Development 103 Supplement, 3-15 (1988) Printed in Great Britain © The Company of Biologists Limited 1988
Craniofacial growth, evolutionary questions
Department of Biology, The University of Michigan, Ann Arbor, Michigan 48109-1048, USA
Introduction Theory Principles Tasks of the craniofacial system The process of change Predictions from the record Functional stages in the vertebrate head The system in the prevertebrates Transition to vertebrates
Transition to gnathostomes Diversity offish heads Fish jaws Metamorphosis Transition to terrestrial tetrapody Avian adaptations The mammalian condition Concluding discussion Key words: functional morphology, cephalization, cranial kinesis, craniofacial evolution, adaptation.
Understanding the growth of craniofacial systems in mammals, particularly in man, has always posed problems. Such craniofacial systems are formed ontogenetically of multiple tissue types, and the contributions of these tissues do not obviously match the divisions of adult skeletal elements (see Thorogood, this volume). Even the kind and number of segments in the head region continue to attract attention (Maderson, 1987). Furthermore, craniofacial systems appear to show trends toward an unusual number of developmental abnormalities or teratologies. Many of these teratologies suggest that we are not looking at a simple coordinated whole (Salinas, 1982; Shprintzen, 1982); rather, it seems as if multiple cranial and facial components incur differential growth either symmetrically or asymmetrically. It seems instructive to treat the basis of this curious array of complications from an evolutionary viewpoint, considering two aspects, adaptation and history. Adaptation implies that the structures of organisms are not randomly assembled, but have been and remain at any moment under the influence of selection (Gans, 1988). Implicit within this concept of adaptation is that each phenotypic array must incur both a cost and a benefit, the cost in terms of generating and of maintaining the phenotype, the benefit in terms of the roles in which the phenotype is
involved. In contrast, the concept of history documents that adaptation does not act de novo to generate phenotypes out of infinitely plastic raw material. As the phenotypes of extant organisms derive from those of ancestral ones, the phenotypic match to new environments reflects the genetic and developmental plasticity of possible precursor organisms. This evolutionary viewpoint is here utilized in a brief review. It begins with the primary roles of the structures infishesthat are homologous to the craniofacial system of mammals. (Role is here considered to be that part of the function of a phenotypic aspect that contributes evolutionary benefit, i.e. for those organisms that have it, the role of a structure is its adaptive function in a particular environment.) In the process, I attempt to clarify some aspects about the way the fossil and surviving members of early vertebrate groups should be considered. This evolutionary analysis is based upon past scenario generation and is obviously reconstructive. There being but a limited fossil record, the gaps are filled by extrapolations based upon the structure, physiology and ecology of animals living today (Gans, 1985). After developing the roles of the system in fishes, I shall review the several changes of role from fishes to mammals. Throughout, I emphasize the components of the head, the separate changes each has undergone and the aspects that keep them associ-
It is hoped that such a data set will provide a framework setting the stage for interpretation of the more developmental aspects. (B) braincase. the assembly will reflect different initial (and subsequent) roles. The anterior end of vertebrates retains the front of the alimentary canal and the external openings of the gas exchange system. The components performing most of the roles thus far listed presumably were homologous to the mammalian cranial component. It is unlikely that the demands occurred in parallel or were equivalent. (C) mandibular apparatus. sensory capsules and an 'upper jaw' generally fused into a single unit. Each of them continues to incur and respond to independent demands of the environment. 1. and shifts incurred in their component materials and proportions that are coordinated neither phylogenetically nor ontogenetically.
The craniofacial system of mammals is supported by a skeletal array consisting of a braincase. 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. it encapsulated the central nervous system. Just posterior to the jaw joint lies the auditory meatus leading to the middle ear. protecting them and permitting them accurately to scan the anterior environment by maintaining their position relative to the axis of the trunk. The craniofacial system consequently must maintain its patency during the acquisition and ingestion of nutrients and respiratory fluids.C. 1). earlier vertebrates incorporated extensive portions of the anterior pharyngeal tube in the
Fig. protecting it both from anteriorly and posteriorly directed forces. 1980). Gans ated. (A) Sensory system. Whereas these tasks are the major ones in mammals. Three sketches of a cat skull each with one major functional system emphasized by shading. Next. Tasks of the craniofacial system The craniofacial system of mammals is homologous to parts of the anterior end of the earliest vertebrates.
