Development 103 Supplement, 3-15 (1988)Printed in Great Britain © The Company of Biologists Limited 1988

Craniofacial growth, evolutionary questions

CARL GANS

Department of Biology, The University of Michigan, Ann Arbor, Michigan 48109-1048, USA

Contents

IntroductionTheory

PrinciplesTasks of the craniofacial systemThe process of changePredictions from the record

Functional stages in the vertebrate headThe system in the prevertebratesTransition to vertebrates

Transition to gnathostomesDiversity offish headsFish jawsMetamorphosisTransition to terrestrial tetrapodyAvian adaptationsThe mammalian condition

Concluding discussion

Key words: functional morphology, cephalization, cranialkinesis, craniofacial evolution, adaptation.

Introduction

Understanding the growth of craniofacial systems inmammals, particularly in man, has always posedproblems. Such craniofacial systems are formed onto-genetically of multiple tissue types, and the contri-butions of these tissues do not obviously match thedivisions of adult skeletal elements (see Thorogood,this volume). Even the kind and number of segmentsin the head region continue to attract attention(Maderson, 1987). Furthermore, craniofacial systemsappear to show trends toward an unusual number ofdevelopmental abnormalities or teratologies. Manyof these teratologies suggest that we are not lookingat a simple coordinated whole (Salinas, 1982; Shprint-zen, 1982); rather, it seems as if multiple cranial andfacial components incur differential growth eithersymmetrically or asymmetrically.

It seems instructive to treat the basis of this curiousarray of complications from an evolutionary view-point, considering two aspects, adaptation and his-tory. Adaptation implies that the structures of organ-isms are not randomly assembled, but have been andremain at any moment under the influence of selec-tion (Gans, 1988). Implicit within this concept ofadaptation is that each phenotypic array must incurboth a cost and a benefit, the cost in terms ofgenerating and of maintaining the phenotype, thebenefit in terms of the roles in which the phenotype is

involved. In contrast, the concept of history docu-ments that adaptation does not act de novo togenerate phenotypes out of infinitely plastic rawmaterial. As the phenotypes of extant organismsderive from those of ancestral ones, the phenotypicmatch to new environments reflects the genetic anddevelopmental plasticity of possible precursororganisms.

This evolutionary viewpoint is here utilized in abrief review. It begins with the primary roles of thestructures in fishes that are homologous to the cranio-facial system of mammals. (Role is here considered tobe that part of the function of a phenotypic aspectthat contributes evolutionary benefit, i.e. for thoseorganisms that have it, the role of a structure is itsadaptive function in a particular environment.) In theprocess, I attempt to clarify some aspects about theway the fossil and surviving members of early ver-tebrate groups should be considered.

This evolutionary analysis is based upon pastscenario generation and is obviously reconstructive.There being but a limited fossil record, the gaps arefilled by extrapolations based upon the structure,physiology and ecology of animals living today (Gans,1985). After developing the roles of the system infishes, I shall review the several changes of role fromfishes to mammals. Throughout, I emphasize thecomponents of the head, the separate changes eachhas undergone and the aspects that keep them associ-

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ated. It is hoped that such a data set will provide aframework setting the stage for interpretation of themore developmental aspects.

Theory

Principles

The craniofacial system of mammals is supported by askeletal array consisting of a braincase, sensorycapsules and an 'upper jaw' generally fused into asingle unit, a single lower jaw composed of bilateralmandibular units more or less tightly attached to thatof the opposite side and a varied set of skeletalelements in the throat (Fig. 1). Just posterior to thejaw joint lies the auditory meatus leading to themiddle ear, incorporating several reduced skeletalelements once involved with the jaw suspension (Vande Water et al. 1980).

The historical view will document that the mam-malian craniofacial system derives from severalinitially independent components which probablyaccount for the extent and nature of the observedteratologies. Each of them continues to incur andrespond to independent demands of the environ-ment. It is unlikely that the demands occurred inparallel or were equivalent. Hence, the assembly willreflect different initial (and subsequent) roles, andshifts incurred in their component materials andproportions that are coordinated neither phylogeneti-cally nor ontogenetically.

Tasks of the craniofacial systemThe craniofacial system of mammals is homologous

to parts of the anterior end of the earliest vertebrates.As such, it provided the stiffening and reinforcementof this end, precluding deformation during pen-etration of liquid or solid aspects of the environment.Next, it encapsulated the central nervous system,protecting it both from anteriorly and posteriorlydirected forces. The system also permitted the an-terior end to bear paired, external sensory organs,protecting them and permitting them accurately toscan the anterior environment by maintaining theirposition relative to the axis of the trunk. The com-ponents performing most of the roles thus far listedpresumably were homologous to the mammaliancranial component.

The anterior end of vertebrates retains the front ofthe alimentary canal and the external openings of thegas exchange system. The craniofacial system conse-quently must maintain its patency during the acqui-sition and ingestion of nutrients and respiratoryfluids. Whereas these tasks are the major ones inmammals, earlier vertebrates incorporated extensiveportions of the anterior pharyngeal tube in the

Fig. 1. Three sketches of a cat skull each with one majorfunctional system emphasized by shading. (A) Sensorysystem; (B) braincase; (C) mandibular apparatus.

