Showing papers in "Journal of Morphology in 2015"

Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis.

Abstract: Phylogenetic analyses indicate that viviparity (live-bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid-Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co-opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition.

Details of human middle ear morphology based on micro-CT imaging of phosphotungstic acid stained samples

Abstract: A multitude of morphological aspects of the human middle ear (ME) were studied qualitatively and/or quantitatively through the postprocessing and interpretation of micro-CT (micro X-ray computed tomography) data of six human temporal bones. The samples were scanned after phosphotungstic acid staining to enhance soft-tissue contrast. The influence of this staining on ME ossicle configuration was shown to be insignificant. Through postprocessing, the image data were converted into surface models, after which the approaches diverged depending on the topics of interest. The studied topics were: the ME ligaments; morphometric and mechanical parameters of the ossicles relating to inertia and the ossicular lever arm ratio; the morphology of the distal incus; the contact surface areas of the tympanic membrane (TM) and of the stapes footplate; and the thickness of the TM, round window of the cochlea, ossicle joint spaces, and stapedial annular ligament. Some of the resulting insights are relevant in ongoing discussions concerning ME morphology and mechanical functions, while other results provide quantitative data to add to existing data. All findings are discussed in the light of other published data and many are relevant for the construction of mechanical finite element simulations of the ME. J. Morphol. 276:1025–1046, 2015. © 2015 Wiley Periodicals, Inc.

Differentiation and growth of bone ornamentation in vertebrates: a comparative histological study among the Crocodylomorpha.

Abstract: Bone ornamentation, that is, hollow (pits and grooves) or protruding (ridges) repetitive reliefs on the surface of dermal bones, is a frequent, though poorly studied and understood, feature in vertebrates. One of the most typical examples of this characteristic is given by the Crurotarsi, a taxon formed by the crocodilians and their closest allies, which generally display deep ornamentation on skull roof and osteoderms. However, the ontogenetic process responsible for the differentiation and development of this character remains controversial. This study was conducted to settle the question on histological and microanatomical evidence in several crurotarsan taxa. Observational and experimental data in extant and extinct crocodyliforms show that bone ornamentation is initially created, and later maintained during somatic growth (that is indefinite in crocodilians), by a complex process of bone remodeling comprising local resorption of superficial bone cortices, followed by partial reconstruction. The superficial reliefs of crocodilian dermal bones are thus permanently modified through pit enlargement, drift, stretching, shrinking, or complete filling. Ridges are also remodeled in corresponding ways. These processes allow accommodation of unitary ornamental motifs to the overall dimensions of the bones during growth. A parsimony optimization based on the results of this study, but integrating also published data on bone histology in non-crocodyliform crurotarsans and some non-crurotarsan taxa, suggests that the peculiar mechanism described above for creating and maintaining bone ornamentation is a general feature of the Crurotarsi and is quite distinct from that attributed by previous authors to other vertebrates. J. Morphol. 276:425–445, 2015. © 2014 Wiley Periodicals, Inc.

Fetal adaptations for viviparity in amphibians.

Abstract: Live-bearing has evolved in all three orders of amphibians--frogs, salamanders, and caecilians. Developing young may be either yolk dependent, or maternal nutrients may be supplied after yolk is resorbed, depending on the species. Among frogs, embryos in two distantly related lineages develop in the skin of the maternal parents' backs; they are born either as advanced larvae or fully metamorphosed froglets, depending on the species. In other frogs, and in salamanders and caecilians, viviparity is intraoviductal; one lineage of salamanders includes species that are yolk dependent and born either as larvae or metamorphs, or that practice cannibalism and are born as metamorphs. Live-bearing caecilians all, so far as is known, exhaust yolk before hatching and mothers provide nutrients during the rest of the relatively long gestation period. The developing young that have maternal nutrition have a number of heterochronic changes, such as precocious development of the feeding apparatus and the gut. Furthermore, several of the fetal adaptations, such as a specialized dentition and a prolonged metamorphosis, are homoplasious and present in members of two or all three of the amphibian orders. At the same time, we know little about the developmental and functional bases for fetal adaptations, and less about the factors that drive their evolution and facilitate their maintenance.

Articular soft tissue anatomy of the archosaur hip joint: Structural homology and functional implications

Abstract: Archosaurs evolved a wide diversity of locomotor postures, body sizes, and hip joint morphologies. The two extant archosaurs clades (birds and crocodylians) possess highly divergent hip joint morphologies, and the homologies and functions of their articular soft tissues, such as ligaments, cartilage, and tendons, are poorly understood. Reconstructing joint anatomy and function of extinct vertebrates is critical to understanding their posture, locomotor behavior, ecology, and evolution. However, the lack of soft tissues in fossil taxa makes accurate inferences of joint function difficult. Here, we describe the soft tissue anatomies and their osteological correlates in the hip joint of archosaurs and their sauropsid outgroups, and infer structural homology across the extant taxa. A comparative sample of 35 species of birds, crocodylians, lepidosaurs, and turtles ranging from hatchling to skeletally mature adult were studied using dissection, imaging, and histology. Birds and crocodylians possess topologically and histologically consistent articular soft tissues in their hip joints. Epiphyseal cartilages, fibrocartilages, and ligaments leave consistent osteological correlates. The archosaur acetabulum possesses distinct labrum and antitrochanter structures on the supraacetabulum. The ligamentum capitis femoris consists of distinct pubic- and ischial attachments, and is homologous with the ventral capsular ligament of lepidosaurs. The proximal femur has a hyaline cartilage core attached to the metaphysis via a fibrocartilaginous sleeve. This study provides new insight into soft tissue structures and their osteological correlates (e.g., the antitrochanter, the fovea capitis, and the metaphyseal collar) in the archosaur hip joint. The topological arrangement of fibro- and hyaline cartilage may provide mechanical support for the chondroepiphysis. The osteological correlates identified here will inform systematic and functional analyses of archosaur hindlimb evolution and provide the anatomical foundation for biomechanical investigations of joint tissues.

