Alan H. Brush

The Evolutionary Origin And Diversification Of Feathers

Progress on the evolutionary origin and diversification of feathers has been hampered by conceptual problems and by the lack of plesiomorphic feather fossils. Recently, both of these limitations have been overcome by the proposal of the developmental theory of the origin of feathers, and the discovery of primitive feather fossils on nonavian theropod dinosaurs. The conceptual problems of previous theories of the origin of feathers are reviewed, and the alternative developmental theory is presented and discussed. The developmental theory proposes that feathers evolved through a series of evolutionary novelties in developmental mechanisms of the follicle and feather germ. The discovery of primitive and derived fossil feathers on a diversity of coelurosaurian theropod dinosaurs documents that feathers evolved and diversified in nonavian theropods before the origin of birds and before the origin of flight. The morphologies of these primitive feathers are congruent with the predictions of the developmental theory. Alternatives to the theropod origin of feathers are critiqued and rejected. Hypotheses for the initial function of feathers are reviewed. The aerodynamic theory of feather origins is falsified, but many other functions remain developmentally and phylogenetically plausible. Whatever their function, feathers evolved by selection for a follicle that would grow an emergent tubular appendage. Feathers are inherently tubular structures. The homology of feathers and scales is weakly supported. Feathers are composed of a suite of evolutionary novelties that evolved by the duplication, hierarchical organization, interaction, dissociation, and differentiation of morphological modules. The unique capacity for modular subdivision of the tubular feather follicle and germ has fostered the evolution of numerous innovations that characterize feathers. The evolution of feather keratin and the molecular basis of feather development are also discussed.

The molecular heterogeneity and diversity of reptilian keratins.

SummaryReptile keratins produce complex electrophoretic patterns, contain a number of size classes, and contain protein fractions analogous to the fractions found in other keratins. Thus, reptile keratins are similar to the heterogenous keratins of birds and mammals, and quite different from amphibian epidermal keratins. This heterogeneity may be related to the multiple functions performed by the epidermis of these organisms.The chemical diversity of reptile keratins seems to depend on the morphological differences between the tissues in which they occur. This situation is also found among these proteins in mammals and birds suggesting that keratin diversity is related to the morphological and presumably functional differentiation of epidermal tissues. The distribution of the keratin fractions in each tissue contributes to this diversity but the significance of these fractional differences is uncertain.A comparison of the half-cystine and glycine content of vertebrateα andØ keratins suggests that theα andØ proteins of reptiles may be related to the softα keratins of mammals and amphibians. Mammalian hard keratins probably represent a uniquely derived group of proteins which are unlike the other vertebrate keratins. The presence of a “high sulphur” matrix component in both hard mammalianα and reptilian Ø keratins may represent some form of molecular convergence which provides these distantly related proteins with similar physical or organizational properties.

Functional-morphological and biochemical correlations of the keratinized structures in the African Grey Parrot, Psittacus erithacus (Aves)

SummaryKeratinized structures from the African Grey Parrot (feather, down, claw, scale, rhamphotheca, soft lingual epithelium, and lingual nail) were compard by combining biochemical and functional-morphological approaches. At the molecular level, the keratinized structures of Psittacus erithacus are organized essentially like those of other avian species. Correlations were established (or verified) between the mechanical properties of the tissues and the molecular size of the keratin monomers, between the mechanical properties and the x-ray diffraction patterns of the tissues, and between the Polyacrylamide gel electrophoresis (PAGE) patterns of the keratins and certain aspects of growth patterns of the structures. The keratin proteins of the lingual nail, described here for the first time, resemble those of the claw and rhamphotheca. Morphological, biochemical and functional differences between the lingual nail and the rest of the lingual epithelium were established.

[29] Identification of carotenoid pigments in birds

Publisher Summary This chapter discusses the identification of carotenoid pigments in birds. One extraordinary feature of avian carotenoids is their packaging. Feathers are unique to birds and form the interface between a remarkable metabolic machine and an unforgiving environment. The colors and patterns of their display are exceedingly important in individual and species recognition and in myriad aspects of communication. Carotenoids in birds are not limited to the feathers. The skin of various exposed parts, such as legs, feet, bill, caruncles, and comb, may contain carotenoids, and the skin color of chickens is a marketing consideration. The type and age of the feed influences the chicken skin color and can influence public acceptance of the product. Commercial poultry houses pay considerable attention to the relationship between feed and skin or yolk color. Carotenoids have been identified in integumentary structures, such as feathers, bill, and feet of birds from about 19 families and 10 of the extant orders, and are presumed to be widespread in the group. Standard techniques have been adapted for the isolation and characterization of carotenoids to study a series of natural situations. With this, documentation of chemical changes responsible for seasonal plumage change, sexual dimorphism, and subspecific differences in species has been possible. This success has been subsequently extended to speculation regarding both metabolic regulation and genetic control.

