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 11210SYNOPSIS. The basic structure of the vertebrate integument is briefly reviewed. Thesystem is either scaled, non-scaled, or a mixture of the two. Scales are not appendagesof the integument, but are patterned folds in which the dermal and/or epidermalcomponents may be elaborated. An appendage is the product of specialized patterns ofcell differentiation localized within the dermis and/or epidermis. Scales, and append-ages (whether borne within scaled or non-scaled integuments), can only be correctlydefined with reference to the chemical or molecular nature of the end-products ofdermal and/or epidermal cell differentiation. Truly homologous integumentarystructures probably do not exist above the class level in modern vertebrates.

Anatomical, developmental, neurological, and paleontological data are presented insupport of a model for the origin of mammalian hair. It is suggested that hairs arosefrom highly specialized sensory appendages of mechanoreceptor function which facili-tated thermoregulatory behavioral activity in early synapsids. Specialization of cellulardifferentiation within these units led to the appearance of dermal papillae. A chancemutation led to subsequent multiplication of the originally sparsely, but spatiallyarranged papillae, causing the induction of a sufficient density of "sensory hairs" toconstitute an insulatory body covering. The insulatory properties of this "prolopelage"were the subject of subsequent selection, but the sensory function of mammalian hairsremains important.

INTRODUCTION

The papers presented at this symposiumhave indicated the wide scope of currentlyavailable data on the vertebrate integu-ment, which greatly facilitates an evolu-tionary review. We can now turn awayfrom those treatments of the past centurywhich have tended to focus on anatomicaland embryological differences, and rarely,if ever, considered the problems of func-tion or natural selection with reference tothe origin of specific integumentary struc-tures.

Initial emphasis will be placed upondenning certain fundamental terms whichare 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 similarstructures have been retained throughoutevolution — the conservative interpreta-tion — or whether the known developmen-

The author's studies on the reptilian integumenthave been supported by N. I. H. Grants CA -10844 and 1-PO1-AM-15515. Mrs. Una Madersonkindly typed the manuscript.

tal plasticity of the integument has per-mitted the repeated appearance of analo-gous specializations in convergent responseto functional demands — the radical view.Finally, the evolution of hair is discussedto illustrate the parameters which shouldbe considered in dealing with the origin ofapparently unique integumentary modifi-cations.

FUNDAMENTALS

While the "mixed" ectodermal-mesodermal nature of the vertebrate integ-ument is well-known, less emphasis isplaced on the fact that of all the majorphyla, only the vertebrates have a mul-ticellular epidermis. This is significantwhen we recall that the vertebrate integu-ment never forms a confining exoskeletoncomparable 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 likelythat the most fundamental patterns of or-

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160 PAUL F. A. MADERSON

ganization of the vertebrate integumentare responses to problems posed by thebasic locomotory patterns.

Whatever the actual protovertebratelooked like (Berrill, 1955), the small soft-bodied creature probably possessed an in-tegument similar to that of Amphioxus.Millions of unrecorded years of evolutionseparate this ancestor from the profusionof early Paleozoic fish forms, but we knowthat during this period, increase in bodysize was accompanied by a mechanicalstrengthening of the body surface. Whilethe reasons for this are debatable (see dis-cussion, Moss, 1968a), the question pre-sents itself as to how the integument couldbe strengthened at all in an animalwhose fundamental locomotory pattern de-pended on free lateral flexure of the body(Gray, 1968). Easily envisaged intermedi-ates, with obvious selective advantages, atleast for mechanical protection, lead even-tually to either a partial abandonment ofthe body mobility — "the turtle strategy"— or else folding. As a result of thelatter, any one segment of the body axisbecame covered by two or more unitswhich could move relatively freely overone another. Since either the epidermaland/or dermal components of such unitscould thereafter be strengthened, thisoffered possibilities for mechanical strength-ening while retaining the fundamentalfunctional requirement of lability of theorgan system in toto. We recognize thesefolds as "scales," which can thereforebe defined as serial, patterned folds of theintegument in which the epidermal and/or dermal components may be variouslyelaborated so that one or the other type oftissue may be present in greater quantity,or be superficially more obvious, than theother.

