AM. ZOOLOGIST, 12:27-34 (1972).

The Vertebrate Dermis and the Integumental Skeleton

MELVIN L. MOSS

Department of Anatomy, College of Physicians and Surgeons,School of Dental and Oral Surgery, Columbia University,

New York, Netu York 10032

SYNOPSIS. The comparative histology of the dermis is reviewed. Some recent data on theconnective tissue components of this vertebrate organ are summarized withemphasis on collagen and ground substance. The biomechanical role of the dermis isstressed within the concept of the integumental skeleton. The series of homologousdevelopmental events involved in the formation of these "skeletal" structures aredescribed, with some emphasis on the hypothesis of epidermal co-participation. Finally,a classification of the spectrum of integumental skeletal structures is given.

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INTRODUCTION

The dermis shares a common character-istic with many other organs; it is capableof encompassing a substantial number ofscientific disciplines. Accordingly, it is notsurprising that dermatologists, anatomists,surgeons, immunologists, endocrinologists,neurologists, and chemists of many varie-ties, to enumerate but a few of the moreobvious, have seemingly disparate, buthopefully interrelated, common interests inan integumentary layer common to allvertebrates. Further, there is little reasonto hope that any truly comprehensive re-view of this organ has yet appeared. Eachapproach inevitably is flavored by the par-ticular interests of individual students.The diversity of this symposium is an ac-curate reflection of this condition. Nor isthis paper an exception, placing its majoremphasis upon the structural, or skeletal,role of dermis. It is specifically stated thatthis paper is intended as a review for thenon-specialist. However, if the period ofconceptual synthesis is not yet arrived forthe integument, it is still possible to re-view, yet once again, the general proper-ties of the dermis.

The dermis is defined here as the con-nective tissue layer of vertebrates immedi-ately subjacent to the epidermis, together

Aided in part by research giants DE-01206 andDE-01715 and a training grant DE-00132, NationalInstitute of Dental Research.

with which it forms the skin. Considered asan organ, the dermis variably contains anumber of epidermal derivatives, glands ofseveral types, scales, bone, feathers, andhair. Further, its adipose, pigment cell,vascular, and neural components arerelated importantly to the several func-tions the dermis subserves. Finally, the der-mis generally is competent to interact withthe overlying epidermis in a number ofimportant developmental and structurallymaintaining processes. Accordingly, whileit may be appropriate to study the dermisin isolation with respect to some of itsproperties or components (to study col-lagen fibrillogenesis, for example), it isfrequently difficult to isolate it from thefunctions of the skin as a whole.

COMPARATIVE HISTOLOGY

A basic source of information on the ver-tebrate dermis is found in Bolk et al.,(1931). Similar encyclopedic treatment ofmammalian dermis is given by Horstmann(1957) and by Pinkus (1927). Andrew(1959) has reviewed the comparative his-tology of this layer. Dermis proper is auniquely vertebrate structure. Its structureis related both to the mode of life as wellas to the phylogenetic position of the ani-mal. In Amphioxus, a thin (2-4 )̂ denselyfibrous layer is found subjacent to the epi-dermis, beneath which there is a muchthicker gelatinous layer containing single

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28 MELVIN L. MOSS

collagen fibers. The cyclostome Petro-myzon has coarse bundles of collagenfibers, often crossing at right angles to eachother. Fine, "pre-elastic" fibers form anadditional fine meshwork. Fat tissue is alsoobserved in these agnatha. It is in elasmo-branchs that true elastic fibers are foundfor the first time in conjunction with thedivision of the dermis into a superficiallayer of looser construction and a deeper,more compact, layer of collagen fibers. Analternating pattern of collagen bundles isseen, with diagonal intersections forming aregular pattern. In the higher fishes, thebilaminar dermis is seen also. Importantly,chromatophores may now be found, usu-ally subjacent to the epidermis. As a gener-al rule, but with significant exceptions, thedermis is thinner in fishes with scales thanit is in those without them. In the fins ofall fishes only a basement membrane ispresent; otherwise the dermis is absent inthese sites.