Craniofacial growth, evolutionary questions 5

cephalic structures, and all of these, as well, wereassociated with the tasks of food handling and gasextraction. This is a second set of roles for thestructures contributing to what later became knownas the facial component.

The process of changeThe mechanism of evolutionary change, the in-

vasions of adaptive niches and radiation into these,are fundamental to understanding evolutionary pro-cesses. As in all our attempts to trace history, theRecent animals we see are but remnants of pasthistorical processes. The meaning of this idea ofremnant is important because it establishes the kindsof biological conclusions permitted on the basis ofsurviving members of a group.

We must begin with a population or populations oforganisms characterized by a set of phenotypes allow-ing them to make a living in the niches they thenoccupy. For various reasons, a substantial fraction ofthe population will have phenotypes that exceed theminimal level characterized as necessary (Gans,1979). This lets them be opportunistic, to 'test' theedges of the environmental niche they occupy andsometimes to discover new sites located in rangesperipheral to their ancestral ones.

The earliest invaders of a 'new' niche may be lesseffective at exploiting its resources than will sub-sequent forms. Adequacy rather than perfection isdemanded. The new habitat imposes new selectivefactors and may lead to 'improved' genotypes.

If the resources of the new habitat are living ones,they will in turn incur advantages for defence mech-anisms or other aspects that make the task of thepredator more difficult. From this viewpoint, the RedQueen metaphor, of running as fast as possible just tostay in one place, is a most appealing description(Van Valen, 1973).

Predictions from the recordConsideration in this fashion of the rate and

direction of a particular evolutionary change wouldseem to make prediction of future directions justabout impossible (Tatarinov, 1985). After all, thedirection of evolution will be affected by the geneticand developmental capacity of the species. It will beinfluenced by the way that the developmental pro-gram forms its phenotype and by the kind of variationthat this permits or incorporates. Next, it will beinfluenced by the capacity of its genotype to mutateand by the phenotypes likely to be generated by suchmutations and their various recombinations. Finally,there is change of the environment against which thisplay proceeds. As the predator evolves, so does itsprey. Other competing predators will also incursimilar processes. Hence, prediction about the direc-

tions of evolutionary change requires informationabout the genetics of their developmental mechan-isms. There are too many unknowns, making thesystem too complex for facile analysis.

However, it is possible to predict the kinds ofgenetic and hence phenotypic changes that would belikely in such a framework. It is probable that therewill be a relatively large number of what might beconsidered to be variations on a theme; thus, manydifferent phenotypes will be produced by relativelysmall changes in their various components. Thiswould be impossible if the shape and growth rate ofindividual structural elements, for instance of theskeleton, were to be determined on what might becalled a one character/one gene basis. However, weknow that changes are interactive and coevolved sothat modification of individual components is stilllikely to generate viable phenotypes after a numberof minor genetic changes.

There remains the potential for more substantialphenotypic changes, resulting from mutations whichare minor with respect to gene alteration, but majorin their effect on the phenotype. Such early minorchanges in the sequence forming a particular charac-teristic (Gans, 1987), will affect more of the develop-mental pathway and, by implication, more pathways.However, in stochastic terms, viable changes of thismagnitude are likely to be less frequent; the greaterthe change the less the potential that the resultingphenotype will be viable and reproductively success-ful.

Now, what has all this to do with fish heads,whether pertaining to fishes surviving now or to thoseseen in the fossil record? First of all, it explains theseemingly random experimentation often encoun-tered early in the fossil record of a particular radi-ation (i.e. explosive radiation). See, for instance,Halstead's observations on the dermal armour offossil agnathans, which led him to conclude that allpossible variants of integumentary structure seemedto have arisen roughly simultaneously (Halstead,1987). What likely arose initially was the capacity ofthe integument to ossify, to sequester calcium de-posits, and to modify these. Many of the observedvariants then may be considered as experimentationsaround a theme, with the earliest among such variantsbeing indeterminable, unless pointed to by otherevidence. As long as the variants formed met theminimal demands of the animal, the detail of ossifica-tion pattern each displayed may be less critical to thesurvival of the individual.

The pattern of change may also generate a differenteffect, further likely to confuse interpretation basedupon surviving members of a group and making anyfossil more useful. The potential confusion is due tothe decreasing probability that the survivors of any

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very old radiation will mirror the dominant biologicalpattern of the line at the time that they derived fromit, eons ago. Beyond the expected phenomenon thatthe passage of time since the radiation separatedwould lead to a gradual accumulation of changes, wesee the increasing probability that the originallymajor niches belonging to the radiation have becomefragmented and occupied by competitors pertainingto quite distinct groups. In turn, the surviving speciesare likely to be highly specialized and to occupyperipheral, perhaps restricted, niches in which theyhave become further modified. This is the likelyexplanation for the agnathan condition, as bothsurviving lines differ markedly in major character-istics, such as their egg type (Hardisty, 1979; Mallatt,1985), pituitary (Gorbman & Tamarin, 1985), gillfunction (Mallatt, 1981; Mallatt & Paulsen, 1986),circulation (Lewis & Potter, 1982; Wells et al. 1986)and kidney function (Riegel, 1986). Certainly, neitherhagfish nor lampreys obviously represent an offshootof the ostracoderm pattern; in some way this patternis better modelled by present gnathostomes(Hardisty, 1979; Stensio, 1968; Yalden, 1985).

