Scaleless Skin Research Articles

The internal braincase anatomy of Thalattosuchus superciliosus – with implications for the endocranial evolution of metriorhynchid crocodylomorphs

ABSTRACT Thalattosuchian crocodylomorphs underwent a major evolutionary transition, evolving from semiaquatic forms reminiscent of extant crocodylians, into pelagic marine forms with flippers, a tail fin and smooth scaleless skin. These fully aquatic forms – the Metriorhynchidae – evolved a novel suite of endocranial anatomies hypothesised to be related to living in saltwater. However, much remains to be discovered about the evolution of these internal braincase structures. Herein, we describe the endocranial anatomy of an early diverging metriorhynchid, Thalattosuchus superciliosus, using microfocus computed tomography (μCT) data and three-dimensional modelling. We compared it against geosaurine and metriorhynchine metriorhynchids, as well as the early diverging metriorhynchoid Pelagosaurus. We found that non-geosaurine metriorhynchids differ from geosaurines in having less laterally expanded cerebral hemispheres, shallower curvatures of the brain’s dorsal margin, and lacking the ventral deflection of the pneumatic diverticulum ventral to the pituitary fossa chamber. However, early-diverging metriorhynchids have well-defined otoccipital diverticula and lacked the ‘extreme pelagic’ endosseous labyrinth morphology. We hypothesise that early metriorhynchids were not adapted to a sustained pursuit lifestyle. Moreover, we posit that within both metriorhynchid subfamilies there was parallel evolution towards becoming pursuit predators.

Chromosome-Level Genome Assembly of Protosalanx chinensis and Response to Air Exposure Stress.

Protosalanx chinensis is a suitable particular species for genetic studies on nearly scaleless skin, transparency and high sensitivity to hypoxia stress. Here, we generated a high-quality chromosome-level de novo assembly of P. chinensis. The final de novo assembly yielded 379.47 Mb with 28 pseudo-chromosomes and a scaffold N50 length of 14.52 Mb. In total, 21,074 protein-coding genes were predicted. P. chinensis, Esox lucius and Hypomesus transpacificus had formed a clade, which diverged about 115.5 million years ago. In the air exposure stress experiment, we found that some genes play an essential role during P. chinensis hypoxia, such as bhlh, Cry1, Clock, Arntl and Rorb in the circadian rhythm pathway. These genomic data offer a crucial foundation for P. chinensis ecology and adaptation studies, as well as a deeper understanding of the response to air exposure stress.

An ancestral hard-shelled sea turtle with a mosaic of soft skin and scutes

The transition from terrestrial to marine environments by secondarily aquatic tetrapods necessitates a suite of adaptive changes associated with life in the sea, e.g., the scaleless skin in adult individuals of the extant leatherback turtle. A partial, yet exceptionally preserved hard-shelled (Pan-Cheloniidae) sea turtle with extensive soft-tissue remains, including epidermal scutes and a virtually complete flipper outline, was recently recovered from the Eocene Fur Formation of Denmark. Examination of the fossilized limb tissue revealed an originally soft, wrinkly skin devoid of scales, together with organic residues that contain remnant eumelanin pigment and inferred epidermal transformation products. Notably, this stem cheloniid—unlike its scaly living descendants—combined scaleless limbs with a bony carapace covered in scutes. Our findings show that the adaptive transition to neritic waters by the ancestral pan-chelonioids was more complex than hitherto appreciated, and included at least one evolutionary lineage with a mosaic of integumental features not seen in any living turtle.

A new species of Stoliczkia Jerdon, 1870 (Serpentes: Xenodermidae) from Mizoram, India.

We describe a new species of Stoliczkia from Mizoram, India. Stoliczkia vanhnuailianai sp. nov. is identified as a member of the genus Stoliczkia by distinct scale arrangements on the posterior of the head, and by scales on the body being separated by scaleless skin, and it differs from the two known congeners in body and head scalation. This is only the third specimen of Stoliczkia collected from India, and the sixth reported specimen for the genus. A revised key to the identification of the species of Stoliczkia is provided.

Soft-tissue evidence for homeothermy and crypsis in a Jurassic ichthyosaur.