Amphibia mark the acquisition by thedermis of the secretory function formerlyheld by the epidermis. Multicellular glandsare found now in the dermis. Excludingthe thin basement membrane, the dermismay be said to be bilaminar. The loose,more superficial layer is highly cellular inamphibia, and it may contain many largeglands as well as a large amount of"ground substance." This layer is especial-ly well marked in amphibia. Elastic fiberstend to form "arches" here, and smoothmuscle is found for the first time, either assingle fibers or as small bundles. Addition-al specializations of amphibian dermis in-clude large lymph spaces, related to theirsmooth muscles, which play a role in wateruptake. The same layer may containmany capillaries, playing a significant rolein respiration, especially in those formswith essentially functionless lungs. Chro-matophores may be plentiful. Dermalglands are missing in both reptiles andbirds. In the former the typical vertebratebilaminar structure is seen, while in birdsthe dermis frequently contains both soli-tary lymph follicles and masses of diffuselymphoid tissue. Further, birds usually

have a very loose skin, with a relativelythin dermis which contains an irregularlywoven meshwork of fibers and is especiallyrich in sensory end-organs.

The mammalian dermis may also be saidto be bilaminar. It is customary to differ-entiate between the more superficial papil-lary layer, containing blood vessels, nerves,lymphatics, glands, and fat, and the deep-er reticular layer, some of whose densecollagen fiber bundles pass down to thesubcutaneous fascia, while others pass up-wards towards the epidermis (see alsoBallard, 1964; Waterman et al., 1970).

INDUCTIVE INTERACTIONS

This topic is reviewed elsewhere in thissymposium (Kollar, 1972) as it has beenrecently by us (Moss, 1969a). (See alsoFleischmajer and Billingham, 1968.) It issufficient to state here that many dermalstructures and functions originate fromsuch processes operative between the epi-dermis and dermis.

Dermal-epidermal interactions continuethroughout life. The maintenance of adultepidermal characteristics seemingly re-quires a constant dermal contribution. In-terestingly, it is not necessary for this der-mis to be histologically intact, nor is thiseffect dermal site specific. Further, othernon-dermal connective tissues are equallycapable of supporting continued epider-mal structures. In this aspect, it is the typeof tissue comprising the dermis, ratherthan any specifically structured "dermal"attribute which is operative (Briggamanand Wheeler, 1971).

DERMAL CONTENTS

The dermis recently has been the sub-ject of an excellent review (Montagna etal., 1970; see also Montagna, 1962).

The dermis, as a connective tissue maybe said to consist of a fibrillar framework,enmeshed in, and partially united with, an"amorphous" ground substance. Thefibers are predominantly collagenous withlesser, yet functionally significant, elasticcomponent;,. The ground substance is rich

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INTEGUMENTAL SKELETON 29

in a variety of mucopolysaccharides (gly-cosaminoglycans). Fibroblasts (and fibro-cytes, according to the terminology of someworkers) are the predominant cell type,while most cells, histiocytes, and melano-cytes are found variable. Considered as anorgan, the dermis variably contains holo-crine, merocrine, and apocrine glands,smooth mucle, nerves, and sensory end or-gans, epidermal derivatives (feathers, hair,scale, teeth) and circulatory vessels. Anexcellent review of the biochemical param-eters of the dermal connective tissues isfound in Schubert and Hamerman (1968).

FIBERS

Collagen which forms approximately 30percent by weight of normal dermis is thesubject of much work, and many aspectsof its formation, composition, structure,and physical parameters are known (seeRamachadran and Gould, 1968, for a sys-tematic treatise). Dermal collagen forms athree-dimensional, highly oriented, andcovalently linked fibrous network whoseprecise topography is not yet completelyclear, although it seemingly is related tothe mechanical needs of specific dermalregions (Jackson, 1970; Szirmai, 1971). Itis reasonably clear that at higher levels ofstructural organization collagen is boundto at least one quantitatively significantglycosaminoglycan component of theground substance, dermatan sulfate (chon-droitin sulfate B). Hence the older dicho-tomy between fibrous and amorphous der-mal components may not be strictly true invivo.

Collagen is aggregated into increasinglylarger structural elements by several pro-cesses. The fibrils themselves are stabilizedby covalent cross-linkages. Larger fibrilsare then bound to mucoproteins, while inlarge fibers mucopolysaccharides such asdermatan sulfate play a significant role intheir further structural stabilization. Itneed only be added here that yet furthercross-linkages and further "stabilization"can account for the gradual alteration inelastic properties of the dermis with age

(Elden, 1970). It remains only to notehere that there are many specific variationsin the composition of collagen at mostlevels of taxonomic organization whosefurther biological significance is not yetknown (see Mathews, 1967).

Elastic fibers are relatively sparse in thedermis. Elastin polymerizes extracellularlyto form a cross-linked, three-dimensionalgel, which exists in a two-phase hydrophil-ic and hydrophobic system. This excellentelastomer also undergoes significant alter-ation of physical properties with age, per-haps related to the fact that mature cross-linked elastin has an unusual metabolicinertia (Partridge, 1970).