Functional stages in the vertebrate head

The system in the prevertebratesPrevertebrates were presumably similar to amphi-oxus (or some tunicate larvae) in that they had anaxial skeletal element, likely providing stiffness forsculling and burrowing (Gans, 1987). Initially, thesupportive apparatus involved a notochord and as-sociated fluid-filled spaces which provided hydrostaticeffects due to the tensile components in their epitheli-oid walls. Ventral to these stiffened axes were sup-ports for a pharyngeal basket, the skeleton of which isformed of collagenous rods, enhanced with a stiffen-ing coating. The pharynx permits extraction from thewater of finely particulate food by a kind of filtration.The flow is first divided into a multiplicity of streams.These streams turn, causing particles entrained in thewater to impinge onto a mesh of cilia-driven mucusbands which then transport them through the gut.

It must be stressed that amphioxus shows minimalcephalization and that its anterior sense organs areunpaired and mainly positioned within the nervecord. It is likely that an ancestral animal modelledupon such a body plan would not have required askeletal apparatus with any significant role in protect-ing an anterior nervous system or associated senseorgans. Also, amphioxus lacks particular specializ-ation for ingestion of large food particles, much lessfor pursuit of mobile food objects. Presumably theearliest ancestors were similar (Barrington, 1965;Berrill, 1950; Romer, 1972; Young, 1981).

Transition to vertebratesThe transition to vertebrates is signalled in the fossilrecord by the appearance of bone, representingskeletal elements formed of hydroxyapatite, ratherthan calcite. However, the origin of bone likelyfollowed the origin of cartilage (but rarely preservedin the fossil record) which formed a supportive tissuenew to vertebrates (Northcutt & Gans, 1983). Theutilization of the pharynx for gas exchange wasassociated with a shift from cilia to muscles forventilatory pumping and the development of carti-lage, perhaps as a 'new' structural material. Theinvestment 'with cartilage' of an initially collagenousframework of the pharyngeal skeleton allowed bettermodelling for support of more convoluted gasexchange surfaces, as well as of elastic recoil. Thelatter permitted a unidirectional power stroke topump water with a two-phase contraction-expansionpharyngeal movement.

The muscularized pharynx was then associatedwith an increase in the anteriorly placed motorportion of the central nervous system, a shift thatstressed the somatic rather than the visceral motorportion. Perhaps coincidentally we see a shift from astochastically sampling pattern of filter feeding to onein which larger living particles are detected andingested. The prey-detecting arrays involved distancereceptors, namely paired external sense organs, notknown in any hemichordates or protochordates(Bone, 1959,1960). It has been argued elsewhere thatelectroreception was likely the first distance sensorymode and that the detecting system may have playeda role in the acquisition of hydroxyapatite as askeletal material in the integument (Northcutt &Gans, 1983). In association with the modified phar-ynx, we see the first extranotochordal skeletal appar-atus, reflecting anterior outgrowth and later calcifi-cation of the intermediate connective tissues, bothlikely to have been formed from neural crest ma-terials (Gans & Northcutt, 1983; Le Douarin, 1982).Calcified head cartilages, known only from sharksamong recent fishes, occurred in heterostracan fishes(Denison, 1967) and in some fossil lampreys (Bardack& Zangerl, 1972), and perichondral bone in ostraco-derms (Moy-Thomas & Miles, 1971).

This stage then led to a modification of the anteriorend of the animal. The increase of the motor portionof the anterior CNS was followed by amplification ofthe sensory component. The resultant addition oftissues, reflecting both of these events generated thebasis for the anterior enlargement and forward exten-sion of the primary nerve cord. This enlargementgenerated the anteriorly prolonged nervous system,in short a primary brain. With this we see themodification of the initial armour, which shifts fromsupport of mainly the dermis to an inward extension

Craniofaclal growth, evolutionary questions

of calcification along the connective tissue planes ofthe head that outlined the sensory capsules andbraincase. We may consider this stage to reflect theorigin of the cranial component of what will becomethe craniofacial system. Much of the facial com-ponent derives from the pharyngeal system, whichhere supports the roles of gas exchange and feeding;it remained loosely suspended ventral to the anteriortip of the axial skeleton.

As the several components developed skeletalsupports, their association posed problems duringgrowth (Fig. 2). Bone grows by apposition and evenfibrous and calcified cartilages cannot truly increase insize by interstitial growth. Hence, fusion of com-ponents could only occur after allometric growth hadbeen completed.