Within the definition of a scale givenabove, we can describe the integument ofany vertebrate as being "scaled," "non-scaled," or a mixture of the two. In thecase of those forms which definitely do nothave scaled integuments, e.g., cyclostomes,elasmobranchs, holocephalans, anguilli-form teleosts, most modern amphibia,

birds, and most mammals, it is most proba-ble that they are derived from ancestralstocks whose integument was scaled. Fur-thermore, the integument of each of thesetaxa is characterized by the presence ofcomplex derivatives — various multicellu-lar glands, dermal denticles, hairs, andfeathers. These structures are fundamen-tally localized centers of specialized epider-mal and/or dermal cell proliferation anddifferentiation, within an otherwise gener-alized integument, of which they mayproperly be described as "appendages."Analagous structures may be found withinscaled 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 "scaledintegument" is made up of scales, logicallyany individual scale is a part of the integu-ment, and cannot therefore be regarded asan appendage. This distinction is pertinentto any discussion of integumentary evolu-tion. Where the adult integument isscaled, the epidermal-dermal cell popula-tions over the embryonic body surface wereoriginally sub-divided into developmentalfields. Within these fields, appendagesmay subsequently differentiate. As will bediscussed later, the evolution, embryo-genesis, and adult distribution of hairs andfeathers (Maderson, 1972a) can only beunderstood by relating them to such de-velopmental fields.

Vertebrate integumentary structures canonly be defined accurately if one combinesthe descriptive terms mentioned abovewith a reference to the chemical or molec-ular nature of the material synthesized bythe constituent cell populations (Table I).The term "dermal scale," so often used todescribe integumentary structures in pis-cine vertebrates, has little meaning unlessone refers to the specific end-product ofthe interaction between dermis and epider-mis in any particular taxon (Moss, 19686,1972). 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 terminologyand definitions discussed in the text.

TaxonGeneral

description1 Appendages2 Most conspicuous features3

CyclostomesChondrichthyesSarcopterygiansActinopterygians

Amphibians

Chelonia

Archosauria

Lepidosaurs

Birds

Mammals

UnsealedUnsealedScaledScaled

Unsealed

Scaled*

Scaled

Scaled

Mixed

Unsealed

YesYesYesYes

No

No

No

No

Yes

Yes

Unicellular epidermal mucous glandsDenticles*Dermal ossification with superficial COSMINE layer*Dermal ossifications with a variety of superficial

mineralizations*Weak epidermal keratinization: dermal ossifications

in some scaled apodansVaried horizontal distribution of epidermal keratin

typesHorizontal alternation of a- and /3-epidermal keratin

types: dermal ossifications in many regionsVertical alternation of a- and ^-epidermal keratin

types: dermal ossifications in many lizardsFeathers of j3-keratin* arising from a-synthesizing

general epidermis: horizontal alternation of a-andj9-keratin types on leg scales

Hairs of o-keratin* arising from a-synthesizing gen-eral epidermis: dermal ossifications in some forms1 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 thegroup.

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 ossifi-

cations, obviously inhibits flexibility. Data from: Alexander (1970); Baden and Maderson (1970);Moss (1968a,6); Quay (1972); Spearman (I960).

chosaurian scale surfaces (Baden andMaderson, 1970) makes these units as diff-erent in their own way as are feathers andhairs.

The integumentary morphology of pis-cine fossils is usually clearly demonstratedby impressions in the surrounding matrix,but we need some "rule-of-thumb" for tet-rapod fossils. Many extant squamates havescales which do not contain dermal ossifi-cations. However, with the exception ofDermochelys (the leatherback turtle), Iknow of no living tetrapod which normallyhas a wide-spread distribution of dermalossifications which does not have a visiblyscaled integument. While this does notnecessarily indicate a 1:1 relationship be-tween externally recognizable units andindividual ossification centers (Zangerl,1969), it does suggest that in those systemswhere developmental fields exist in theembryonic integument and produce a pat-tern of dermal ossification, similar fieldsinfluence the topography of the entire in-tegument. Therefore, I suggest that ifpaleontologists describe "scales" (dermal

ossifications) in their material, the formsconcerned probably had scaled integu-ments in the sense defined earlier.