Genetic Polymorphism in New Guinea Starlings of the Genus Aplonis

of Hubby and Lewontin (1966) and Lewontin and Hubby (1966), there has been considerable interest in determining the percentage of the genome that may be either heterozygous in individuals or polymorphic in populations. Comparable data for natural populations of many species, both vertebrates and invertebrates being represented, are now available. However, the extent of protein polymorphism and individual heterozygosity in natural avian populations is known for relatively few species (Bush 1967; Sibley and Corbin 1970; Nottebohm and Selander 1972). Several other studies of protein polymorphism in bird populations have dealt with only a few loci (Stratil and Valenta 1966; Brush 1968, 1970; Bush et al. 1970; Ferguson 1971; Brush and Scott 1972). Most of the work on the specific variation of bird proteins involved domestic species. In this category, proteins found to be polymorphic include the serum esterases of the Japanese Quail (Coturnix coturnix) (Kaminski 1964; Manwell and Baker 1969), several species of pigeons (species of Columba and ALAN H. BRUSH

Self-assembly of avian φ-keratins

Solubilized proteins from avian epidermal structures are heterogeneous in sequence, share a common tertiary structure, and have similar tissue-specific molecular weights. The proteins, in the thiol (SH-) form, will self-associate in urea-free, neutral-pH, low-salt buffers and form tonofilaments indistinguishable from native filaments. The mechanics of these processes are similar to those of the α-keratins of various mammalian tissues, although the size and nature of the subunit, filament geometry, and relation to tissue morphology are different.

Pigmentation in the Scarlet Tanager, Piranga olivacea

Conspicuous coloration of passerines and probably of many other birds is important in species recognition and sexual behavior (Hamilton, 1961). The signal functions of plumages have accompanied the evolution of sexual dimorphism and play an important role in the maintenance of the integrity of the species. The tropical avian subfamily Thraupinae (the tanagers) has many brightly colored members. But in most species the sexes are similarly colored, and the majority of the species are nonmigratory and remain paired throughout the year. Sexual dichromatism occurs chiefly in migratory species and in nonmigratory species of which the male is brilliantly colored and which flock during the nonbreeding season (Skutch, 1954). Nuptial color changes are found less frequently and seem to be limited exclusively to migratory species (e.g., Piranga) . In spite of the extensive documentation of the occurrence of dichromatism in avian plumage, there is a paucity of data on the chemical nature of this phenomenon. The bright colors characteristic of the plumage of birds offer challenging problems in the fields of pigment chemistry and biochemical evolution and variation. Except for the work of Fox (1962a, b, c; 1965; 1966), on the display and fractionation of carotenoids in the Ciconiiformes and the work of Vijlker and his colleagues on the canary (1961, 1962), there is relatively little known about the metabolism and biochemistry of avian carotenoid pigments. There have been no extensive investigations of variability in pigmentation on the generic or specific level, and there is only the work of Test (1942) on the pigmentation of hybrid birds. The following report concerns the seasonal and sexual variation of pigmentation in the Scarlet Tanager, Piranga okvacea, and includes comparative data from other North American representatives of the genus Piranga.

Correlation of protein electrophoretic pattern with morphology of normal and mutant feathers.

Differences are demonstrated in electrophoretic patterns of SCM proteins extracted from the shaft and vane between the plumulaceous and pennaceous portions of normal feathers. Supportive evidence for these differences is given by scanning electron micrographs. In various mutant feathers, the observed structural and electrophoretic differences were due to the distribution of plumulaceous and pennaceous parts, not to new proteins. Feather mutants appear to be due to regulatory gene changes rather than to structural gene products.

An Electrophoretic Study of Avian Eye-Lens Proteins

resulted in comparative studies of many different characters. Within the past few years it has become clear that the structure of protein molecules is a potentially productive source of systematic data, because of the relationship which exists between the genetic material (DNA) and the linear sequence of the amino acids composing a protein molecule. The rationale behind the use of protein structure in taxonomic studies has been discussed in previous papers (Sibley, 1960, 1962, 1964, 1965). Several protein systems in vertebrate animals have been explored as sources of data for classification. Among the more extensive electrophoretic comparisons are those of Dessauer and Fox (1956) on the serum proteins of amphibians and reptiles, Johnson and Wicks (1959) on mammalian serum proteins, and Sibley (1960) on avian egg-white proteins. The symposium volume edited by Leone (1964) contains several papers relating to proteins as sources of taxonomic data. The lens of the vertebrate eye possesses several characteristics which suggest that its proteins should be an excellent source of taxonomic information. It is a discrete, easily isolated structure which is extremely simple to collect even under field conditions and it contains the highest concentration of protein of any structure in the vertebrate body, 35 per cent by weight. The lens becomes cytologically isolated early in embryonic development, contains only epithelial cells, and grows slowly throughout the life of the animal, thus becoming more dense with age. There is no direct blood supply to the lens and its metabolism is sluggish, with metabolic processes limited almost exclusively to glycolysis in which about one-fifth of the glucose pathway is through the pentose-phosphate shunt (Ely, 1949). Aerobic metabolism may be confined to the epithelium and cortex (van Heyningen and Pirie, 1953). The only other significant metabolic pathway is proteolysis, a process mediated by peptidase enzymes with esterase activity. Recently Swanson (1966) demonstrated the existence of lysosomes in the lens epithelium. The functions of other substances, for example ophthalmic acid, ascorbic acid, and glutathione are obscure. Van Heyningen (1962) suggests that they may function as co-

