and How?: Some Speculations on the Evolution of the Vertebrate

A M . ZOOLOCIST, 12:159-171 (1972).

When? Why? and How?: Some Speculations on the Evolution of the Vertebrate Integument PAUL F. A. MADERSON

Biology Department, Brooklyn College, Brooklyn, New York 11210 SYNOPSIS. The basic structure of the vertebrate integument is briefly reviewed. The system is either scaled, non-scaled, or a mixture of the two. Scales are not appendages of the integument, but are patterned folds in which the dermal and/or epidermal components may be elaborated. An appendage is the product of specialized patterns of cell differentiation localized within the dermis and/or epidermis. Scales, and appendages (whether borne within scaled or non-scaled integuments), can only be correctly defined with reference to the chemical or molecular nature of the end-products of dermal and/or epidermal cell differentiation. Truly homologous integumentary structures probably do not exist above the class level in modern vertebrates. Anatomical, developmental, neurological, and paleontological data are presented in support of a model for the origin of mammalian hair. It is suggested that hairs arose from highly specialized sensory appendages of mechanoreceptor function which facilitated thermoregulatory behavioral activity in early synapsids. Specialization of cellular differentiation within these units led to the appearance of dermal papillae. A chance mutation led to subsequent multiplication of the originally sparsely, but spatially arranged papillae, causing the induction of a sufficient density of "sensory hairs" to constitute an insulatory body covering. The insulatory properties of this "prolopelage" were the subject of subsequent selection, but the sensory function of mammalian hairs remains important.

INTRODUCTION

The papers presented at this symposium have indicated the wide scope of currently available data on the vertebrate integument, which greatly facilitates an evolutionary review. We can now turn away from those treatments of the past century which have tended to focus on anatomical and embryological differences, and rarely, if ever, considered the problems of function or natural selection with reference to the origin of specific integumentary structures. Initial emphasis will be placed upon denning certain fundamental terms which are important to any discussion of the existence or non-existence of general trends. Then follows a consideration of the problem of deciding whether apparently similar structures have been retained throughout evolution — the conservative interpretation — or whether the known developmenThe author's studies on the reptilian integument have been supported by N. I. H. Grants CA 10844 and 1-PO1-AM-15515. Mrs. Una Maderson kindly typed the manuscript.

tal plasticity of the integument has permitted the repeated appearance of analogous specializations in convergent response to functional demands — the radical view. Finally, the evolution of hair is discussed to illustrate the parameters which should be considered in dealing with the origin of apparently unique integumentary modifications. FUNDAMENTALS

While the "mixed" ectodermalmesodermal nature of the vertebrate integument is well-known, less emphasis is placed on the fact that of all the major phyla, only the vertebrates have a multicellular epidermis. This is significant when we recall that the vertebrate integument never forms a confining exoskeleton comparable to that of Arthropods, Molluscs, or Echinoderms. Freedom from direct association with locomotory muscle action has not meant, however, that the vertebrate integument does not reflect locomotory needs. Indeed, it is more likely that the most fundamental patterns of or-

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ganization of the vertebrate integument are responses to problems posed by the basic locomotory patterns. Whatever the actual protovertebrate looked like (Berrill, 1955), the small softbodied creature probably possessed an integument similar to that of Amphioxus. Millions of unrecorded years of evolution separate this ancestor from the profusion of early Paleozoic fish forms, but we know that during this period, increase in body size was accompanied by a mechanical strengthening of the body surface. While the reasons for this are debatable (see discussion, Moss, 1968a), the question presents itself as to how the integument could be strengthened at all in an animal whose fundamental locomotory pattern depended on free lateral flexure of the body (Gray, 1968). Easily envisaged intermediates, with obvious selective advantages, at least for mechanical protection, lead eventually to either a partial abandonment of the body mobility — "the turtle strategy" — or else folding. As a result of the latter, any one segment of the body axis became covered by two or more units which could move relatively freely over one another. Since either the epidermal and/or dermal components of such units could thereafter be strengthened, this offered possibilities for mechanical strengthening while retaining the fundamental functional requirement of lability of the organ system in toto. We recognize these folds as "scales," which can therefore be defined as serial, patterned folds of the integument in which the epidermal and/ or dermal components may be variously elaborated so that one or the other type of tissue may be present in greater quantity, or be superficially more obvious, than the other. Within the definition of a scale given above, we can describe the integument of any vertebrate as being "scaled," "nonscaled," or a mixture of the two. In the case of those forms which definitely do not have scaled integuments, e.g., cyclostomes, elasmobranchs, holocephalans, anguilliform teleosts, most modern amphibia,

