3881739

When? Why? and How?: Some Speculations on the Evolution of the Vertebrate IntegumentAuthor(s): Paul F. A. MadersonReviewed work(s):Source: American Zoologist, Vol. 12, No. 1 (Feb., 1972), pp. 159-171Published by: Oxford University PressStable URL: http://www.jstor.org/stable/3881739 .Accessed: 06/11/2011 04:36

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Am. Zoologist, 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 sealed, 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 append? ages (whether borne within sealed 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 facili- tated 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 "protopelage" 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 integu? ment, which greatly facilitates an evolu?

tionary 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 func?

tion or natural selection with reference to

the origin of specific integumentary struc?

tures. Initial emphasis will be placed upon

defining certain fundamental terms which

are important to any discussion of the exis?

tence or non-existence of general trends.

Then follows a consideration of the prob? lem of deciding whether apparently similar

structures have been retained throughout evolution ? the conservative interpreta? tion ? or whether the known developmen-

The author's studies on the reptilian integument have been supported by N. I. H. Grants CA - 10844 and l-POl-AM-15515. Mrs. Una Maderson

kindly typed the manuscript.

tal plasticity of the integument has per? mitted the repeated appearance of analo?

gous 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'' ectodermal- mesodermal nature of the vertebrate integ? ument is well-known, less emphasis is

placed on the fact that of all the major phyla, only the vertebrates have a mul? ticellular epidermis. This is significant when we recall that the vertebrate integu? ment never forms a confining exoskeleton

comparable to that of Arthropods, Mol? luscs, or Echinoderms. Freedom from di? rect association with locomotory muscle ac? tion has not meant, however, that the ver? tebrate integument does not reflect lo?

comotory needs. Indeed, it is more likely that the most fundamental patterns of or-

159

160 Paul F. A. Maderson

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 soft-

bodied creature probably possessed an in?

tegument 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 dis?

cussion, Moss, 1968a), the question pre? sents itself as to how the integument could

be strengthened at all in an animal

whose fundamental locomotory pattern de-

pended on free lateral flexure of the body

(Gray, 1968). Easily envisaged intermedi-

ates, with obvious selective advantages, at

least for mechanical protection, lead even?

tually 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. SinGe either the epidermal

and/or dermal components of such units

could thereafter be strengthened, this

offered possibilities for mechanical strength?

ening 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 "sealed," "non-

scaled," or a mixture of the two. In the

case of those forms which definitely do not

have sealed integuments, e.g., cyclostomes, elasmobranchs, holoeephalans, anguilli- form teleosts, most modern amphibia,

birds, and most mammals, it is most probable that they are derived from ancestral stocks whose integument was scaled. Fur?

thermore, the integument of each of these taxa is characterized by the presence of

complex derivatives ? various multicellu? lar glands, dermal denticles, hairs, and feathers. These structures are fundamen-

tally localized centers of specialized epider? mal and/or dermal cell proliferation and

differentiation, within an otherwise gener- alized integument, of which they may properly be described as "appendages." Analagous structures may be found within scaled integuments, in which case the ap? pendages are borne upon (epidermal spe? cializations) (Maderson, 1971), or con? tained 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 integu? ment, and cannot therefore be regarded as an appendage. This distinction is pertinent to any discussion of integumentary evolu? tion. Where the adult integument is

scaled, the epidermal-dermal cell popula? tions 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, embryo- genesis, and adult distribution of hairs and feathers (Maderson, 1972a) can only be understood by relating them to such de?

velopmental fields. Vertebrate integumentary structures can

only be defined accurately if one combines the descriptive terms mentioned above with a reference to the chemical or molec? ular 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 epider? mis in any particular taxon (Moss, 1968&, 1972). Similarly, the term "reptilian scale" has no exact meaning since the differen? tial distribution of keratinaceous protein- types across the lepidosaurian and ar-

Vertebrate Integumentary Evolution 161

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

TJnicellular epidermal mucous glands Denticles* Dermal ossification with superficial COSMINE layer* Dermal ossifications with a variety of superficial

miner alizations* Weak epidermal keratinization: dermal ossifications

in some sealed apodans Varied horizontal distribution of epidermal keratin

types Horizontal alternation of a- and /3-epidermal keratin

types: dermal ossifications in many regions Vertical alternation of a- and j3-epidermal keratin

types: dermal ossifications in many lizards Feathers of /3-keratin* arising from a-synthesizing

general epidermis: horizontal alternation of a- and jS-keratin types on leg scales

Hairs of a-keratin* arising from a-synthesizing gen? eral epidermis: dermal ossifications in some forms

1Apphes to the great majority of species in the taxon cited. 2

Only those appendages are mentioned which are usually cited as primary diagnostic features of the group. 3 Structures or features which are known to involve dermal-epidermal interactions are marked thus *.

