© 2000 by The Society for Integrative and Comparative Biology
Avian Epidermal Lipids: Functional Considerations and Relationship to Feathering1
1 California Academy of Sciences, Golden Gate Park, San Francisco, California 94118
2 Department of Biology, 300 Pompton Road, William Paterson University of New Jersey, Wayne, New Jersey 07470
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SYNOPSIS |
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 SYNOPSIS INTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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The avian epidermis is composed of unique sebokeratinocytes that elaborate and secrete sebum-like lipids as they cornify. In addition to the lipid droplets, the avian epidermis elaborates, but rarely secretes, lipid—enriched organelles, the multigranular bodies. The multigranular bodies are analogous to the lamellar bodies of mammals (Menon et al., 1991
), the secretion of which results in formation of occlusive lipid bilayers characteristic of mammalian stratum corneum and providing the permeability barrier. However, in contrast to mammals, the avian multigranular bodies form the reserve barrier mechanism. In the basal state, when multigranular bodies are not secreted, the avian cutaneous barrier is deficient, but allows evaporative cooling for thermoregulation. However, under conditions of water deficit, multigranular body secretion allows for rapid facultative waterproofing, as shown in zebra finches (Taenyopygia guttata). In certain glabrous regions of the skin, such as the maxillary rictus, interdigital web, and combs and wattles in the domestic fowl, there is a high degree of epidermal lipid secretion. Also specialized feathers such as powder downs elaborate lipid rich material, which can be classified as secretion. Additionally, an inverse relation between epidermal lipogenesis and the degree of feathering has been demonstrated, as in temporarily bare areas (e.g., brood patches) and following permanent feather loss from the head accompanying attainment of maturity in certain ibises and storks. In the latter, the neo-apteria often hold large reserves of carotenoids dissolved in the lipid droplets, possibly related to an altered gradient of retinoids influencing feather morphogenesis. Unusual secondary functions of epidermal lipids include cosmetic coloration (e.g., in the Japanese Crested Ibis) and chemical defense (e.g., in the Pitohui). |
INTRODUCTION |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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The avian integument exhibits structural and functional features that are as unique as the class Aves, reflecting a wide range of adaptive radiation (Stettenheim, 1972). This review will focus on 1) the unique sebokeratinocytes that make up the avian epidermis; 2) epidermal lipid secretion and permeability barrier formation 3) the modifications of integumentary structures and their influence on epidermal lipogenesis, and 4) the possible functions of epidermal lipids in birds.
Recent studies on avian epidermal differentiation show that it differs significantly from that of reptiles and mammals despite basically similar functional demands of a terrestrial environment. As in all terrestrial vertebrates, the primary function of avian epidermis is to provide a permeability barrier to curtail excessive evaporative water loss and prevent death by dehydration. Such a barrier, already in place in reptilian ancestors, can be viewed as a protoadaptation, available to be modified and exploited by birds as they evolved to fill their varied ecological niches. However, birds evolved a less stringent barrier that facilitates evaporative cooling while retaining the capacity for facultative waterproofing (Menon et al., 1996).
From a microscopist's perspective, the complexity of reptilian epidermis has been lost in birds. The vertical alternation of keratin expression of reptilian scales is indeed retained in feathers (Maderson and Alibardi, 2000). The horizontal alternation of keratin expression as defined by Baden and Maderson (1970) is a temporal artifact. The avian interfollicular epidermis represents an expansion of the reptilian hinge region, which retains and combines characters of reptilian alpha keratinizing tissues (mesos and alpha layers) in the mode of lipogenesis. While the foregoing is an oversimplification, which may lead to many a raised eyebrow, we use this analogy for the avian interfollicular epidermis whose structural and functional similarities to reptiles will be brought up at appropriate sections of this review.
