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Skin derivatives in vertebrate ontogeny and


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Article in Biology Bulletin January 2009


DOI: 10.1134/S1062359009020101

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ISSN 1062-3590, Biology Bulletin, 2009, Vol. 36, No. 2, pp. 175183. Pleiades Publishing, Inc., 2009.
Original Russian Text O.F. Chernova, 2009, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2009, No. 2, pp. 218227.

CONFERENCE
PROCEEDINGS

Skin Derivatives in Vertebrate Ontogeny and Phylogeny


O. F. Chernova
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences,
Leninskii pr. 33, Moscow, 109117 Russia
e-mail: chernova@sevin.ru
Received June 24, 2008

AbstractThe skin of vertebrates has numerous and diverse derivatives, either located within the epithelial sheet
itself (glands) or extending above its surface (teeth, scales, feathers, hairs, etc.). Many of them have a modular struc-
ture and constitute structuralfunctional units. Ontogenetically, all skin derivatives are of ectomesodermal origin, and
their morphogenesis is subject to metabolic control, heterochronies (divergence in the timing of origination and
development), and regulation by means of tissue interactions and molecular signaling via similar pathways. The
diversification (origination of morphological diversity) of skin derivatives within the same morphological type is
explained by the development of new generations of ectomesodermal structures separated by heterochronies and
regulated by changes in the gradients of molecular signaling pathways under the influence of environmental factors.
Evolutionary relationships between the majority of skin derivatives are obscure, except for teeth and glands asso-
ciated with sensory organs that have evolved together with these organs. Apparently, many vertebrate skin derivatives
(scales, feathers, hairs, and glands) originated as novelties at nodal stages of phylogeny and subsequently evolved
convergently or in parallel.
DOI: 10.1134/S1062359009020101

INTRODUCTION Attempts to discuss the problem with regard to compar-


The problem of origination and diversification of ative morphological, biochemical, molecular biologi-
skin derivatives in vertebrates is still a challenge to cal, and tissue engineering data show that such a com-
zoologists. The main difficulty in solving it is that, in prehensive approach holds much promise for solving it
contrast to the situation with other organ systems (mus- (Chuong and Homberger, 2003; Wu et al., 2004; Cher-
culoskeletal, nervous, excretory, etc.), it is hardly pos- nova, 2006, 2008a, 2008b; Fuchs, 2007).
sible to trace evolutionary relationships between the This article deals with only a few aspects of the prob-
derivatives characteristic of representatives of different lem, with attention being paid to (1) skin derivatives as
classes. Moreover, numerous cases of parallelism and modular structures, (2) ways to resolve antagonism
convergence make identification of the general trend of between the glandular and supporting functions of the
their evolution even more difficult. The discussion of skin, (3) morphogenesis of skin derivatives and hetero-
the problem is accompanied by the advancement of chronies, (4) convergence and parallelism as trends in the
numerous hypotheses and conjectures that cannot yet evolution of skin derivatives, (5) hypotheses concerning
clarify the evolutionary scenario concerning the origi- evolutionary relationships between the skin derivatives,
nation, morphogenesis, diversification, and homology and (6) substantiation of the generative concept of the
or historical divergence of these structures. This is due origination and diversification of skin derivatives. The
to the scarcity of relevant paleontological, embryologi- analysis is based on the most recent results of research in
cal, and comparative morphological data. Views on comparative anatomy, developmental biology, molecular
evolutionary transformations of skin derivatives based biology, and tissue engineering, as well as on our generali-
on their morphology are largely contradictory, since zations of empirical data and original long-term studies
they are not supported by factual data on the initial and on the morphology of feathers, hairs, and glands in more
transitional forms of these derivatives, induction of than 100 bird species and 400 mammal species (Sokolov
their morphogenesis, differences in the biochemical et al., 1988a, 1994; Sokolov and Chernova, 1994a,
composition of tentative homologous structures, etc. 1994b, 2001; Chernova, 1996, 2006, 2008a, 2008b;
Many of them have the typical drawback noted by Chernova and Tselikova, 2004; Shabadash and Cher-
Matveev (1932): they are based on the analysis of mor- nova, 2006; etc.).
phological structures in a direct consecutive series of The integument epithelium of chordates underwent
extant forms, but this approach does not allow their major transformations in the course of phylogeny,
evolutionary relationships to be revealed, since com- changing from a monolayer sheet of uniform nonkerati-
parisons are made not between ancestors and descen- nized cells capable of secretion (in Acrania and Tunicata)
dants but rather between definitive forms representing to a multilayer stratified epithelium, either nonkerati-
terminals of lateral branches of the phylogenetic tree. nized (in cyclostomes and fishes, with a few exceptions)