GROUND SUBSTANCE

This ill-defined dermal component hasbeen called the "extravascular, extracellu-lar, extrafibrillar phase of dermis" (Pearceand Grimmer, 1970). As noted abovethere is good reason to suggest that manyglycosaminoglycans do not exist freely inthe ground substance, but rather arebound to fibrous components. Plasma pro-tein and hyaluronate are the two principalmacromolecular components of the groundsubstance. The role these materialsplay in regulating dermal characteristicsand properties remains unknown. For datacovering the composition of the groundsubstance, see Pearce and Grimmer (1970)and their included references.

It is reasonable to believe that groundsubstance significantly enables connectivetissues to bind cations, and so act as anoth-er reservoir for mineral homeostasis. It isinteresting to speculate that the role ofosseous tissues in this process may simplybe a specific example of a more generalconnective tissue phenomena (Bentley,1970). This same author describes otherpossible roles of the ground substance. Ofparticular interest is the concept that thedermis may play a role in glucose home-ostasis (Fusaro and Johnson, 1970).

OTHER DERMAL FUNCTIONS

As an organ, the dermis contains many

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MELVIN L. MOSS

structures and carries out associated func-tions. The scope of this paper precludestheir encyclopedic consideration. The neu-ral, vascular, and secretory structures andfunctions have been ably reviewed in manyplaces (see particularly the several vol-umes of the Advances in Biology of theSkin, Montagna, 1960-1965). In passing, itis noteworthy that the view is gaining thatthe structures of dermal sensory end organsare not as specifically related to functionas was held previously (Sinclair, 1967;Grossman and Hattis, 1967).

Having reviewed some salient features ofdermal structure and function, we willconsider now one specific function in de-tail, that of mechanical protection andsupport. The combination of dermal struc-tures carrying out this function is the in-tegumental skeleton.

THE INTEGUMENTAL SKELETON

The vertebrate skin participates in anumber of functions: sensations, secre-tions, water balance, thermal regulation,and many others. The degree to which anyparticular function is taxonomically sig-nificant obviously is variable, and as wehave indicated above, is reflected in thespecific histologic attributes of the dermis,as well as of the epidermis. There is onefunction, however, which appears to beuniversally carried out, that of providingprotection and/or support for the enclosedbody mass. It is possible to consider thatall vertebrates possess an integumentalskeleton, which while participating varia-bly in several other functions, also playsthis bio-mechanically important role.

Both fossil and recent materials easilydemonstrate that a number of distinctiveand characteristic structural (and bio-chemical) modifications have occurred toboth the dermal and epidermal layers ofthe skin which presumably have been ofselective advantage to specific vertebrates.The earliest known vertebrates from theearly and middle Ordovician present uswith a picture of a highly organized andstructurally complex dermis containing os-

FIG. 1. The regular, alternating structural array ofthe dense dermal collagen fiber bundles ofAcipenser oxyrhynchus (the Atlantic sturgeon) isseen. This uncalcified tissue serves well as an inte-gumental skeleton. This figure serves as a proto-type of the fiber pattern array of many othermineralized dermal skeletal structures.

seous and dental tissues aranged in severalways (see Orvig, 1967; Moss, 1964, 1968a).We do not know, and we may never, whatthe integumental skeleton of still earliervertebrate ancestral forms was like; itseems unlikely that they were as fully ar-mored as those of the earliest remains. It isat least reasonable, if not provable, thatsuch earlier forms did possess a dermiswithin which the organized collagen fibertracts were so arranged as to give the re-quisite protection and support. It might beargued, for example, that the fiber pat-terns of the dermal bone of the earliestknown agnathic fishes may have pre-existed in ancestral forms which did notyet possess the ability to form ossified tis-sues (Figs. 1-5). It is important to note

FIG. 2. The uncalcified dermal collagen fibers ofHeloderma horridum (Gila) show an array essen-tially similar to that in Figure (1).

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INTEGUMENTAL SKELETON 31

FIG. 3. This view o£ a mineralized osteodcrm ofHeloderma horridum well illustrates that the denseregular array of collagen bundles is main-tained. The outermost tissue is bone, while themain mass of this osteoderm is a tissue of indeter-minate nature.

that the presence of dental tissues sur-mounted and joined to underlying dermalbone also indicates that the epidermisprobably played some co-participatoryrole. Arguing by homology, the presence ofdentin in these Ordovician agnatha sug-gests that the series of mutually reciprocalinductive interactions characteristic of re-cent dental tissue odontogenesis was impli-cated here, too. The problem of fossil ag-nathic fish enamel as a structured eipider-mal tissue in the integumental skeleton isstill controversial (Moss, 1970).