Bone‐conduction hearing and seismic sensitivity of the late permian anomodont Kawingasaurus fossilis

Abstract: An investigation of the internal cranial anatomy of the anomodont Kawingasaurus from the Upper Permian Usili Formation in Tanzania by means of neutron tomography revealed an unusual inner and middle ear anatomy such as extraordinarily inflated vestibules, lateroventrally orientated stapes with large footplates, and a small angle between the planes of the anterior and lateral semicircular canals. The vestibule has a volume, which is about 25 times larger than the human vestibule, although Kawingasaurus has only a skull length of approximately 40 mm. Vestibule inflation and enlarged stapes footplates are thought to be functionally correlated with bone-conduction hearing; both morphologies have been observed in fossorial vertebrates using seismic signals for communication. The firmly fused triangular head with spatulate snout was probably used for digging and preadapted to seismic signal detection. The quadrate-quadratojugal complex was able to transmit sound from the articular to the stapes by small vibrations of the quadrate process, which formed a ball and socket joint with the squamosal. Mechanical considerations suggest that the ventrolaterally orientated stapes of Kawingasaurus was mechanically better suited to transmit seismic sound from the ground to the fenestra vestibuli than a horizontal orientated stapes. The low sound pressure level transformer ratio of 2–3 in Kawingasaurus points to a seismic sensitivity of the middle ear and a vestigial or reduced sensitivity to airborne sound. Three hypothetical pathways of bone conduction in Kawingasaurus are discussed: 1) sound transmission via the spatulate snout and skull roof to the otic capsules, 2) relative movements resulting from the inertia of the mandible if sound is percepted with the skull, and 3) bone conduction from the substrate via mandible, jaw articulation, and stapes to the inner ear. J. Morphol. 276:121–143, 2015. © 2014 Wiley Periodicals, Inc.

Otolith patterns of rockfishes from the northeastern Pacific

Abstract: Sagitta otolith shape was analysed in twenty sympatric rockfishes off the southern California coast (Northeastern Pacific). The variation in shape was quantified using canonical variate analysis based on fifth wavelet function decomposition of otolith contour. We selected wavelets because this representation allow the identifications of zones or single morphological points along the contour. The entire otoliths along with four subsections (anterior, ventral, posterodorsal, and anterodorsal) with morphological meaning were examined. Multivariate analyses (MANOVA) showed significant differences in the contours of whole otolith morphology and corresponding subsection among rockfishes. Four patterns were found: fusiform, oblong, and two types of elliptic. A redundancy analysis indicated that anterior and anterodorsal subsections contribute most to define the entire otolith shape. Complementarily, the eco-morphological study indicated that the depth distribution and strategies for capture prey were correlated to otolith shape, especially with the anterodorsal zone.

Armored geckos: A histological investigation of osteoderm development in Tarentola (Phyllodactylidae) and Gekko (Gekkonidae) with comments on their regeneration and inferred function.

Abstract: Osteoderms are bone-rich organs found in the dermis of many scleroglossan lizards sensu lato, but are only known for two genera of gekkotans (geckos): Tarentola and Gekko. Here, we investigate their sequence of appearance, mode of development, structural diversity and ability to regenerate following tail loss. Osteoderms were present in all species of Tarentola sampled (Tarentola annularis, T. mauritanica, T. americana, T. crombei, T. chazaliae) as well as Gekko gecko, but not G. smithii. Gekkotan osteoderms first appear within the integument dorsal to the frontal bone or within the supraocular scales. They then manifest as mineralized structures in other positions across the head. In Tarentola and G. gecko, discontinuous clusters subsequently form dorsal to the pelvis/base of the tail, and then dorsal to the pectoral apparatus. Gekkotan osteoderm formation begins once the dermis is fully formed. Early bone deposition appears to involve populations of fibroblast-like cells, which are gradually replaced by more rounded osteoblasts. In T. annularis and T. mauritanica, an additional skeletal tissue is deposited across the superficial surface of the osteoderm. This tissue is vitreous, avascular, cell-poor, lacks intrinsic collagen, and is herein identified as osteodermine. We also report that following tail loss, both T. annularis and T. mauritanica are capable of regenerating osteoderms, including osteodermine, in the regenerated part of the tail. We propose that osteoderms serve roles in defense against combative prey and intraspecific aggression, along with anti-predation functions.

