Craniofacial Growth, Evolutionary Questions

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 Transition to gnathostomes Diversity offish heads Introduction Fish jaws Theory Metamorphosis Principles Transition to terrestrial tetrapody Tasks of the craniofacial system Avian adaptations The process of change The mammalian condition Predictions from the record Concluding discussion Functional stages in the vertebrate head The system in the prevertebrates Key words: functional morphology, cephalization, cranial Transition to vertebrates kinesis, craniofacial evolution, adaptation.

Introduction involved. In contrast, the concept of history docu- ments that adaptation does not act de novo to Understanding the growth of craniofacial systems in generate phenotypes out of infinitely plastic raw mammals, particularly in man, has always posed material. As the phenotypes of extant organisms problems. Such craniofacial systems are formed onto- derive from those of ancestral ones, the phenotypic genetically of multiple tissue types, and the contri- match to new environments reflects the genetic and butions of these tissues do not obviously match the developmental plasticity of possible precursor divisions of adult skeletal elements (see Thorogood, organisms. this volume). Even the kind and number of segments This evolutionary viewpoint is here utilized in a in the head region continue to attract attention brief review. It begins with the primary roles of the (Maderson, 1987). Furthermore, craniofacial systems structures in fishestha t are homologous to the cranio- appear to show trends toward an unusual number of facial system of mammals. (Role is here considered to developmental abnormalities or teratologies. Many be that part of the function of a phenotypic aspect of these teratologies suggest that we are not looking that contributes evolutionary benefit, i.e. for those at a simple coordinated whole (Salinas, 1982; Shprint- organisms that have it, the role of a structure is its zen, 1982); rather, it seems as if multiple cranial and adaptive function in a particular environment.) In the facial components incur differential growth either process, I attempt to clarify some aspects about the symmetrically or asymmetrically. way the fossil and surviving members of early ver- It seems instructive to treat the basis of this curious tebrate groups should be considered. array of complications from an evolutionary view- This evolutionary analysis is based upon past point, considering two aspects, adaptation and his- scenario generation and is obviously reconstructive. tory. Adaptation implies that the structures of organ- There being but a limited fossil record, the gaps are isms are not randomly assembled, but have been and filled by extrapolations based upon the structure, remain at any moment under the influence of selec- physiology and ecology of animals living today (Gans, tion (Gans, 1988). Implicit within this concept of 1985). After developing the roles of the system in adaptation is that each phenotypic array must incur fishes, I shall review the several changes of role from both a cost and a benefit, the cost in terms of fishes to mammals. Throughout, I emphasize the generating and of maintaining the phenotype, the components of the head, the separate changes each benefit in terms of the roles in which the phenotype is has undergone and the aspects that keep them associ- C. Gans ated. It is hoped that such a data set will provide a framework setting the stage for interpretation of the more developmental aspects.

Theory

Principles The craniofacial system of mammals is supported by a skeletal array consisting of a braincase, sensory capsules and an 'upper jaw' generally fused into a single unit, a single lower jaw composed of bilateral mandibular units more or less tightly attached to that of the opposite side and a varied set of skeletal elements in the throat (Fig. 1). Just posterior to the jaw joint lies the auditory meatus leading to the middle ear, incorporating several reduced skeletal elements once involved with the jaw suspension (Van de Water et al. 1980). The historical view will document that the mammalian craniofacial system derives from several initially independent components which probably account for the extent and nature of the observed teratologies. Each of them continues to incur and respond to independent demands of the environment. It is unlikely that the demands occurred in parallel or were equivalent. Hence, the assembly will reflect different initial (and subsequent) roles, and shifts incurred in their component materials and proportions that are coordinated neither phylogeneti- cally nor ontogenetically.