birds, and most mammals, it is most probable that they are derived from ancestral stocks whose integument was scaled. Furthermore, the integument of each of these taxa is characterized by the presence of complex derivatives — various multicellular glands, dermal denticles, hairs, and feathers. These structures are fundamentally localized centers of specialized epidermal and/or dermal cell proliferation and differentiation, within an otherwise generalized integument, of which they may properly be described as "appendages." Analagous structures may be found within scaled integuments, in which case the appendages are borne upon (epidermal specializations) (Maderson, 1971), or contained within (dermal ossifications) (Moss, 1972), individual scales. Thus, if a "scaled integument" is made up of scales, logically any individual scale is a part of the integument, and cannot therefore be regarded as an appendage. This distinction is pertinent to any discussion of integumentary evolution. Where the adult integument is scaled, the epidermal-dermal cell populations over the embryonic body surface were originally sub-divided into developmental fields. Within these fields, appendages may subsequently differentiate. As will be discussed later, the evolution, embryogenesis, and adult distribution of hairs and feathers (Maderson, 1972a) can only be understood by relating them to such developmental fields. Vertebrate integumentary structures can only be defined accurately if one combines the descriptive terms mentioned above with a reference to the chemical or molecular nature of the material synthesized by the constituent cell populations (Table I). The term "dermal scale," so often used to describe integumentary structures in piscine vertebrates, has little meaning unless one refers to the specific end-product of the interaction between dermis and epidermis in any particular taxon (Moss, 19686, 1972). Similarly, the term "reptilian scale" has no exact meaning since the differential distribution of keratinaceous proteintypes across the lepidosaurian and ar-

VERTEBRATE INTEGUMENTARY EVOLUTION

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TABLE 1. A general characterization, of the integument of extant vertebrates following the terminology and definitions discussed in the text. Taxon

General description1

Appendages2

Most conspicuous features3

Unicellular epidermal mucous glands Denticles* Dermal ossification with superficial COSMINE layer* Dermal ossifications with a variety of superficial mineralizations* Weak epidermal keratinization: dermal ossifications No Amphibians Unsealed in some scaled apodans No Chelonia Scaled* Varied horizontal distribution of epidermal keratin types No Archosauria Scaled Horizontal alternation of a- and /3-epidermal keratin types: dermal ossifications in many regions No Lepidosaurs Scaled Vertical alternation of a- and ^-epidermal keratin types: dermal ossifications in many lizards Yes Birds Mixed Feathers of j3-keratin* arising from a-synthesizing general epidermis: horizontal alternation of a -and Yes Unsealed Mammals j9-keratin types on leg scales Hairs of o-keratin* arising from a-synthesizing general epidermis: dermal ossifications in some forms 1 Applies to the great majority of species in the taxon cited. 3 Only those appendages are mentioned which are usually cited as primary diagnostic features of the group. a Structures or features which are known to involve dermal-epidermal interactions arc marked thus *. 4 The body is primarily scaled, but the development of the carapace, with its associated dermal ossifications, obviously inhibits flexibility. Data from: Alexander (1970); Baden and Maderson (1970); Moss (1968a,6); Quay (1972); Spearman (I960). Cyclostomes Chondrichthyes Sarcopterygians Actinopterygians

Unsealed Unsealed Scaled Scaled

Yes Yes Yes Yes

chosaurian scale surfaces (Baden and Maderson, 1970) makes these units as different in their own way as are feathers and hairs. The integumentary morphology of piscine fossils is usually clearly demonstrated by impressions in the surrounding matrix, but we need some "rule-of-thumb" for tetrapod fossils. Many extant squamates have scales which do not contain dermal ossifications. However, with the exception of Dermochelys (the leatherback turtle), I know of no living tetrapod which normally has a wide-spread distribution of dermal ossifications which does not have a visibly scaled integument. While this does not necessarily indicate a 1:1 relationship between externally recognizable units and individual ossification centers (Zangerl, 1969), it does suggest that in those systems where developmental fields exist in the embryonic integument and produce a pattern of dermal ossification, similar fields influence the topography of the entire integument. Therefore, I suggest that if paleontologists describe "scales" (dermal

ossifications) in their material, the forms concerned probably had scaled integuments in the sense defined earlier. Was the primitive tetrapod epidermis keratinized? Spearman (1966) indicated that the potential for keratin synthesis is widespread among vertebrates, and the reports on the ultrastructure of epidermal cells (Flaxman, 1972) show that all epidermal basal cells contain the 70-80A wide filaments which are associated with a-keratin. However, it is also known that in those tissues where the /?-protein is synthesized (characterized by 30A wide filaments) , the 70A filaments occur first, and the 30A units appear later and eventually fill the cells. To me, this implies that the /?-protein is a later phylogenetic development than the a-form, and this is supported by the distribution of epidermal protein types in extant amniotes (Baden and Maderson, 1970). It appears that those lower Pennsylvanian captorhinomorphs which gave rise to synapsids and mammals possessed only the capacity to synthesize a-keratin. The remainder of the cap-