Transition to gnathostomesThe next stage involved the modification of some ofthe anterior arches of the segmented pharyngealskeleton into a kind of loose jaws, in short anapparatus in which the dorsal and ventral portionscould be folded and exert pressure one upon theother. This development of jaws would have facili-tated the catching and break-up of food objects andtheir ingestion into the pharynx and the oesophagus.Presumably, sclerification of the jaws was adaptive,as it added strength and capacity to cut prey moreeffectively. Also, the increased potential for handlingand ingestion of larger prey increased the existingadvantage for detection of distant prey. This appearsto have provided the basis for development of newsense organs - eyes, noses, ears - paired, externaldistance receptors. They likely triangulated the pos-ition of prey, acting synergistically and requiring fixedsites.

Although the anterior portion acquired a new rolein feeding, the more posterior portions of the pharyn-geal skeleton still supported the gas exchange sur-faces. All in all, we see at least four, actuallyconflicting roles in the head during the agnathan-early gnathostome transition, namely, the demandfor encapsulation of the enlarged brain, the require-ment for protection and positioning of enlarged andanteriorly placed sense organs, the demand for sup-port of the gill basket and the demand for theplacement and support of jaws.

The gnathostome pattern was associated with theposterior extension of the skull past the otic capsules.This postotic portion allowed anchoring of the phar-yngo-branchial skeleton to the braincase, althoughmost early gnathostomes displayed ligamentous con-nections rather than extensive fusion of the jaw andpalatal elements (Moy-Thomas & "Miles, 1971). Evenmore far reaching is the development of an articu-

(A)

11111111111111 ( be d

d2 c2 a b c, d,

(B)

Fig. 2. Sketches to show the kinds of association that canoccur among appositionally growing skeletal elements.The small arrows show direction of growth and only onelinear dimension is shown. (A) Two adjacent skeletalelements grow equivalently; the three potential resultsreflect growth on different surfaces and retention or shiftof the relative position of the initial elements. In 1, bothgrow in parallel permitting points on the originalelements and the newly grown positions to remain inrelative contact. In 2 and 3, growth occurs at oppositeends. In 2, the geometry changes markedly, whereas in 3the elements slide past each other precluding fusionduring growth. (B) Equivalent sketches for allometricgrowth in which the two elements grow at different rates.

lated vertebral column leading to the gradual (oftenontogenetic) reduction of the notochord.

Diversity of fish heads

Is it indeed possible to make generalizations aboutthe overall pattern of gnathostome head organizationseen in fishes? The adults of both fossil and Recentfishes (a useful term likely to grate the sensibilities ofthe cladistically inclined) disclose an enormous diver-sity in cranial structure (Jarvik, 1980; Jollie, 1962).Interestingly enough, there are certain environmental

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(B)

Integument

Dermal armour

Closed braincase

Open braincase

Muscle

Bony brain case(closed)

Muscle x-sec.

Pharynx

Mandible

Fig. 3. Sections through schematized vertebrate skulls to show the sites of bone formation. (A) In simple fish skulls,there is a dermal armour, the medial surface of which provides attachment sites for the jaw adductor muscles. Thebraincase retains membranous fenestrations. (B) In many tetrapods, we see the results of inward migration of dermalelements and formation of a closed braincase with the mandibular adductor muscles lying external to this.

constraints that affect fishes in general, and a remark-able number of the specializations we see in the fishhead reflects these.

One sees two variably expressed concentric levelsof cephalic enclosure (Fig. 3). The first is an externaldermal armour composed of variously fused andsculptured plates; the second is the internal brain-case. The relative positions of the two systems aremaintained by radial skeletal braces within the softintermediate tissues. Generally the cephalic shieldsare larger than those on the trunk, perhaps due tofusion or to accretion (Halstead, 1987). Ventral tothese is an astounding range of diversifications of thepharyngeal skeleton, which may or may not be linkedto the central skeletal axis.

The external cephalic skeleton presumably aroseinitially in association with the developing sensorysystem (Schaeffer, 1977; 0rvig, 1972; Northcutt &Gans, 1983); however, physical protection, calciumstorage and similar roles were most likely involved inits maintenance (Romer, 1933). The presence of anexternal armour also involves issues of scaling(Schmidt-Nielsen, 1984) and energetic cost. The shiftto undulant muscular propulsion provided verte-brates with the means for rapid movement; coinci-dentally, it increased potential for larger body size inagnathans and even more in gnathostomes (thus theplacoderms include some spectacularly large fishes).

Both of these factors also made it advantageous tostrengthen the integument against damage upon con-tact with other objects. However, the cost of acceler-ating an external calcified mass is substantial (particu-larly in aquatic locomotion: Webb, 1978; Webb &Weihs, 1986); this has led to reduction of externalossification in each vertebrate group that developed it(Olson, 1971; Richmond, 1964; Romer, 1966). Asecond energetic consideration is the acidification ofthe extracellular fluids coincident with increasedmetabolism during exercise. Ruben & Bennett (1980,1981) have shown that this leads to dissolution ofskeletal armour and may provide the explanations forsuch phenomena as acellular bone, and sequestrationof scales (from the circulation) seen in some fishes.