Tasks of the craniofacial system The craniofacial system of mammals is homologous to parts of the anterior end of the earliest vertebrates. As such, it provided the stiffening and reinforcement of 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 posteriorly directed forces. The system also permitted the anterior end to bear paired, external sensory organs, protecting them and permitting them accurately to scan the anterior environment by maintaining their position relative to the axis of the trunk. The components performing most of the roles thus far listed presumably were homologous to the mammalian cranial component. The anterior end of vertebrates retains the front of the alimentary canal and the external openings of the gas exchange system. The craniofacial system consequently must maintain its patency during the acquisition and ingestion of nutrients and respiratory fluids. Whereas these tasks are the major ones in Fig. 1. Three sketches of a cat skull each with one major mammals, earlier vertebrates incorporated extensive functional system emphasized by shading. (A) Sensory portions of the anterior pharyngeal tube in the system; (B) braincase; (C) mandibular apparatus. Craniofacial growth, evolutionary questions 5 cephalic structures, and all of these, as well, were tions of evolutionary change requires information associated with the tasks of food handling and gas about the genetics of their developmental mechan- extraction. This is a second set of roles for the isms. There are too many unknowns, making the structures contributing to what later became known system too complex for facile analysis. as the facial component. However, it is possible to predict the kinds of genetic and hence phenotypic changes that would be The process of change likely in such a framework. It is probable that there The mechanism of evolutionary change, the in- will be a relatively large number of what might be vasions of adaptive niches and radiation into these, considered to be variations on a theme; thus, many are fundamental to understanding evolutionary pro- different phenotypes will be produced by relatively cesses. As in all our attempts to trace history, the small changes in their various components. This Recent animals we see are but remnants of past would be impossible if the shape and growth rate of historical processes. The meaning of this idea of individual structural elements, for instance of the remnant is important because it establishes the kinds skeleton, were to be determined on what might be of biological conclusions permitted on the basis of called a one character/one gene basis. However, we surviving members of a group. know that changes are interactive and coevolved so We must begin with a population or populations of that modification of individual components is still organisms characterized by a set of phenotypes allow- likely to generate viable phenotypes after a number ing them to make a living in the niches they then of minor genetic changes. occupy. For various reasons, a substantial fraction of There remains the potential for more substantial the population will have phenotypes that exceed the phenotypic changes, resulting from mutations which minimal level characterized as necessary (Gans, are minor with respect to gene alteration, but major 1979). This lets them be opportunistic, to 'test' the in their effect on the phenotype. Such early minor edges of the environmental niche they occupy and changes in the sequence forming a particular charac- sometimes to discover new sites located in ranges teristic (Gans, 1987), will affect more of the develop- peripheral to their ancestral ones. mental pathway and, by implication, more pathways. The earliest invaders of a 'new' niche may be less However, in stochastic terms, viable changes of this effective at exploiting its resources than will sub- magnitude are likely to be less frequent; the greater sequent forms. Adequacy rather than perfection is the change the less the potential that the resulting demanded. The new habitat imposes new selective phenotype will be viable and reproductively success- factors and may lead to 'improved' genotypes. ful. If the resources of the new habitat are living ones, Now, what has all this to do with fish heads, they will in turn incur advantages for defence mech- whether pertaining to fishes surviving now or to those anisms or other aspects that make the task of the seen in the fossil record? First of all, it explains the predator more difficult. From this viewpoint, the Red seemingly random experimentation often encoun- Queen metaphor, of running as fast as possible just to tered early in the fossil record of a particular radi- stay in one place, is a most appealing description ation (i.e. explosive radiation). See, for instance, (Van Valen, 1973). Halstead's observations on the dermal armour of fossil agnathans, which led him to conclude that all Predictions from the record possible variants of integumentary structure seemed Consideration in this fashion of the rate and to have arisen roughly simultaneously (Halstead, direction of a particular evolutionary change would 1987). What likely arose initially was the capacity of seem to make prediction of future directions just the integument to ossify, to sequester calcium de- about impossible (Tatarinov, 1985). After all, the posits, and to modify these. Many of the observed direction of evolution will be affected by the genetic variants then may be considered as experimentations and developmental capacity of the species. It will be around a theme, with the earliest among such variants influenced by the way that the developmental pro- being indeterminable, unless pointed to by other gram forms its phenotype and by the kind of variation evidence. As long as the variants formed met the that this permits or incorporates. Next, it will be minimal demands of the animal, the detail of ossifica- influenced by the capacity of its genotype to mutate tion pattern each displayed may be less critical to the and by the phenotypes likely to be generated by such survival of the individual. mutations and their various recombinations. Finally, The