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FIG. 1. Sagittal section through ventral body scales of the gekkonid lizard Eublcpharis macularius just before skin-shedding. The ^-layers of the outer (/So) and inner (fii) epidermal generations are thick on the outer scale surface (OSS) , but are reduced to a single layer of cells on the inner surface and in the hinge region (ISS, H) . Ddermis; sc- sub-cutaneous tissue.

torhinomorphs, which gave rise to all the other reptilian groups and birds (Carroll, 1969(1$/:), possessed an additional capacity for /3-protein synthesis in their epidermis, which was variously expressed in different lineages (Table I). What then of the paleozoic amphibia? Romer and Witter (1941), Colbert (1955), and Kitching (1957) described ossified units suggesting a scaled integument (see above) which was secondarily modified in their lissamphibian descendents (Cox, 1967). Findlay (1968a) suggested that haematite deposits around the matrix of the lower Triassic Uranocentrodon resulted from the decomposition of sulphur-containing epidermal proteins. While this intriguing interpretation suggests the presence of keratin, it does not reveal whether it was of the a- or /J-variety! Microscopic and ultrastructural studies indicate that the epidermal tissues on the inner surface and hinge region of amniote scales tend to be thinner, less compact, and more lamellate in their organization than those on the outer scale surfaces. Different fluorescent properties of different regions of amniote scales (Cane and Spearman, 1967; Spearman, 1964, 1966, 1967) cannot be explained by reference to the presence of a- or /J-keratins alone (Baden and Maderson, 1970). However, they may reflect differences in inter-cellular bonding, which endow the different epidermal regions

with different mechanical properties, and these originally augmented the flexibility of the entire integumentary system. This end is still extremely important in squamates where numerous subtle differences in patterns of cell production and differentiation modify the basic epidermal generation pattern (Maderson, 1965, 1966; Maderson and Licht, 1967) over the inner scale surface and hinge (Fig. 1). However, the persistent a-protein in these regions in crocodiles and birds (Baden and Maderson, 1970) and centers of granular layer formation in mammalian tail scale "hinges" (Spearman, 1964, 1966) should be interpreted as relics of the ancestral functional modifications. TRENDS IN VERTEBRATE INTEGUMENTARY EVOLUTION

Raising the question of the possible homology between feathers, hairs, and scales, Cohen (1964) wrote: "If by homology we mean that the organs concerned, may, we believe, be traced back along lines of ancestors until a comparable structure is reached in the common ancestor, then the assessment is always made more difficult by more facts." This conclusion is germane to the entire topic of integumentary evolution. On the basis of the facts presented above and their combination with the most conservative possible deductions regarding possible integumentary anatomy in fossil forms, we are forced to conclude that no two integumentary features in two major assemblages can be strictly considered to be homologous. This concept must be restricted to such examples as pelage hair and spines in mammals, or climbing setae and the normal Oberhautchen in lizards (Maderson, 1970). Even the recognition of general anatomical trends is of limited value. While piscine vertebrates tend to have scaled integuments or conspicuous elaborations of dermal skeletal structures or both, attempts to define the degree of homology therein are important only insofar as they lead to consideration of whether dermo-epidermal interactions have or


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phological diversity. THE EVOLUTION OF HAIR

FIG. 2. An epidermal "Haareorgane" from the dorsal body scales of the gekkonid lizard Gekho gecko. The epidermis shows a stage 4 condition of the shedding cycle (Maderson and Licht, 1967) and shows that the "hair" derives from a modified Oberhautchen cell (SpOb) . In a sense organ of this type, although the structure of the epidermal generation is modified, the subjacent germinal cells (sg), closely resemble those of the adjacent non-specialized epidermis. Note the cluster of cells in the dermis (X) beneath the sense organ here and in Figures 4 and 5. The /3-layer of the outer epidermal generation is not seen in the photograph. Other abbreviations, here and in Figures 4 and 5: oo — o-layer of the outer generation; /3i — /3-layer of the inner generation; clo — clear layer of the outer generation; lto — lacunar tissue of the outer generation; mi — mesos layer of the inner generation; Obi — Oberhautchen of the inner generation; Obis —spinules of the unspecialized Oberhaulchen cells.

have not changed during evolution. The question "Are tetrapod scales retained from the piscine ancestors?" has no meaning except to emphasize that there is a general capacity for patterned integumentary structure in different taxa with varying degrees of phyletic affinity. Whatever general trend we define or recognize, it is always subject to major or minor revision of execution. In short, I favor the "radical" view of integumentary evolution to such a degree that I would suggest that in any instance, a functional question should be asked, a functional investigation should follow, and any subsequent detailed anatomical study should be expected to demonstrate yet another example of mor-