Fish jaws

Support of the gas exchange and feeding functionsseems initially to have involved skeletal elementsassociated with the integument and the pharyngealbasket. However, as the anterior pharyngeal archesbecame modified into articulated jaws (and theirsupports) that allowed larger prey items to be trappedand partitioned, the forces that could be applied tothe prey (and by struggling prey to the predator)became substantial. This led to the need for improvedmechanisms for transmitting such forces (1) betweenthe mandible and the upper jaw, (2) between the jaws

Craniofacial growth, evolutionary questions 9

and the units encapsulating the brain and senseorgans (neurocranium), and (3) (via a head joint)between the anterior head skeleton and the moreposterior axial one.

The initial development of jaws in an aquaticenvironment could not have occurred independent ofancillary behavioural and physiological patterns, be-cause the biting they made possible involved morethan the mere act of closure of any oral opening. Asthe opening closes, it displaces water, some of whichflows out of the mouth and exerts flow pressure ontoobjects against which fish bite. If these objects weresmall they would be deflected during the bite. (Aspoon is a poor tool for catching fishes in an aquar-ium.) Additionally, the water displaced by the headof a moving fish would produce similar effects.Perhaps the system originated initially by slowlybringing the mouth into contact with attached prey orforcing it against a fixed site and then closing theincipient jaws. This is similar to the prey attack usedby members of both lines of Recent agnathans whichforce their buccal region into contact with potentialprey (and is the method predicted for the evolution ofprey engulfment by fossil agnathans, Northcutt &Gans, 1983).

However, biting at floating prey or biting while thefish was swimming could only have occurred aftersubstantial advances in the sensory and motor coordi-nation pattern, and utilization of the intrinsic pharyn-geal mobility. Not only must the fish be steered to theprey, which is moving in three-dimensional space, butthe moving fish must compensate for the effect of itspressure wave which will tend to displace smallfloating objects. The opening mouth will furthermorechange the streamline pattern. These constraintshave been overcome in a variety of ways. The mostobvious is the displacement of the jaws out of thestreamlined shape of the predator. The second is thedistension of the posterior pharynx during the bite.This generates suction which interferes temporarilywith the pressure wave in front of the head and pullsthe prey into the mouth. Furthermore, the posteriorpharynx of many fishes often sees the development ofa secondary food grinding mill that is mounted on thebranchial skeleton, although it may rasp the foodagainst the base of the braincase. The first pattern isseen in sharks, as witnessed by the protrusion of thepalatoquadrate and Meckel's cartilage; it is also seen,although differently, in some abyssal fishes (Tcherna-vin, 1953). The second pattern initially utilizing thepharyngeal gill-ventilating mechanism is common toteleosts, indeed to most aquatic vertebrates (Lauder,1983, 1985). It is not only used for the initial preycapture, but also for the manipulation of the food.The details of these patterns are not important in thepresent context. The critical thing is that in both cases

the constraints of feeding in water establish anadvantage for the retention of a loose and flexibleconnection between the elements of the jaws andother components of the pharyngeal skeleton and themore dorsal elements including both the sensorycapsules and the braincase.

Most of these specializations involve chondrich-thians and actinopterygians. From a human perspec-tive, they occur in side branches of the vertebratesequence and their mechanical states are not reallypertinent to the biting mechanisms of tetrapods(Liem, 1978). The lever systems, the packing of themuscles and the intrinsic elasticity of the system(often constrained by linkage to an external armour),all differ profoundly from the simpler rhipidistianamphibian (McCosker & Lagios, 1979) and dipnoanpatterns (Bemis et al. 1987). Even in teleosts thathave a short powerful bite, such as parrot-fishes, thelinkages remain complex. The reptilian condition,referred to as cranial kinesis, may be seen as aderivative of this continuing separation of the pharyn-geal apparatus from the braincase. With this, themammalian condition, in which the upper jaw andpalate are tightly associated with the braincase,becomes a late specialization in the pattern of cranio-facial evolution.

MetamorphosisThe preceding account has dealt entirely with adultconditions. However, juvenile fishes are more thanminiature adults. Small size allows early larvae to usehydrostatic skeletons (Gutmann & Bonik, 1981);rigid skeletons involving ossification and chondrifica-tions only form later. They are often redesigned to adifferent Bauplan at metamorphosis.

As the food utilized by an animal almost alwayschanges at metamorphosis (this being a major reasonfor incorporating metamorphosis in the life cycle, Justet al. 1981) so will the feeding mechanism, in this casethe jaws. Hence the developmental rates of thejaw-pharyngeal system then change. Also, the sen-sory pattern changes at the time of metamorphosis;new sense organs then come into play (Kennedy &Rubinson, 1984; Rubinson et al. 1977) and old onesare remodelled (de Jongh, 1967). However, remodel-ling of the brain is limited as particular motorneurones then shift function and control the newmuscles (Barnes & Alley, 1983).