Ichthyosaurs are extinct marine reptiles that display a notable external similarity to modern toothed whales. Here we show that this resemblance is more than skin deep. We apply a multidisciplinary experimental approach to characterize the cellular and molecular composition of integumental tissues in an exceptionally preserved specimen of the Early Jurassic ichthyosaur Stenopterygius. Our analyses recovered still-flexible remnants of the original scaleless skin, which comprises morphologically distinct epidermal and dermal layers. These are underlain by insulating blubber that would have augmented streamlining, buoyancy and homeothermy. Additionally, we identify endogenous proteinaceous and lipid constituents, together with keratinocytes and branched melanophores that contain eumelanin pigment. Distributional variation of melanophores across the body suggests countershading, possibly enhanced by physiological adjustments of colour to enable photoprotection, concealment and/or thermoregulation. Convergence of ichthyosaurs with extant marine amniotes thus extends to theultrastructural and molecular levels, reflecting the omnipresent constraints of their shared adaptation to pelagic life.

Whole genome sequencing of Chinese clearhead icefish, Protosalanx hyalocranius.

Background: Chinese clearhead icefish, Protosalanx hyalocranius, is a representative icefish species with economic importance and special appearance. Due to its great economic value in China, the fish was introduced into Lake Dianchi and several other lakes from the Lake Taihu half a century ago. Similar to the Sinocyclocheilus cavefish, the clearhead icefish has certain cavefish-like traits, such as transparent body and nearly scaleless skin. Here, we provide the whole genome sequence of this surface-dwelling fish and generated a draft genome assembly, aiming at exploring molecular mechanisms for the biological interests. Findings: A total of 252.1 Gb of raw reads were sequenced. Subsequently, a novel draft genome assembly was generated, with the scaffold N50 reaching 1.163 Mb. The genome completeness was estimated to be 98.39 % by using the CEGMA evaluation. Finally, we annotated 19 884 protein-coding genes and observed that repeat sequences account for 24.43 % of the genome assembly. Conclusion: We report the first draft genome of the Chinese clearhead icefish. The genome assembly will provide a solid foundation for further molecular breeding and germplasm resource protection in Chinese clearhead icefish, as well as other icefishes. It is also a valuable genetic resource for revealing the molecular mechanisms for the cavefish-like characters.

Contrasting expression of immune genes in scaled and scaleless skin of Atlantic salmon infected with young stages of Lepeophtheirus salmonis

Atlantic salmon skin tissues with and without scales were taken from two preferred sites of salmon louse (Lepeophtheirus salmonis) attachment, behind the dorsal fin (scaled) and from the top of the head (scaleless), respectively. Tissues were profiled by qPCR of 32 genes to study responses to copepodids, 4 days post infection (dpi), and during the moult of copepodids to the chalimus stage, at 8 dpi. Basal/constitutive differences were found for many immune-related genes between the two skin sites; e.g., mannose binding protein C was over 100 fold higher expressed in the scaled skin from the back in comparison to the skin without scales from the head. With lice-infection, at 4 dpi most genes in both tissues showed lower values than in the non-infected control. By 8 dpi, the majority of responses increased towards the control levels, including cytokines of Th1, Th17 and Th2 pathways. Immunohistochemistry of three immune factors revealed an even distribution of MHC class II positive cells throughout epidermis, including the top layer of keratinocytes, marked compartmentalization of Mx+ and CD8α+ cells close to stratum basale, and an increase in numbers of CD8α+ cells in response to infection. In conclusion, suppression of immune genes during the copepodid stage likely sets off a beneficial situation for the parasite. At the moult to chalimus stage 8 dpi, only few genes surpassed the non-infected control levels, including CD8α. The gene expression pattern was reflected in the increased number of CD8α expressing cells, thus revealing a relatively minor activation of skin T-cell defenses in Atlantic salmon in response to L. salmonis infection.