Ontogeny of an iridescent nanostructure composed of hollow melanosomes

Abstract: Iridescent colors in feathers are some of the brightest in nature, and are produced by coherent light scattering from periodic arrangements of melanosomes (melanin-containing organelles). Hollow melanosomes, an evolutionary innovation largely restricted to birds, contain an optically powerful combination of high and low refractive indices (from the melanin and air, respectively) that enables production of brighter and more saturated colors than solid melanosomes. However, despite their significance to avian color and potential utility as optical biomaterials, little is known about the ontogeny of either the melanosomes themselves or the nanostructures they comprise. We used light and electron microscopy to characterize nanostructural development in regenerating feathers of wild turkeys, a species with iridescent color produced by a hexagonally close-packed array of hollow melanosomes. We found that melanosomes form as solid bodies in melanocytes. Later in development, largely after placement in developing barbules, their interiors dissolve and leave hollow cores. These now hollow melanosomes are initially disorganized in the barbule, but become close-packed as they are pulled to the edge of the barbule, likely through a combination of forces including depletion–attraction. These data suggest that these structurally colored tissues are self-assembled and represent novel pathways of development. J. Morphol. 276:378–384, 2015. © 2014 Wiley Periodicals, Inc.

Development and microstructure of tooth histotypes in the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae) and the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae).

Abstract: Elasmobranchs exhibit two distinct arrangements of mineralized tissues in the teeth that are known as orthodont and osteodont histotypes. Tra- ditionally, it has been said that orthodont teeth main- tain a pulp cavity throughout tooth development whereas osteodont teeth are filled with osteodentine and lack a pulp cavity when fully developed. We used light microscopy, scanning electron microscopy, and high-resolution micro-computed tomography to compare the structure and development of elasmobranch teeth representing the two histotypes. As an example of the orthodont histotype, we studied teeth of the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae). For the osteodont histotype, we studied teeth of the great white shark, Carcharodon carcharias (Lamni- formes: Lamnidae). We document similarities and dif- ferences in tooth development and the microstructure of tissues in these two species and review the history of definitions and interpretations of elasmobranch tooth histotypes. We discuss a possible correlation between tooth histotype and tooth replacement and review the history of histotype differentiation in sharks. We find that contrary to a long held misconception, there is no orthodentine in the osteodont teeth of C. carcharias. J. Morphol. 276:797-817, 2015. V C 2015 Wiley Periodicals, Inc.

Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

Abstract: Living vertebrates are divided into those that possess a fully formed and fully mineralised skele- ton (gnathostomes) versus those that possess only unmineralised cartilaginous rudiments (cyclostomes). As such, extinct phylogenetic intermediates of these living lineages afford unique insights into the evolu- tionary assembly of the vertebrate mineralised skeleton and its canonical tissue types. Extinct jawless and jawed fishes assigned to the gnathostome stem evi- dence the piecemeal assembly of skeletal systems, revealing that the dermal skeleton is the earliest mani- festation of a homologous mineralised skeleton. Yet the nature of the primitive dermal skeleton, itself, is poorly understood. This is principally because previous histo- logical studies of early vertebrates lacked a phyloge- netic framework required to derive evolutionary hypotheses. Nowhere is this more apparent than within Heterostraci, a diverse clade of primitive jawless verte- brates. To this end, we surveyed the dermal skeletal histology of heterostracans, inferred the plesiomorphic heterostracan skeleton and, through histological com- parison to other skeletonising vertebrate clades, deduced the ancestral nature of the vertebrate dermal skeleton. Heterostracans primitively possess a four- layered skeleton, comprising a superficial layer of odontodes composed of dentine and enameloid; a com- pact layer of acellular parallel-fibred bone containing a network of vascular canals that supply the pulp canals (L1); a trabecular layer consisting of intersecting radial walls composed of acellular parallel-fibred bone, show- ing osteon-like development (L2); and a basal layer of isopedin (L3). A three layered skeleton, equivalent to the superficial layer L2 and L3 and composed of enam- eloid, dentine and acellular bone, is possessed by the ancestor of heterostracans 1 jawed vertebrates. We conclude that an osteogenic component is plesiomorphic with respect to the vertebrate dermal skeleton. Consequently, we interpret the dermal skeleton of den- ticles in chondrichthyans and jawless thelodonts as independently and secondarily simplified. J. Morphol. 276:657-680, 2015. V C 2015 The Authors Journal of Morphology

The shrew tamed by Wolff's law: Do functional constraints shape the skull through muscle and bone covariation?

Abstract: Bone is a highly plastic tissue that reflects the many potential sources of variation in shape Here, we focus on the functional aspects of bone remodeling We choose the skull for our analyses because it is a highly integrated system that plays a fundamental role in feeding and is thus, likely under strong natural selection Its principal mechanical com- ponents are the bones and muscles that jointly produce bite force and jaw motion Understanding the covaria- tions among these three components is of interest to understand the processes driving the evolution of the feeding apparatus In this study, we quantitatively and qualitatively compare interactions between these three components in shrews from populations known to differ in shape and bite force Bite force was measured in the field using a force transducer and skull shape was quantified using surface geometric morphometric approaches based on mCT-scans of the skulls of same individuals The masseter, temporalis, pterygoideus, and digastricus muscles of these individuals were dis- sected and their cross sectional areas determined Our results show strong correlations between bite force and muscle cross sectional areas as well as between bite force and skull shape Moreover, bite force explains an important amount of skull shape variation We con- clude that interactions between bone shape and muscle characteristics can produce different morpho-functional patterns that may differ between populations and may provide a suitable target for selection to act upon J Morphol 000:000-000, 2014 V C 2014 Wiley Periodicals,

The structure of the gas bladder of the spotted gar, Lepisosteus oculatus.