Consequently, the growth rates of brain case,sensory capsules, gill apparatus and jaws will differboth before and after metamorphosis. The functionalbases underlying their allometric growth rates areclearly distinct. Also, there need be no obvious linksamong the changing functional influences affectingthese structures. Hence, heterochronies will beunpredictable. Fusion of the cranial and (future)

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facial components of the skull can only occur aftergrowth has ceased and the relative position of adjac-ent parts will no longer change.

Reptiles differ from fishes and amphibians by notdisplaying metamorphosis, so that they maintain asingle cranial configuration after hatching or birth.Only allometric, but no absolute, changes occurduring growth. The mechanical designs involvedoften are scaled up in size between one and threeorders of magnitude. It is interesting that the greatestrange of skull sizes is shown by animals (turtles andcrocodilians) that show secondary palates and non-kinetic skulls.

Transition to terrestrial tetrapodyThe first stage toward a future invasion of the landpresumably occurred in rhipidistian fishes with theshift to aspiration breathing (Gans, 1970). This re-structuring of the gas exchangers permitted changesof integument and kidneys that protoadapted theanimals for terrestrial life. Also, constraints on theshape of the buccal cavity associated with pulsepumping of air disappeared and the posterior pharyn-geal skeleton no longer had to support gills (Hughes,1984). With this change, the ingestion system was nolonger constrained by the need for a major adaptivecompromise (Gans, 1974), and the stage was set forthe development of new techniques of prey manipu-lation, such as inertial feeding.

With the transition from water to land, movements(of head and jaws) no longer had to act against theresisting effects of a dense medium; also, suctionfeeding using air was ineffective. The transition alsoremoved the benefits of buoyancy and requiredmuscular effort for support and resisting the effects ofgravity, which was reflected in the modification of thelocomotor pattern and in the ventilation-movementconflict seen in Recent ectotherms (Carrier, 1987). Agiven muscular effort now would accelerate parts ofthe skeleton to higher velocities (i.e. lead to poten-tially greater sudden reaction forces on the skeleton).All of these aspects led to tighter articulations amongits skeletal elements (autostyly). Certainly the brain-case became better defined and composed of morecentral elements, often modelling the outline of theCNS. The array of externally placed, articulateddermal bones either migrated inward or was replacedfunctionally by central ossifications. In a number ofgroups, the external protective cover shows degreesof fenestration, permitting attachment of the increas-ingly large adductor muscles, that could swell duringcontraction without pressing against the brain prior tothe development of an internal braincase (Fox, 1964;Frazetta, 1968; Romer, 1966).

Whereas various fishes could already lift the snoutabove the axis of the vertebral column (Romer,

1966), fusion of the braincase was soon followed bydevelopment of a true head joint on the level of theanteriormost vertebrae. More important is the separ-ation of the head and pectoral girdle; with develop-ment of cervical flexibility, the head, rather than theentire trunk, could now address the prey.

With terrestriality there is a tighter association ofthe axial skeleton with the upper jaw, comprisingpalatomaxillary and other branchial derivatives. Mul-tiple support schemes occur, classified by the numberand sites of the connections between pharynx andbraincase. However, in most reptiles the junction ofthe elements of the upper jaw to the sensory capsulesand brain case remains loose. This so-called kinesiswas first noted by Versluys (1912) some 75 years ago.Unfortunately, the exact roles of the multiple kinds ofkinesis are still poorly understood, as the majority ofmodels derive from extrapolations from dried skullsrather than observations and measurements on livingorganisms.

The issue is complicated by organismic diversity;thus kinesis differs among species of reptiles and birds(Fig. 4). The more anterior brain case may shiftvertically relative to the back of the lepidosaurianskull; more anterior portions of the nasal capsulesand snout may rotate further about distinct transverseaxes. The maxilla, premaxilla, ectopterygoid, pala-tines and pterygoids may be lifted, rotated,depressed, protruded and retruded. The dorsal as-pect of the quadrate may articulate and shift aboutthe supratemporal (tabular of some authors) ordirectly about the surface of the braincase. Theventral aspect of the quadrate may or may not beanchored by attachment to the pterygoid and/or jugalarch. In the latter case, the quadrate, the lower end ofwhich supports the mandible in all nonmammalianvertebrates, may be protruded, thus shifting themandibular articulation. This occurs most spectacu-larly in certain snakes (Cundall & Gans, 1979) andanalogously in some deep-sea fishes (Tchernavin,1953). One group of snakes has even subdivided itsmaxilla into anterior and posterior moieties. Theseanimals and certain geckos can thus close the front ofthe mouth, even though the posterior parts of thetooth row remain separated, locking prey in place(Cundall & Irish, 1987; de Vree & Gans, 1986).