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BASIC MORPHOLOGY OF AVIAN SEBOKERATINOCYTES |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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The basic pattern of epidermal proliferation, progressive accumulation of differentiation-specific products such as keratins, and terminal differentiation (i.e. transformation into non-nucleated, flattened corneocytes) is similar in all higher vertebrates. However, the inherent lipogenic nature of avian epidermis (Fig. 1) distinguishes it from epidermis of terrestrial mammals (Matoltsy, 1969
; Freinkel, 1972; Lavker, 1975). Histochemical studies revealed that the basal cells contain mostly acidic lipids, but neutral lipids begin to predominate as the cells stratify with the stratum corneum showing the most prominent staining for neutral lipids (Shah and Menon, 1972). Free, non-membrane bound lipid droplets appear perinuclearly in basal cells, and as these cells stratify, a gradual increase both in number and size of the lipid droplets occurs. In addition to the free lipid droplets, large membrane bound lipid-enriched organelles known as multigranular bodies also appear in the epidermal cells. Ultrastructurally, multigranular bodies display multiple stacks of disk shaped internal contents, similar to the mesos granules of squamate reptilian epidermis and lamellar bodies of mammalian epidermis (Fig. 2b, Inset). However, typically they show signs of dissolution and transformation into electron lucent lipid droplets within the cytosol of the transitional cell layers prior to their terminal differentiation (Fig. 2a). During terminal differentiation, coalescence of lipid droplets and dissolution of cell organelles occur, and keratin filaments are displaced towards the cell periphery where they fortify the thickened marginal band—the principal proteinaceous component of corneocytes (Fig. 2a; Menon et al., 1986). Typically, the lowermost corneocytes are elongated and spindle shaped in cross sections due to a single large lipid droplet forming the core (Fig. 2a). Two or three cell layers higher in the stratum corneum, these intracellular lipids escape into the extracellular domains via porosities or breaks in the cell membranes, akin to what occurs in the mammalian holocrine sebaceous secretion as well as the uropygial glands in birds (Menon et al., 1981). The mode of lipid secretion described above justifies the term "Sebokeratinocytes" for the avian epidermal cell, and Lucas (1970) considered the whole of avian epidermis as a holocrine secretory unit. While this is the general pattern, the degree of epidermal lipogenesis and mode of secretion, as well as sequestration of lipids within the stratum corneum depends on the location in the body and may vary in different species of birds (Wrench et al., 1980; Menon et al., 1981). The functional implications of such variations and their adaptive significance are discussed next.
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STRATUM CORNEUM AND PERMEABILITY BARRIER FUNCTION |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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In all groups of terrestrial vertebrates, the ultimate fate of epidermal cell differentiation is to form a cornified tissue, the stratum corneum that provides a flexible yet tough protective covering for the body. Aside from the barrier functions, the stratum corneum is shown to have an amazing array of functional properties that include sensory transduction, piezo and pyro electric properties (Hoath et al., 1998
). Almost all studies characterizing the stratum corneum properties have employed glabrous or nearly glabrous skin from neonatal rodents, hairless mice or human skin where it provides a tough and flexible covering. However in birds and most mammals it is the plumage or pelage which provides the mechanical protection while keeping the skin in toto flexible, and hence Aves do not rely on the corneocytes for physical protection except in a few apterous zones. This is reflected in the much-reduced keratin content and the effete nature of avian corneocytes compared to those of mammals (Elias et al., 1987). However, even in mammals, the lipids of stratum corneum are crucial to survival as they form a permeability barrier, reducing transcutaneous water loss and making possible life on land. A brief description of how the barrier is formed in mammals is instructive in understanding its versatile use by aves. As this is a lipocentric review, the complex process of keratin synthesis and assembly will not be discussed here.
Typically, the mammalian stratum corneum shows a basket weave pattern in histological preparations, and transmission electron micrographs show empty spaces between corneocytes. Both these features are artifacts of tissue preparation. When appropriately fixed with lipophilic post-fixatives such as ruthenium tetroxide, the intercellular domains are resolved to be filled with a tight array of lipid bilayers that occlude efflux and influx of water across the skin (Madison et al., 1987). These lipids have their origin within the epidermal keratinocytes as discreet lipid enriched secretory organelles known as the lamellar bodies (Odland bodies, keratinosomes, membrane-coating granules, mesos granules) that appear first within the spinous layers. This is not unique to mammals, as similar organelles characterize amniote epidermis in general. These are termed mesos granules in squamate reptiles and multigranular bodies in birds (Landmann, 1980). The synthesis of lamellar bodies is upregulated as the cells progressively differentiate, and in the outermost cells of the stratum granulosum, about 20% of the cytosol is occupied by lamellar bodies, polarized in the apical parts of the cells and poised to be secreted into the extracellular domain of the stratum granulosum–stratum corneum interface. These domains appear engorged with the secreted disc-like contents of the lamellar bodies. The end-to-end fusion of such pro-barrier lipid discs, and their further processing into compact lipid bilayers occluding the extracellular domains of adjacent and overlapping corneocytes, give rise to a "brick-and-mortar" organization of the stratum corneum. The keratin-enriched corneocytes form the bricks, and the extracellular lipids provide the mortar, that is the basis of water permeability barrier (Elias, 1983; Elias and Menon, 1991).