Abstract: We report here on the macroscopic, light microscopic, and electron microscopic structure of the gas bladder (GB) of the spotted gar, Lepisosteus oculatus. The GB opens into the pharynx, dorsal to the opening of the oesophagus, through a longitudinal slit bordered by two glottal ridges. Caudal to the ridges, the GB is an elongated sac divided into a central duct and right and left lobes. The lobes are formed by a cranio-caudal sequence of large air spaces that open into the central duct. The structure of the GB is that of a membranous sac supported by a system of septa arising from the walls of a central duct. The septa contain variable amounts of striated and smooth muscle might function to maintain the bladder shape and in providing contractile capabilities. The presence of muscle cells, nerves, and neuroepithelial cells in the wall of the GB strongly suggests that GB function is tightly regulated. The central duct and the apical surface of the thickest septa are covered by mucociliated epithelium. Most of the rest of the inner bladder surface is covered by a respiratory epithelium which contains goblet cells and a single type of pneumocyte. These two cell types produce surfactant. The respiratory barrier contains thick areas with fibrillar material and cell prolongations, and thin areas that only contain basement membrane material between the capillary wall and the respiratory epithelium. Lungs and GBs share many anatomical and histological features. There appears to be no clear criterion for structural distinction between these two types of respiratory organs. J. Morphol. 276:90–101, 2015. © 2014 Wiley Periodicals, Inc.

Three-dimensional virtual histology of silurian osteostracan scales revealed by synchrotron radiation microtomography

Abstract: We used propagation phase contrast X-ray synchrotron microtomography to study the three-dimensional (3D) histology of scales of two osteostracans, Tremataspis and Oeselaspis, members of a jawless vertebrate group often cited as the sister group of jawed vertebrates. 3D-models of the canal systems and other internal structures are assembled based on the virtual thin section datasets and compared with previous models based on real thin sections. The primary homology framework of the canal systems in the two taxa is revised and new histological details are revealed based on the results of this work. There is no separation of vascular canals and lower mesh canals in the Tremataspis scale, contrary to previous results. The secondary upper mesh canals have a limited distribution to the anterior region of the Tremataspis scale. The upper and lower mesh canal systems of Tremataspis have different geometries, inferred to reflect different developmental origins: we interpret the upper system as a probable epithelial invagination, the lower system as entirely vascular. Oeselaspis has no equivalent of the upper mesh canal system. The upper mesh canal system of Tremataspis may have been sensory in function. In Oeselaspis, numerous polyp-shaped structures opening from the canal system onto the surface of the scale resemble the innervation tracts for neuromast organs. The growth of the Oeselaspis scale proceeds by addition of small odontodes containing unmineralized lacunae, which may further mineralize and become more compact. Our results highlight that 3D-histological investigation on scales and other dermal skeletons of osteostracans is necessary to fully appreciate the diversity of skeletal histologies in the group. Traditional 3D-models based on thin sections alone are not reliable and should no longer be used as the basis for homology assessments or functional hypotheses. J. Morphol. 276:873–888, 2015. © 2015 Wiley Periodicals, Inc.

Digging adaptation in insectivorous subterranean eutherians. The enigma of Mesoscalops montanensis unveiled by geometric morphometrics and finite element analysis.

Abstract: The enigmatic Early Miocene fossorial mammal Mesoscalops montanensis shows one of the most modified humeri among terrestrial mammals. It has been suggested, on qualitative considerations, that this species has no extant homologues for humerus kinematics and that, functionally, the closest extant group is represented by Chrysochloridae. We combine here three dimensional geometric morphometrics, finite element analysis and phylogenetic comparative methods to explore the shape and mechanical stress states of Mesoscalops montanensis as well as of extant and extinct Talpidae and Chrysochloridae under realistic digging simulations. Evolutionary convergence analyses reveal that the shape of Mesoscalops montanensis represents a unique morphology in the context of fossorial mammals and that its functional performance, albeit superficially similar to that of extant Chrysochloridae, still represents a nonconvergent optimum for adaptation to digging. J. Morphol. 276:1157–1171, 2015. © 2015 Wiley Periodicals, Inc.

Evolutionary morphology of the organ systems in squat lobsters and porcelain crabs (crustacea: Decapoda: Anomala): an insight into carcinization.

Abstract: Porcelain crabs (Porcellanidae) are one of three taxa within anomuran crustaceans (Anomala) which possess a crab-like body form. Curiously, these three lineages evolved this shape independently from true crabs (Brachyura) in the course of the evolutionary process termed carcinization. The entire pleon in porcelain crabs is flexed under the cephalothorax and the carapace is approximately as broad as long. Despite their crab-like habitus, porcelain crabs are phylogenetically nested within squat lobsters (Munidopsidae, Munididae, Galatheidae). With a pleon which is only partly flexed under the cephalothorax and a cephalothorax which is longer than it is broad, squat lobsters represent morphologically intermediate forms between lobster-like and crab-like body shapes. Carcinization has so far mostly been studied with respect to outer morphology; however, it is evident that internal anatomical features are influenced through this change of body shape too. In this paper, the situation in Galatheoidea is elucidated by adding more taxa to existing descriptions of the hemolymph vascular systems and associated structures and organs. Micro-computer tomography and 3D reconstruction provide new insights. Autapomorphic states of various internal anatomical characters are present in nearly all the studied species, also reflecting some degree of anatomical disparity found within Galatheoidea. The ventral vessel system of porcelain crabs differs distinctly from that of squat lobsters. The differences in question are coherent (i.e. structural dependent) with morphological transformations in the integument, such as the shortening of the sternal plastron, which evolved in the course of carcinization. Shifts in the gonads and the pleonal neuromeres are coherent with the loss of the caridoid escape reaction, which in turn is a consequence of carcinization. The arterial transformations, however, are minor compared to other instances of carcinization in anomuran crustaceans since the last common ancestor of squat lobsters and porcelain crabs was already “half carcinized”. J. Morphol. 276:1–21, 2015. © 2014 Wiley Periodicals, Inc.