Was the primitive tetrapod epidermiskeratinized? Spearman (1966) indicatedthat the potential for keratin synthesis iswidespread among vertebrates, and the re-ports on the ultrastructure of epidermalcells (Flaxman, 1972) show that all epi-dermal basal cells contain the 70-80A widefilaments which are associated with a-ker-atin. However, it is also known that inthose tissues where the /?-protein is synthe-sized (characterized by 30A wide fila-ments) , the 70A filaments occur first, andthe 30A units appear later and eventuallyfill 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 proteintypes in extant amniotes (Baden andMaderson, 1970). It appears that thoselower Pennsylvanian captorhinomorphswhich gave rise to synapsids and mammalspossessed only the capacity to synthesizea-keratin. The remainder of the cap-

162 PAUL F. A. MADERSON

FIG. 1. Sagittal section through ventral body scalesof the gekkonid lizard Eublcpharis maculariusjust before skin-shedding. The ^-layers of the outer(/So) and inner (fii) epidermal generations arethick on the outer scale surface (OSS) , but arereduced to a single layer of cells on the innersurface and in the hinge region (ISS, H) . D-dermis; sc- sub-cutaneous tissue.

torhinomorphs, which gave rise to all theother reptilian groups and birds (Carroll,1969(1$/:), possessed an additional capaci-ty for /3-protein synthesis in their epider-mis, which was variously expressed in diff-erent lineages (Table I). What then of thepaleozoic amphibia? Romer and Witter(1941), Colbert (1955), and Kitching(1957) described ossified units suggesting ascaled integument (see above) which wassecondarily modified in their lissamphibiandescendents (Cox, 1967). Findlay (1968a)suggested that haematite deposits aroundthe matrix of the lower Triassic Urano-centrodon resulted from the decomposi-tion of sulphur-containing epidermal pro-teins. While this intriguing interpretationsuggests the presence of keratin, it does notreveal whether it was of the a- or /J-variety!

Microscopic and ultrastructural studiesindicate that the epidermal tissues on theinner surface and hinge region of amniotescales tend to be thinner, less compact, andmore lamellate in their organization thanthose on the outer scale surfaces. Differentfluorescent properties of different regionsof amniote scales (Cane and Spearman,1967; Spearman, 1964, 1966, 1967) cannotbe explained by reference to the presenceof a- or /J-keratins alone (Baden and Mad-erson, 1970). However, they may reflectdifferences in inter-cellular bonding, whichendow the different epidermal regions

with different mechanical properties, andthese originally augmented the flexibilityof the entire integumentary system. Thisend is still extremely important in squa-mates where numerous subtle differencesin patterns of cell production and differen-tiation modify the basic epidermal gener-ation pattern (Maderson, 1965, 1966;Maderson and Licht, 1967) over the innerscale surface and hinge (Fig. 1). However,the persistent a-protein in these regions incrocodiles and birds (Baden and Mader-son, 1970) and centers of granular layerformation in mammalian tail scale"hinges" (Spearman, 1964, 1966) shouldbe interpreted as relics of the ancestralfunctional modifications.

