocation. However, the debate about the evolutionary origin of laryngeal echolocation in bats remains unresolved. The morphology of the larynx is known to reflect vocal adaptation and thus can potentially help in resolving this controversy. However, the mor...

Background The hyolaryngeal apparatus generates biosonar pulses in the laryngeally echolocating bats. The cartilage and muscles comprising the hyolarynx of laryngeally echolocating bats are morphologically modified compared to those of non-bat mammals, as represented by the hypertrophied intrinsic laryngeal muscle. Despite its crucial contribution...

Shape measurements are crucial for evolutionary and developmental biology; however, they present difficulties in the objective and automatic quantification of arbitrary shapes. Conventional approaches are based on anatomically prominent landmarks, which require manual annotations by experts. Here, we develop a machine-learning approach by presentin...

This study integrates analyses of mitochondrial DNA sequences and morphological and acoustic data to re-evaluate the taxonomic status of Rhinolophus rex rex , R. r. paradoxolophus and R. schnitzleri throughout their distribution ranges. Based on a dense geographic sampling of specimens hitherto referred to these taxa and contrary to the current tax...

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, t...

Among bats, rhinolophoids and yangochiropterans, but not pteropodids, exhibit laryngeal echolocation. Although Rousettus has been regarded as the only pteropodid capable of echolocation using tongue clicks, recent evidence suggests that other species of pteropodids are also capable of echolocation using wing clicks. Studies on laryngeal echolocator...

Bats can be phylogenetically classified into three major groups: pteropodids, rhinolophoids, and yangochiropterans. While rhinolophoids and yangochiropterans are capable of laryngeal echolocation, pteropodids lack this ability. Delicate ear movements are essential for echolocation behavior in bats with laryngeal echolocation. Caudal auricular muscl...

Shape measurements are crucial for evolutionary and developmental biology; however, they present difficulties in the objective and automatic quantification of arbitral shapes. Conventional approaches are based on anatomically prominent landmarks, which require manual annotations by experts. Here, we present morphological regulated variational AutoE...

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 embryo...

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 communicatio...

The inner ear controls hearing and balance, while the temporal molecular signatures and transcriptional regulatory dynamics underlying its development are still unclear. In this study, we investigated time-series transcriptome in the mouse inner ear from embryonic day 11.5 (E11.5) to postnatal day 7 (P7) using bulk RNA-Seq. A total of 10,822 differ...

Acquiring a subterranean lifestyle entails a substantial shift for many aspects of terrestrial vertebrates’ biology. Although this lifestyle is associated with multiple instances of convergent evolution, the relative success of some subterranean lineages largely remains unexplained. Here, we focus on the mammalian transitions to life underground, q...

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 disea...

The inner ear controls hearing and balance, while the temporal molecular signatures and transcriptional regulatory dynamics underlying its development are still unclear. In this study, we investigated time-series transcriptome in the mouse inner ear from embryonic day 11.5 (E11.5) to postnatal day 7 (P7) using bulk RNA-Seq. A total of 10,822 differ...

The phylogenetic relationships of major groups within the Order Eulipotyphla was once highly disputed, but the advent of molecular studies has greatly improved our understanding about the diversification history of talpids, soricids, erinaceids, and solenodontids. Their resolved phylogenetic relationships now allow us to revisit the turbinal and la...

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,...

During development, the embryonic, cartilaginous skull in vertebrates is partially replaced by bones with endochondral and perichondral ossifications. In order to investigate the association between muscle attachments and early ossifications of late term reptilian embryos, we conducted digital 3d reconstructions of the cranium, the head-, and the n...

The present 3D Dataset contains the 3D models analyzed in: Abel P., Pommery Y., Ford D. P., Koyabu D., Werneburg I. 2022 . Skull sutures and cranial mechanics in the Permian reptile Captorhinus aguti and the evolution of the temporal region in early amniotes. Frontiers in Ecology and Evolution. https://doi.org/10.3389/fevo.2022.841784

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 morpholog...

While most early limbed vertebrates possessed a fully-roofed dermatocranium in their temporal skull region, temporal fenestrae and excavations evolved independently at least twice in the earliest amniotes, with several different variations in shape and position of the openings. Yet, the specific drivers behind this evolution have been only barely u...