pattern of change may also generate a different there is change of the environment against which this effect, further likely to confuse interpretation based play proceeds. As the predator evolves, so does its upon surviving members of a group and making any prey. Other competing predators will also incur fossil more useful. The potential confusion is due to similar processes. Hence, prediction about the direc- the decreasing probability that the survivors of any C. Gans very old radiation will mirror the dominant biological Transition to vertebrates pattern of the line at the time that they derived from The transition to vertebrates is signalled in the fossil it, eons ago. Beyond the expected phenomenon that record by the appearance of bone, representing the passage of time since the radiation separated skeletal elements formed of hydroxyapatite, rather would lead to a gradual accumulation of changes, we than calcite. However, the origin of bone likely see the increasing probability that the originally followed the origin of cartilage (but rarely preserved major niches belonging to the radiation have become in the fossil record) which formed a supportive tissue fragmented and occupied by competitors pertaining new to vertebrates (Northcutt & Gans, 1983). The to quite distinct groups. In turn, the surviving species utilization of the pharynx for gas exchange was are likely to be highly specialized and to occupy associated with a shift from cilia to muscles for peripheral, perhaps restricted, niches in which they ventilatory pumping and the development of carti- have become further modified. This is the likely lage, perhaps as a 'new' structural material. The explanation for the agnathan condition, as both investment 'with cartilage' of an initially collagenous surviving lines differ markedly in major character- framework of the pharyngeal skeleton allowed better istics, such as their egg type (Hardisty, 1979; Mallatt, modelling for support of more convoluted gas 1985), pituitary (Gorbman & Tamarin, 1985), gill exchange surfaces, as well as of elastic recoil. The function (Mallatt, 1981; Mallatt & Paulsen, 1986), latter permitted a unidirectional power stroke to circulation (Lewis & Potter, 1982; Wells et al. 1986) pump water with a two-phase contraction-expansion and kidney function (Riegel, 1986). Certainly, neither pharyngeal movement. hagfish nor lampreys obviously represent an offshoot The muscularized pharynx was then associated of the ostracoderm pattern; in some way this pattern with an increase in the anteriorly placed motor is better modelled by present gnathostomes portion of the central nervous system, a shift that (Hardisty, 1979; Stensio, 1968; Yalden, 1985). stressed the somatic rather than the visceral motor portion. Perhaps coincidentally we see a shift from a stochastically sampling pattern of filter feeding to one Functional stages in the vertebrate head in which larger living particles are detected and ingested. The prey-detecting arrays involved distance The system in the prevertebrates receptors, namely paired external sense organs, not Prevertebrates were presumably similar to amphi- known in any hemichordates or protochordates oxus (or some tunicate larvae) in that they had an (Bone, 1959,1960). It has been argued elsewhere that axial skeletal element, likely providing stiffness for electroreception was likely the first distance sensory sculling and burrowing (Gans, 1987). Initially, the mode and that the detecting system may have played supportive apparatus involved a notochord and as- a role in the acquisition of hydroxyapatite as a sociated fluid-filled spaces which provided hydrostatic skeletal material in the integument (Northcutt & effects due to the tensile components in their epitheli- Gans, 1983). In association with the modified phar- oid walls. Ventral to these stiffened axes were sup- ynx, we see the first extranotochordal skeletal appar- ports for a pharyngeal basket, the skeleton of which is atus, reflecting anterior outgrowth and later calcifi- formed of collagenous rods, enhanced with a stiffen- cation of the intermediate connective tissues, both ing coating. The pharynx permits extraction from the likely to have been formed from neural crest ma- water of finely particulate food by a kind of filtration. terials (Gans & Northcutt, 1983; Le Douarin, 1982). The flow is first divided into a multiplicity of streams. Calcified head cartilages, known only from sharks These streams turn, causing particles entrained in the among recent fishes, occurred in heterostracan fishes water to impinge onto a mesh of cilia-driven mucus (Denison, 1967) and in some fossil lampreys (Bardack bands which then transport them through the gut. & Zangerl, 1972), and perichondral bone in ostraco- It must be stressed that amphioxus shows minimal derms (Moy-Thomas & Miles, 1971). cephalization and that its anterior sense organs are This stage then led to a modification of the anterior unpaired and mainly positioned within the nerve end of the animal. The increase of the motor portion cord. It is likely that an ancestral animal modelled of the anterior CNS was followed by amplification of upon such a body plan would not have required a the sensory component. The resultant addition of skeletal apparatus with any significant role in protect- tissues, reflecting both of these events generated the ing an anterior nervous system or associated sense basis for the anterior enlargement and forward exten- organs. Also, amphioxus lacks particular specializ- sion of the primary nerve cord. This enlargement ation for ingestion of large food particles, much less generated the anteriorly prolonged nervous system, for pursuit of mobile food objects. Presumably the in short a primary brain. With this we see the earliest ancestors were similar (Barrington, 1965; modification of the initial armour, which shifts from Berrill, 1950; Romer, 1972; Young, 1981). support of mainly the dermis to an inward extension Craniofaclal growth, evolutionary questions of calcification along the connective tissue planes of (A) the head that outlined the sensory capsules and braincase. We