TRENDS IN VERTEBRATE INTEGUMENTARYEVOLUTION

Raising the question of the possible ho-mology between feathers, hairs, and scales,Cohen (1964) wrote: "If by homology wemean that the organs concerned, may, webelieve, be traced back along lines of an-cestors until a comparable structure isreached in the common ancestor, then theassessment is always made more difficult bymore facts." This conclusion is germaneto the entire topic of integumentary evolu-tion. On the basis of the facts presentedabove and their combination with the mostconservative possible deductions regardingpossible integumentary anatomy in fossilforms, we are forced to conclude that notwo integumentary features in two majorassemblages can be strictly considered to behomologous. This concept must be re-stricted to such examples as pelage hair andspines in mammals, or climbing setae andthe normal Oberhautchen in lizards(Maderson, 1970). Even the recognition ofgeneral anatomical trends is of limitedvalue. While piscine vertebrates tend tohave scaled integuments or conspicuouselaborations of dermal skeletal structuresor both, attempts to define the degree ofhomology 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 Gekho gecko.The epidermis shows a stage 4 condition of theshedding cycle (Maderson and Licht, 1967) andshows that the "hair" derives from a modifiedOberhautchen cell (SpOb) . In a sense organ of thistype, although the structure of the epidermalgeneration is modified, the subjacent germinal cells(sg), closely resemble those of the adjacentnon-specialized epidermis. Note the cluster of cellsin the dermis (X) beneath the sense organ hereand in Figures 4 and 5. The /3-layer of the outerepidermal generation is not seen in the photo-graph. Other abbreviations, here and in Figures 4and 5: oo — o-layer of the outer generation;/3i — /3-layer of the inner generation; clo — clearlayer of the outer generation; lto — lacunar tissueof the outer generation; mi — mesos layer of theinner generation; Obi — Oberhautchen of the innergeneration; Obis —spinules of the unspecializedOberhaulchen cells.

have not changed during evolution. Thequestion "Are tetrapod scales retainedfrom the piscine ancestors?" has no mean-ing except to emphasize that there is ageneral capacity for patterned integumen-tary structure in different taxa with vary-ing degrees of phyletic affinity. Whatevergeneral trend we define or recognize, it isalways subject to major or minor revisionof execution. In short, I favor the "radi-cal" view of integumentary evolution tosuch a degree that I would suggest that inany instance, a functional question shouldbe asked, a functional investigation shouldfollow, and any subsequent detailed ana-tomical study should be expected todemonstrate yet another example of mor-

VERTEBRATE INTEGUMENTARY EVOLUTION 163

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 thereother structures which resemble mammal-ian hair in other vertebrates, or indeed inother animals? Third, have hairs alwaysserved an insulatory function, and if not,what other functions could they haveserved? Finally, is it possible to present amodel for the steps in the phylogeneticdevelopment of hair, with plausible expla-nations for the accompanying selectivepressures?

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 neuroanatomicalstudies) strongly suggest that the commonancestor of monotremes and therians wasalso mammalian in a majority of essentialfeatures e.g. hair, lungs, diaphragm, heart,and kidneys, to name a few." How many ofthese features might have characterizedthe early Triassic cynodonts which Hopsonand Crompton (1969) proposed as mam-malian ancestors? Reference to possible in-tegumentary structures of therapsids is socommon-place that we may tend to forgetthat there is no direct information avail-able. Watson (1931), Brink (1956), andFindlay (1968ft) interpreted depressions inskull bones as probably having housed vi-brissae or "skin glands of a sweat glandnature" (Brink, p. 87). These interpreta-tions were extrapolated to suggest pelagehairs and normal sweat glands over therest 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 asituation so close to circuitous argumentthat it is time to seek a new approach tothe problem of the origin of hair.

No extant vertebrates have integumen-

164 PAUL F. A. MADERSON

tary appendages which anatomically re-semble hairs. The structures seen in manylizards (Fig. 2), once invoked as "ancestralhairs" (Elias and Bortner, 1957), are sen-sory units (Miller and Kasahara, 1967) de-rived from individual cells of the Ober-hautchen (Schmidt, 1920; Maderson andLicht, 1967; Maderson, 1971), which layeris a unique constituent of the lepidosauri-an epidermis (Maderson, 1968a). Whilethe anatomy of the individual units is cer-tainly not homologous with that of anyvertebrate epidermal derivative, a numberof insects have a "pelage" (Heath, 1968).

Although the pelage plays a primaryrole 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 thistype. Conversely, the presence of a cover-ing pelage does not necessarily indicate anabsolutely constant internal temperaturethroughout life (Heath, 1968). There istherefore no a priori reason for assumingthat therapsid thermoregulation could nothave evolved in the absence of a pelage.Indeed, the physical laws which govern thefunctioning of a pelage indicate that eachconstituent unit must have a certain mini-mum length, and there must be a certainminimum density per unit area of the bodybefore any selective advantage accrueswith 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 asteady accumulation of "neutral traits"affecting epidermal morphogenesis overseveral thousand generations. A moreplausible hypothesis is that the insulatingfunction of hair is secondary and becamepossible only after completely different se-lective advantages had favored suitablemorphogenic changes in the epidermis.These primary selective pressures can beidentified if we consider the probable ecol-ogy of the extinct forms concerned, andthence deduce the obligatory minimalfunctions of their integument.