The integumental skeleton can bestudied in many ways. One of the morefruitful recent fields is that of bioengineer-ing research into the physical properties of

dermis (see Millington et al., 1971; El-den, 1970). It is tempting, if possibly haz-ardous factually, to consider the potentialrelationships between the factors responsi-ble for the "split-line" pattern of dermalcollagen bundles (Langer's Lines) and theat least analogous, if not homologous,study of split-line patterns in partially de-calcified bone. While the immediate causesmay well be different (Moss, 1954), ulti-mately they may be held to show that der-mal bones really retain much of the essen-

FIG. 4. The dcrmis of Egernia kingi (Sauria, Scin-cidae) shows an extremely well ordered array ofcollagen to which is superimposed (above) a diff-use calcification.

FIG. 5. Dermal sclerifications in the armadillo(Dasypus novemcinctus) show an alternating array

of collagen fiber bundles basically not dissimi-lar to those pictured above.

tial patterning of the organized fiber bun-dles of their possibly uncalcified ancestors.It is true also that as a general rule theosseous components of the vertebrate in-tegumental skeleton show evolutionarytrends leading, in general terms, to both adiminution in the number of such osseousstructures as well as to their elimination.

We may now describe the integumentalskeleton as a protective organ — one inwhich the epidermis and dermis co-participate developmentally in a numberof ways. In the dermis it is possible to finda number of "hard" tissues in addition tocollagen fiber bundles. The histologicalcomposition of these "hard" tissues tendsto be very variable, forming a true spec-trum of types with many "intermediate"forms. Accordingly, we prefer to term themsclerified tissues. All vertebrate classes,save Aves, contain some representativeforms whose dermis contains some sort of

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32 MELVIN L. MOSS

sclerified tissue. While these tissues un-doubtedly add in some significant way tothe better fulfillment of a mechanicallyprotective role, these same sclerificationspossibly perform some additional role inmineral homeostasis, with the probable ex-ception of the acellular bone found inboth fossil and recent fishes (the dermalarmor of agnathic Heterostraci and theacellular bone of the dermal denticles ofrecent elasmobranchs, for example) (seeMoss, 1970).

The integumental skeleton is rep-resented by a number of structural modifi-cations of both epidermis and dermiswhich variably combine to form a struc-tural and functional whole. I believe it isreasonable to suppose that despite the ap-parent and oft-times great differences instructural expressivity demonstrated in thevertebrate integumental skeleton, a seriesof basically homologous developmental pro-cesses underlies them all. Previously, Ihave discussed these concepts as the epi-dermal co-participation hypothesis (Moss,1968&). It is suggested that (1) inductiveinteractions occur between the epidermisand dermis (and in some cases at leastinvolves ectomesenchymal cells); (2) ei-ther or both the epidermis and dermisform structural derivatives; (3) the epider-mis always contributes something, even ifit is an unstructured but important com-ponent of a dermal structural derivative;and (4) delamination plays an importantrole in topographically organizing the der-mal portion of the integumental skeleton.References are given below as I outline thespecifics of this hypothesis. Three types ofintegumental skeletons are found.

A. Epidermal Derivatives: In passing wemention here some types of integumentalskeletal forms which are produced solelyby structural epidermal derivatives. Thereare no organized dermal contributions tothese forms, although the dermis does playa necessarily initial role in the inductioninteractions between ectoderm and mesen-chyme (see Spearman, 1964, 1966). A par-tial list would include hair, feathers, rhino-cerous horn, whale baleen, reptile scales,

turtle scutes, mammalian bones, beaks,claws, and nails. Interestingly, the forma-tion of some sort of epidermal-dermal pa-pilla is associated in one way or anotherwith all of these structures.

B. Epidermal-Dermal Derivatives: Thisgroup of structures contains structural ele-ments from both sources. In this sense, thetwo skin layers co-participate in the forma-tion of their skeletal structures. There arethree subdivisions in this grouping, inwhich the evidence of epidermal participa-tion to the formation of visible skeletalderivatives ranges from the most obviousto the least (see Moss, 1968&, for a morecomplete discussion). A partial listing in-cludes:

1. a) vertebrate teethb) dermal denticles

2. c) cosmoid scalesd) ganoid scales (paleoniscoid

and lepidosteoid)3. e) fin-ray elastoidin (ceratotri-

chia)f) lepido- and actinotrichia (of

fins)g) teleost scales (cycloid and

ctenoid)h) scutes of armored cat fishes,

sticklebacks, sea horses, pipefishes, etc.