The morphological changes in the lipid structures underscore biochemical modulations of the phospholipid rich pro-barrier lipids mediated by a battery of lipolytic enzymes that are co-packaged and secreted with the lipids within the lamellar bodies. A critical molar ratio between three major species of stratum corneum lipids, viz., cholesterol, ceramides and fatty acids, is crucial for the formation of mature lipid bilayers and hence for the permeability barrier formation. Inhibition of the synthesis of any one of these lipids, or the enzymatic processing of the lamellar body derived discs, causes defective water barrier, excess transepidermal water loss (TEWL) and threatens survival (Reviewed in Menon and Ghadially, 1997).
Transepidermal water loss can be measured directly over the skin using a ventilated chamber technique (Meeco electrolytic moisture analyzer) or an evaporimeter (Servomed or TEWAMETER). While the evaporimeter gives values as g/cm2/hr of water loss, the ventilated chamber technique provides ppm values, which can be converted to the former using a standard formula. These two kinds of instruments have been employed extensively in clinical dermatological research (Wilson and Maibach, 1994) and are useful in assessing the barrier damage due to lipid removal from the stratum corneum as well as the time course of barrier restoration in vivo that follows experimental barrier disruption (Elias and Menon, 1991).
Transepidermal water loss has been assessed in pigeons and zebra finches using the ventilated chamber technique as well as the evaporimeter (Menon et al., 1986, 1988, 1989, and 1996). As the avian stratum corneum is more fragile than that of mammals, the absolutely non-invasive evaporimeter is to be preferred for measuring avian trans epidermal water loss (TEWL). Feathers overlapping apteric regions should be trimmed, rather than plucked, as plucking feathers disrupts the barrier function of the follicles and elevates trans epidermal water loss to a non-physiological range (Maderson and Alibardi, 2000). Typically, the trans epidermal water loss values are much higher for birds compared to mammals (humans, mice) indicating a poorly functioning permeability barrier. This itself is of great adaptive value for birds whose thermoregulation is largely dependent on evaporative cooling. The higher basal body temperature, increased thermogenesis due to flight, insulation by plumage and the lack of sweat glands, necessitate a higher rate of evaporative cooling through a "leaky" epidermal permeability barrier. In fact, the heat-acclimated pigeons described by Marder and colleagues can survive in temperature ranges of up to 55;dgC only due to superior evaporative cooling ability compared to non-acclimated or cold-acclimated pigeons (Marder et al., 1987; Peltonen et al., 1998).
As in mammals, the basis of the permeability barrier in birds is also lipids in the stratum corneum, but they differ significantly in biochemical composition and morphological organization. As mentioned earlier, the keratinocytes of avian epidermis synthesize multigranular bodies (MGBs), organelles that resemble to the lamellar bodies but 3 to 4 times larger and appear as multiple lamellar bodies enclosed in a membrane. In addition to multigranular bodies the cells also synthesize large non-membrane bound lipid droplets that resemble sebum or oil. In the outermost cells of the stratum transitivum (the topographic equivalent of the mammalian stratum granulosum, but lacking keratohyalin granules), most of the multigranular bodies undergo progressive dissolution, and are transformed into electron lucent lipid droplets coalescing with the nascent lipid droplets. The cornified cells thus hold a large core of electron lucent lipids that eventually escape from the cell through porosities or breaks in the membranes. These lipids thus are deposited in the extracellular domains of the stratum corneum. However, unlike the case in mammals, they fail to form bilayered structures. Some of the undegraded multigranular bodies are retained within the corneocytes where these are visible as lamellar sheets when stained with ruthenium tetroxide (Fig. 2b). Thus, in the basal state, large scale secretion of multigranular bodies is absent, and there is no deposition of lamellar lipids within the interstices of stratum corneum. The resultant barrier is weaker than that of mammals, yet quite suited for the needs of birds whose priority is evaporative cooling.
