Towards a comprehensive model of feather regeneration

Understanding of the regeneration of feathers, despite a 140 year tradition of study, has remained substantially incomplete. Moreover, accumulated errors and mis‐statements in the literature have confounded the intrinsic difficulties in describing feather regeneration. Lack of allusion to Rudall's (Rudall [ 1947 ] Biochem Biophys Acta 1:549–562) seminal X‐ray diffraction study that revealed two distinct keratins, β‐ and α‐, in a mature feather, is one of the several examples where lack of citation long inhibited progress in understanding. This article reviews and reevaluates the available literature and provides a synthetic, comprehensive, morphological model for the regeneration of a generalized, adult contour feather. Particular attention is paid to several features that have previously been largely ignored. Some of these, such as the β‐keratogenic sheath and the α‐keratogenic, supra‐umbilical, pulp caps, are missing from mature, functional feathers sensu stricto because they are lost through preening, but these structures nevertheless play a critical role in development. A new developmental role for a tissue unique to feathers, the medullary pith of the rachis and barb rami, and especially its importance in the genesis of the superior umbilical region (SUR) that forms the transition from the spathe (rachis and vanes) to the calamus, is described. It is postulated that feathers form through an intricate interplay between cyto‐ and histodifferentiative processes, determined by patterning signals that emanate from the dermal core, and a suite of interacting biomechanical forces. Precisely regulated patterns of loss of intercellular adhesivity appear to be the most fundamental aspect of feather morphogenesis and regeneration: rather than a hierarchically branched structure, it appears more appropriate to conceive of feathers as a sheet of mature keratinocytes that is “full of holes. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Observations on the histochemistry and ultrastructure of the epidermis of the tuatara,Sphenodon punctatus (Sphenodontida,Lepidosauria, Reptilia): a contribution to an understanding of the lepidosaurian epidermal generation and the evolutionary origin of the squamate shedding complex

Histochemical and TEM analysis of the epidermis of Sphenodon punctatus confirms previous histological studies showing that skin-shedding in this relic species involves the periodic production and loss of epidermal generations, as has been well documented in the related Squamata. The generations are basically similar to those that have been described in the latter, and their formation involves a cyclic alternation between beta- and alpha-keratogenesis. The six differences from the previously described squamate condition revealed by this study include: 1) the absence of a well-defined shedding complex; 2) the persistence of plasma membranes throughout the mature beta-layer, including the oberhautchen; 3) the concomitant presence of lipogenic lamellar bodies and PAS-positive mucous granules in most presumptive alpha-keratinizing cells; 4) the presence of the secreted contents of these organelles in the intercellular domains of the three derived tissues, the homologues of the squamate mesos, alpha-, and lacunar cells; 5) the paucity of lamellated lipid deposits in such domains; 6) the presence of keratohyalin-like granules (KHLG) in the presumptive lacunar, clear, and oberhautchen cells. In toto, the absence of many of the precisely definable, different pathways of cytogenesis discernible during squamate epidermal generation production might be interpreted as primitive for lepidosaurs. However, when the evolutionary significance of each of the six differences listed is evaluated separately, it becomes clear that the epidermis of S. punctatus possesses primitive amniote, shared and derived lepidosaurian, and some unique characters. This evaluation further elucidates the concept of a lepidosaurian epidermal generation as a derived manifestation of the sauropsid synapomorphy of vertical alternation of keratin synthesis and shows that further study of keratinocyte differentiation in the tuatara may contribute to our understanding of the origin and evolution of beta-keratinization in sauropsid amniotes.     

The microscopic anatomy of epidermal glands in two species of gekkonine lizards, with some observations on testicular activity.

The gross and microscopic anatomy of epidermal glands has been studied in laboratory maintained tokays (Gekko gecko), and house geckos (Hemidactylus bowringii) captured from the wild throughout the year. Annual testicular activity in the house gecko has also been studied. While no significant differences in glandular development at various times have been observed in G. gecko, there are clear-cut annual cycles in H. bowringii. The evolution of epidermal glands in gekkonid lizards is reviewed; the cellular dynamics of beta-glands are compared with those of unspecialized epidermis; the possibility that gekkonine epidermal glands respond to quantitative variation in circulating testosterone titers is discussed.     

The post-natal development of holocrine epidermal specializations in gekkonid lizards.

The abdominal escutcheon, and certain aspects of pre-anal organ morphology, have been studied in Sphaerodactylus spp. and Gekko vittatus respectively. These epidermal modifications are male characteristics. The sphaerodactyline escutcheon becomes larger by the peripheral addition of specialized scales with increasing size of the individuals: this relationship is much more clearcut in S. cinereus than in the notatus species group (sensu Shreves, '68), and the possible reasons for this are discussed. The number of pre-anal organs varies between populations of G. vittatus, but within populations remains constant throughout life. Individual organs increase steadily in size throughout life. These data are discussed with reference to current interpretations of gekkonid gland evolution, and of factors controlling epidermal cell proliferation and differentiation.     