Plumage pigment differences in Manakins of the Pipra erythrocephala superspecies

-We investigated the carotenoids found in the head feathers of three members of the Pipra erythrocephala superspecies by chromatographic, spectrophotometric, and chemical means. The Golden-headed Manakin (P. erythrocephala) primarily deposited yellow hydroxycarotenoids in its head feathers, predominately lutein. Red keto-carotenoids were also deposited locally. Canthaxanthin, for instance, was identified in the tips of nape feathers. In contrast, the Red-headed Manakin (P. rubrocapilla) deposited mostly orange and red ketocarotenoids. An orange pigment identified as a-doradexanthin was the most abundant. The common red pigments astaxanthin and canthaxanthin were also present. Finally, feathers of the red-headed Round-tailed Manakin (P. chloromeros) yielded a complement of carotenoids very similar to the Red-headed Manakins. In addition, the Round-tailed Manakin deposited moderate amounts of rhodoxanthin, a plant keto-carotenoid of pronounced red hue. Within individual Red-headed Manakins, we observed differences in total carotenoid content and composition among head regions that differed slightly in color. The distal and proximal portions of individual feathers also differed markedly. We discuss possible physiological and biochemical mechanisms for these conditions, and suggest their relationship to the mechanisms responsible for the species-specific differences in manakin coloration. We reveal the probable origin of the Latin misnomer for the Golden-headed Manakin. Received 2 August 1988, accepted 2 August 1988. THE four species of Neotropical manakins that compose the Pipra erythrocephala superspecies (Snow 1979) differ conspicuously in the combination of their head, thigh, and underwing colors (Table 1). The difference in head color is particularly striking between the Golden-headed Manakin (Pipra erythrocephala) and its close relatives. The golden top and sides of the head of P. erythrocephala, belying its scientific name, contrast sharply with the bright red head of the other three allospecies. The colors involved are generally bright, and presumably implicate carotenoid pigments (Brush 1981). However, the biochemical and genetic basis of the color differences remains unexplored. P. erythrocephala is closely related to the Redheaded Manakin (P. rubrocapilla), with which it has been grouped in a single species (P. e. erythrocephala and P. e. rubrocapilla of Hellmayr 1929). The distribution of P. erythrocephala and P. rubrocapilla at their area of closest contact is delimited largely by the Amazon River. The 3To whom all reprint requests should be sent. occurrence of morphological differentiation associated with rivers is often found among understory Amazonian forest birds, a pattern largely unique to Amazonia (e.g. Hellmayr 1910, Snethlage 1913). One interpretation is that rivers act as barriers to gene flow and serve as geographical isolating mechanisms (Sick 1967). Capparella (1987, in press) reported large genetic distances between the two manakins, in excess of the mean for avian species [Neis (1978) D = 0.101; avian mean 0.0440 ? 0.0221 SD, Barrowclough 1980] based on allozyme studies. Moreover, fixed differences were detected at three loci, a condition often lacking between undisputed avian species. Carotenoid pigments, responsible for most of the bright colors in birds, are relatively wellknown chemically. Furthermore, considerable work has been concerned with their biochemical modification and processing in birds (reviewed in Brush 1981). Differences in feather carotenoids are determined by both the processes responsible for their absorption and transport, and the metabolic capacities of the 34 The Auk 106: 34-41. January 1989 This content downloaded from 157.55.39.135 on Sun, 03 Jul 2016 06:06:41 UTC All use subject to http://about.jstor.org/terms January 1989] Pigment Differences in Pipra 35 birds to modify the pigments. Hence, carotenoid analysis can be used to infer physiological, and the underlying genetic, differences. In addition to providing specific plumage color and patterns (Fox and Hopkins 1966, Fox et al. 1967, Brush 1970, Brush and Johnson 1976, Troy and Brush 1983), carotenoid differences account for color polymorphisms (Volker 1964, Brush and Seifried 1968, Johnson and Brush 1972), subspecific plumage variation (Test 1942, Ford and Simpson 1987), and plumage variants (Volker 1964, Brush 1970, Hudon and Brush in press). To elucidate the nature of the physiological differences that confer species specificity of coloration in the manakins, we determined the pigment constitutions responsible for the difference in head color between P. erythrocephala and P. rubrocapilla. The Round-tailed Manakin (P. chloromeros), another member of the P. erythrocephala superspecies, was also ex-