Studies of Pennsylvania reptile fossils(Carroll, 1964, 1969a,bjC, 1970a,b) suggestthat they were small, highly terrestrial, for-est-dwelling forms. Carroll (1970&) writesof the captorhinomorph Hylonomus lyelli:"in size and general form it resembles amedium-sized lizard. It may have had simi-lar habits as well." I suggest that function-ally the integument of such forms wouldhave resembled that of modern lizards.The epidermis would have possessed awell-developed outer cornified regionwhich would have provided a degree ofprotection against dessication (Madersonet al., 1970). Carroll's (1964) descriptionsof osteoscutes suggest a scaled integument(see above), so that both dermal and epi-

dermal components probably contributedto mechanical protection. Since holocrinesecretion is a very important function inmodern lizards (Maderson, 1970), this mayhave been true for the earliest reptiles.However, in most modern amniotes,odoriferous sources are localized on thebody surface: the pheromonal function ofsweat-glands in some mammals is probablysecondary. My own observations on agreat variety of modern lizards suggest thatif behavioral thermoregulation character-ized the earliest reptiles, this would nothave necessitated any particular morpholo-gical structure of the integument, exceptperhaps with regard to the distribution ofpigment cells (Porter, 1967). If the integu-ment of primitive reptiles manifested othersecondary functions (e.g., climbing claws,poison glands, sexual or territorial warn-ing appendages), comparative observationson modern amniotes indicate that associ-ated structural modifications would havebeen localized on the body surface.

Apart from the "primary barrier func-tion" of physiological and mechanical pro-tection which influences the fundamentalmorphology 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 quitedifferent types of sensory stimulus havealways impinged upon the terrestrial in-

VERTEBRATE INTEGUMENTARY EVOLUTION 165

<?«/*.

FIG. 3. Schematic representation of a mammaliantylotrich hair follicle modified after Straile (1969) .1 - hair shaft; 2 - internal root sheath; 3 - externalroot sheath; 4 - germinal region of the ty-lotrich follicle; 5 - dermal papilla; 6 - connectivetissue sheath; 7 - annular complex; 8 - epidermalpad 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 ambienttemperature, or casual contact with thesubstrate during locomotion, are inter-preted by the brain quite differently thanare sudden temperature changes, or sharppressures. Any or all of any variety oftypes, or levels, of stimulation might chal-lenge any part of the body surface. It istherefore predictable that there would be aspatial pattern of functional differentia-tion across the integument, which might bereflected anatomically in patterns of nervedistribution and/or the morphology ofthe receptor-transducer units.

I propose that mammalian hairs are de-rived from complex epidermal modifica-tions of mechanoreceptor function, whichwere originally "sparsely," but regularly,distributed over the surface of the body. Atsome stage in the evolution of the therap-sid integument, the competence of the de-velopmental fields centered around theoriginal units changed, resulting in a mul-tiplication of basically similar morphogen-ic events. These events produced a suffi-cient density of "sense organs" per unitarea of the body to produce a "pelage," theinsulative properties of which were the fo-cus for subsequent selection. The sensoryfunction of hair in modern mammals doesnot exactly resemble that of the originalunits, but this does not affect the morpho-logical model which will be presented. Thedata supporting this hypothesis will nowbe discussed.

Straile (1969) proposed "repeating ver-tical units" in the mammalian integumentcontaining epidermal, neural, and vascularelements arranged around a "tylotrich"hair follicle (Fig. 3). The tylotrich is asso-ciated with two innervated regions, an an-nular complex surrounding the upperthird of the follicle, and an adjacent epi-dermal pad complex. Although the exactconstruction of the vertical unit variesacross the body, and between taxa, tylo-trichs have been observed in monotremesand many therian mammals (Mann, 1968).While there is some disagreement as to

166 PAUL F. A. MADERSON

mm 4FIG. 4. Sense organ from a labial scale of theiguanid lizard Iguana iguana. The epidermis is inthe resting phase of the shedding cycle (Madersonand Licht, 1967) . In this type of sense organ, theassociated germinal cells are always columnar andhave vesicles at their distal tips. The mature ker-atinized elements of the outer epidermal gener-ation are indicated by dotted lines. /So - /3-layer o£the outer generation.