The purported advantages of the more classicalcranial kinesis, seen in lepidosaurs, include retentionof an ontogenetic state, facilitation of the strike,expansion of the throat, widening of the gape, andshock absorption (see Bock, 1964 for one list).Recent studies (Condon, 1986; de Vree & Gans,1986, 1987; K. Smith, in preparation) suggest thatroles differ and are species-specific; in some cases,kinesis facilitates prey manipulation and in othersaids in shock absorption during crushing of hard prey.

Craniofacial growth, evolutionary questions 11

Whatever its role, kinesis assures that the growth ofthe brain case need not be constrained by functionaldemands on the facial system. (However, trogono-phid amphisbaenians, burrowing squamate reptilesthat form tunnels with their head, show a clearcompromise among the shape and position of brain,sensory capsules and jaws and the outline of thecranial periphery; Gans, 1974.)

The general capacity for interelement flexibility isprobably an ancestral (plesiomorphic) condition insquamates, although it may be expressed in differentways. Certainly some degree of such flexibility simpli-fies growth, permitting individual skeletal elements tochange proportions according to local demands.Also, we see variation of the way in which kinesis mayfacilitate shock absorption and may permit the maxil-

Fig. 4. Sketches of the light, but strong,and highly kinetic skulls of a pitviper (A)and an owl (B). In the snake, the bonyelements are connected by ligamentousarticulations. The bird skull is fused, andflexibility is obtained by allowing someslender elements to bend. Note the relativesizes of orbits as one indication of differentmodification of these animals.

lary and mandibular tooth rows to move relative toeach other. Still, it seems to be appropriate to arguethat in lepidosaurs akinesis, rather than kinesis, is thederived (and perhaps the adaptive) state (de Vree &Gans, 1988).

Avian adaptationsBirds and mammals apparently invented endothermyindependently. It is generally taught that both ofthese groups retain the reptilian absence of metamor-phosis. However, this is only partly correct as theyinvented a developmental pattern involving pro-longed parental care, that in some ways incorporatesswitches of food type, already noted as a key aspect ofmetamorphosis. In birds and mammals, the high level

12 C. Gans

of parental care may have led to complex socialsystems.

Other major avian specializations are the substan-tial increase of the volume of the sense organs andcertainly of the brain (Quiring, 1950; Jerison, 1973).Brain weight is related to metabolic rate, but therelation is far from clear (Bennett & Harvey, 1985).For example, note that three herbivores (weighingapproximately 24 g), lizard, mouse and sparrow, eachhave brain weights equivalent respectively to 0-55,2-8 and 4-4% of body weight.

This effect is even greater for the visual organs.The eye of the starling represents 15 % of the weightof the head, whereas that of an ostrich is the largest inany terrestrial vertebrate (Pumphrey, 1961). Theincrease in relative brain size was apparently coupledwith an early development of determinate neuronalarrangement. It is well known that during post-termontogeny, the size of the brain increases only afraction as much as that of the body. Birds annuallygenerate new neurones during the restructuring ofcentres involved in vocal control (Paton & Notte-boom, 1984). This phenomenon does not seem toinvolve changes of overall brain volume or of that ofthe braincase.

The constraints of development within a hard eggshell may keep the bill short and the greatest allo-metric growth takes place here (and perhaps in thelegs of waders). However, altricial (nidicolous) birdsneed not rely on a single feeding pattern, as theirbody size changes through an order of magnitude.Precocial (nidifugous) species tend to be born largerand generally show linear scaling over less than oneorder of magnitude (Quiring, 1950; Rickleffs, 1983).Also, and unlike ectotherms (but see Andrews,1982), birds and mammals show determinate growthso that developmental instructions for interelementfusion may more easily be specified at a particularsize.

The shift to birds involved a series of supplemen-tary cranial specializations presumably associatedwith the evolution of flight. Three major ones are ageneral lightening of the skull, the loss of teeth andthe use of air-filled spaces surrounded by bony strutsso that the external shape of the head may bemaintained with minimal expenditure of mass. Thereis emphasis on vision, reflected in large eyes, and aminimal olfactory system. Various species of birdsshow cranial kinesis (Bock, 1964; Zusi, 1984); how-ever, rather than movement among elements, aviankinesis involves localized bending of bones, such asthose connecting the top of the beak and the eyecapsules. Some birds even have a mandibular pseu-darthrosis, an analogue of the new jaw joint ofmammals (Bock, 1960). Substantial allometricchanges occur in the proportions of the growing skull;

whereas such changes have been documented for legsand wings; they remain to be studied for cranialdimensions (Rickleffs, 1983).

The mammalian conditionMammals are unique among vertebrates in havingonly the dentary bone in the mandible, the elementsof the old jaw joint having been incorporated into themiddle ear (Van de Water, 1980). In mammals, someachieve relative brain size values larger than those inany other vertebrates (Jerison, 1973; Bennett &Harvey, 1985). (The special conditions seen in mono-tremes and marsupials are omitted here.) The feedingspecializations have been refined by allowing den-tition and general cranial arrangement to maintain anadult feeding pattern over a linear range of only two-or three-to-one. Mammals have reinvented metamor-phosis even more completely than birds; they alwayssubdivide the life cycle, at least into a lactation(reprocessing of food by the adults) and a freelyfeeding stage.