175
176 CHERNOVA

or keratinized partially (in amphibians) or completely (in which is due to their various morphological modifica-
amniotes). The skin is an exclusive evolutionary acquire- tions; (7) specific features of skin morphology and
ment of vertebrates, and it should be discriminated from functions acquired as adaptations to environmental
the integuments of other animals. The skin consists of conditions; and (8) the absence of evolutionary succes-
two tissues differing in origin, namely, the epithelial and sion between skin glands that have evolved in different
connective tissue layers separated by a basal membrane. classes of Vertebrates.
The surface epidermis is of ectodermal origin, while the Skin derivatives as modular structures. Skin deriva-
underlying derma is a mesodermal derivative developing tives may be considered in terms of methodological
on account of the somite dermatome. These layers exert approaches aimed at systematizing data on the morpho-
reciprocal influences on each other when forming differ- logical diversity of structures in a complex organ, such
ent derivatives during ontogeny. The emergence of verte- as structural histology (Savostiyanov, 2005), the con-
brates on land, the main historical event in their phylog- cept of structuralfunctional units (Khrushchev and
eny, was reflected in the development of two basic types Brodsky, 1961; Terskikh et al., 2003), or a theory of
of the cover epithelium, essentially aquatic and terres- modular structure of the organisms and their organs
trial, with the transitional amphibiontic or ichthyoid type (Marfenin, 1999; Notov, 1999; Savostyanov, 2005).
(Chernova, 2008b). Feathers, nails, hairs, horns, as well as fish scales and
Skin derivatives are numerous and diverse. They can animal epithelial tissues are classified as modular
be divided into appendages, or structures extending objects. The reason for identifying structuralfunc-
above the skin surface, and glands, which lie within the tional units within an intricately functioning organ is
skin. However, this division is obviously tentative. For that such an organ is always heterogeneous and the
example, hair and feather follicles lie in the dermal or properties of its compartments may vary widely (but
even hypodermal layer, with only the keratinous shaft within limits of the norm), whereas the properties of its
of these structures protruding outward. Glands lie structuralfunctional unit are much more stable and
within the skin but often have accompanying skin or different variations do not affect the principles of its
keratinous protrusions. The same applies to keratiniza- organization (unless in pathological cases). For exam-
tion. Scales, feathers, and hairs are keratinous struc- ple, we consider that a structuralfunctional unit of a
tures, whereas glands are not keratinized. However, the hepatoid SG is its individual lobe with a system of
follicles of feathers and hairs are not subject to kerati- secretory ducts, accessory structures (the hair, hair fun-
nization and remain capable of regeneration, while the nel, and cistern in which the secretion accumulates and
ducts of many glands are keratinized. matures), and associated apocrine and sebaceous
glands (together with the hepatoid SG, they form com-
The presence of glands is a characteristic feature of bined lobes and ducts). This complex provides for the
the skin of vertebrates and chordates in general. synthesis, maturation, and release of the complete
Although the skin of reptiles and birds is traditionally hepatoid gland secretion, supplementing it with addi-
considered nonglandular, it does contain specialized tional protein or glycoprotein, lipids, and melanin.
structures analogous to glands. Skin glands are capable
of production and release of secretions synthesized by The hair follicle complex is also an example of
glandulocytes (glandular cells). They are convention- structural-functional unit. In addition to the follicle
ally separated into common glands (CGs) and specific itself, it includes the connective tissue envelope, dermal
glands (SGs), which differ in numbers, topography, papilla, glands, muscles, vessels, nerves, epidermal hair
structure, the composition and amount of secretion, and funnel, and hair shaft.
biological significance. Glands also demonstrate the modular type of orga-
Some trends in the evolutionary development of nization, which is known to pertain to systems with a
integuments can be noted in the phylogeny of verte- modular structure, sustainable growth, and cyclic mor-
brates. They are as follows: (1) gradual thickening of phogenesis. Glandular fields may be classified as dis-
the cover epithelium and its differentiation into special crete modular objects, since they consist of CGs
cells, layers, and structures; (2) maintenance of similar equivalent, interchangeable elements showing rela-
structure and omnipotence of the germinative epider- tively loose connections with one another. On the other
mal layer, which gives rise to all other skin structures, hand, SGs consisting of indispensable, strongly inter-
including glands; (3) similar differentiation of glandu- connected elements and firmly integrated compact
lar structures into CGs and SGs in all vertebrate classes; organs are examples of unitary objects.
(4) gradual improvement of morphophysiological coor- Ways to resolve antagonism between the glandular
dination between the structure of the secretory gland and supporting functions of the skin. Skin keratiniza-
region and the mode of its secretory activity; (5) multi- tion accompanied by degeneration of epithelial cells
functionality of the skin cover and its glandular appara- (keratinocytes and corneocytes) and the secretory
tus, with their different functions being in a dynamical capacity of glandulocytes are in antagonism to each
equilibrium and offering examples of antagonism, sub- other. This antagonism can be resolved by means of (1)
stitution, or mutual complementation; (6) functional spatial segregation or (2) heterochronies of anlagen and
analogy between the glands of different vertebrates, their derivatives in the course of development or (3)