. precluding deformation during penetration of liquid or solid aspects of the environment. it provided the stiffening and reinforcement of this end. incorporating several reduced skeletal elements once involved with the jaw suspension (Van de Water et al. The system also permitted the anterior end to bear paired. 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. external sensory organs. As such. Hence.
so does its prey. the greater the change the less the potential that the resulting phenotype will be viable and reproductively successful. to sequester calcium deposits. to 'test' the edges of the environmental niche they occupy and sometimes to discover new sites located in ranges peripheral to their ancestral ones. Finally. we know that changes are interactive and coevolved so that modification of individual components is still likely to generate viable phenotypes after a number of minor genetic changes. is a most appealing description (Van Valen. the Red Queen metaphor. were to be determined on what might be called a one character/one gene basis. After all. were associated with the tasks of food handling and gas extraction. As in all our attempts to trace history. making the system too complex for facile analysis. As long as the variants formed met the minimal demands of the animal. and to modify these. 1979). will affect more of the developmental pathway and. Now. What likely arose initially was the capacity of the integument to ossify. 1985). more pathways. This is a second set of roles for the structures contributing to what later became known as the facial component. resulting from mutations which are minor with respect to gene alteration. This would be impossible if the shape and growth rate of individual structural elements. This lets them be opportunistic. As the predator evolves. Next. Halstead's observations on the dermal armour of fossil agnathans. prediction about the direc-
tions of evolutionary change requires information about the genetics of their developmental mechanisms. it will be influenced by the capacity of its genotype to mutate and by the phenotypes likely to be generated by such mutations and their various recombinations. Hence. The meaning of this idea of remnant is important because it establishes the kinds of biological conclusions permitted on the basis of surviving members of a group. Many of the observed variants then may be considered as experimentations around a theme. However. For various reasons. evolutionary questions cephalic structures.Craniofacial growth. However. further likely to confuse interpretation based upon surviving members of a group and making any fossil more useful. 1987). for instance. The earliest invaders of a 'new' niche may be less effective at exploiting its resources than will subsequent forms. the direction of evolution will be affected by the genetic and developmental capacity of the species. many different phenotypes will be produced by relatively small changes in their various components. the invasions of adaptive niches and radiation into these. explosive radiation). The potential confusion is due to the decreasing probability that the survivors of any
. There remains the potential for more substantial phenotypic changes. It will be influenced by the way that the developmental program forms its phenotype and by the kind of variation that this permits or incorporates. the detail of ossification pattern each displayed may be less critical to the survival of the individual. it explains the seemingly random experimentation often encountered early in the fossil record of a particular radiation (i. From this viewpoint. See. it is possible to predict the kinds of genetic and hence phenotypic changes that would be likely in such a framework. the Recent animals we see are but remnants of past historical processes. they will in turn incur advantages for defence mechanisms or other aspects that make the task of the predator more difficult. The new habitat imposes new selective factors and may lead to 'improved' genotypes. in stochastic terms. Such early minor changes in the sequence forming a particular characteristic (Gans. a substantial fraction of the population will have phenotypes that exceed the minimal level characterized as necessary (Gans. Predictions from the record Consideration in this fashion of the rate and direction of a particular evolutionary change would seem to make prediction of future directions just about impossible (Tatarinov. Adequacy rather than perfection is demanded. whether pertaining tofishessurviving now or to those seen in the fossil record? First of all. The process of change The mechanism of evolutionary change. with the earliest among such variants being indeterminable. 1973). viable changes of this magnitude are likely to be less frequent. as well. of running as fast as possible just to stay in one place. It is probable that there will be a relatively large number of what might be considered to be variations on a theme. are fundamental to understanding evolutionary processes. which led him to conclude that all possible variants of integumentary structure seemed to have arisen roughly simultaneously (Halstead. but major in their effect on the phenotype. There are too many unknowns.e. However. Other competing predators will also incur similar processes. what has all this to do with fish heads. by implication. for instance of the skeleton. there is change of the environment against which this play proceeds. The pattern of change may also generate a different effect. 1987). We must begin with a population or populations of organisms characterized by a set of phenotypes allowing them to make a living in the niches they then occupy. thus. unless pointed to by other evidence. and all of these. If the resources of the new habitat are living ones.