C. Structured Mesodermal Derivatives(Sclerifications): In this group there is no

visible evidence of a structured epidermalcontribution to the integumental skeletalstructure. The hypothesis that the epider-mis does indeed play a role in the formationof these tissues has been previously dis-cussed (Moss, 19686) and derives impor-tantly from the conjunction of the work ofHay (1964) and of Jarvik (1959). The par-tial listing includes dermal fibers, calcifiedtendon, calcified "plates" (Bufo), "interme-diate" skeletal tissues (branchial arch offish), antlers, dermal bones in fishes, am-phibia, reptiles, and mammalia.

Finally, I wish to consider the dermalsclerifications found in Reptilia. A com-pletely uncalcified yet somewhat structuredarra)r of dermal collagenous fibers repre-

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INTEGUMENTAL SKELETON 33

sents, in a sense, a primordial type of der-mal sclerification. Above I stated that thereis some reason to believe that dense dermalfiber bundles did precede dermal bone phy-logenetically; the more significant point isthat such a three-dimensional structuralfibrous network seems to have anticipatedthe structure of fibrillar phase of dermalbone tissues, at least in some forms, par-ticularly reptiles (Moss, 19696).

Reptilian bone tissue histology has re-cently been reviewed by Enlow (1969)without a detailed study of dermal bone(see Moss, 1969a). Reptilian dermal scle-rifications exhibit quite a variety of histo-logical types, and they may be compoundin nature. When bone tissue is formed, itmay be produced in at least three ways:periosteal osteogenesis, tendonous ossifica-tion, and metaplasis of secondary cartilage.These dermal skeletal structures are poorlyvascularized and remodeled but little.We would observe no strong associationbetween the structure or type of dermalsclerification and the taxonomic position ofthe species. Further, no evolutionary trendsin their structure are apparent. Yet, takenas a whole, the comparative study of histo-logical composition of reptilian dermis per-mits us to view virtually the entire rangeof expressivity of the vertebrate dermalskeleton. It only remains to note that thevertebrate dermis apparently retains theability to produce, not only sclerifications,but specifically, ossifications in normal on-togenetics as well as pathological circum-stances by seeming parallel developmentalprocesses. For students of calcified tissues,no less than for workers in many cognatefields, the dermis will continue to providean exciting and rewarding locale for furtherinvestigation.

REFERENCES

Andrew, W. 1959. TcxLbook of comparative histolo-gy. Oxford Univ. Press, New York.

Ballard, W. W. 1964. Comparative anatomy andembryology. The Ronald Press, New York.

Bentley, J. P. 1970. The biological role of groundsubstance. Advan. Biol. Skin 10:108-121.

Bolk, L., E. Goppert, E. Kallius, and W. Lubosch.

1931. Handbuch der vergleichenden Anatomie derWirbeltiere. Urban and Schwarzenberg, Ber-lin.

Briggaman, R. A., and C. E. Wheeler. 1971. Epider-mal-dermal interactions in adult skin. II. Thenature of the dermal influence. J. Invest. Derma-tol. 56:18-26.

Elden, H. R. 1970. Biophysical properties of agingskin. Advan. Biol. Skin 10:231-252.

Enlow, D. H. 1969. The bone of reptiles, p. 45-80.In C. Gans, A. d'A. Bellairs, and T. S. Parsons[ed.], Biology of the reptilia. Vol. 1. AcademicPress, New York.

Fleischrnajer, R., and R. E. Billingham. 1968. Epi-thelial-mesenchymal interactions. Williams andWilkins Co., Baltimore.

Fusaro, R. M., and J. A. Johnson. 1970. Thedermal glucose compartment. Advan. Biol. Skin10:269-278.

Grossman, R. C, and B. F. Hattis. 1967. Oralmucosal sensory innervation and sensory experi-ence, p. 5-62. In J. F. Bosnia [ed.], S\mposiumon oral sensation and perception. C. C. Thomas,Springfield.

Hay, E. 1964. Secretion of a connective tissue pro-tein by developing epidermis, p. 97-116. In W.Montagna and W. Lobitz, Jr. [ed.], The epider-mis. Academic Press, New York.