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SKIN DERIVATIVES IN VERTEBRATE ONTOGENY AND PHYLOGENY 177

combination of both functions at the cell level, i.e., in atives, with the influence of mesenchyme on the forma-
the same epithelial cell. In the first case, glands develop tion of ectodermal structures being either positive (in
in the areas that are neither keratinized nor covered the morphogenesis of skin appendages) or negative (in
with skeletal structures or descend to the derma or gland morphogenesis). For example, Schmalhausen
under the skin. Thus, glandulocytes are isolated from (1964) refers to the inhibitory effect of mesenchyme on
corneocytes (in most glands of mammals). In the sec- the development of paired cement SGs in tadpoles. In
ond case, glands originate and develop prior to the the norm, these glands develop on the ventral head sur-
onset of keratinization. In the third case, epithelial cells face only in the area where the ectoderm is separated
acquire the ability to combine the glandular function from the mesenchyme by the anterior gut wall. This
with keratinization (i.e., with the supporting function). effect is confirmed by the fact that the whole ectoder-
Such a combination is observed, for example, in sebok- mal explant can transform into a sucker in the absence
eratinocytes of birds or in certain epidermal layers of of contact with the mesenchyme.
reptiles. Feathers and scales arise via mesenchyme-induced
The problem of antagonism between the secretory evagination of the epithelium and mesenchyme. If hairs
and supporting functions can also be considered on the and all glands had arisen only via invagination of the
premise that keratinization is a secretory process epithelium and mesenchyme, this would have been one
involving the synthesis and secretion of specific protein more perfect example of alternative bifurcation of
(keratin) accompanied by cell degeneration. In such a developmental programs (Oster and Albrech 1982). It
case, all integuments are regarded as secretory organs should be noted that, in the English literature, the term
with different types of secretory activities, which com- invagination is applied to the morphogenesis of
plement rather than oppose each other. The epidermal appendages such as hairs and glands, which is incorrect
corneous layer is actively shed off. In many mammal in our opinion, insofar as this term refers to the forma-
species, SGs have epidermal thickenings (callosities) tion of an embryonic layer or organ by its infolding into
whose corneous layer is shed off to be accumulated in the subsiding lower layer. In fact, actual epidermal
the saccular gland cavity. Thus, it becomes an essential invagination occurs only in morphogenesis of saccular
component of the secretions of many glands, obviously SGs, in which the central cavity is formed due to invag-
enriching them with additional odoriferous substances. ination of the epidermis into the subsiding dermal layer,
followed by the growth of glandular parenchyma. For
Morphogenesis of skin derivatives and heterochro-
example, saccular poison and luminescent glands of
nies. Self-organization and tissue interactions provide a
fishes, most SGs of reptiles, and various saccular
basis for morphogenesis of different organs, including
glands of mammals are formed in this way. Moreover,
ectodermal organs (Beloussov, 1987; Cherdantsev,
these saccular organs do not necessarily have a duct that
2003; Terskikh et al., 2007). In interactions of the cover
opens on the body surface, as in most SGs of amniotes:
epithelium and mesenchyme, a major role is played by
there also are glands confined within the dermal layer,
somatic stem cells and signal proteins inducing their
as is the case with saccular photophores of fishes. In
proliferation (Shh, FGF, Wnt, notch, BMP, etc.), which
many cases, such saccular SGs are capable of protrud-
are common to all skin derivatives. This role is well
ing above the skin surface or even everting, releasing or
studied for the morphogenesis of feathers (Wu et al.,
ejecting an odorous secretion.
2004), hairs (Fuchs, 2007), sebaceous CGs, and mam-
mary SGs (Fuchs, 2007; Terskikh et al., 2007). It has Invagination occurs at later stages of morphogenesis
been shown that minor shifts in the genetic develop- of the feather follicle: the epidermis invaginates around
mental program result in significant structural changes the feather anlage to form the sheath of the cylindrical
such as conversion of hair anlagen into CGs in tissue follicle. Feather morphogenesis involves specific pro-
culture, the growth of hairs in the mouth, or develop- cesses such as the displacement of the growth zone
ment of teeth in chicks. from the apical end of skin outgrowth down to the sides
of the follicle (which rarely takes place in the skin),
What are the features of similarity and difference in localization of several stem cell populations, and
the morphogenesis of skin derivatives that can be branching of the vane via apoptosis of marginal plate
revealed by comparative analysis? The features com- cells rather than via differential cell proliferation
mon to all amniotes are (1) segregation of special skin (Lucas and Stettenheim, 1972). This is why feather his-
fields in which these derivatives arise (pterylae in birds, togenesis is referred to as reverse branching morpho-
vibrissa pads, food pads, glandular fields, etc.); (2) het- genesis, in contrast to simple branching morphogene-
erogenization of initially homogeneous skin fields sis characteristic of, e.g., the lungs and mammary
through the formation of dermal condensations subja- glands (Lucas and Stettenheim, 1972; Wu et al., 2004).
cent to placodes (epithelial cell clusters); and (3) actual The dorsal and ventral sides of the feather produced by
morphogenesis of skin derivatives, which proceeds by the intermediate epidermal layer of the cylindrical fol-
different scenarios but always on the basis of epithe- licle are not homologous to the corresponding sides of
lialmesenchymal interactions. the scale, which are derived from the upper epidermal
Reciprocal epithelialmesenchymal interactions are layers. This contradicts the hypothesis concerning the
of great significance for the development of skin deriv- origin of feathers from scales of the ancestral forms