An examination of the variation in maternal placentae across the genus Poeciliopsis (Poeciliidae).

Abstract: Placentae show considerable diversity in a number of nonmammalian, viviparous organisms, including amphibians, reptilian sauropsids, teleost fish, and chondrichthyes. However, the evolutionary processes driving the evolution of placenta are still debated. In teleost fishes, the genus Poeciliopsis (Poeciliidae) offers a rare opportunity for studying placental evolution: extensive placentation has evolved three independent times within the last 750,000 years and there is substantial interspecific variation in the degree of embryonic, maternal nutrient provisioning and development of the placenta. In poeciliids, the placenta is composed of a hypertrophied maternal follicular epithelium apposed to a highly vascularized embryonic pericardial sac. To better understand placental evolution, we have undertaken a comprehensive comparative study of the maternal follicle in eight closely related Poeciliopsis species that span the range in postfertilization, embryonic, maternal nutrient provisioning (from lecithotrophs, to moderate matrotrophs, to extensive matrotrophs). Using light and scanning electron microscopy, we found that the species that provide extensive postfertilization maternal nutrient provisioning (extensive matrotrophs) have thicker follicles and more extensive folding of the follicular epithelium compared to the lecithotrophs and moderate matrotrophs. Follicle sections and histology revealed that epithelial folds of the extensive matrotrophs are comprised primarily of cuboidal and columnar cells and are richly supplied with capillaries. Among the extensive matrotrophs, enhancements of follicle traits corresponded with increases in the level of maternal nutrient provisioning. Hypertrophied maternal follicles with richly vascularized folds can serve to increase the surface area and, thus, facilitate the transfer of substances between the mother and developing embryo. Finally, we found egg envelopes in the lecithotrophs and moderate matrotrophs, but not in the extensive matrotrophs. Morphological studies, like this one, can provide a better understanding of the natural variation in the structure and functioning of maternal and offspring traits associated with matrotrophy and, thus, insights into the processes driving placental evolution. J. Morphol. 276:707-720, 2015. © 2015 Wiley Periodicals, Inc.

Virtual reconstruction and description of the cranial endocast of Pristerodon mackayi (Therapsida, Anomodontia)

Abstract: The cranial endocast of Pristerodon mackayi is described, which has been virtually reconstructed on the basis of neutron tomographic data. The gross anatomy of the cranial endocast of Pristerodon resembles other nonmammalian synapsids such as Thrinaxodon liorhinus in having a narrow, tubular forebrain, well developed olfactory bulbs, a large parietal foramen and unossified zone. As it is the case in cynodonts the hindbrain of Pristerodon is broader than the mid- and forebrain. Large paraflocculi are developed. The medulla oblongata can be well distinguished from the pons. The pons is divided by a median ridge into two portions. There is no evidence for a neocortex, which seems to be also reflected in the low encephalization quotient of 0.18 estimated according to the method of Eisenberg.

The evolution of digit form in Gonatodes (Gekkota: Sphaerodactylidae) and its bearing on the transition from frictional to adhesive contact in gekkotans.

Abstract: Although the phenomenon of adhesion in geckos has been intensively studied for over 200 years, our understanding of how the morphological apparatus associated with this arose is less clear. Indeed, whether or not all of the intricate morphological hierarchy that is implicated in the attachment and removal of the adhesive setae originated at the same time is unknown. To explore whether setae may have arisen prior to the other parts of this structural hierarchy, we undertook morphological observations of Gonatodes, an ancestrally padless, sphaerodatyline genus known to exhibit the expression of incipient subdigital pads in some species. Focusing on this geographically and morphologically well-circumscribed genus, for which intraspecific relationships are adequately known and ecology is quite well documented, allowed us to deduce trends in digit proportions, shape, scalation, and skeletal structure, and associate these with the micro-ornamentation of the subdigital surfaces. Our findings indicate that in Gonatodes, setae capable of inducing adhesion are present without the modifications of the digital musculotendinous, circulatory and skeletal systems that are generally considered to be necessary for the operation of a functional adhesive apparatus. The acquisition of these latter characteristics (independently in many lineages of gekkotans, and incipiently so in Anolis) may have been preceded by a suite of modifications of the digits that enhanced static clinging in relation to sit-and-wait predation and the ability to take refuge on surfaces unavailable to other taxa. These possibilities await further testing.

Structure, molting, and mineralization of the dorsal ossicle complex in the gastric mill of the blue crab, Callinectes sapidus.