FIG. 5. Sense organ from a lateral body scale ofthe xantusiid lizard Xantusia vigilis. The epidermisis in stage 4 of the shedding cycle, and we notethat although this type of sense organ does notprotrude above the general level of the skinsurface, it is associated with a modification of thehistogenesis of the inner generation which producesmature elements (dotted outlines) analagousto those seen in Figure 4.

how the electro-physiological data shouldbe related to the anatomical data (see dis-cussion, Straile, 1969), there is good evi-dence that both rapid and slowly adaptingmechanoreceptors are represented withinrepeating vertical units so that: "The de-tection of a tactile stimulus moving frompoint 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, whereeven cursory examination reveals a pleas-ing geometric order, has long made mesuspicious of the apparent heterogeneity ofthe mammalian system. Straile's "re-peating vertical unit" seems to me toprovide 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 ofany single type available, but the distribu-tion of "Haareorganes" suggests a functionof monitoring inter-scale contact (Mader-son, 1971). Bailey (1969) demonstratedfast and slow-adapting mechanoreceptorsby electro-physiological techniques, butdid not provide an anatomical correlation.The anatomy and functioning of the in-fra-red sensitive cutaneous pit organs insnakes have been extensively studied (Bar-rett, 1970; Meszler, 1970). Although thedata are sparse, we can say that cutaneoussensory 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 thepremise of a direct relationship to the la-certilian "Haareorgane" which is no long-er acceptable (see above). While themorphogenic events in hair developmentare difficult to relate to any possible evolu-tionary sequence, if one ignores the detailsinvolved, one can derive a useful, simply-stated overview. A portion of the germinalpopulation becomes specialized so that itsdaughter cells stick together as a rod whichprojects above the skin surface, while thedaughter cells of adjacent, unspecializedinter-follicular epidermis do not stick to-gether so tightly and therefore desqua-mate. The process of initial specializationand adult homeostasis involves mesodermcells ("the dermal papilla"), and the twocell populations influence one another viaa sequence of inductive processes which weterm "epithelial-mesenchymal interac-tions" (see Kollar, 1972). The elegantcomplexity of the hair follicle, which atfirst sight seems so difficult to explain inevolutionary terms, may be readily ex-plained. It permits a "good rod" to growfrom a "good hole," a mere refinementwhich could have occurred quite late inthe phylogeny of hair. It should be noted

VERTEBRATE INTEGUMENTARY EVOLUTION 16?

FIG. 6. Suggested model for the sequence of mor-phological changes in the evolution of mammalianhair, a - suggested integumentary structure of aprimitive cotylosaur; b - suggested integumentarystructure of a cotylosaur associated with synapsidlineage; c - suggested integumentary structure of apelycosaur associated with the therapsid/mammal-ian lineage; d - e - magnified views of suggestedevolutionary changes in the original "hinge" regionof 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-adapt-ing mechanoreceptors; heavy dotted lines — neuronsassociated with slow-adapting mechanoreceptors;cross-hatching — dermal ossification. For explana-tion, see text.

that holocrine secretion from lacertilianpre-anal organs (Maderson, 19686, 1970,1971, 19726) frequently produces a dura-ble "rod" of mature cells which may pro-trude a considerable distance from the skinsurface. However, there are no specializa-tions comparable to the various layers ofthe inner and outer root sheath seen in ahair follicle.