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178 CHERNOVA

(Chernova, 2008a). In the formation of feathers, the dular parenchyma and cyclic regeneration of glandular
upper epidermal layers produce only a corneous sheath epithelium on account of stem cells of the epidermis and
that is shed when the feather unfolds. hair follicle.
The molecular mechanisms of feather morphogene- One more pathway of gland morphogenesis, alterna-
sis have been studied in detail. Different signal proteins tive to the ingrowth of the epidermal anlage into the
operate on each stage of feather development, regulating derma, is the ingrowth of mesenchyme into the epider-
morphogenesis. A detailed model of gene influence on mis. For example, CG anlagen in salamanders appear at
feather development (the transgenic feather protocol) early stages of larval development as spherical cell
has been proposed, which hypothesizes that the diversity buds in the epidermis. Such a bud does not submerge
of feathers depends on the orientation and slope of into the dermal layer; conversely, the mesenchyme
molecular gradients that condition the topological struc- actively penetrates the epidermis and surrounds the bud,
ture of the feather epithelium. Thus, the relationship isolating it from supporting epidermal cells (Sokolov
between the activity of signal proteins and the shape and et al., 1988a). Further differentiation of myocytes and
novel function of the organ has been revealed (Widelitz glandulocytes takes place in this isolated structure, and
et al., 2003, 2007; Wu et al, 2004; Yue et al., 2006). For only then does the gland sink into the corium. This devel-
example, the inductive activity of the dermal papilla cre- opmental scenario principally differs from the above
ates a gradient of the signal protein Wnt3, which deter- process of gland formation in the majority of amniotes,
mines a helical pattern of barb ridges and guides the in which the proliferating and differentiating epidermal
symmetrical branching of the vane. The Wnt gradient bud actively grows into the corium, where its further
accounts for the transformation of bilaterally symmetric morphogenesis takes place. Common to these alternative
contour feathers into radially symmetric down feathers. processes is early isolation of glandular structures from
The Noggin protein increases the degree of feather
supporting cells, which is achieved either with the aid of
branching, while BMPs increase the size of the feather
mesodermal envelopes or due to the bud submergence
shaft (Yu et al., 2004). The ratio of antagonistic noggin
into the corium. Both mechanisms provide for spatial
and BMP4 plays an essential role in feather branching,
separation of glandular and supporting integumental
determining the number and size of barbs; BMP4 regu-
structures.
lates the formation of the feather shaft and the interlock-
ing of barbs; Shh induces apoptosis of the marginal plate In mammals, CG morphogenesis is associated with
epithelium, which leads to the formation of barbs (Yu et hair morphogenesis (except for initially independent
al., 2002; Chang et al., 2004a, 2004b). In general, the eccrine and sebaceous glands): both sebaceous and