may consider this stage to reflect the origin of the cranial component of what will become 11111111111111 ( be d the craniofacial system. Much of the facial component derives from the pharyngeal system, which here supports the roles of gas exchange and feeding; it remained loosely suspended ventral to the anterior tip of the axial skeleton. As the several components developed skeletal supports, their association posed problems during d c growth (Fig. 2). Bone grows by apposition and even 2 2 a b c, d, fibrous and calcified cartilages cannot truly increase in size by interstitial growth. Hence, fusion of components could only occur after allometric growth had been completed. (B) Transition to gnathostomes The next stage involved the modification of some of the anterior arches of the segmented pharyngeal skeleton into a kind of loose jaws, in short an apparatus in which the dorsal and ventral portions could be folded and exert pressure one upon the other. This development of jaws would have facilitated the catching and break-up of food objects and their ingestion into the pharynx and the oesophagus. Presumably, sclerification of the jaws was adaptive, as it added strength and capacity to cut prey more effectively. Also, the increased potential for handling and ingestion of larger prey increased the existing advantage for detection of distant prey. This appears Fig. 2. Sketches to show the kinds of association that can to have provided the basis for development of new occur among appositionally growing skeletal elements. sense organs - eyes, noses, ears - paired, external The small arrows show direction of growth and only one distance receptors. They likely triangulated the pos- linear dimension is shown. (A) Two adjacent skeletal ition of prey, acting synergistically and requiring fixed elements grow equivalently; the three potential results sites. reflect growth on different surfaces and retention or shift Although the anterior portion acquired a new role of the relative position of the initial elements. In 1, both in feeding, the more posterior portions of the pharyn- grow in parallel permitting points on the original geal skeleton still supported the gas exchange sur- elements and the newly grown positions to remain in faces. All in all, we see at least four, actually relative contact. In 2 and 3, growth occurs at opposite conflicting roles in the head during the agnathan- ends. In 2, the geometry changes markedly, whereas in 3 the elements slide past each other precluding fusion early gnathostome transition, namely, the demand during growth. (B) Equivalent sketches for allometric for encapsulation of the enlarged brain, the require- growth in which the two elements grow at different rates. ment for protection and positioning of enlarged and anteriorly placed sense organs, the demand for sup- lated vertebral column leading to the gradual (often port of the gill basket and the demand for the ontogenetic) reduction of the notochord. placement and support of jaws. The gnathostome pattern was associated with the Diversity of fish heads posterior extension of the skull past the otic capsules. Is it indeed possible to make generalizations about This postotic portion allowed anchoring of the phar- the overall pattern of gnathostome head organization yngo-branchial skeleton to the braincase, although seen in fishes? The adults of both fossil and Recent most early gnathostomes displayed ligamentous con- fishes (a useful term likely to grate the sensibilities of nections rather than extensive fusion of the jaw and the cladistically inclined) disclose an enormous diver- palatal elements (Moy-Thomas & "Miles, 1971). Even sity in cranial structure (Jarvik, 1980; Jollie, 1962). more far reaching is the development of an articu- Interestingly enough, there are certain environmental C. Gans

(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. The braincase retains membranous fenestrations. (B) In many tetrapods, we see the results of inward migration of dermal elements and formation of a closed braincase with the mandibular adductor muscles lying external to this. constraints that affect fishes in general, and a remark- Both of these factors also made it advantageous to able number of the specializations we see in the fish strengthen the integument against damage upon con- head reflects these. tact with other objects. However, the cost of acceler- One sees two variably expressed concentric levels ating an external calcified mass is substantial (particu- of cephalic enclosure (Fig. 3). The first is an external larly in aquatic locomotion: Webb, 1978; Webb & dermal armour composed of variously fused and Weihs, 1986); this has led to reduction of external sculptured plates; the second is the internal brain- ossification in each vertebrate group that developed it case. The relative positions of the two systems are (Olson, 1971; Richmond, 1964; Romer, 1966). A maintained by radial skeletal braces within the soft second energetic consideration is the acidification of intermediate tissues. Generally the cephalic shields the extracellular fluids coincident with increased are larger than those on the trunk, perhaps due to metabolism during exercise. Ruben & Bennett (1980, fusion or to accretion (Halstead, 1987). Ventral to 1981) have shown that this leads to dissolution of these is an astounding range of diversifications of the skeletal armour and may provide the explanations for pharyngeal skeleton, which may or may not be linked such phenomena as acellular bone, and sequestration to the central skeletal axis. of scales (from the circulation) seen in some fishes. The external cephalic skeleton presumably arose initially in association with the developing sensory Fish jaws system (Schaeffer, 1977; 0rvig, 1972; Northcutt & Support of the gas exchange and feeding functions Gans, 1983); however, physical protection, calcium seems initially to have involved skeletal elements storage and similar roles were most likely involved in associated with the integument and the pharyngeal its maintenance (Romer, 1933). The presence of an basket. However, as the anterior pharyngeal arches external