The synthesis of multigranular bodies and their retention till the stratum transitivum provides birds with a reserve barrier mechanism to be activated at times of xeric stress. Nestlings of zebra finches have a remarkably impermeable integument, which displays very low trans epidermal water loss values, but as they develop into fledglings their skin becomes increasingly permeable, gradually reaching adult values characteristic of a leaky barrier. However, adult zebra finches under water deficit are capable of facultative waterproofing (Table 1). Menon et al. (1996) showed that within 16 h of water deprivation, adult zebra finches drop their trans epidermal water loss values by 50% and continue to improve barrier efficacy until mammal-like values are reached. The basis for this phenomenon is rapid secretion of multigranular bodies, sequestration of lamellar lipids in the interstices of the stratum corneum, and decreased production of neutral lipid droplets. If water deprivation is prolonged, overall synthesis of multigranular bodies is upregulated at the cost of neutral lipid droplets, even in the lower cell layers. But replenishment of water is followed by dissolution of multigranular bodies in situ into neutral lipid droplets.
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On a morphological basis, then, the stratum corneum and underlying cells of a waterproof Zebra finch resemble the mesos and alpha layers of a squamate reptilian epidermal generation (Landmann, 1980
) Reptiles have their barrier located in the extracellular lamellar bilayers of the mesos layer. Unlike mammalian or avian stratum corneum, there is no continuous loss by exfoliation and replenishment of the corneocytes in reptiles, the mesos layer and the underlying alpha layer being protected by the ß layer (Landmann et al., 1981; Maderson et al., 1998). However, it is known that low humidity acclimation induces reptiles to fortify their barrier without skin shedding and renewal (Kattan and Lillywhite, 1989). Cell proliferation and lipogenesis within the alpha layer achieve this. The dynamics of how these newly synthesized lipids are secreted or where they are sequestered remains to be elucidated, but the resemblance to the scheme of avian epidermal lipogenesis is striking. |
SPECIALIZED REGIONS SHOWING HIGH DEGREE OF LIPOID SECRETION |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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Lucas and Stettenheim (1972)
documented that the lipogenic activity of the epidermis is greater in certain glabrous regions of the skin like the comb, wattle, interdigital web including dorsal and ventral scales, and the edge of the maxillary rictus in the domestic fowl. Ultrastructural features of epidermal lipogenesis in the rictus and the holocrine mode of lipoid secretion therein, have been described in detail by Menon et al., (1981). Some notable differences at the ultrastructural level between the secretory epidermal cells from the rictus and the toe web were reported by Menon and Aggarwal (1982b), essentially due to intrinsic differences in the mode of keratinization in these locations. Lipogenesis and keratinization are inseparably associated with each other in avian epidermis (Wrench et al., 1980), and it appears that an inverse relation exists between sebogenesis and keratinization even within the secretory epidermis from different locations in the body, as exemplified by the rictus and the toe web. While there is a remarkable similarity in the initial phase of lipogenesis and keratinization, evident in both the origin and ultrastructural features of keratin filaments and lipid droplets in the basal cells, the pathway of differentiation or rather, the emphasis on the synthetic potential shifts from the intermediate layer onwards. In the rictus and the free edge of the web (Fig. 3a), enhancement of lipogenesis is predominant, while in the sulcus of the ventral reticulate scales of the toe web, alpha keratin synthesis predominates. It has been suggested that some of the lipids may be utilized for the energetics of keratinization (Menon and Aggarwal, 1982b). Histochemical studies have also shown that in the hard dorsal scales on the web, neutral lipid distribution is restricted to the basal cell layer, the suprabasal cells showing a virtual absence of lipid staining (Menon and Aggarwal, 1982a). Another instance of a keratinizing epithelia showing high lipogenesis is the cere of the pigeon (Purton, 1988). The epidermis from all these locations also shows multigranular bodies to be present in various degrees, but the role of these organelles here has not been assessed.