Before we consider the model, it shouldbe mentioned that all recent accounts ofthe amphibian-reptilian-mammalian line-

age (Carroll, 1964, 1969a,b,c, 1970a,6; Cle-mens, 1970; Hopson, 1969; Hopson andCrompton, 1969; Jenkins, 1970) indicatethat the creatures concerned were of smallsize —less than 18" total length. However,throughout the geological eras concerned,related forms and other amphibian andreptilian groups radiated to produce gen-era of considerable size. The mammaliangrade of organization with its attendantmorphological characteristics, e.g., hair,was perfected over a period of 200 millionyears by small animals, possibly crevicedwellers, who probably attained their evo-lutionary destiny by exploiting nocturnalniches, following gradual refinement ofthermoregulatory mechanisms.

A possible structure of the early coty-losaurian integument is shown in Figure6a. The epidermis contained only a-ker-atin, and the tissue was thinned on theinner scale surface and hinge region. Aplausible suggestion for the differentialdistribution of mechanoreceptors wouldplace fast-adapting units on the outer scalesurface. These monitored transient envi-ronmental contact during normal locomo-tion. Locomotory activities involvingstretching or compression of the integu-ment (e.g., twisting of the body into smallcrevices and hiding) could have been mon-itored by slow-adapting receptors in thehinge region. Dermal ossifications werepresent and possibly played some mechani-cal protective role.

In those cotylosaurs associated with thebasic synapsid stock and the derived forms,certain modifications characterized the in-tegument (Fig. 6b). I propose that theinvolvement of keratohyalin in the kerat-inization process, at first confined to thehinge region (Spearman, 1964, 1966), en-hanced the overall flexibility of the integu-ment and permitted a reduction of scaleoverlap. This additional protein couldhave 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 thescarcity, or absence, of dermal ossifications

168 PAUL F. A. MADERSON

in synapsid material. The modified pat-tern of protein synthesis may have per-mitted a thickened epidermis on the outerscale surface to provide mechanical protec-tion and perhaps decrease percutaneouswater-loss. The groups of fast-adaptingmechanoreceptors probably became local-ized within regions of hypoplasia. The re-duction of scale overlap diminished theoriginal function of the slow-adapting re-ceptors in the hinge region for monitoringinter-scale contact. However, the functionof providing sensory data during hidingcould have been maintained if the nerveendings became associated with a small ep-idermal papilla which protruded to a leveljust beneath the general level of the outerscale surfaces during normal locomotion.

The widespread occurrence of thermo-regulatory behavior patterns in modernreptiles (Bellairs, 1969) implies that theyarose very early in reptilian evolution. If,indeed, Triassic therapsids did manifestsome 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 organizationrelative 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 whileperipheral temperature receptors modulatehypothalamic responses to environmentaltemperature change in mammals, hestated: "The cold-blooded terrestrial ani-mals may rely largely on internal recep-tors." Such receptors can only provide in-formation regarding heat energy after ithas been absorbed; they cannot criticallyexamine possible differential heat-sourcesin the environment on a "minute-by-minute basis." For this reason, the ther-moregulatory behavior patterns of modernlizards involve quite sudden movementsfrom 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 ofheat absorbed by the deep body tissues

depends upon the cooling influences at theskin surface. Any animal which could mon-itor such influences, and accordingly ad-just its position in the environment, couldachieve 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 ofa pelycosaur at the base of the therapsid-mammalian lineage. Certain general trendsdescribed earlier have continued, i.e., re-duction of scale overlap, spread of thegranular layer, epidermal thickening. Theslow-adapting mechanoreceptors originallyseen in the hinge region are now associ-ated with a longer papilla, the primaryfunction of which is still monitoring envi-ronmental contact during hiding activity.When the body is still during sun-basking,these papillae protrude above the generalbody 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 whichgrows out from a follicle; movement of thedistal tip of the rod distorts the entirestructure leading to activation of the neu-rons which are now associated with theupper third of the follicle. The daughtercells arising from the germinal region ofthe follicle form a tightly adhering mass,and specialization of the outermost celllayers would endow this "rod" with specificmechanical properties associated withflexibility. These patterns of cellular activ-ity are sufficiently distinct from those ofsurrounding "interfollicular" epidermalcells to imply the presence of a distinctmorphogenetic mechanism responsible fortheir control. At this stage in evolution,the dermal papilla appeared. It does notmatter whether this structure arose initial-ly as an embryonic or an adult "inducer,"since its fundamental role — maintenanceof a specialized sequence of differentiativeevents for a circumscribed germinal/

VERTEBRATE INTEGUMENTARY EVOLUTION 169

-.** MFIG. 7. Sagittal section through rat tail scaleshowing a hair follicle growing from the "hingeregion." The restriction of the granular layer to

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

daughter cell population within an other-wise homogeneous epidermal system — isthe same at all stages of the life cycle.