Sex steroids and epidermal glands in two species of gekkonine lizards.

In vivo and in vitro experiments on the endocrine relationships of epidermal glands in the tokay Gekko gecko, and the common house gecko Hemidactylus bowringii are reported. The results show that certain aspects of beta-gland differentiation involve a synergistic action between androgens and those hormones responsible for controlling the normal shedding cycle, while other aspects are solely under androgenic control. Pre-anal organ activity appears to be solely under androgenic control.     

Ultrastructural organization of avian stratum corneum lipids as the basis for facultative cutaneous waterproofing

The ultrastructure of naked neck epidermis from the ostrich (Struthio camelus) and ventral apterium from watered, and water-deprived, Zebra finches (Taeniopygia [Poephila] guttata castanotis) is presented. The form and distribution of the fully differentiated products of the lipid-enriched multigranular bodies are compared in biopsies post-fixed with osmium tetroxide or ruthenium tetroxide. The fine structure of ostrich epidermis suggests it is a relatively poor barrier to cutaneous water loss (CWL). The fine structure from watered, and 16-hr water-deprived Zebra finches, considered in conjunction with measurements of CWL, confirms previous reports of “facultative waterproofing,” and emphasizes the rapidity of tissue response to dehydration. The seemingly counterintuitive facts that one xerophilic avian species, the ostrich, lacks a “good barrier” to CWL, whereas another, the Zebra finch, is capable of forming a good barrier, but does not always express this capability, are discussed. An explanation of these data in comparison to mammals centers on the dual roles of the integument of homeotherms in thermoregulation and conserving body water. It is concluded that birds, whose homeothermic control depends so much on CWL, cannot possess a permanent “good barrier,” as such would compromise the heat loss mechanism. Facultative waterproofing (also documented in lizards) protects the organism against sudden reductions in water availability. In birds, and probably in snakes and lizards, facultative waterproofing involves qualititative changes in epidermal cell differentiation. Possible control mechanisms are discussed. © 1996 Wiley-Liss, Inc.     

Interaction between thermal environments and hormones affecting skin-shedding frequency in the tokay (Gekko gecko) (Gekkonidae, Lacertilia)

Effects of thyroidectomy and/or hypophysectomy on the skin-shedding frequency (SF) in the tokay Gekko gecko and of thyroid hormones on the oxygen consumption (OCR) at various temperature regimes have been determined. Surgery invariably protracted the cycle length, thus decreasing SF; the extent of these changes was temperature dependent, the higher the temperature, the less the difference. Effects of hypophysectomy on cycle length were expressed in two phases; an extended first post-operative cycle was followed by a further extended second post-operative cycle, with cycle length forming a plateau thereafter. With time, the operated tokays would die without shedding during a greatly protracted cycle. OCRs in the tokay were temperature dependent, but between 28 and 34 degrees C, no significant difference could be seen. Effects of thyroid hormones on OCR were also temperature dependent. Furthermore, tokays having higher OCR were shown to have shorter cycles and vice versa. Results showed that whatever effect hormone(s) have on SF is indirect through general metabolic changes. SF is merely a reflection of the general metabolic status of the animal. It is proposed that the role of hormone(s), those of the thyroid in particular, is to act as "fine-tuning" devices in the regulation of metabolism and, as such, of the viability of the animal.     

The Development of the Sauropsid Integument: A Contribution to the Problem of the Origin and Evolution of Feathers

Developmental anatomical data are insufficient to discuss plausibleintermediates between an ancestral, scaled, reptilian skin andappendage-bearing, avian skin. We also review adult tissue replacementand ubiquitous mechanisms underlying skin morphogenesis. Combiningdevelopmental data sensu lato with consideration of necessarybiological roles permits evaluation of major form/function trendsin skin evolution. New data on feathers reveal retention ofthe sauropsid synapomorphy of vertical alteration of - and ß-keratogenesis.By identifying roles that were obligatorily maintained throughoutevolution, we demonstrate constraints on hypothetical skin morphologiesin preavian taxa. We analyze feather origins as a problem ofemergence of complex form via modulations of morphogenesis.While existing data do not permit presentation of sequential,hypothetical, intermediates culminating in a plumage, the analysis:(1) implies that a protofeather and its follicle are most easilyderived from isolated, flattened, elongate, reptilian scales;(2) explains diversification of feather morphs from a contour-like"basic" feather and the similarity between feather and hairfollicles; and thus (3) reveals several developmental constraintson structures proposed as antecedent to avian feathers, whetherhypothetical constructs or palaeontological interpretations.Although these conclusions do not depend on any previous scenario,they are consistent with Regal's (1975) model and the limited,fossil evidence, especially that of the "basal archosaur" Longisquama.