order of appearance of signal molecules in feather apocrine glands are derivatives of the hair follicle. The
morphogenesis is as follows: FGF4, BMP4 Shh, hair follicle itself is formed via the ingrowth of the epi-
Wnt-7a notch-1, Serrate-l, Delta-1 Msx-1, thelium into the mesenchyme (Sokolov et al., 1988b).
Msx-2 Hox, NCAM. Thus, topological transforma- Processes characteristic of different stages of hair mor-
tions of the feather from a cylindrical corneous to a hier- phogenesis are as follows: (1) aggregation, prolifera-
archically branching structure are controlled by molecu- tion, and differentiation of epithelial and mesenchymal
lar mechanisms, which have apparently provided the cells in the follicle anlage region; (2) the intimate inter-
possibility of development of different feather forms action of the epithelium and mesenchyme, which can
both in ontogeny and in phylogeny. even come in direct contact with each other, being not
The morphogenesis of CGs proceeds via the separated by a basal membrane; hairs fail to form with-
ingrowth of the epithelium into the dermal layer out the involvement of mesenchyme; (3) the appear-
(Sokolov et al., 1988b), and no invagination takes place. ance of first keratinization centers in the hair anlage
In Anamnia, the morphogenesis of glandulocytes is a rather than in the epidermis; 4) the growth of the hair
process of proliferation and differentiation of basal-layer bulb in two directions simultaneously: its further
epithelial cells or of other glandular cells tightly attached ingrowth deeper into the derma is accompanied by the
to the basal membrane. In the lamprey, for example, the upward movement of differentiating cells; and (5)
sequence of events is as follows: undifferentiated simultaneous formation of the anlagen of sebaceous,
cells glomerular supporting-glandular cells apocrine, and hepatoid glands (on account of the epi-
protein glands protein secretion. In amniotes, the thelium of the follicle anlage), the bulge zone, and then
CG lumen starts to form in lower secretory regions, the hair erector muscle (on account of mesenchymal
along with an increase in the mass and secretory activity cells). The bulge zone is not only the site of muscle
of glandular parenchyma; consequently, the central cav- attachment, but it also accommodates a population of
ity and ducts are formed, with the excretory duct opening hair follicle stem cells accounting for the formation of
on the surface. Therefore, CG structures differentiate in a new hair follicle and participating in regeneration of
the outward direction, and this concerns both alveolar the epidermis (Terskikh et al., 2007; Fuchs, 2007). One
and tubular glands. It should be noted that sebaceous and more stem cell population is hidden deep in the hair
hepatoid glands of mammals during the postnatal period bulb matrix, above and around the dermal papilla. Sub-
undergo continuous processes such as, the formation of sequent growth and differentiation of the hair follicle
secondary ducts and cavities due to cell death in the glan- lead to the upward extension of the hair shaft and its

