Daisuke Koyabu

City University of Hong Kong, Jockey Club College of Veterinary Medicine and Life Sciences, Faculty Member

The University of Tokyo, The University Museum, Assistant Professor

Followers

Following

Co-author

Public Views

Main interest: evolutionary morphology & comparative anatomy of the mammalian cranium.

less

Norberto Giannini

James Cotton

The Wellcome Trust Sanger Institute

Stephen Rossiter

Queen Mary, University of London

Gregg F. Gunnell

Burton Lim

Royal Ontario Museum

Mette E Steeman

Museum of Southern Jutland

Ronald Van Den Bussche

Santiago Hernández Del Pino

CONICET - CCT-MENDOZA

Geeta Eick

Adriana Jerez

Universidad Nacional de Colombia

InterestsView All (10)

Uploads

Papers by Daisuke Koyabu

Prenatal cranial bone development of Thomas's horseshoe bat (Rhinolophus thomasi): with special reference to petrosal morphology

by Taro Nojiri and Daisuke Koyabu

Cochlear morphology has been regarded as one of the key traits to understand the origin and evolu... more 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 post-natal 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 laryn-geal 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. K E Y W O R D S bony labyrinth, ear, echolocation, evo-devo, Haeckel's recapitulation theory, ossification

Download

Mammalian development does not recapitulate suspected key transformations in the evolution of the mammalian middle ear

Cranial morphological homogeneity in two subspecies of water deer in China and Korea

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 7, 2015

The water deer (Hydropotes inermis) has conventionally been classified into two subspecies accord... more 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 morphological variation in craniodental measurements of these two subspecies. Results of univariate and multivariate analyses demonstrated that these two subspecies are not well-differentiated, suggesting that individuals of the two populations share common morphological traits. Despite the distribution of the subspecies at different latitudes, no clear morphocline was detected, suggesting that Bergmann's rule does not apply in this case. Discriminant analysis indicated that the characteristics of individuals are shared by both populations, suggesting that not all individuals can be assigned to their original population. Results of princi...

Positional strategy of trunk muscles among aquatic, semi-aquatic and terrestrial species in Urodela

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 6, 2015

Clarification of the trunk structure in Urodela is important in understanding the locomotive evol... more 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 t...

Ontogenetic changes of trunk muscle structure in the Japanese black salamander (Hynobius nigrescens)

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 30, 2015

We investigated ontogenetic changes in the trunk muscles of the Japanese black salamander (Hynobi... more 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 pos...

Furuuchi et al. 2013 in press

Functional Morphology of the Enlarged Pharynx and Hyoid Bone of the Shoebill

Japanese Journal of Zoo and Wildlife Medicine, 2014

ABSTRACT The cavity of the pharynx and hyoid bone of the shoebill (Balaeniceps rex) were examined... more ABSTRACT 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 morphological characteristics functionally enable the species to receive the large prey item peculiar to the feeding behavior of the shoebill. The structure of the pharynx region may totally act as a flexible pouch to pass the large food to the alimentary tract. The bilateral asymmetry was also confirmed in the hyoid bone, cavities of the pharynx and cranial esophagus. We think that these asymmetrical forms may also contribute to the deglutition of large prey fish in the shoebill.

Physiological Cross-Sectional Area of the Masticatory Muscles in the Giraffe ( Giraffa camelopardalis )

Mammal Study, 2013

Download

Heterochrony and post‐natal growth in mammals–an examination of growth plates in limbs

Comparative functional anatomy of hindlimb muscles and bones with reference to aquatic adaptation of the sea otter

Journal of Veterinary Medical Science, 2015

Although the sea otter (Enhydra lutris) is a complete aquatic species, spending its entire life i... more 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 four 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.

Patterns of postcranial ossification and sequence heterochrony in bats: Life histories and developmental trade-offs

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2014

How changes in development are related to shifts in life-history parameters has been a central qu... more How changes in development are related to shifts in life-history parameters has been a central question for studies of heterochrony. Sequence heterochronies have the potential to lead to differences in morphology between species, and it is hence regarded that evolutionary changes in developmental sequences contribute to modifying the function of morphological traits (Alberch and Alberch, '81; Shubin and Alberch, '86; Alberch and Blanco, '96; Jeffery et al., 2002a,b; Wilson and Sánchez-

Download

Phylogenetic Position of Callosciurus erythraeus griseimanus from Vietnam in the Genus Callosciurus

Mammal Study, 2013

Sexual Dimorphism of Craniomandibular Size in the Korean Water Deer, Hydropotes inermis argyropus

Journal of Veterinary Medical Science, 2013

Sexual dimorphism in the craniomandibular traits in the Korean water deer Hydropotes inermis argy... more 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.

Heterochrony and post-natal growth in mammals - an examination of growth plates in limbs

Journal of Evolutionary Biology, 2014

Mammals display a broad spectrum of limb specializations coupled with different locomotor strateg... more 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.