Lactation is associated with an ability to suck andthis involved development of a bony secondary palatederiving from extension and modification of thedentigerous bones. The snout is also relatively shortduring the suckling period; this in turn involvessubstantial allometric growth for species in whichadults have an elongate snout. Development of asecondary palate presumably required relative immo-bility of the facial region; as noted above, crocodiliansand some turtles which have secondary palates arethe only Recent reptiles with rigid and reinforcedskulls. Among mammals, only the lagomorphs show acondition analogous to cranial kinesis (Bramble,1984). Lactation also required modification of theossification sequence; the dentary ossifies muchearlier than do elements of the braincase and upperjaw (Bellairs & Kamal, 1981; Pond, 1977).

Two physiological processes may markedly influ-ence the shape of various mammalian faces. The firstis the use of thermoregulation for cooling the brain;this involves use of the heat exchange capacity of thenasal passages. The second is the selection of differ-ent primary sensory modalities; thus the face of atarsier with primarily visual orientation is markedlydifferent from that of a canid with a primarilyolfactory one.

The early determination of the anterior region ofthe mandible and determinate growth have presum-ably provided the basis for the mammalian pattern ofallowing only a single replacement wave for thedentition which becomes functional only as the lac-tation period is completed. Even the milk dentition islarge and tooth size and length of tooth row areapparently determined by cues independent of thelength of the jaws. Hence, the 'wisdom tooth' prob-

Craniofacial growth, evolutionary questions 13

lem, impacting of the posterior end of the tooth rowinto the mandibular ramus, also occurs in variousdwarf races of domesticated animals (Moss-Salentijn,1978).

Previously we have referred to the increased brainsize. Mammals show a substantial further increaseover the condition disclosed by Recent reptiles.Various reasons, such as the development of parentalcare and social systems, may be involved in thisphenomenon; however, the issue of brain size andmental capacity is one best avoided here. Theincreased brain size does make for extreme allometricchange of the cranial portion of the skull. The earlydetermination of brain size furthermore assures thatbetween term and sexual maturity the cranium growsrelatively more slowly than does the mandibularsystem. Still, post-term growth leads to relatively lateclosure of cranial sutures.

Concluding discussion

The preceding summary should have documentedthat the mammalian craniofacial system is truly com-pound, deriving from at least four disjunct portions inearly vertebrates. The several parts have each passedthrough repeated functional changes in phylogeny.Furthermore, they encounter changing demands dur-ing ontogeny. History has generated the basis forallometric growth within any one species and we seeevidence of heterochrony in comparing interspecificchange. A byproduct of the requirement for allo-metric changes among adjacent elements has beenrelative flexibility among the mechanical componentsthroughout much of ontogeny.

The trend to ontogenetic fusion among the el-ements of the braincase, the formerly anterior sen-sory capsules and the dorsal elements of the pharyn-geal skeleton may then be considered as involvingrelatively late developmental events modifying theresults of processes that arose in history. Unfortu-nately, we as yet lack detailed understanding of thedevelopmental pathways in enough organisms to seewhich of the changes reflect current role and whichreflect history and at what level.

What is perhaps most interesting in evaluating thecephalic array is the amazing constancy of theportions of the developmental patterns already dis-closed for diverse vertebrates. In hindsight, it seemsas if the potential of the pattern for generatingsubstantially distinct phenotypes by minor changes ona theme may have been one reason for the ability ofthe vertebrates to radiate successfully into mostmajor environments. In this view, the vertebratehead may represent a new structure. Utilization ofneural crest tissues as a source of preotic mesenchyme

allowed modification of parts of the head withoutsimultaneous restructuring of the trunk. Usage ofpharyngeal slits as an organizational frame for pala-tal, mandibular, hyoid and posthyoid structures mayhave facilitated phenotypic shifts. Examples arechanges of jaw articulation without modification ofthe posterior gill arches or the loss of posterior gillarches without major shifts of the mandibular pat-tern.

In any case, the several craniofacial componentshave been shown to have a long independent history.It has been demonstrated that their roles oftendemanded retention and even redevelopment of amechanically loose association. These circumstancespresumably established advantages to a developmen-tal pattern in which the fate of some several cranio-facial subunits could be independently controlled,whereas that of other subunits is associated. Perhaps,comparative studies considering history and function(role) retain the promise of providing answers todevelopmental questions, answers that may well becomplementary to those furnished by the recentelegant studies about the detailed mechanisms util-ized in the development of particular forms.

Thanks are due to the organizers of this Symposium forthe invitation that permitted me to participate. I ambeholden to David Carrier, A. S. Gaunt and Paul F. A.Maderson for comments on the manuscript, and to variousfriends for references about specific situations. Preparationof the report was supported by US National ScienceFoundation grant G-BSR-850940. Miss Lucy Alejandroinked the sketches.

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