Abstract: This study examined the mesocardiac and urocardiac ossicles in the gastric mill of the blue crab to describe its structure, mineralization, and dynamics throughout the molt cycle, and to assess its possible utility in age determination. Morphologically, the mineralized ossicles are similar to the calcified dorsal carapace having a lamellate structure comprised of sheets of chitin/protein fibrils. Staining with acridine orange showed the same arrangement of an epicuticle, exocuticle, and endocuticle. In much of the mesocardiac and urocardiac ossicles, the endocuticle is very reduced, with the exocuticle predominating; the reverse of the dimensions of the exoskeleton. The lamellate structure of the ossicles was confirmed with scanning electron microscopy; however, elemental mapping by energy-dispersive analysis of X-rays revealed that the ossicles are mineralized with calcium phosphate, in contrast to the calcium carbonate biomineral of the exoskeleton. The medial tooth of the urocardiac ossicle is not calcified, but the epicuticle is highly elaborated and impregnated with silica. Histological examination of the ossicles demonstrated that they are molted during ecdysis, so despite the appearance of bands in the mesocardiac ossicle, it is difficult to hypothesize how the bands could represent a record of chronological age. J. Morphol. 276:1358–1367, 2015. © 2015 Wiley Periodicals, Inc.

The interbranchial lymphoid tissue of Atlantic Salmon (Salmo salar L) extends as a diffuse mucosal lymphoid tissue throughout the trailing edge of the gill filament

Abstract: The teleost gill forms an extensive, semipermeable barrier that must tolerate intimate contact with the surrounding environment and be able to protect the body from external pathogens. The recent discovery of the interbranchial lymphoid tissue (ILT) has initiated an anatomical and functional investigation of the lymphoid tissue of the salmonid gill. In this article, sectioning of gill arches in all three primary planes revealed an elongation of the ILT outward along the trailing edge of the primary filament to the very distal end, a finding not previously described. This newly found lymphoid tissue was investigated using a range of morphological and transcriptional tools. Avoiding potential salinity-related effects, the study focused on two fresh-water life stages-smoltifying juveniles and mature adults. Aggregates of T-cells continuous with the ILT were found within the thick epithelial lining of the trailing edge of the filament in considerably larger numbers than seen in the epithelium of the leading edge and of the interlamellar area. Only a few of these cells were identified as CD8α(+) -cells, and there was a significantly (P < 0.05) higher relative expression of CD4- than of CD8- related genes in all gill segments investigated. Numerous major histocompatibility complex class II(+) -cells were distributed uniformly throughout the filament epithelial tissue. Few Ig(+) -cells were detected. Overall, the morphological features and comparable immune gene expression of the previously described ILT and the filament trailing edge lymphoid tissue suggest a close functional and anatomical relationship. We propose that the anatomical definition of the ILT must be broadened to include both the previously described ILT (to be renamed proximal ILT) and the trailing edge lymphoid tissue (to be named distal ILT). This extended anatomical localisation identifies the ILT as a widely distributed mucosal lymphoid tissue in the gill of Atlantic salmon.

Morphology-function relationships and repeatability in the sperm of Passer sparrows.

Abstract: Sperm performance is likely to be an important determinant of male reproductive success, especially when females copulate with multiple males. Understanding sperm performance is therefore crucial to fully understand the evolution of male reproductive strategies. In this study, we examined the repeatability of sperm morphology and motility measures over three breeding seasons, and we studied relationships between sperm morphology and function. We conducted this study in wild-derived captive house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis). Results for the two species were similar. As predicted from results in other passerine species, total sperm length was highly repeatable across ejaculates, and repeatability for the length of other components was moderate. The repeatability of sperm swimming speed across ejaculates was lower, but statistically significant, suggesting that sperm velocity may be a relatively dynamic trait. Surprisingly, swimming speed did not correlate with the relative length of the midpiece, and it correlated negatively with the relative length of the flagellum and with total sperm length. This pattern is the opposite of what theory predicts and differs from what has been found in house sparrows before. Also contrary to previous work, we found no evidence that total sperm length correlates with sperm longevity. These results therefore highlight the need for a better understanding of relationships between sperm morphology and function in passerine birds. (C) 2014 Wiley Periodicals, Inc. (Less)

Immunolocalization of the telomerase-1 component in cells of the regenerating tail, testis, and intestine of lizards

Abstract: Using an antibody against a lizard telomerase-1 component the presence of telomerase has been detected in regenerating lizard tails where numerous cells are proliferating. Immunoblots showed telomerase positive bands at 75-80 kDa in normal tissues and at 50, 75, and 90 kDa in those regenerating. Immunofluorescence and ultrastructural immunolocalization showed telomerase-immunoreactivity in sparCe (few/diluted) mesenchymal cells of the blastema, early regenerating muscles, perichondrium of the cartilaginous tube, ependyma of the spinal cord, and in the regenerating epidermis. Clusters of gold particles were detected in condensing chromosomes of few mesenchymal and epithelial cells in the regenerating tail, but a low to undetectable labeling in interphase cells. Telomerase-immunoreactivity was intense in the nucleus and sparCe (few/diluted) in the cytoplasm of spermatogonia and spermatocytes and drastically decreased in early spermatids where some nuclear labeling remains. Some intense immunoreactivity was seen in few cells near the basal membrane of intestinal enterocytes or in leukocytes (likely lymphocytes) of the intestine mucosa. In spermatogonia, spermatids and in enterocytes part of the nuclear labeling formed cluster of gold particles in dense areas identified as Cajal Bodies, suggesting that telomerase is a marker for these stem cells. This therefore suggests that also the sparCe (few/diluted) telomerase positive cells detected in the regenerating tail may represent sparCe (few/diluted) stem cells localized in regenerating tissues where transit amplifying cells are instead preponderant to allow for tail growth. This observation supports previous studies indicating that few stem cells are present in the stump after tail amputation and give rise to transit amplifying cells for tail regeneration.