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LIPID SECRETION BY FEATHERS |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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Specialized feathers such as the powder downs produce a talcum-like substance that supplements the uropygial gland secretion in preening and waterproofing the feathers, (Wetmore, 1920
; Hindwood, 1933). Although some semiplumes and downy portions of contour feathers produce some powder, in their most specialized form, the powder feathers are downy. Highly developed powder downs occur in herons, mesites, tinamous and cuckoo-rollers (Stettenheim, 1972). In herons and egrets, clumps of such feathers (120–160 feathers/cm2) occurring in specific tracts, in breast and flank, grow continuously and disintegrate from the distal parts shedding a copious amount of powder. Scanning electron microscopy (Menon, Baptista and Stettenheim, unpublished) shows that the powder is composed mainly of keratinized cells that are presumptive barbule cells stuck together by an adherent material (Fig. 3b) that is lipoid in nature. Treatment with lipid solvents completely removes the powder from the feathers, as well as disaggregates the cells that constitute the powder. Frozen sections of powder feathers of herons show the pulp and epithelia to be rich in neutral lipids. Multigranular bodies are absent from ß-keratinizing cells in birds, but free lipid droplets have been seen. Transmission electron microscopic studies are in progress to assess if lipids are sequestered within the mature powder or synthesized and secreted by parts of the growing feather. In view of the continuous growth of the powder downs providing an uninterrupted supply of the lipid-cell complex forming the powder, Menon (1984) considered these as glandular structures that are everted out, instead of having the typical anatomical profile of an invaginated structure. Feathers that are not so specialized, but are variants of the same theme include the creamy feathers of pied imperial pigeon, Ducula bicolor (Abdulali, 1966), the fat quills of archangel pigeons (Stettenheim, 1972) and the feathers on the back of the heart spotted woodpecker (Hemicircus canente) that may be source of a resinous material (Bock and Short, 1971). All these feathers produce a notable amount of lipoid material during their keratinization process, and thus differ from ordinary feathers that are chiefly geared to synthesize structural proteins such as ß keratin. |
FUNCTIONS OF AVIAN EPIDERMAL LIPIDS |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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The functional significance of avian epidermal lipids continues to be unraveled, and we expect the list to grow in the near future. Aside from the global and primary facultative permeability barrier/evaporative cooling (crucial for thermal adaptation), epidermal lipids discharge specific and specialized functions in certain species. These include anti microbial (Purton, 1986
) visual signaling and ultraviolet rays protection by dissolved carotenoid pigments in neo-apteria (Menon, 1984), possible morphogenetic gradients by the same mechanism (as above) and sterol precursors for Vitamin D. Two of the species specific and unusual functions, i.e., cosmetic coloration (Uchida, 1970) and chemical defense (Dumbacher et al., 1992) deserve special mention. In the Japanese Crested Ibis, Nipponia nippon, a "Black Substance" produced by a specialized region of skin on the face, is reportedly smeared over the plumage by a characteristic daubing behavior during breeding season. Thus the birds undergo a color transformation, from white to grey, without a molt. This "cosmetic coloration unique for the species (Uchida, 1970) has unfortunately not been studied in any detail. Discovery of a toxin, similar to the homobatracotoxin in the skin and feathers of several species of the New Guinean bird, the Pitohui by Dumbacher et al., (1992) has opened up a truly amazing facet of avian adaptations. About 60% of the toxin in the Hooded Pitohui, the most toxic species, are found in the skin and feathers (Dumbacher, personal communication), its possible origin from the epidermis and/or specialized glandular units is currently under investigation. Exploitation of epidermal fatty acids (in the web and feet) of domestic ducks (Anas platyrhyncos), by circeria larvae of the duck blood flukes has recently been reported (Haas and van de Roemer, 1998). The larvae "home in" on their host by using the fatty acids as chemical cues or host signals. The role of epidermal lipids in host-parasite interactions and potential immune modulation is an area of great research interest. |
THE INVERSE RELATION BETWEEN FEATHERING AND EPIDERMAL LIPOGENESIS |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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As is evident from the forgoing account, higher lipogenic potential is expressed by epidermis from glabrous areas of skin such as the wattles and comb, the toe web, the cere in pigeons etc. The finding that epidermal lipogenesis is highly exaggerated in the neo-apteria of the painted storks following permanent loss of feathers from their capital tracts (a developmental phenomenon that accompanies their attainment of maturity) led to a hypothesis that there is an inverse relation between the degree of feathering and epidermal lipogenesis (Shah et al., 1977). Subsequently we have examined several instances of changes in the degree of feathering (i.e., insulation) and its relation to epidermal lipogenesis. The changes in ptilosis (feathering) can be grouped into three categories.
In the first, a special molt (restricted to a specific area and without the existing feathers being pushed out by outgrowths of the next generation of feathers) occurs resulting in a patch of skin that remains glabrous for a definite period of time. Examples of such temporarily bare areas include the brood (incubation) patches of many species and the head of male wattled starlings during the breeding season. The epidermis in the brood patches become hyperplastic, while the dermis becomes highly vascularized and edematous (Jones, 1971). The hyperplastic epidermis also shows a higher degree of lipogenesis (Jani et al., 1985) yet the permeability barrier deteriorates, with an increase in trans epidermal water loss (Menon and Baptista, unpublished observations). The increased blood supply and dermal hydration, together with an ineffective barrier, provide moisture for the eggs during incubation, an obvious adaptive strategy.