Toxic coral gobies reduce the feeding rate of a corallivorous butterflyfish on Acropora corals

The obligate coral-dwelling gobiid genus Gobiodon inhabits Acropora corals and has developed various physiological, morphological and ethological adaptations towards this life habit. While the advantages of this coral-fish association are well documented for Gobiodon, possible fitness-increasing factors for the host coral are unknown. This study examines the influence of coral-dwelling gobies on the feeding behaviour of obligate corallivorous butterflyfishes. In an aquarium experiment using video observation, the corallivorous butterflyfish Chaetodon austriacus fed significantly less on corals inhabited by two Gobiodon species compared to unoccupied coral colonies of similar size. The more agonistic species G. histrio, which mostly displayed directed movements towards butterflyfishes, decreased butterflyfish bite rate by 62–98 % compared to uninhabited colonies. For Gobiodon sp. 3, which mostly displayed undirected movements in response to visits by C. austriacus, bite rate reduction was 64–68 %. The scale-less skin of Gobiodon spp. is covered by mucus that is toxic and multi-functional by reducing predation as well as affecting parasite attachment. A choice flume experiment suggests that the highly diluted skin mucus of Gobiodon spp. also functions as a corallivore repellent. This study demonstrates that Gobiodon spp. exhibit resource defence against coral-feeding butterflyfishes and also that coral colonies without resident Gobiodon suffer higher predation rates. Although the genus Gobiodon is probably a facultative corallivore, this study shows that by reducing predation on inhabited colonies by other fishes, these obligate coral-dwellers either compensate for their own fitness-decreasing impact on host colonies or live in a mutualistic association with them.

Smart as a frog

Studies in frogs have demonstrated for the first time the in vivo induction of defense peptides in a vertebrate. The soft, scale-less skin of frogs, coupled with the moist, warm environments inhabited by these amphibians, is an ideal breeding ground for microbial pathogens. The skin glands of frogs provide relief from this onslaught by secreting an array of structurally diverse peptides with antibiotic activity. A research group led by Maurizio Simmaco and Donatella Barra at the University of Rome ‘La Sapienza’ (Italy) now shows that the synthesis of antimicrobial peptides in the skin of Rana esculenta is, in fact, stimulated by microorganisms [FASEB J.(2001) 10.1096/fj.00-0695fje]. Frogs kept in a sterile environment did not produce antimicrobial peptides; however, exposure to even a single type of microorganism (one which contributes to the frog's natural flora) was sufficient to elicit a marked production of these peptides. In support of this observation, the secretions of frogs kept in bacteria-containing water (but not of those kept under sterile conditions) contained NF-κB-binding activity; a characteristic previously associated with the production of antimicrobial peptides. These findings will help researchers learn more about the molecular mechanisms governing the role of peptide antibiotics in the innate immune system. AR

Physiological adaptive mechanisms of catfish (Siluroidei) to environmental changes

Emphasis on physiological adaptations to environmental changes in the catfish (Siluroidei), is a rather recent development like that of their use in aquaculture. The siluroid fishes with smooth scaleless skin and sensory barbels are adapted to live in a variety of aquatic environments ranging from freshwater and brackishwater to swamps and marshes both in temperate and tropical regions. However, very little has been explored on their expected wide range of physiological adaptations. Most of the results obtained in siluroid fishes are similar to those reported for other teleosts such as cypriniform species. However, there are some air-breathing siluroids, found in the tropical areas, with accessory air-breathing organs. Besides tolerating periods of water deprivation, some of these fishes have been shown to possess-special physiological and biochemical adaptive mechanisms to tolerate a wide range of adverse physico-chemical conditions in the ambient environment. Some of the physiological adaptive mechanisms of Siluroidei in general, and air-breathing species in particular, to important physico-chemical factors such as oxygen,temperature, ammonia and xenobiotics are reviewed and discussed.

Role of epidermal-dermal tissue interactions in regulating tenascin expression during development of the chick scutate scale.

During normal chicken development tenascin begins to accumulate in the dermis of anterior metatarsal skin at the time of scutate scale ridge formation, and is localized in a distinct pattern along the outer scale surface. Anterior metatarsal skin from scaleless (sc/sc) embryos, which do not form scutate scales, begins to accumulate tenascin 4 days later than normal skin. This study shows that normal and scaleless anterior metatarsal dermis accumulate the same tenascin isoforms and undergo the same isoform changes in the post-hatch period, but there is less tenascin accumulated in scaleless dermis and there is no pattern to its distribution. In both normal and scaleless anterior metatarsal skin, tenascin mRNA is localized in the dermis and is distributed in the same way as the protein. Thus, scaleless skin is defective in the ability to accumulate appropriate amounts of tenascin and to maintain the tenascin in the patterned manner of normal. Recombinant skin cultures show that epidermal-dermal interactions are required for tenascin accumulation. The dermis specifies the way that tenascin is organized, but interaction with epidermis is required to maintain this organization. The epidermal role appears to be permissive because in heterotypic recombinants, neither scaleless anterior metatarsal epidermis nor normal footpad epidermis changes the way that tenascin appears in the normal anterior metatarsal dermis; and in reciprocal recombinants, normal anterior metatarsal epidermis does not change the way tenascin is accumulated in either scaleless anterior metatarsal dermis or normal footpad dermis.