Evolutionary allometry of the thoracolumbar centra in felids and bovids

Abstract: Mammals have evolved a remarkable range of body sizes, yet their overall body plan remains unaltered. One challenge of evolutionary biology is to understand the mechanisms by which this size diversity is achieved, and how the mechanical challenges associated with changing body size are overcome. Despite the importance of the axial skeleton in body support and locomotion, and much interest in the allometry of the appendicular skeleton, little is known about vertebral allometry outside primates. This study compares evolutionary allometry of the thoracolumbar centra in two families of quadrupedal running mammals: Felidae and Bovidae. I test the hypothesis that, as size increases, the thoracolumbar region will resist increasing loads by becoming a) craniocaudally shorter, and b) larger in cross-sectional area, particularly in the sagittal plane. Length, width, and height of the thoracolumbar centra of 23 felid and 34 bovid species were taken. Thoracic, prediaphragmatic, lumbar, and postdiaphragmatic lengths were calculated, and diameters were compared at three equivalent positions: the midthoracic, the diaphragmatic and the midlumbar vertebra. Allometric slopes were calculated using a reduced major axis regression, on both raw and independent contrasts data. Slopes and elevations were compared using an ANCOVA. As size increases the thoracolumbar centra become more robust, showing preferential reinforcement in the sagittal plane. There was less allometric shortening of the thoracic than the lumbar region, perhaps reflecting constraints due to its connection with the respiratory apparatus. The thoracic region was more robust in bovids than felids, whereas the lumbar region was longer and more robust in felids than bovids. Elongation of lumbar centra increases the outlever of sagittal bending at intervertebral joints, increasing the total pelvic displacement during dorsomobile running. Both locomotor specializations and functional regionalization of the axial skeleton appear to have influenced its response to increasing size. J. Morphol. 276:818–831, 2015. © 2015 Wiley Periodicals, Inc.

Structure and function of placental exchange surfaces in goodeid fishes (Teleostei: Atheriniformes)

Abstract: The species of the family Goodeidae have evolved reproductive strategies involving intraovarian gestation, early evacuation of nearly yolk-exhausted embryos from the ovigerous tissue into the ovarian cavity, placental matrotrophy during intraluminal gestation, and the birth of highly developed fry. The inner ovarian lining becomes hypervascularized during gestational periods and functions as the maternal component of the placental association. Embryotrophic liquid is secreted by the inner ovarian epithelium into the ovarian cavity. Comparative electrophoretic analyses of embryotrophe and maternal blood serum provide evidence for the transfer of maternal serum proteins into the embryotrophe. Trophotaeniae, proctodaeal processes of the embryos, provide a surface for nutrient absorption. Endocytic activity was demonstrated by ingestion of unspecific tracer proteins in various species. Moreover, the trophotaenial absorptive cells (TACs) in Ameca splendens ingest various proteins or random copolymers conjugated to colloidal gold as well as radioiodinated proteins in a way that satisfies the criteria of receptor-mediated endocytosis. Several aminopeptidases (APs) on the surface of TACs were identified as protein binding sites as evidenced by inhibition of binding and uptake of marker proteins in the presence of AP substrates or AP inhibitors. Morphological adaptations of the embryonic circulatory system pertaining to nutrient and gas exchange were characterized. The embryonic epidermis comprises two layers of squamous cells closely underlain by a dense capillary net. Efficient gas exchange is facilitated by a thin embryotrophe-blood barrier of both the embryonic skin and the intraovarian lining.

Multilevel analysis of elastic morphology: The mantis shrimp's spring.

Abstract: Spring systems, whether natural or engineered, are composed of compliant and rigid regions. Biological springs are often similar to monolithic structures that distribute compliance and rigidity across the whole system. For example, to confer different amounts of compliance in distinct regions within a single structure, biological systems typically vary regional morphology through thickening or elongation. Here, we analyze the monolithic spring in mantis shrimp (Stomatopoda) raptorial appendages to rapidly acquire or process prey. We quantified the shape of cross-sections of the merus segment of the raptorial appendage. We also examined specific regions of the merus that are hypothesized to either store elastic energy or provide structural support to permit energy storage in other regions of the system. We found that while all mantis shrimp contain thicker ventral bars in distal cross-sections, differences in thickness are more pronounced in high-impact “smasher” mantis shrimp than in the slower-striking “spearer” mantis shrimp. We also found that spearer cross-sections are more circular while those of smashers are more eccentric with elongation along the dorso-ventral axis. The results suggest that the regional thickening of ventral bars provides structural support for resisting spring compression and also reduces flexural stiffness along the system's long axis. This multilevel morphological analysis offers a foundation for understanding the evolution and mechanics of monolithic systems in biology. J. Morphol. 276:1123–1135, 2015. © 2015 Wiley Periodicals, Inc.

Comparative finite element analysis of the cranial performance of four herbivorous marsupials.