armour also involves issues of scaling became modified into articulated jaws (and their (Schmidt-Nielsen, 1984) and energetic cost. The shift supports) that allowed larger prey items to be trapped to undulant muscular propulsion provided verte- and partitioned, the forces that could be applied to brates with the means for rapid movement; coinci- the prey (and by struggling prey to the predator) dentally, it increased potential for larger body size in became substantial. This led to the need for improved agnathans and even more in gnathostomes (thus the mechanisms for transmitting such forces (1) between placoderms include some spectacularly large fishes). the mandible and the upper jaw, (2) between the jaws Craniofacial growth, evolutionary questions 9 and the units encapsulating the brain and sense the constraints of feeding in water establish an organs (neurocranium), and (3) (via a head joint) advantage for the retention of a loose and flexible between the anterior head skeleton and the more connection between the elements of the jaws and posterior axial one. other components of the pharyngeal skeleton and the The initial development of jaws in an aquatic more dorsal elements including both the sensory environment could not have occurred independent of capsules and the braincase. ancillary behavioural and physiological patterns, be- Most of these specializations involve chondrich- cause the biting they made possible involved more thians and actinopterygians. From a human perspec- than the mere act of closure of any oral opening. As tive, they occur in side branches of the vertebrate the opening closes, it displaces water, some of which sequence and their mechanical states are not really flows out of the mouth and exerts flow pressure onto pertinent to the biting mechanisms of tetrapods objects against which fish bite. If these objects were (Liem, 1978). The lever systems, the packing of the small they would be deflected during the bite. (A muscles and the intrinsic elasticity of the system spoon is a poor tool for catching fishes in an aquar- (often constrained by linkage to an external armour), ium.) Additionally, the water displaced by the head all differ profoundly from the simpler rhipidistian of a moving fish would produce similar effects. amphibian (McCosker & Lagios, 1979) and dipnoan Perhaps the system originated initially by slowly patterns (Bemis et al. 1987). Even in teleosts that bringing the mouth into contact with attached prey or have a short powerful bite, such as parrot-fishes, the forcing it against a fixed site and then closing the linkages remain complex. The reptilian condition, incipient jaws. This is similar to the prey attack used referred to as cranial kinesis, may be seen as a by members of both lines of Recent agnathans which derivative of this continuing separation of the pharyn- force their buccal region into contact with potential geal apparatus from the braincase. With this, the prey (and is the method predicted for the evolution of mammalian condition, in which the upper jaw and prey engulfment by fossil agnathans, Northcutt & palate are tightly associated with the braincase, Gans, 1983). becomes a late specialization in the pattern of cranio- However, biting at floating prey or biting while the facial evolution. fish was swimming could only have occurred after substantial advances in the sensory and motor coordi- Metamorphosis nation pattern, and utilization of the intrinsic pharyn- The preceding account has dealt entirely with adult geal mobility. Not only must the fish be steered to the conditions. However, juvenile fishes are more than prey, which is moving in three-dimensional space, but miniature adults. Small size allows early larvae to use the moving fish must compensate for the effect of its hydrostatic skeletons (Gutmann & Bonik, 1981); pressure wave which will tend to displace small rigid skeletons involving ossification and chondrifica- floating objects. The opening mouth will furthermore tions only form later. They are often redesigned to a change the streamline pattern. These constraints different Bauplan at metamorphosis. have been overcome in a variety of ways. The most As the food utilized by an animal almost always obvious is the displacement of the jaws out of the changes at metamorphosis (this being a major reason streamlined shape of the predator. The second is the for incorporating metamorphosis in the life cycle, Just distension of the posterior pharynx during the bite. et al. 1981) so will the feeding mechanism, in this case This generates suction which interferes temporarily the jaws. Hence the developmental rates of the with the pressure wave in front of the head and pulls jaw-pharyngeal system then change. Also, the sen- the prey into the mouth. Furthermore, the posterior sory pattern changes at the time of metamorphosis; pharynx of many fishes often sees the development of new sense organs then come into play (Kennedy & a secondary food grinding mill that is mounted on the Rubinson, 1984; Rubinson et al. 1977) and old ones branchial skeleton, although it may rasp the food are remodelled (de Jongh, 1967). However, remodel- against the base of the braincase. The first pattern is ling of the brain is limited as particular motor seen in sharks, as witnessed by the protrusion of the neurones then shift function and control the new palatoquadrate and Meckel's cartilage; it is also seen, muscles (Barnes & Alley, 1983). although differently, in some abyssal fishes (Tcherna- Consequently, the growth rates of brain case, vin, 1953). The second pattern initially utilizing the sensory capsules, gill apparatus and jaws will differ pharyngeal gill-ventilating mechanism is common to both before and after metamorphosis. The functional teleosts, indeed to most aquatic vertebrates (Lauder, bases underlying their allometric growth rates are 1983, 1985). It is not only used for the initial prey clearly distinct. Also, there need be no obvious links capture, but also for the manipulation of the food. among the changing functional influences affecting The details of these patterns are not important in the these