4 The body is primarily sealed, but the development of the carapace, with its associated dermal ossifi? cations, obviously inhibits flexibility. Data from: Alexander (1970); Baden and Maderson (1970); Moss (1968a,6); Quay (1972); Spearman (1966).

chosaurian scale surfaces (Baden and

Maderson, 1970) makes these units as diff? erent 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 tet-

rapod 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 be? tween 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 pat? tern of dermal ossification, similar fields influence the topography of the entire in?

tegument. Therefore, I suggest that if

paleontologists describe "scales" (dermal

ossifications) in their material, the forms concerned probably had scaled integu? ments 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 re?

ports on the ultrastructure of epidermal cells (Flaxman, 1972) show that all epi? dermal 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 synthe? sized (characterized by 30A wide fila?

ments) , 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 develop? ment than the a-form, and this is support? ed 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-


?Qss ?ft,

FIG. 1. Sagittal section through ventral body scales of the gekkonid lizard Eublepharis macularius

just before skin-shedding. The ?-layers of the outer

(?o) and inner (?i) 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). D- dermis; sc- sub-cutaneous tissue.

torhinomorphs, which gave rise to all the other reptilian groups and birds (Carroll, 1969a,b,c), possessed an additional capaci? ty for ^-protein synthesis in their epider? mis, which was variously expressed in diff? erent lineages (Table I). What then of the

paleozoic amphibia? Romer and Witter

(1941), Colbert (1955), and Kitching

(1957) described ossified units suggesting a

sealed 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 Urano-

centrodon resulted from the decomposi? tion of sulphur-containing epidermal pro? teins. While this intriguing interpretation suggests the presence of keratin, it does not

reveal whether it was of the a- or /3-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 /?-keratins alone (Baden and Mad?

erson, 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 differen? tiation modify the basic epidermal gener? ation 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 Mader?

son, 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 ho-

mology 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 evolu? tion. 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 re? stricted 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 inso- far as they lead to consideration of wheth? er dermo-epidermal interactions have or


FIG. 2. An epidermal "Haareorgane" from the dor? sal body scales of the gekkonid lizard Gekko 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 0-layer of the outer epidermal generation is not seen in the photo? graph. Other abbreviations, here and in Figures 4 and 5: ao ? a-layer of the outer generation; ?i ? ?-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 Oberhautchen cells.

have not changed during evolution. The

question "Are tetrapod scales retained from the piscine ancestors?" has no mean?

ing except to emphasize that there is a

general capacity for patterned integumen? tary structure in different taxa with vary? ing 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 ana? tomical study should be expected to demonstrate yet another example of mor-

phological diversity.

THE EVOLUTION OF HAIR

This problem has a number of facets.

First, we must ask, is hair a unique mam? malian characteristic? Second, are there other structures which resemble mammal? ian 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; Hop-

son and Crompton, 1969; Jenkins, 1970) suggest a monophyletic origin for mam? mals in the late Triassic -

early Jurassic. Hopson (1969) concluded: ". . . (anatomi? cal, 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 mam? malian ancestors? Reference to possible in?

tegumentary structures of therapsids is so

common-place that we may tend to forget that there is no direct information avail? able. Watson (1931), Brink (1956), and

Findlay (1968&) interpreted depressions in skull bones as probably having housed vi? brissae 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 be? tween these "extrapolated interpretations" and actual mammal-like osteological fea? tures in support of suggestions of endo-

thermy 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-


tary appendages which anatomically re?

semble hairs. The structures seen in many lizards (Fig. 2), once invoked as "ancestral

hairs" (Elias and Bortner, 1957), are sen?

sory units (Miller and Kasahara, 1967) de? rived from individual cells of the Ober? hautchen (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 cer-

tainly 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 verte?

brates, e.g., lizards, or man, manifest en- dothermic regulatory mechanisms of vary? ing degrees of "perfection," but do not pos? sess a continuous body covering of this

type. Conversely, the presence of a cover?

ing 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 mini? mum 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 "pre- adapted proto-pelage," upon which selec? tion 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 se? lective advantages had favored suitable

morphogenic changes in the epidermis. These primary selective pressures can be identified if we consider the probable ecol?

ogy of the extinct forms concerned, and thence deduce the obligatory minimal functions of their integument.