Horstmann, E. 1957. Die Haut, p. 1-276. In W.Mollendorf [ed.], Handbuch der Mikroskop-ischen des Menchen. Vol. 3. Springer-Vcrlag, Ber-lin.

Jackson, D. S. 1970. Biological function of collagenin the dermis. Advan. Biol. Skin 10:39-48.

Jarvik, E. 1959. Dermal fin-rays and Holmgren'sprinciple of delamination. Kgl. Svenska Veten-skapsakad. Handl. 6:3-49.

Mathews, M. B. 1967. Macromolecular evolution ofconnective tissue. Biol. Rev. 42:499-551.

Millington, P. F., T. Gibson, J. H. Evans, and J. C.Barbenel. 1971. Structural and mechanical aspectsof connective tissue, p. 189-248. In R. M.Keredi [ed.], Advances in biomedical engineer-ing 1. Academic Press, New York.

Montagna, W. 1962. The structure and function ofskin. 2nd ed. Academic Press, New York.

Montagna, W. (Ed.) . 1960-1965. Advances in biol-ogy of skin. Vol. 1. Cutaneous innervation. Vol.2. Blood vessels and circulation. Vol. 3. Eccrinesweat glands and eccrine sweating. Vol. 4. Thesebaceous glands. Vol. 5. Wound healing. Vol. 6.Aging. Pergamon Press, Oxford.

Montagna, W., J. P. Bentley, and R. L. Dobson(Ed.). 1970. Advances in biology of skin. Vol. 10.The dermis. Appleton-Century-Crofts, New York.

Moss, M. L. 1954. Demonstration of the in-trinsic vascular pattern of compact bone. Amer.J. Phys. Anthropol. 12:373-383.

Moss, M. L. 1964. The phylogeny of mineralizedtissues. Int. Rev. Gen. Exp. Zool. 1:297-313.

Moss, M. L. 1968a. The origin of vertebrate cal-cified tissues. Nobel Symp. 4:359-371.

Dow

nloaded from https://academ

ic.oup.com/icb/article-abstract/12/1/27/2107461 by guest on 05 April 2020

34 MELVIN L. MOSS

Moss, M. L. 1968b. Comparative anatomy of verte-brate dermal bone and teeth. 1. The epidermalco-participation hypothesis. Acta Anat. 71:178-208.

Moss, M. L. 1969a. Phylogeny and comparativeanatomy of oral ectodermal-ectomesenchymal in-ductive interactions. J. Dent. Res. 48:732-737.

Moss, M. L. 19696. Comparative histology of der-mal sclerification in reptiles. Acta Anat.73:510-533.

Moss, M. L. 1970. Enamel and bone in shark teeth.Acta Anat. 77:161-187.

Orvig, T. 1967. Phylogeny of tooth tissues: evolu-tion of some clacified tissues in early vertebrates,p. 45-110. In A. E. W. Miles [ed.], Structuraland chemical organizations of teeth. AcademicPress, New York.

Partridge, S. M. 1970. Biological role of cutaneouselastin. Advan. Biol. Skin 10:69-88.

Pearce, R. H., and B. J. Grimmer. 1970. The valueof ground substance. Advan. Biol. Skin 10:89-101.

Pinkus, F. 1927. Die normale Anatomie der

Haul, p. 1-378. In B. Bloch, F. Pinkus, and W.Spatleholz [ed.], Handbuch der Haut undGeschlechtskrankheitcn. Vol. 1. Springer-Verlag,Berlin.

Ramachandran, G. N. and B. S. Gould (Ed.) . 1967.Treatise on collagen. Academic Press, NewYork.

Schubert, M., and D. Hamermann. 1968. A pri-mer on connective tissue biochemistry. Lea andFebiger, Philadelphia.

Sinclair, D. 1967. Cutaneous sensation. Oxford Uni-versity Press, London.

Spearman, R. I. C. 1964. The evolution of mam-malian keratinized structures. Symp. Zool. Soc.London 12:67-81.

Spearman, R. I. C. 1966. The keratinization ofepidermal scales, feathers and hairs. Biol. Rev.(Cambridge) 41:59-96.

Szirmai, J. A. 1970. The organization of the dermis.Advan. Biol. Skin 10:1-18.

Waterman, A. J. et al. 1970. Chordate structureand function. MacMillan Co., New York.

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ic.oup.com/icb/article-abstract/12/1/27/2107461 by guest on 05 April 2020