Download

Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals

BMC Evolutionary Biology, 2013

Background: Talpids include forms with different degree of fossoriality, with major specializatio... more 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.

Download

Locomotion pattern and trunk musculoskeletal architecture among Urodela

Acta Zoologica, 2014

We comparatively examined the trunk musculature and prezygapophyseal angle of mid-trunk vertebra ... more 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 lichenatus and Ambystoma tigrinum). We found that the more terrestrial species were characterized by larger dorsal and abdominal muscle weight ratios compared with those of the more aquatic species, whereas muscle ratios of the lateral hypaxial musculature were larger in the more aquatic species. The lateral hypaxial muscles were thicker in the more aquatic species, whereas the M. rectus abdominis was more differentiated in the more terrestrial species. Our results suggest that larger lateral hypaxial muscles function for lateral bending during underwater locomotion in aquatic species. Larger dorsalis and abdominal muscles facilitate resistance against sagittal extension of the trunk, stabilization and support of the ventral contour line against gravity in terrestrial species. The more aquatic species possessed a more horizontal prezygapophyseal angle for more flexible lateral locomotion. In contrast, the more terrestrial species have an increasingly vertical prezygapophyseal angle to provide stronger column support against gravity. Thus, we conclude trunk structure in urodeles differs clearly according to their locomotive modes.

Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size

The multiple skeletal components of the skull originate asynchronously and their developmental sc... more 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.

Download

Functional Morphology of the Aardvark Tail

Summary The musculoskeletal system of the aardvark (Orycteropus afer) tail was morphologically ex... more Summary The musculoskeletal system of the aardvark (Orycteropus afer) tail was morphologically examined in two adult specimens. The tail musculature comprised three muscular groups, viz. a dorsal sacrocaudal system that consisted of the irregularly oriented Musculus sacrocaudalis dorsalis medialis and M. sacrocaudalis dorsalis lateralis, a lateral inter-vertebral connecting system, and a ventral sacrocaudal system characterized by the thick M. sacrocaudalis ventralis lateralis and M. sacrocaudalis ventralis medialis.

Sexual Dimorphism of Craniodental Morphology in the Raccoon Dog Nyctereutes procyonoides from South Korea.

We examined sexual dimorphism in the craniodental traits of the raccoon dog Nyctereutes procyonoi... more 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.

Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal

The homologies of mammalian skull elements are now fairly well established, except for the contro... more 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." embryology | morphological evolution | synapsids | fossil | occipital

Download

Prenatal cranial bone development of Thomas's horseshoe bat (Rhinolophus thomasi): with special reference to petrosal morphology

by Taro Nojiri and Daisuke Koyabu

Download

Mammalian development does not recapitulate suspected key transformations in the evolution of the mammalian middle ear

Cranial morphological homogeneity in two subspecies of water deer in China and Korea

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 7, 2015

Positional strategy of trunk muscles among aquatic, semi-aquatic and terrestrial species in Urodela

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 6, 2015

Ontogenetic changes of trunk muscle structure in the Japanese black salamander (Hynobius nigrescens)

The Journal of veterinary medical science / the Japanese Society of Veterinary Science, Jan 30, 2015

Furuuchi et al. 2013 in press

Functional Morphology of the Enlarged Pharynx and Hyoid Bone of the Shoebill

Japanese Journal of Zoo and Wildlife Medicine, 2014

Physiological Cross-Sectional Area of the Masticatory Muscles in the Giraffe ( Giraffa camelopardalis )

Mammal Study, 2013

Download

Heterochrony and post‐natal growth in mammals–an examination of growth plates in limbs

Comparative functional anatomy of hindlimb muscles and bones with reference to aquatic adaptation of the sea otter

Journal of Veterinary Medical Science, 2015

Patterns of postcranial ossification and sequence heterochrony in bats: Life histories and developmental trade-offs

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2014

Download

Phylogenetic Position of Callosciurus erythraeus griseimanus from Vietnam in the Genus Callosciurus

Mammal Study, 2013

Sexual Dimorphism of Craniomandibular Size in the Korean Water Deer, Hydropotes inermis argyropus

Journal of Veterinary Medical Science, 2013

Heterochrony and post-natal growth in mammals - an examination of growth plates in limbs

Journal of Evolutionary Biology, 2014

Download

Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals

BMC Evolutionary Biology, 2013

Download

Locomotion pattern and trunk musculoskeletal architecture among Urodela

Acta Zoologica, 2014

Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size

Download

Functional Morphology of the Aardvark Tail

Sexual Dimorphism of Craniodental Morphology in the Raccoon Dog Nyctereutes procyonoides from South Korea.

Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal

Download

Daisuke Koyabu

Related Authors

Uploads

Papers by Daisuke Koyabu

Log In