Studies of Pennsylvania reptile fossils

(Carroll, 1964, I969a,b,c, 1970a,fe) suggest that they were small, highly terrestrial, for-

est-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 simi? lar habits as well." I suggest that function-

ally 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 epi?

dermal 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 character? ized the earliest reptiles, this would not have necessitated any particular morpholo? gical structure of the integument, except perhaps with regard to the distribution of

pigment cells (Porter, 1967). If the integu? ment of primitive reptiles manifested other

secondary functions (e.g., climbing claws,

poison glands, sexual or territorial warn-

ing appendages), comparative observations on modern amniotes indicate that associ? ated structural modifications would have been localized on the body surface.

Apart from the "primary barrier func? tion" of physiological and mechanical pro? tection which influences the fundamental

morphology of the entire integument (Maderson, 1971), there is only one secon?

dary integumentary function which poten? tially involves the entire organ system ?

that of sensory reception. Two quite different types of sensory stimulus have

always impinged upon the terrestrial in-


m*.

FIG. 3. Schematic representation of a mammalian

tylotrich hair follicle modified after Straile (1969) . 1 - hair shaft; 2 - internal root sheath; 3 - external root sheath; 4 - germinal region of the ty? lotrich follicle; 5 - dermal papilla; 6 - connective tissue sheath; 7 - annular complex; 8 - epidermal pad complex; 9 - neurons associated with slow-

adapting mechanoreceptors; 10 - mouth of se? baceous gland (body of gland not shown) ; 11 - venular complex associated with tylotrich unit (ar- teriolar complex not shown).

tegument ? temperature and touch.

These categories can be further sub- divided since gradual changes in ambient

temperature, or casual contact with the substrate during locomotion, are inter?

preted by the brain quite differently than are sudden temperature changes, or sharp pressures. Any or all of any variety of

types, or levels, of stimulation might chal-

lenge any part of the body surface. It is therefore predictable that there would be a

spatial pattern of functional differentia? tion across the integument, which might be reflected anatomically in patterns of nerve distribution and/or the morphology of the receptor-transducer units.

I propose that mammalian hairs are de? rived from complex epidermal modifications of mechanoreceptor function, which were originally "sparsely," but regularly, distributed over the surface of the body. At some stage in the evolution of the therapsid integument, the competence of the de?

velopmental fields centered around the

original units changed, resulting in a mul-

tiplication of basically similar morphogenic events. These events produced a sufficient density of "sense organs" per unit area of the body to produce a "pelage," the insulative properties of which were the fo? cus for subsequent selection. The sensory function of hair in modern mammals does not exactly resemble that of the original units, but this does not affect the morpho? logical model which will be presented. The data supporting this hypothesis will now be discussed.

Straile (1969) proposed "repeating ver? tical units" in the mammalian integument containing epidermal, neural, and vascular elements arranged around a "tylotrich" hair follicle (Fig. 3). The tylotrich is asso? ciated with two innervated regions, an annular complex surrounding the upper third of the follicle, and an adjacent epi? dermal pad complex. Although the exact construction of the vertical unit varies across the body, and between taxa, tylotrichs have been observed in monotremes and many therian mammals (Mann, 1968). While there is some disagreement as to


FIG. 4. Sense organ from a labial scale of the iguanid lizard Iguana iguana. The epidermis is in the resting phase of the shedding cycle (Maderson and Licht, 1967) . In this type of sense organ, the associated germinal cells are always columnar and have vesicles at their distal tips. The mature ker? atinized elements of the outer epidermal gener? ation are indicated by dotted lines. ?o - jS-layer of the outer generation.