structures. Hence, heterochronies will be present context. The critical thing is that in both cases unpredictable. Fusion of the cranial and (future) 10 C. Gans facial components of the skull can only occur after 1966), fusion of the braincase was soon followed by growth has ceased and the relative position of adjac- development of a true head joint on the level of the ent parts will no longer change. anteriormost vertebrae. More important is the separ- Reptiles differ from fishes and amphibians by not ation of the head and pectoral girdle; with develop- displaying metamorphosis, so that they maintain a ment of cervical flexibility, the head, rather than the single cranial configuration after hatching or birth. entire trunk, could now address the prey. Only allometric, but no absolute, changes occur With terrestriality there is a tighter association of during growth. The mechanical designs involved the axial skeleton with the upper jaw, comprising often are scaled up in size between one and three palatomaxillary and other branchial derivatives. Mul- orders of magnitude. It is interesting that the greatest tiple support schemes occur, classified by the number range of skull sizes is shown by animals (turtles and and sites of the connections between pharynx and crocodilians) that show secondary palates and non- braincase. However, in most reptiles the junction of kinetic skulls. the elements of the upper jaw to the sensory capsules and brain case remains loose. This so-called kinesis Transition to terrestrial tetrapody was first noted by Versluys (1912) some 75 years ago. The first stage toward a future invasion of the land Unfortunately, the exact roles of the multiple kinds of presumably occurred in rhipidistian fishes with the kinesis are still poorly understood, as the majority of shift to aspiration breathing (Gans, 1970). This re- models derive from extrapolations from dried skulls structuring of the gas exchangers permitted changes rather than observations and measurements on living of integument and kidneys that protoadapted the organisms. animals for terrestrial life. Also, constraints on the The issue is complicated by organismic diversity; shape of the buccal cavity associated with pulse thus kinesis differs among species of reptiles and birds pumping of air disappeared and the posterior pharyn- (Fig. 4). The more anterior brain case may shift geal skeleton no longer had to support gills (Hughes, vertically relative to the back of the lepidosaurian 1984). With this change, the ingestion system was no skull; more anterior portions of the nasal capsules longer constrained by the need for a major adaptive and snout may rotate further about distinct transverse compromise (Gans, 1974), and the stage was set for axes. The maxilla, premaxilla, ectopterygoid, pala- the development of new techniques of prey manipu- tines and pterygoids may be lifted, rotated, lation, such as inertial feeding. depressed, protruded and retruded. The dorsal as- With the transition from water to land, movements pect of the quadrate may articulate and shift about (of head and jaws) no longer had to act against the the supratemporal (tabular of some authors) or resisting effects of a dense medium; also, suction directly about the surface of the braincase. The feeding using air was ineffective. The transition also ventral aspect of the quadrate may or may not be removed the benefits of buoyancy and required anchored by attachment to the pterygoid and/or jugal muscular effort for support and resisting the effects of arch. In the latter case, the quadrate, the lower end of gravity, which was reflected in the modification of the which supports the mandible in all nonmammalian locomotor pattern and in the ventilation-movement vertebrates, may be protruded, thus shifting the conflict seen in Recent ectotherms (Carrier, 1987). A mandibular articulation. This occurs most spectacu- given muscular effort now would accelerate parts of larly in certain snakes (Cundall & Gans, 1979) and the skeleton to higher velocities (i.e. lead to poten- analogously in some deep-sea fishes (Tchernavin, tially greater sudden reaction forces on the skeleton). 1953). One group of snakes has even subdivided its All of these aspects led to tighter articulations among maxilla into anterior and posterior moieties. These its skeletal elements (autostyly). Certainly the brain- animals and certain geckos can thus close the front of case became better defined and composed of more the mouth, even though the posterior parts of the central elements, often modelling the outline of the tooth row remain separated, locking prey in place CNS. The array of externally placed, articulated (Cundall & Irish, 1987; de Vree & Gans, 1986). dermal bones either migrated inward or was replaced The purported advantages of the more classical functionally by central ossifications. In a number of cranial kinesis, seen in lepidosaurs, include retention groups, the external protective cover shows degrees of an ontogenetic state, facilitation of the strike, of fenestration, permitting attachment of the increas- expansion of the throat, widening of the gape, and ingly large adductor muscles, that could swell during shock absorption (see Bock, 1964 for one list). contraction without pressing against the brain prior to Recent studies (Condon, 1986; de Vree & Gans, the development of an internal braincase (Fox, 1964; 1986, 1987; K. Smith, in preparation) suggest that Frazetta, 1968; Romer, 1966). roles differ and are species-specific; in some cases, Whereas various fishes could already lift the snout kinesis facilitates prey manipulation and in others above the axis of the vertebral column (Romer, aids in shock absorption during crushing of hard prey. Craniofacial growth, evolutionary questions 11

Fig. 4. Sketches of the light, but strong, and highly kinetic skulls of a pitviper (A) and an owl (B). In the snake, the bony elements are connected by ligamentous articulations. The bird skull is fused, and flexibility is obtained by allowing some slender elements to bend. Note the relative sizes of orbits as one indication of different modification of these animals.