Abstract: Marsupial herbivores exhibit a wide variety of skull shapes and sizes to exploit different ecological niches. Several studies on teeth, dentaries, and jaw adductor muscles indicate that marsupial herbivores exhibit different specializations for grazing and browsing. No studies, however, have examined the skulls of marsupial herbivores to determine the relationship between stress and strain, and the evolution of skull shape. The relationship between skull morphology, biomechanical performance, and diet was tested by applying the finite element method to the skulls of four marsupial herbivores: the common wombat (Vombatus ursinus), koala (Phascolarctos cinereus), swamp wallaby (Wallabia bicolor), and red kangaroo (Macropus rufus). It was hypothesized that grazers, requiring stronger skulls to process tougher food, would have higher biomechanical performance than browsers. This was true when comparing the koala and wallaby (browsers) to the wombat (a grazer). The cranial model of the wombat resulted in low stress and high mechanical efficiency in relation to a robust skull capable of generating high bite forces. However, the kangaroo, also a grazer, has evolved a very different strategy to process tough food. The cranium is much more gracile and has higher stress and lower mechanical efficiency, but they adopt a different method of processing food by having a curved tooth row to concentrate force in a smaller area and molar progression to remove worn teeth from the tooth row. Therefore, the position of the bite is crucial for the structural performance of the kangaroo skull, while it is not for the wombat which process food along the entire tooth row. In accordance with previous studies, the results from this study show the mammalian skull is optimized to resist forces generated during feeding. However, other factors, including the lifestyle of the animal and its environment, also affect selection for skull morphology to meet multiple functional demands.

Correlative 3D-imaging of Pipistrellus penis micromorphology: Validating quantitative microCT images with undecalcified serial ground section histomorphology.

Abstract: Detailed knowledge of histomorphology is a prerequisite for the understanding of function, variation, and development. In bats, as in other mammals, penis and baculum morphology are important in species discrimination and phylogenetic studies. In this study, nondestructive 3D-microtomographic (microCT, µCT) images of bacula and iodine-stained penes of Pipistrellus pipistrellus were correlated with light microscopic images from undecalcified surface-stained ground sections of three of these penes of P. pipistrellus (1 juvenile). The results were then compared with µCT-images of bacula of P. pygmaeus, P. hanaki, and P. nathusii. The Y-shaped baculum in all studied Pipistrellus species has a proximal base with two club-shaped branches, a long slender shaft, and a forked distal tip. The branches contain a medullary cavity of variable size, which tapers into a central canal of variable length in the proximal baculum shaft. Both are surrounded by a lamellar and a woven bone layer and contain fatty marrow and blood vessels. The distal shaft consists of woven bone only, without a vascular canal. The proximal ends of the branches are connected with the tunica albuginea of the corpora cavernosa via entheses. In the penis shaft, the corpus spongiosum-surrounded urethra lies in a ventral grove of the corpora cavernosa, and continues in the glans under the baculum. The glans penis predominantly comprises an enlarged corpus spongiosum, which surrounds urethra and baculum. In the 12 studied juvenile and subadult P. pipistrellus specimens the proximal branches of the baculum were shorter and without marrow cavity, while shaft and distal tip appeared already fully developed. The present combination with light microscopic images from one species enabled a more reliable interpretation of histomorphological structures in the µCT-images from all four Pipistrellus species.

A quantitative assessment of bone area increase due to ornamentation in the Crocodylia.

Abstract: Bone ornamentation, in the form of highly repetitive motives created by pits and ridges, is a frequent feature on vertebrate skull roofs and osteoderms. The functional significance of this character remains a matter of controversy and speculation. The many diverging hypotheses proposed to explain it all share a common logical prerequisite: bone ornamentation should increase significantly the surface area of the bones that bear it. In order to test this assumption in the Crocodylia, we developed a method for quantifying the gain in area due to ornamentation using a three-dimensional-surface scanner. On crocodylian osteoderms, the gain in area can be up to 40%, and on the cranial table, it ranges between 10 and 32% in adult specimens (in both cases, it shows substantial differences between the adults of the various species included in the sample). Area gain on the snout is lesser (0–20% in adults), and more variable between species. In general, bone ornamentation is less pronounced, and results in fewer area gains in juvenile specimens. The main morphometric results yielded by this study are discussed in reference to the few comparative data available hitherto, and to the functional interpretations proposed by previous authors. J. Morphol. 276:1183–1192, 2015. © 2015 Wiley Periodicals, Inc.

Functional morphology of the copulatory system of box crabs with long second gonopods (Calappidae, Eubrachyura, Decapoda, Crustacea).

Abstract: Male True Crabs use two pairs of gonopods to deliver mating products during copulation. Commonly, the second pair is shorter than the first pair, and most research to date has focused on species with short second gonopods. We investigated male and female copulatory organs in Calappula saussurei and Calappa pelii, two species of box crabs (Calappidae) with second gonopods which are longer than the first pair. Scanning electron microscopy and histological cross sectioning show that the female copulatory system is unique in several aspects: the genital duct is part concave and part simple type. The seminal receptacle is divided into two chambers, a ventral chamber of ectodermal and mesodermal origin, and a dorsal chamber of ectodermal origin. This dorsal chamber is the location of spermatophore reception during copulation. A sperm plug closes the dorsal chamber off. We propose that long second gonopods deliver male mating products directly into the dorsal chamber. To date, spermatophore reception has been associated with the mesodermal tissue of the seminal receptacle. The copulatory system of box crabs with long second gonopods shows novel deviations from this general pattern.