FIG. 5. Sense organ from a lateral body scale of the xantusiid lizard Xantusia vigilis. The epidermis is in stage 4 of the shedding cycle, and we note that although this type of sense organ does not protrude above the general level of the skin surface, it is associated with a modification of the histogenesis of the inner generation which produces mature elements (dotted outlines) analagous to those seen in Figure 4.

how the electro-physiological data should be related to the anatomical data (see dis? cussion, Straile, 1969), there is good evi? dence that both rapid and slowly adapting mechanoreceptors are represented within

repeating vertical units so that: "The de? tection of a tactile stimulus moving from

point to point probably involves the inter?

pretation of a complex series of nerve im?

pulses that are received by the brain"

(Straile, 1969). My own familiarity with the scaled reptilian integument, where even cursory examination reveals a pleas- ing geometric order, has long made me

suspicious of the apparent heterogeneity of the mammalian system. Straile's "re?

peating vertical unit" seems to me to

provide the required conceptual link be-

tween the two conditions. There is an impressive variety of epider?

mal sensory modifications in reptiles (Mil? ler and Kasahara, 1967) (Figs. 2, 4, 5). There are no systematic investigations of

any single type available, but the distribu? tion of "Haareorganes" suggests a function of monitoring inter-scale contact (Mader? son, 1971). Bailey (1969) demonstrated fast and slow-adapting mechanoreceptors by electro-physiological techniques, but did not provide an anatomical correlation. The anatomy and functioning of the in? fra-red sensitive cutaneous pit organs in snakes have been extensively studied (Bar- rett, 1970; Meszler, 1970). Although the data are sparse, we can say that cutaneous

sensory reception does occur in reptiles, and the diversity of associated morphologi? cal specializations suggests that it is an ex?

tremely important function. Elias and Bortner's (1957) morphologi?

cal schema of hair phylogeny rests on the

premise of a direct relationship to the lacertilian "Haareorgane" which is no long? er acceptable (see above). While the

morphogenic events in hair development are difficult to relate to any possible evolu?

tionary sequence, if one ignores the details

involved, one can derive a useful, simply- stated overview. A portion of the germinal population becomes specialized so that its

daughter cells stick together as a rod which

projects above the skin surface, while the

daughter cells of adjacent, unspecialized inter-follicular epidermis do not stick to?

gether so tightly and therefore desqua- mate. The process of initial specialization and adult homeostasis involves mesoderm cells ("the dermal papilla"), and the two cell populations influence one another via a sequence of inductive processes which we term "epithelial-mesenchymal interac? tions" (see Kollar, 1972). The elegant complexity of the hair follicle, which at first sight seems so difficult to explain in

evolutionary terms, may be readily ex?

plained. It permits a "good rod" to grow from a "good hole," a mere refinement which could have occurred quite late in the phylogeny of hair. It should be noted


FIG. 6. Suggested model for the sequence of mor?

phological changes in the evolution of mammalian hair. a - suggested integumentary structure of a

primitive cotylosaur; b - suggested integumentary structure of a cotylosaur associated with synapsid lineage; c - suggested integumentary structure of a

pelycosaur associated with the therapsid/mammalian lineage; d - e - magnified views of suggested evolutionary changes in the original "hinge" region of c (outlined). Medium dense fine stipple ? epi? dermis showing basic a-protein synthetic capacity; dense fine stipple ? epidermis where cell matura? tion involves keratohyalin; sparse fine stipple ? der? mis; clusters of fine stipple ? dermal papilla; dashed lines ? neurons associated with fast-adapting mechanoreceptors; heavy dotted lines ? neurons associated with slow-adapting mechanoreceptors; cross-hatching ? dermal ossification. For explana? tion, see text.

that holocrine secretion from lacertilian

pre-anal organs (Maderson, 1968&, 1970, 1971, 1972&) frequently produces a dura-

ble "rod" of mature cells which may protrude a considerable distance from the skin

surface. However, there are no specializa? tions comparable to the various layers of

the inner and outer root sheath seen in a

hair follicle. Before we consider the model, it should

be mentioned that all recent accounts of the amphibian-reptilian-mammalian line-

age (Carroll, 1964, I969a,b,c, 1970a,&; Cle?

mens, 1970; Hopson, 1969; Hopson and

Crompton, 1969; Jenkins, 1970) indicate that the creatures concerned were of small size ?less than 18" total length. However,

throughout the geological eras concerned, related forms and other amphibian and

reptilian groups radiated to produce gen? era of considerable size. The mammalian

grade of organization with its attendant

morphological characteristics, e.g., hair, was perfected over a period of 200 million

years by small animals, possibly crevice

dwellers, who probably attained their evo?

lutionary destiny by exploiting nocturnal

niches, following gradual refinement of

thermoregulatory mechanisms.