Semantics and the Leathery Turtle, Dermochelys coriacea

Ever since Blainville (1816) used the generic term for the leathery turtle, several basic morphological facets of this animal have been obscured by redundant, exaggerated, or inaccurate descriptions. This results in unnecessary confusion and misunderstandings about ontogenetic and evolutionary features in Dermochelys coriacea. The specific name coriacea was provided by Vandelli (1761) and adopted by Linnaeus (1766), as Fretey and Bour (1980) explained. This epithet refers to the turtle's distinctive leathery, scaleless skin, as does also Blainville's (1816) generic name. It is unfortunate that both parts of the binomial refer to the same character, not only because of redundancy, but because the repetition exaggerates the true extent of the scaleless condition.

Expression of β keratin genes during skin development in normal and [formula omitted] chick embryos

The expression of RNA sequences specific for scale beta (β)-keratins has been followed during skin development in normal and scaleless ( sc sc ) embryos. Total RNA from skin at various stages (36–46) of development, as well as newly hatched chicks, was immobilized on nitrocellulose paper and hybridized with a [ 32P]cDNA probe to β-keratins (pCSK-12). Sequences for β-keratins showed patterns of expression which were specific for each genotype and scale type examined. During the development of normal scutate scales, which are characterized by the formation of a beta stratum, RNA with β-keratin sequences first appeared at stage 40, and continued to accumulate through hatching. RNA with β keratin sequences appeared in scaleless skin between stages 40 and 41, was greatly diminished by stage 44, and was no longer present at stage 46. In normal reticulate scales, which like scaleless skin, do not develop a beta stratum accumulation of RNA with β-keratin sequences was limited to a brief embryonic period between stages 42 and 44. These patterns of RNA expression correlated well with the appearance of β-keratin polypeptides, suggesting that β-keratin synthesis may be controlled at the level of keratin mRNA transcription. Correlations between the patterns of β-keratin expression and histological events suggest that the brief accumulation of β-keratin mRNA in scaleless skin and normal reticulate scales is related to the formation of the subperiderm (a protective layer of cells, peculiar to embryonic skin) while the continuous accumulation of β-keratin mRNA during scutate scale development reflects the formation of a beta stratum.

Avian scale development: XI. Initial appearance of the dermal defect in scaleless skin

The chicken mutant, scaleless, is characterized by the total absence of scutate scales. Previous experiments have shown that the scaleless defect is expressed by the epidermal cells while the dermal cells are able to participate in normal scale morphogenesis. However, in association with 14- to 16-day scaleless dermis, normal epidermis or the simple ectoderm of the chorion failed to develop scutate scale epidermis with its characteristic beta stratum. Thus the question arises: since the scaleless dermis starts out functioning normally, when does it become defective? Heterogenetic, heterotopic associations have been performed between 7.5-day to 11.5-day scaleless dermis and a neutral responding tissue, the midventral apteric epidermis, from 10.5-day normal embryos. The results show that up until 9.5 days of incubation the scaleless dermis is able to give instructions for normal scutate scale formation, if combined with normal epidermis. However, after 9.5 days, the scaleless dermis is not able to induce scale formation in normal apteric epidermis. Thus, the functional defect of the scaleless dermis occurs during the time (9 to 10 days of incubation) when epidermal placodes appear in normal embryos. From the present data, at least two explanations are possible. Either the scaleless epidermis is unable to respond to the placode inducing properties being provided by the scaleless dermis and because an epidermal placode does not form the scaleless dermis becomes defective, or the scaleless epidermis does not provide some earlier cue necessary for the scaleless dermis to acquire its placode inducing capabilities.

Immunofluorescent localization of collagen types I, III, IV, fibronectin and laminin during morphogenesis of scales and scaleless skin in the chick embryo.