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SKIN DERIVATIVES IN VERTEBRATE ONTOGENY AND PHYLOGENY 179

eventual emergence on the surface through a special the cover epithelium for proliferation and differentiation,
cleft in the epidermis, above the hair follicle. under conditions of unity and antagonism of the support-
Molecular mechanisms of the morphogenesis of ing and glandular functions of the integument.
hairs and their sebaceous glands are known (Fuchs, Analogies among skin derivatives are readily dis-
2007). Thus, the formation of a placode, its further cernible. For example, many SGs in representatives of
growth, and differentiation of hairs into different mor- phylogenetically segregated taxa have similar structure,
phological types are under control of the Wnt/BMPs which is especially true of signal SGs involved in scent
signal protein gradient with the involvement of other communication or of SGs whose secretions protect sen-
regulators such as the Wnt/noggin gradient, Shh, Lef1, sory organs and mucous membranes. Skin glands are
and Lef2. For example, mice devoid of Lef1 have only the derivatives of germ layers and function as heteroge-
guard hairs, while other hair types are absent. All these neous organs consisting of compartments derivative
processes are subject to mesenchymal induction. For from the epithelial, connective, nervous, blood, and
example, the derma has an effect on the size and density muscle tissues. These integrated SG are present in all
of follicles, which is confirmed by molecular differ- classes of Chordata, except for Acrania.
ences between dermal cells from different body
regions. The Sonic hedgehog gene (Shh), identified The feather follicles of birds have no CGs, which is
among genes expressed early in the placode, plays a explained by the need for reducing the weight of integ-
key role in condensation of dermal cells into dermal uments; the impossibility of feather lubrication from
papillae, which are an essential component of the hair the follicular funnel opening; the development of the
follicle. The dermal papilla is the source of signal for uropygial gland specialized for taking care of feathers,
the placode ingrowth leading to the formation of the with body aerodynamics remaining unimpaired (due to
hair follicle, which subsequently matures under the a certain position of the gravity center); and the hydro-
effect of further epithelialmesenchymal interactions. phobic properties of feather keratin itself. Nevertheless,
Stem cells in the bulge zone become active during the sebocytes of the outer peripheral (sebaceous) part of
anagen phase, when the dermal papilla reaches this the uropygial gland are very similar to those of mam-
region and apparently induces dormant stem cells. malian sebaceous glands in both morphological and
However, these processes differ from those of embry- biochemical features. This appears to result from con-
onic hair anlage formation. vergence or may be an organotypic trait of sebaceous
Precursor cells of sebaceous glands appear at later glandulocytes.
stages of intrauterine development (in mice), but the Historically segregated structures such as hairs and
glands themselves begin to function only after birth. feathers can also provide an example of convergent
The processes of sebocyte differentiation are also sub- similarity. It is known that mammals and birds repre-
ject to the effect of signal proteins, such as c-myc and sent two autonomous phylogenetic branches. Among
the adipogenic transcriptional factor PPAR-gamma. In vertebrates, only they are homoiothermal. The outer
analyzing the periodicity of gland functioning, the coats in both classes, fur in mammals and plumage in
question arises as to the source of new glandulocyte birds, serve to maintain body homeostasis. Hence,
generations. It has been proved in many cases that they questions logically arise as to the degree of similarity in
originate from nondifferentiated somatic stem cells structural adaptations of hair and feather coats provid-
located in the germinative layer of the epidermis, which ing for their heat-insulating properties as well as in
is additional evidence for the potential secretory func- morphological structures accounting for performance
tion of epithelial cells. In the sebaceous glands of mam- and interrelation of their different functions. In addition
mals, for example, the glandular parenchyma is to structural similarity of hair and feather coats (strati-
restored due to epidermal stem cell migration along fication, distinct differentiation, regeneration capacity,
duct walls to the glandular acini, where these cells dif- production of different generations, cyclicity of growth,
ferentiate into glandulocytes. Stem cells take part in periodic molting, etc.), their main structuralfunctional
restoring the functioning of sebaceous glands after the units are similar as microanatomical corneous struc-
death of sebocytes: as shown in tissue culture, they tures (similar development of air cavities, three-layered
form a layer of nondifferentiated cells that are precur- structure, etc.) (Chernova 2005a, 2005b, 2006, 2008a).
sors of sebocytes. Stem cells from the bulge zone also Polymorphism of hairs and feathers is due to the exist-
participate in regeneration of sebaceous glands during ence of their several generations produced by the folli-
skin wound healing. cles during ontogeny, while specificity of their topogra-
Convergence and parallelism in the evolution of skin phy and structure is accounted for by molecular mech-
derivatives. The evolution of skin derivatives in verte- anisms and other factors, including developmental
brate phylogeny apparently followed parallel and con- changes in metabolism. From this standpoint, hair and
vergent pathways against the background of adaptive feather follicles can be defined as dynamic systems
radiation of taxa. It proceeded due to quantitative and with sufficiently high plasticity (allowing changes in
qualitative morphological transformations based on the the morphological type of a hair or feather) that are sub-
capacity of the germinative layer (stem somatic cells) of ject to age-related and seasonal changes. Hair and