A possible structure of the early coty- losaurian integument is shown in Figure 6a. The epidermis contained only a-ker-

atin, and the tissue was thinned on the

inner scale surface and hinge region. A

plausible suggestion for the differential distribution of mechanoreceptors would

place fast-adapting units on the outer scale surface. These monitored transient envi?

ronmental contact during normal locomo? tion. Locomotory activities involving

stretching or compression of the integu? ment (e.g., twisting of the body into small

crevices and hiding) could have been mon?

itored by slow-adapting receptors in the

hinge region. Dermal ossifications were

present and possibly played some mechani? cal protective role.

In those cotylosaurs associated with the basic synapsid stock and the derived forms, certain modifications characterized the in?

tegument (Fig. 6b). I propose that the

involvement of keratohyalin in the kerat?

inization process, at first confined to the

hinge region (Spearman, 1964, 1966), en- hanced the overall flexibility of the integu? ment and permitted a reduction of scale

overlap. This additional protein could have resulted from a single gene change, since similar proteins exist in the epider? mis of modern reptiles (Maderson et al.,

1972) and birds (Alexander, 1970). Re? duction of scale overlap is suggested by the

scarcity, or absence, of dermal ossifications


in synapsid material. The modified pat? tern of protein synthesis may have per? mitted a thickened epidermis on the outer

scale surface to provide mechanical protec? tion and perhaps decrease per cutaneous

water-loss. The groups of fast-adapting

mechanoreceptors probably became local?

ized within regions of hypoplasia. The re?

duction of scale overlap diminished the

original function of the slow-adapting re?

ceptors in the hinge region for monitoring inter-scale contact. However, the function

of providing sensory data during hiding could have been maintained if the nerve

endings became associated with a small ep? idermal papilla which protruded to a level

just beneath the general level of the outer

scale surfaces during normal locomotion.

The widespread occurrence of thermo-

regulatory behavior patterns in modern

reptiles (Bellairs, 1969) implies that they arose very early in reptilian evolution. If, indeed, Triassic therapsids did manifest

some degree of homeothermy (Heath,

1968), we might postulate that the coty-

losaur-synapsid lineage possessed some spe? cial feature permitting the precocious de?

velopment of this grade of organization relative to other reptilian lineages. Bailey's

(1969) data suggest that cutaneous ther-

moception in lizards is insufficiently sensi?

tive to facilitate thermoregulatory behav?

ior. Heath (1968) indicated that while

peripheral temperature receptors modulate

hypothalamic responses to environmental

temperature change in mammals, he stated: "The cold-blooded terrestrial ani?

mals may rely largely on internal recep? tors." Such receptors can only provide in?

formation regarding heat energy after it

has been absorbed; they cannot critically examine possible differential heat-sources

in the environment on a "minute-by- minute basis." For this reason, the ther?

moregulatory behavior patterns of modern

lizards involve quite sudden movements

from one type of exposure to another, fol?

lowed by equally rapid increases or de?

creases in deep body temperature (McGin- nis and Dickson, 1967). The amount of

heat absorbed by the deep body tissues

depends upon the cooling influences at the

skin surface. Any animal which could mon-

itor such influences, and accordingly ad-

just its position in the environment, could achieve more subtle temperature regula? tion. More importantly, it could take ad?

vantage of "heat availability situations" which would be beyond the sensory analyt? ical capacities of other forms.

Figure 6c is a suggested skin structure of a pelycosaur at the base of the therapsid- mammalian lineage. Certain general trends described earlier have continued, i.e., re? duction of scale overlap, spread of the

granular layer, epidermal thickening. The

slow-adapting mechanoreceptors originally seen in the hinge region are now associ? ated with a longer papilla, the primary function of which is still monitoring envi? ronmental contact during hiding activity. When the body is still during sun-basking, these papillae protrude above the general body surface. Their mechanoreceptor ac? tion could detect displacement of their dis? tal tips by air-movements. Figures 6d-f sug? gest how further selection might have im-

proved the functioning of this lever- activated mechanoreceptor.

Figure 6f shows a rod of cells which

grows out from a follicle; movement of the distal tip of the rod distorts the entire structure leading to activation of the neu? rons which are now associated with the

upper third of the follicle. The daughter cells arising from the germinal region of the follicle form a tightly adhering mass, and specialization of the outermost cell

layers would endow this "rod" with specific mechanical properties associated with

flexibility. These patterns of cellular activ?

ity are sufnciently distinct from those of

surrounding "interfollicular" epidermal cells to imply the presence of a distinct

morphogenetic mechanism responsible for their control. At this stage in evolution, the dermal papilla appeared. It does not matter whether this structure arose initial?

ly as an embryonic or an adult "inducer," since its fundamental role ? maintenance of a specialized sequence of differentiative events for a circumscribed germinal/

Vertebrate Integumentary Evolution

^*#';^

*#

169

a

Ph^^H

FIG. 7. Sagittal section through rat tail scale showing a hair follicle growing from the "hinge region." The restriction of the granular layer to

daughter cell population within an other? wise homogeneous epidermal system ?is the same at all stages of the life cycle.