The second category involves changes in the quality or type of feathers produced by the follicles in specific body loci (head and neck). The replacement of contour feathers by structurally simpler bristles results in an apparant "naked" condition, exposing the epidermis in the head and neck of several species, e.g., domestic turkey, sarus crane. When contour feathers in the head and neck of a young Sarus crane, (Grus antigone) are replaced by bristles in the adult, which now has a striking red papillose skin, epidermal lipogenesis shows an inverse correlation with the degree of insulation. Adult Sarus cranes show three distinct zones in their head and neck skin: capital areas covered by bristles, a band of non-feather and non-bristle bearing area in the neck where the bright red skin shows a highly papillose nature, and an adjacent area bearing contour feathers. The epidermal lipogenesis, as evaluated by histochemical distribution of neutral lipids, is highest in the featherless areas, least in feathered areas and intermediate in the bristle bearing areas (Menon et al., 1980).
A third category involves total loss of the feather follicles, again in restricted loci as in the head of many species of storks, or head and neck of certain ibises resulting in a true neo-apterium (Menon et al., 1979, 1980; Shah et al., 1977). A general survey of birds showing such changes in the feathering/ptylosis (Menon and Stettenheim, in preparation) shows that the secondarily exposed skin is usually brightly colored and/or highly melanised (Ibises) so as to be in sharp contrast to an otherwise drab plumage. Two different and interesting biological questions are raised by these observations. First, what induces the formation of simplified epidermal appendages (bristles) from a follicle that produced a more complex appendage (a contour feather) in the previous generation? The domestic turkey should prove to be a good model to study the transition from feather to bristle. In the other instance, where a neo-apterium is formed, there is complete feather loss (Fig. 4a, b) and obliteration of the feather follicles that may be mediated by a programmed cell death.
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What genetic and hormonal factors determine the onset and progression of these events? Both instances exemplify an ontogenic recapitulation of a peculiar "devolution" of feathers. In the neo-apterium of the Painted stork, the basal cells become highly columnar, with their cytoplasm packed with lipid droplets that hold dissolved carotenoid pigments (Fig. 4c, Menon et al., 1986
). Whether these changes precede or follow the permanent feather loss is not presently known. Yet, it is tempting to consider that carotenoids, precursors of retinoids, may have something to do with a locally altered retinoid gradient, changing feather morphogenesis. Indeed, retinoids are increasingly being implicated in morphogenesis, homeobox gene transcription etc., (Marshall et al., 1996) and injection of retinoic acid into a chick egg has long been known to induce ptilopody (Sengel, 1976). Retinoids might hold the key to study both feather evolution (from reptilian scales?), as well as devolution of feathers in the secondarily naked areas of skin in modern birds that may have significance in thermoregulation (Crowe and Withers, 1979; Larochelle et al., 1982).
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ACKNOWLEDGMENTS |
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We thank Paul Maderson and Dominique Homberger, Organizers of the symposium, for giving us the opportunity to participate. Peter Stettenheim and Paul Maderson are thanked for stimulating discussion. Thanks are due to L. F. Baptista and Peter Elias, collaborators in many of the studies on barrier functions, and colleagues and Ph.D. students at the University of Baroda, India. Jaishri Menon thanks William Paterson University of New Jersey for assigned released time.
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FOOTNOTES |
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1 From the Symposium Evolutionary Origin of Feathers presented at the Annual Meeting of the Society for Integrative and comparative Biology, 6–10 January 1999, at Denver, Colorado.
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References |
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SYNOPSISINTRODUCTIONBASIC MORPHOLOGY OF AVIAN...STRATUM CORNEUM AND PERMEABILITY...SPECIALIZED REGIONS SHOWING HIGH...LIPID SECRETION BY FEATHERSFUNCTIONS OF AVIAN EPIDERMAL...THE INVERSE RELATION BETWEEN...References |
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Dumbacher, J. P., B. M. Beehler, T. F. Spande, H. M. Garraffo, and J. W. Daly. 1992. Homobatrachotoxin in the genus Pitohui—Chemical defence in birds? Science, 258:799-801.
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Kattan, G. H., and H. B. Lillywhite. 1989. Humidity acclimation and skin permeability in the lizard, Anolis carolinensis. Physiol. Zool, 62:593-606.
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Larochelle, J., J. Delson, and K. Schmidt-Nielsen. 1982. Temperature regulation in the black vulture. Can. J. Zool, 60:491-494.
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