BIOLOGY BULLETIN Vol. 36 No. 2 2009


180 CHERNOVA

feather follicles are similar in many respects, but this large branches of mucous and protein glandulocytes of
similarity is a result of convergence. Anamnia, with various modifications, and then into
Similarity due to convergent evolution, in contrast to sebaceous and sweat glands of Amniota. The branch of
that due to parallelism, is always superficial and con- mucous glands terminates in the class Amphibia
cerns only a few structural traits of the convergent (although in amniotes they are preserved only in mucous
groups (Schmalhausen, 1969); in our case, this is the membranes, epithelial cells remain capable of mucous
architecture of feathers and hairs. The analogy in their metaplasia), and the protein gland branch terminates in
architecture can probably be classified as homoplasy the class Reptilia, after giving rise to corneous epidermal
(the term introduced by Lankester (1870); cited from cells. These cells provided a source for the development
Blyakher, 1976), i.e., structural similarity that have of glandular structures in Amniota. The lateral branch of
arisen independently but on a common morphological enamel-secreting protein glandulocytes (ameloblasts
basis. In our case, such a basis is the epithelialmesen- forming the teeth) extends from the ancestors of carti-
chymal interaction. This follows from the unity of both laginous fishes to mammals inclusive. In this attempt at
molecular-genetic mechanisms of developmental regu- phylogenetic reconstruction, the above author makes a
lation and life cycles of hairs and feathers. This phe- typical error, since the phylogeny is typically erroneous,
nomenon provides an example of convergent analogy as comparisons are made between recent forms repre-
(Dogel, 1938) or homotypy (Beklemishev, 1964), senting lateral branches of the phylogenetic tree rather
i.e., of constructional similarity between the structures than direct ancestors and descendants.
under comparison in the absence of genetic succession Other reconstructions, such as attempts to explain
between the corresponding taxa. the polymorphism of homotypic holocrine glands in
Hypotheses concerning evolutionary interrelations reptiles, are also unsuccessful, since their authors
of skin derivatives. As long ago as 1898, Gegenbauer ignore the fact that morphological diversification and
(see Gabe and Saint-irons, 1965) provided an argument complication by no means correspond to phylogenetic
against the hypothesis of evolutionary connection relationships between taxa (Gabe and Saint-Girons,
between the glands of all three classes of amniotes. He 1965; Sokolov et al., 1994; Chernova, 2008b).
argued that sebaceous glands of mammals are closely Lactiferous (mammary) SGs of mammals origi-
associated with hair follicles and, consequently, they nated from apocrine CGs of hairs aggregated into a
are an evolutionary novelty, as is the follicle itself. glandular field (monotremes still have such a field, and
Moreover, their association with hair follicles is main- even hair anlagen are preserved in marsupials). Their
tained throughout ontogeny. However, Severtsov initial function (moistening the eggs laid) changed to
(1949) and Matveev (1949), when considering the evo- that of nourishing the offspring. This was accompanied
lution of hairs, attach no evolutionary significance to by the growth of glandular parenchyma and shaping of
the skin glands and do not regard their origination as an the glandular field into an alveolartubular structure
aromorphosis. In our opinion, it is reasonable to regard with or without a nipple (in the latter case, the secretion
as aromorphosis not only the origination of hairs but trickles down the tufts of hairs). Analogs of lactiferous
also the formation of the glandhair complex as a struc- glands might be present in cynodonts. Signaling path-
turalfunctional unit, insofar as CGs of mammals orig- ways that regulate mammary gland anlage formation
inate from the hair follicle and are closely associated and development in mice were identified. In particular,
with this structure. this concerns the Wnt/-catenin gradient (Veltmaat et al.,
No direct evolutionary connections between the 2003): its blocking in transgenic mice resulted in the
glands of vertebrates belonging to different classes can absence of mammary glands, hairs, and teeth.
be traced, and their structure is not subject to morphologi- Hypotheses concerning the origin of feathers and
cal complication (especially in the case of SGs) even hairs were considered in detail in our previous publica-
upon transition from lower Chordata to Anamnia and tions (Chernova and Tselikova, 2004; Chernova,
then to Amniota. Structural complication of SGs does 2008a). To resolve the widely discussed question of the
not depend on the taxonomic rank of a given group. Even evolutionary connection between the reptile scale and
hagfishes have well-developed mucous SGs with a com- the bird feather, three main approaches has been pro-
plex structure. Very intricate, integrated bacterial and posed: (1) the feather originated from the scale that
luminescent SGs are widespread among fishes. rolled into a tube and then submerged into the derma,
Common to all vertebrate taxa (and Chordata in with consequent formation of a follicle; (2) the feather
general) is that they have the germinative layer of epithe- evolved through the stage of protofeather, a simple
lial cells, whose proliferation and differentiation account tubular corneous outgrowth; and (3) the feather follicle
for the production of all glandulocytes. Quay (1972) as an evolutionary novelty originated first; in due time,
used this fact as a starting point for identifying morpho- it produced a featherlike structure that developed by
genetic lineages of secretory epidermal cells and formu- way of differentiation of a down feather into an asym-
lating the following conclusions. The evolutionary path- metric quill feather, or vice versa.
way starts from the central morphogenetic lineage of epi- Hypotheses concerning the origin of hairs are
dermal stem cells, which subsequently separates into two numerous, but it appears most likely that the hair folli-