Whatever its role, kinesis assures that the growth of lary and mandibular tooth rows to move relative to the brain case need not be constrained by functional each other. Still, it seems to be appropriate to argue demands on the facial system. (However, trogono- that in lepidosaurs akinesis, rather than kinesis, is the phid amphisbaenians, burrowing squamate reptiles derived (and perhaps the adaptive) state (de Vree & that form tunnels with their head, show a clear Gans, 1988). compromise among the shape and position of brain, sensory capsules and jaws and the outline of the cranial periphery; Gans, 1974.) Avian adaptations The general capacity for interelement flexibility is Birds and mammals apparently invented endothermy probably an ancestral (plesiomorphic) condition in independently. It is generally taught that both of squamates, although it may be expressed in different these groups retain the reptilian absence of metamor- ways. Certainly some degree of such flexibility simpli- phosis. However, this is only partly correct as they fies growth, permitting individual skeletal elements to invented a developmental pattern involving pro- change proportions according to local demands. longed parental care, that in some ways incorporates Also, we see variation of the way in which kinesis may switches of food type, already noted as a key aspect of facilitate shock absorption and may permit the maxil- metamorphosis. In birds and mammals, the high level 12 C. Gans of parental care may have led to complex social whereas such changes have been documented for legs systems. and wings; they remain to be studied for cranial Other major avian specializations are the substan- dimensions (Rickleffs, 1983). tial increase of the volume of the sense organs and certainly of the brain (Quiring, 1950; Jerison, 1973). The mammalian condition Brain weight is related to metabolic rate, but the Mammals are unique among vertebrates in having relation is far from clear (Bennett & Harvey, 1985). only the dentary bone in the mandible, the elements For example, note that three herbivores (weighing of the old jaw joint having been incorporated into the approximately 24 g), lizard, mouse and sparrow, each middle ear (Van de Water, 1980). In mammals, some have brain weights equivalent respectively to 0-55, achieve relative brain size values larger than those in 2-8 and 4-4% of body weight. any other vertebrates (Jerison, 1973; Bennett & This effect is even greater for the visual organs. Harvey, 1985). (The special conditions seen in mono- The eye of the starling represents 15 % of the weight tremes and marsupials are omitted here.) The feeding of the head, whereas that of an ostrich is the largest in specializations have been refined by allowing den- any terrestrial vertebrate (Pumphrey, 1961). The tition and general cranial arrangement to maintain an increase in relative brain size was apparently coupled adult feeding pattern over a linear range of only two- with an early development of determinate neuronal or three-to-one. Mammals have reinvented metamor- arrangement. It is well known that during post-term phosis even more completely than birds; they always ontogeny, the size of the brain increases only a subdivide the life cycle, at least into a lactation fraction as much as that of the body. Birds annually (reprocessing of food by the adults) and a freely generate new neurones during the restructuring of feeding stage. centres involved in vocal control (Paton & Notte- Lactation is associated with an ability to suck and boom, 1984). This phenomenon does not seem to this involved development of a bony secondary palate involve changes of overall brain volume or of that of deriving from extension and modification of the the braincase. dentigerous bones. The snout is also relatively short The constraints of development within a hard egg during the suckling period; this in turn involves shell may keep the bill short and the greatest allo- substantial allometric growth for species in which metric growth takes place here (and perhaps in the adults have an elongate snout. Development of a legs of waders). However, altricial (nidicolous) birds secondary palate presumably required relative immo- need not rely on a single feeding pattern, as their bility of the facial region; as noted above, crocodilians body size changes through an order of magnitude. and some turtles which have secondary palates are Precocial (nidifugous) species tend to be born larger the only Recent reptiles with rigid and reinforced and generally show linear scaling over less than one skulls. Among mammals, only the lagomorphs show a order of magnitude (Quiring, 1950; Rickleffs, 1983). condition analogous to cranial kinesis (Bramble, Also, and unlike ectotherms (but see Andrews, 1984). Lactation also required modification of the 1982), birds and mammals show determinate growth ossification sequence; the dentary ossifies much so that developmental instructions for interelement earlier than do elements of the braincase and upper fusion may more easily be specified at a particular jaw (Bellairs & Kamal, 1981; Pond, 1977). size. Two physiological processes may markedly influ- The shift to birds involved a series of supplemen- ence the shape of various mammalian faces. The first tary cranial specializations presumably associated is the use of thermoregulation for cooling the brain; with the evolution of flight. Three major ones are a this involves use of the heat exchange capacity of the general lightening of the skull, the loss of teeth and nasal passages. The second is the selection of differ- the use of air-filled spaces surrounded by bony struts ent primary sensory modalities; thus the face of a so that the external shape of the head may be tarsier with primarily visual orientation is markedly maintained with minimal expenditure of mass. There different from that of a canid with a primarily is emphasis on vision, reflected in large eyes, and a olfactory one. minimal olfactory system. Various species of birds The early determination of the anterior region of show cranial kinesis (Bock, 1964; Zusi, 1984); how- the mandible and determinate growth have presum- ever, rather than movement among elements, avian ably provided the basis for the mammalian pattern of kinesis involves localized bending of bones, such as allowing only a single replacement wave for the those connecting the top of the beak and the eye dentition which becomes functional only as the lac- capsules. Some birds even have a mandibular pseu- tation period is completed. Even the milk dentition is darthrosis, an analogue of the new jaw joint of large and tooth size and length of tooth row are mammals (Bock, 1960). Substantial allometric apparently determined by cues independent of the changes occur in the proportions of the growing skull; length of the jaws. Hence, the 'wisdom tooth' prob- Craniofacial growth, evolutionary questions 13 lem, impacting of the posterior end of the tooth row allowed modification of parts of the head without into the mandibular ramus, also occurs in various simultaneous restructuring of the trunk. Usage of dwarf races of domesticated animals (Moss-Salentijn, pharyngeal slits as an organizational frame for pala- 1978). tal, mandibular, hyoid and posthyoid structures may Previously we have referred to the increased brain have facilitated phenotypic shifts. Examples are size. Mammals show a substantial further increase changes of jaw articulation without modification of over the condition disclosed by Recent reptiles. the posterior gill arches or the loss of posterior gill Various reasons, such as the development of parental arches without major shifts of the mandibular pat- care and social systems, may be involved in this tern. phenomenon; however, the issue of brain size and In any case, the several craniofacial components mental capacity is one best avoided here. The have been shown to have a long independent history. increased brain size does make for extreme allometric It has been demonstrated that their roles often change of the cranial portion of the skull. The early demanded retention and even redevelopment of a determination of brain size furthermore assures that mechanically loose association. These circumstances between term and sexual maturity the cranium grows presumably established advantages to a developmen- relatively more slowly than does the mandibular tal pattern in which the fate of some several cranio- system. Still, post-term growth leads to relatively late facial subunits could be independently controlled, closure of cranial sutures. whereas that of other subunits is associated. Perhaps, comparative studies considering history and function (role) retain the promise of providing answers to Concluding discussion developmental questions, answers that may well be complementary to those furnished by the recent The preceding summary should have documented elegant studies about the detailed mechanisms util- that the mammalian craniofacial system is truly com- ized in the development of particular forms. pound, deriving from at least four disjunct portions in early vertebrates. The several parts have each passed Thanks are due to the organizers of this Symposium for through repeated functional changes in phylogeny. the invitation that permitted me to participate. I am Furthermore, they encounter changing demands dur- beholden to David Carrier, A. S. Gaunt and Paul F. A. ing ontogeny. History has generated the basis for Maderson for comments on the manuscript, and to various friends for references about specific situations. Preparation allometric growth within any one species and we see of the report was supported by US National Science evidence of heterochrony in comparing interspecific Foundation grant G-BSR-850940. Miss Lucy Alejandro change. A byproduct of the requirement for allo- inked the sketches. metric changes among adjacent elements has been relative flexibility among the mechanical components throughout much of ontogeny. References The trend to ontogenetic fusion among the elements of the braincase, the formerly anterior sen- ANDREWS, R. M. 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