This problem has a number of facets. First, we must ask, is hair a unique mammalian characteristic? Second, are there other structures which resemble mammalian hair in other vertebrates, or indeed in other animals? Third, have hairs always served an insulatory function, and if not, what other functions could they have served? Finally, is it possible to present a model for the steps in the phylogenetic development of hair, with plausible explanations for the accompanying selective pressures? Recent reviewers (Hopson, 1969; Hopson and Crompton, 1969; Jenkins, 1970) suggest a monophyletic origin for mammals in the late Triassic - early Jurassic. Hopson (1969) concluded: ". . . (anatomical, physiological and neuroanatomical studies) strongly suggest that the common ancestor of monotremes and therians was also mammalian in a majority of essential features e.g. hair, lungs, diaphragm, heart, and kidneys, to name a few." How many of these features might have characterized the early Triassic cynodonts which Hopson and Crompton (1969) proposed as mammalian ancestors? Reference to possible integumentary structures of therapsids is so common-place that we may tend to forget that there is no direct information available. Watson (1931), Brink (1956), and Findlay (1968ft) interpreted depressions in skull bones as probably having housed vibrissae or "skin glands of a sweat gland nature" (Brink, p. 87). These interpretations were extrapolated to suggest pelage hairs and normal sweat glands over the rest of the body. Repeated associations between these "extrapolated interpretations" and actual mammal-like osteological features in support of suggestions of endothermy in therapsids have produced a situation so close to circuitous argument that it is time to seek a new approach to the problem of the origin of hair. No extant vertebrates have integumen-

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tary appendages which anatomically resemble hairs. The structures seen in many lizards (Fig. 2), once invoked as "ancestral hairs" (Elias and Bortner, 1957), are sensory units (Miller and Kasahara, 1967) derived from individual cells of the Oberhautchen (Schmidt, 1920; Maderson and Licht, 1967; Maderson, 1971), which layer is a unique constituent of the lepidosaurian epidermis (Maderson, 1968a). While the anatomy of the individual units is certainly not homologous with that of any vertebrate epidermal derivative, a number of insects have a "pelage" (Heath, 1968). Although the pelage plays a primary role in insulation in most mammals (Ling, 1970) and in some insects, various vertebrates, e.g., lizards, or man, manifest endothermic regulatory mechanisms of varying degrees of "perfection," but do not possess a continuous body covering of this type. Conversely, the presence of a covering pelage does not necessarily indicate an absolutely constant internal temperature throughout life (Heath, 1968). There is therefore no a priori reason for assuming that therapsid thermoregulation could not have evolved in the absence of a pelage. Indeed, the physical laws which govern the functioning of a pelage indicate that each constituent unit must have a certain minimum length, and there must be a certain minimum density per unit area of the body before any selective advantage accrues with regard to insulating function (Ling, 1970). It seems most unlikely that a "preadapted proto-pelage," upon which selection could act, could have appeared via a steady accumulation of "neutral traits" affecting epidermal morphogenesis over several thousand generations. A more plausible hypothesis is that the insulating function of hair is secondary and became possible only after completely different selective advantages had favored suitable morphogenic changes in the epidermis. These primary selective pressures can be identified if we consider the probable ecology of the extinct forms concerned, and thence deduce the obligatory minimal functions of their integument.

Studies of Pennsylvania reptile fossils (Carroll, 1964, 1969a,bjC, 1970a,b) suggest that they were small, highly terrestrial, forest-dwelling forms. Carroll (1970&) writes of the captorhinomorph Hylonomus lyelli: "in size and general form it resembles a medium-sized lizard. It may have had similar habits as well." I suggest that functionally the integument of such forms would have resembled that of modern lizards. The epidermis would have possessed a well-developed outer cornified region which would have provided a degree of protection against dessication (Maderson et al., 1970). Carroll's (1964) descriptions of osteoscutes suggest a scaled integument (see above), so that both dermal and epidermal components probably contributed to mechanical protection. Since holocrine secretion is a very important function in modern lizards (Maderson, 1970), this may have been true for the earliest reptiles. However, in most modern amniotes, odoriferous sources are localized on the body surface: the pheromonal function of sweat-glands in some mammals is probably secondary. My own observations on a great variety of modern lizards suggest that if behavioral thermoregulation characterized the earliest reptiles, this would not have necessitated any particular morphological structure of the integument, except perhaps with regard to the distribution of pigment cells (Porter, 1967). If the integument of primitive reptiles manifested other secondary functions (e.g., climbing claws, poison glands, sexual or territorial warning appendages), comparative observations on modern amniotes indicate that associated structural modifications would have been localized on the body surface. Apart from the "primary barrier function" of physiological and mechanical protection which influences the fundamental morphology of the entire integument (Maderson, 1971), there is only one secondary integumentary function which potentially involves the entire organ system — that of sensory reception. Two quite different types of sensory stimulus have always impinged upon the terrestrial in-