Collagen types I and III were purified from the skin of 3-or 7-week-old chickens, collagen type IV from bovine skin or EHS mouse tumour, fibronectin from human serum, and laminin from EHS mouse tumour. Antibodies were produced in rabbits or sheep, and used in indirect immunofluorescence on frozen sections of 9-to 16-day-old normal or mutant (scaleless) chick-embryo foot skin. In normal scale-forming skin and inscaleless skin, the distribution of anti-laminin and anti-type IV collagen label was uniform along the dermal-epidermal junction and showed no stage-related variations, except for fluorescent granules located in the dermis of early scale rudiments. By contrast, in normal scale-forming skin, the density of anti-types I and III label decreased in the dermis within scale rudiments, whereas it gradually increased in interscale skin. Conversely, anti-fibronectin label accumulated at a higher density within scale rudiments than in interscale skin. In the dermis of thescaleless mutant, anti-types I and III label and antifibronectin label were distributed evenly: the density of anti-collagen label increased with age, while that of antifibronectin decreased and almost completely vanished in 16-day-old skin, except around blood vessels. The microheterogeneous distribution of some extracellular matrix components, namely interstitial collagen types I and III and fibronectin, is interpreted as part of the morphogenetic message that the dermis is known to transmit to the epidermis during the formation of scales. The even distribution of these components in mutantscaleless skin is in agreement with this view. Basement membrane constituents laminin and type-IV collagen do not appear to be part of the dermal morphogenetic message.

Étude expérimentale de la sensibilité de différentes espèces pisciaires à l'agent de l'érythrodermatite de la carpe (E.C.)

We mean experimentaly to study, the sensibility of carp (Cyprinus carpio), tench (Tinca-tinca), grass carp (Ctenopharyngodon idella) and silver carp (Hypophtalmichtys molitrix) at carp erythrodermatitis bacteria (E.C.). Only Cyprinus carpio is able to develop dermic and epidermic ulcerative lesion typical of the disease on the scaleless skin. Grass and silver carp are very sensitive at erythrodermatitis bacteria and die heavily some days after germ inoculation. When Ctenopharyngodon does not show lesion, Hypophtalmichtys shows a necrosis at the dermic injection location. Tench appears very more resistant than carp.

Respiratory morphometrics of white and red blooded antarctic fish

Abstracto1.The gill area and skin area of Chaenocephalus aceratus increases in proportion to body weight by exponents of 1.09 and 0.59 respectively. The scaleless skin of this fish does not appear to be a necessary respiratory compensation for the lack of hemoglobin.2.The gill area of C. aceratus is similar to that of several other species of red blooded polar fish.3.The heart of C. aceratus is 2–3 times larger than that of the other fish examined. Its spleen and many other parts of its body are comparatively large and it is suggested that this may be a consequence of reduced axial musculature. The gill area and skin area of Chaenocephalus aceratus increases in proportion to body weight by exponents of 1.09 and 0.59 respectively. The scaleless skin of this fish does not appear to be a necessary respiratory compensation for the lack of hemoglobin. The gill area of C. aceratus is similar to that of several other species of red blooded polar fish. The heart of C. aceratus is 2–3 times larger than that of the other fish examined. Its spleen and many other parts of its body are comparatively large and it is suggested that this may be a consequence of reduced axial musculature.

Observations on collagen synthesis, lattice formation, and morphology of scaleless and normal embryonic skin

Intact scaleless skin, from areas which in normal embryos have feathers, lacks a birefringent fibrous lattice which connects the dermal condensations. Recombinations between scaleless and normal skin components have the birefringent dermal lattice and dermal condensations only when either mutant or normal mesoderm is covered with a genetically normal ectoderm. Skins composed of mesoderm of either genotype covered by a scaleless ectoderm do not have the birefringent lattice, nor do they have dermal condensations. In view of the proposed collagenous nature of the fibrous lattice, collagen synthesis was estimated in both normal and mutant skins to investigate the possibility that scaleless skin might synthesize reduced levels of collagen. Our results indicate that scaleless dorsal skin synthesizes at least as much collagen as normal skins. The results suggest that the absence of a fibrous lattice is not the result of a reduced synthesis, but more likely the result of a failure of synthesized collagen to be organized into a lattice.