Bats are among the few mammals that have acquired a sophisticated echolocation ability, attracting considerable attention for their uniqueness. Over the past 50 years, numerous research projects have been designed to study bat echolocation. The overall trend is complex and the dynamics of those publications are difficult to capture. In this study,...

Constrained & Directional Evolution Newsletter Vol. 5 No. S1 (2021), p. 1-8, cover image, https://www.constrained-evo.shigenobulab.org/docs/CDENewsVol5NoS1.pdf [access: 2024-03-01]. (Extended Abstract)

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 theri...

Microbats are capable of utilising echolocation to perceive their surroundings. They generate ultrasonic pulses from their larynx and receive the echoes via the auditory apparatus. Behavioural studies have revealed that the echolocation behaviour and frequencies adopted among bat species are highly diverse. Therefore, the larynx, which is composed...

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 ho...

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 limit...

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...

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 evolu...

Multiple corrugated cartilaginous structures are formed within the mammalian nasal capsule, eventually developing into turbinals. Due to its complex and derived morphology, the homologies of the bat nasal turbinals have been highly disputed and uncertain. Tracing prenatal development has been proven to provide a means to resolve homological problem...

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 st...

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 unoccu...

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...

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 cr...

The present Dataset contains the 3D model of the male genital organs of greater horseshoe bat, Rhinolophus ferrumequinum. This is the first detailed 3D structure of the soft-tissue genital organs of bats. The 3D model was generated using microCT and techniques of virtual reconstruction.

Significance We report a rare example of a 1.4-million-y-old large bone fragment shaped into handaxe-like form. This bone tool derives from the Konso Formation in southern Ethiopia, where abundant early Acheulean stone artifacts show considerable technological progression between ∼1.75 and <1.0 Mya. Technological analysis of the bone tool indicates...

Bats use their forelimbs in different ways, flight being the most notable example of morphological adaptation. However, different behavioural specializations beyond flight have also been described in several bat lineages. Understanding the postcranial evolution during the locomotory and behavioural diversification of bats is fundamental to understa...

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 selecti...

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...

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 developmen...

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...

Despite the growing literature on the underlying factors of geographical phenotypic variation, little is known about how and to what extent biogeographic barriers in South‐East Asia have shaped morphological variation in primates. We aimed to investigate the geographical variations in skull morphology in dusky leaf monkeys by decomposing them into...

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...

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 hav...

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 excepti...

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 mandubula...

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...

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 e...

The ectotympanic, malleus and incus of the developing mammalian middle ear (ME) are initially attached to the dentary via Meckel’s cartilage, betraying their origins from the primary jawjoint of land vertebrates. This recapitulation has prompted mostly unquantified suggestions that several suspected—but similarly unquantified—key evolutionary trans...

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...

The water deer (Hydropotes inermis) has conventionally been classified into two subspecies according to geographic distribution and pelage color pattern: H. i. inermis from China and H. i. argyropus from Korea. However, the results of a recent molecular study have called this into question. To further reappraise this classification, we examined mor...

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 sh...

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 obse...

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 bo...

The recently increased interest in studies on sequence heterochrony has uncovered developmental variation between species. However, how changes in developmental program are related to shifts in life-history parameters remains largely unsolved. Here we provide the most comprehensive data to date on postcranial ossification sequence of bats and compa...

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 evoluti...

The cavity of the pharynx and hyoid bone of the shoebill (Balaeniceps rex) were examined by using the three dimensional computed tomography image analysis. The pharynx and the cranial part of the esophagus were extraordinarily bilaterally enlarged. The unfixed flexible hyoid bone and degenerated tongue were discerned. We suggest that these morpholo...

We comparatively examined the trunk musculature and prezygapophyseal angle of mid-trunk vertebra in eight urodele species with different locomotive modes (aquatic Siren intermedia, Amphiuma tridactylum, Necturus maculosus and Andrias japonicus; semi-aquatic Cynops pyrrhogaster, Cynops ensicauda; and terrestrial Hynobius nigrescens, Hynobius lichena...

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 pl...

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...

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 t...

Specifications on samples.