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SKIN DERIVATIVES IN VERTEBRATE ONTOGENY AND PHYLOGENY 181

cle originated independently, as a novelty, and that the its germinative layer have genetically determined and
formation of vibrissae and hairs in phylogeny followed potentially different capacities for producing certain
parallel pathways, with vibrissae being more ancient. structures within the limits of a given tissue type (epithe-
Since evolutionary connections of skin derivatives lial or loose connective tissue).
are obscure, some authors chose an alternative On the basis of most recent data, Wu et al. (2004)
approach and constructed a hierarchical series of struc- proposed the concept of morpho-regulation, which
tural complication of these derivatives without consid- implies that morphogenetic processes can be modu-
ering their evolutionary connections (Wu et al., 2004).
lated by morphological regulators that lead to changes
In this series, asymmetric quill feathers of birds are
regarded as the peak of structural complication. Such of morphological phenotypes in development and in
an approach, however, does not solve the problem of evolution. In the evolution of vertebrates, variations in
the evolution of skin appendages. the number and size of skin derivatives could provide a
basis for the development of a spectrum of different
Substantiation of the generative concept of the ori- animal phenotypes (i.e., for adaptive radiation). Such
gin and diversification of skin derivatives. The idea of variations provide the material for selection and, upon
autonomous and independent origin of different skin certain environmental changes, may prove to be an
derivatives is not new. For example, a scheme of their advancement.
independent origin based on ectodermalmesodermal
interactions, proliferation, and/or aggregation of epithe- The analysis of recent data on the vertebrate skin
lial and mesenchymal cells into the anlage producing derivatives and the results of our long-term studies on
different structures in representatives of different classes skin glands, hairs, and feathers provide evidence for the
is presented in the book Hymanis Comparative Verte- concept of their independent evolutionary origin, which
brate Anatomy (1979). This idea is supported not only by can be formulated as follows.
morphological data and heterochronies revealed in the
origination of different skin derivatives (in both ontog- In the evolution of vertebrates, different skin deriv-
eny and phylogeny) but also by the results of molecular atives originated at nodal phylogenetic stages as novel
biological studies. It is in full agreement with the theory ectomesodermal formations and developed in different
of phylembryogenesis by Severtsov (1949), who con- classes independently, in parallel or convergent ways,
nected evolutionary transformations of organs to the ear- depending on specific features of tissue interactions,
liest stages of embryogenesis. metabolic changes, and molecular-genetic regulation of
On the basis of molecular biological studies on the morphogenesis for the maintenance of homeostasis.
morphogenesis of skin appendages, a hypothetical Diversification of structures within the same morpho-
model of their development was proposed, which type was due not to their evolution from the simplest to
shows that all appendages are variations on the same a more complicated form (or vice versa) but rather to
theme (Chuong and Homberger, 2003), since the origination of new generations of ectomesodermal
molecular signaling pathways involved in regulation of structures separated by heterochronies and regulated by
their morphogenesis are similar (Chuong et al., 2000; changes in the gradients of molecular signaling path-
Wu et al., 2004; Fuchs, 2007). The same is true of ways under the influence of environmental factors. Skin
derivatives such as glands (Chernova, 2008b). The derivatives as tissue structures are homologous to each
model suggests that de novo formation of derivatives other, since they originate from the epithelium and
(appendages and glands) from the cover epithelium and mesenchyme, but the same derivatives as organs are not
underlying mesenchyme and their diversification in the connected by evolutionary succession and have not
course of evolution took place under the effects of dif- been derived from each other. Thus, there is no use in
ferent factors: induction of the epithelial anlage by the searching for the pathways of their transformation and
mesenchyme, reciprocal interactions of these tissues constructing evolutionary schemes of transitions
under molecular-genetic control, environmental influ- between these structures, since all of them are novel
ences on molecular processes, and heterochronies of formations. Scales, hairs, feathers and glands origi-
morphogenesis. Differences in signaling pathways and nated as independent integumental organs at nodal phy-
ratios of signaling proteins in the period of morphogen- logenetic stages owing to multipotency of epithelial
esis as well as predetermined potencies of the epithe- and mesenchymal stem cells (within the limits imposed
lium and mesenchyme account for variations of epithe- by the properties of epithelial and mesenchymal tissues
lial organs. and their interactions). The independent origin of these
Experimental studies on cellular and molecular appendages can account for the absence of distinct
mechanisms of morphogenesis by methods of tissue intermediate forms between them. Teeth appear to be
engineering have priority in modern science. In particu- an exception, since ameloblasts are homologous in all
lar, they help in understanding the mechanisms of forma- vertebrates. The same probably applies to the glands
tion and evolution of skin derivatives (Matveev, 1932, associated with sensory organs that have evolved
1949; Quay, 1972; Chuong and Homberger, 2003; Wu et together with these organs (for example, the Harderian
al., 2004). The cover epithelium as a tissue structure and gland in amniotes).

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182 CHERNOVA

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