The model to this point suggests thatalthough the postulated specialized mech-anoreceptor — which should be comparedto the tylotrich hair follicle (Fig. 3) —did not evolve from a scale, it wasinitially associated with a morphogenicfield surrounding a scale and eventuallysuperseded it in size and importance. Thispremise receives support from the follow-ing data. First, tylotrichs develop first inthe embryo (Mann, 1968). Second, tylo-trichs are more numerous dorsally thanventrally (Mann, 1969) — a similar condi-tion is seen with regard to scales in most li-zards. Third, recalling that the sequence ofevents under discussion concerned smallanimals, we note that Mann (1969) stated:"The larger the mammal, the fewer thetylotrichs per unit surface area of theskin." Fourth, the described sequence ofevents accounts for hair distribution acrossthe scaled caudal integument of somemodern mammals (Spearman, 1964, 1966)

(Fig- 7) •The integumentary structure shown in

Figure 6f might have characterized a smallearly therapsid with a highly sophisticatedthermoregulatory behavior pattern. How-ever, the function of the spatially dis-

tributed "eotylotrichs" was exclusivelymechanoreceptive, and such structurescould not have served an insulatory func-tion. I suggest that this secondary functionarose following the multiplication of follic-ular units within the original "scale mor-phogenic field" surrounding the eoty-lotrich.

The model suggests an association be-tween a certain level of morphologic com-plexity and the evolutionary appearance ofa dermal papilla. Cohen (1964, 1969) hasemphasized the similarity in organizationof 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 failureof feather development in the talpid3 mu-tant chick embryo and demonstrated a de-fect of dermal papilla formation. Whilecomparable detailed ontogenic analyses arelacking, Mann (1969) listed recessivepoint mutations in mice which disturbednormal tylotrich development. I submitthat it is equally possible that multiplica-tion of follicular units could have occurredas the result of a single gene change inour therapsid ancestors. The only questionis, what selective advantage accrued whichfavored the survival and spread of such agene change? There are two possibilities,

170 PAUL F. A. MADERSON

which are not mutually exclusive. The in-crease in number of units reached or sur-passed the minimum density per unit areanecessary to provide insulatory benefits.Alternatively, since secondary hair folliclesin modern mammals are associated withrapidly adapting touch receptors (Straile,1969), one could argue that the "lever-activated" receptor associated with theslow-adapting receptors (the eotylotrich)was so successful that selection favored theincorporation of the fast-adapting unitsinto secondarily derived similar structures.I favor the second of these explanationssince it does not necessitate quantumchanges in anatomical structure and doesoffer possible successive levels of cutaneousorganization, culminating in an insulatorypelage.

The model which has been presentedhere is highly speculative, but this is inevi-table due to the nature of the subject. Thepremise of a mechanoreceptor origin formammalian hair is not new, but it hasnever before to my knowledge been consid-ered in detail with reference to a series ofselective pressures. I would like to em-phasize in conclusion, that if the level ofmechanoreceptor organization shown inFigure 6f were typical of most cynodonts,enlarged units could have formed the fa-cial vibrissae discussed earlier. If we acceptHeath's (1968) and Bailey's (1969) state-ments with reference to deep and cutane-ous thermoreception in mammals versusreptiles, we might even suggest that it wasonly in the phyletic line leading to mam-mals that peripheral modulation of hy-pothalamic temperature responses de-veloped. This could have been that lastsubtle refinement in endothermy which en-sured the success of the lineage.

Right or wrong, this discussion will haveserved its purpose if it stimulates furtherinterest in mammalian cutaneous recep-tion, but even better, it should lead tocomparable studies on modern lizards, theepidermis of which is, after all, the zenithof amniote integumentary evolution.

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