The model to this point suggests that

although the postulated specialized mech-

anoreceptor ? which should be compared

to the tylotrich hair follicle (Fig. 3) ?

did not evolve from a scale, it was

initially associated with a morphogenic field surrounding a scale and eventually superseded it in size and importance. This

premise receives support from the follow?

ing data. First, tylotrichs develop first in

the embryo (Mann, 1968). Second, tylo? trichs are more numerous dorsally than

ventrally (Mann, 1969) ? a similar condi? tion is seen with regard to scales in most li? zards. Third, recalling that the sequence of events under discussion concerned small

animals, we note that Mann (1969) stated: "The larger the mammal, the fewer the

tylotrichs per unit surface area of the skin." Fourth, the described sequence of events accounts for hair distribution across the scaled caudal integument of some modern mammals (Spearman, 1964, 1966) (Fig- 7).

The integumentary structure shown in

Figure 6f might have characterized a small

early therapsid with a highly sophisticated thermoregulatory behavior pattern. How?

ever, the function of the spatially dis-

the follicle mouth area is indicated by arrows. H ? hair shaft.

tributed "eotylotrichs" was exclusively

mechanoreceptive, and such structures

could not have served an insulatory func?

tion. I suggest that this secondary function

arose following the multiplication of follic?

ular units within the original "scale mor-

phogenic field" surrounding the eo ty? lotrich.

The model suggests an association be?

tween a certain level of morphologic com?

plexity and the evolutionary appearance of

a dermal papilla. Cohen (1964, 1969) has

emphasized the similarity in organization of hairs and feathers, and Maderson

(1972a) has proposed the origin of the

dermal papilla of feathers for similar mor-

phogenic reasons to those presented here.

Ede et al. (1971) investigated the failure

of feather development in the talpid3 mu?

tant chick embryo and demonstrated a de?

fect of dermal papilla formation. While

comparable detailed ontogenic analyses are

lacking, Mann (1969) listed recessive

point mutations in mice which disturbed normal tylotrich development. I submit that it is equally possible that multiplica? tion of follicular units could have occurred

as the result of a single gene change in

our therapsid ancestors. The only question is, what selective advantage accrued which

favored the survival and spread of such a

gene change? There are two possibilities,


which are not mutually exclusive. The in?

crease in number of units reached or sur-

passed the minimum density per unit area

necessary to provide insulatory benefits.

Alternatively, since secondary hair follicles

in modern mammals are associated with

rapidly adapting touch receptors (Straile,

1969), one could argue that the "lever-

activated" receptor associated with the

slow-adapting receptors (the eotylotrich) was so successful that selection favored the

incorporation of the fast-adapting units

into secondarily derived similar structures. I favor the second of these explanations since it does not necessitate quantum changes in anatomical structure and does offer possible successive levels of cutaneous

organization, culminating in an insulatory

pelage. The model which has been presented

here is highly speculative, but this is inevi- table due to the nature of the subject. The

premise of a mechanoreceptor origin for mammalian hair is not new, but it has never before to my knowledge been consid? ered in detail with reference to a series of selective pressures. I would like to em-

phasize in conclusion, that if the level of

mechanoreceptor organization shown in

Figure 6f were typical of most cynodonts, enlarged units could have formed the fa? cial vibrissae discussed earlier. If we accept Heath's (1968) and Bailey's (1969) state-

ments with reference to deep and cutane?

ous thermoreception in mammals versus

reptiles, we might even suggest that it was

only in the phyletic line leading to mam?

mals that peripheral modulation of hy?

pothalamic temperature responses de?

veloped. This could have been that last

subtle refinement in endothermy which en-

sured the success of the lineage.

Right or wrong, this discussion will have

served its purpose if it stimulates further

interest in mammalian cutaneous reception, but even better, it should lead to

comparable studies on modern lizards, the

epidermis of which is, after all, the zenith of amniote integumentary evolution.

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