perhaps as a 'new' structural material. the surviving species are likely to be highly specialized and to occupy peripheral. Beyond the expected phenomenon that the passage of time since the radiation separated would lead to a gradual accumulation of changes. 1986). The prey-detecting arrays involved distance receptors. 1987). 1985).C. 1982). 1967) and in some fossil lampreys (Bardack & Zangerl. in short a primary brain. Gans
very old radiation will mirror the dominant biological pattern of the line at the time that they derived from it. Also. both likely to have been formed from neural crest materials (Gans & Northcutt. This enlargement generated the anteriorly prolonged nervous system. representing skeletal elements formed of hydroxyapatite. 1982. Berrill. pituitary (Gorbman & Tamarin. perhaps restricted. The pharynx permits extraction from the water of finely particulate food by a kind of filtration. In turn. The muscularized pharynx was then associated with an increase in the anteriorly placed motor portion of the central nervous system. neither hagfish nor lampreys obviously represent an offshoot of the ostracoderm pattern. amphioxus lacks particular specialization for ingestion of large food particles. such as their egg type (Hardisty. known only from sharks among recent fishes. Yalden. enhanced with a stiffening coating. 1972). circulation (Lewis & Potter. It must be stressed that amphioxus shows minimal cephalization and that its anterior sense organs are unpaired and mainly positioned within the nerve cord. gill function (Mallatt. Initially.
Functional stages in the vertebrate head The system in the prevertebrates Prevertebrates were presumably similar to amphioxus (or some tunicate larvae) in that they had an axial skeletal element. The investment 'with cartilage' of an initially collagenous framework of the pharyngeal skeleton allowed better modelling for support of more convoluted gas exchange surfaces. The increase of the motor portion of the anterior CNS was followed by amplification of the sensory component. in some way this pattern is better modelled by present gnathostomes (Hardisty. not known in any hemichordates or protochordates (Bone. we see the increasing probability that the originally major niches belonging to the radiation have become fragmented and occupied by competitors pertaining to quite distinct groups. 1986) and kidney function (Riegel. 1979. It is likely that an ancestral animal modelled upon such a body plan would not have required a skeletal apparatus with any significant role in protecting an anterior nervous system or associated sense organs. Young. rather than calcite.1960). a shift that stressed the somatic rather than the visceral motor portion. The utilization of the pharynx for gas exchange was associated with a shift from cilia to muscles for ventilatory pumping and the development of cartilage. 1959. reflecting both of these events generated the basis for the anterior enlargement and forward extension of the primary nerve cord. 1972. niches in which they have become further modified. eons ago. namely paired external sense organs. 1983). reflecting anterior outgrowth and later calcification of the intermediate connective tissues. It has been argued elsewhere that electroreception was likely the first distance sensory mode and that the detecting system may have played a role in the acquisition of hydroxyapatite as a skeletal material in the integument (Northcutt & Gans. Wells et al. 1968. much less for pursuit of mobile food objects. Perhaps coincidentally we see a shift from a stochastically sampling pattern of filter feeding to one in which larger living particles are detected and ingested. likely providing stiffness for sculling and burrowing (Gans. This stage then led to a modification of the anterior end of the animal. the origin of bone likely followed the origin of cartilage (but rarely preserved in the fossil record) which formed a supportive tissue new to vertebrates (Northcutt & Gans. Certainly. 1965. 1985). This is the likely explanation for the agnathan condition. Mallatt. Mallatt & Paulsen. 1979. In association with the modified pharynx. Calcified head cartilages. With this we see the modification of the initial armour. 1983. These streams turn. 1981).
Transition to vertebrates The transition to vertebrates is signalled in the fossil record by the appearance of bone. which shifts from support of mainly the dermis to an inward extension
. Romer. Le Douarin. 1985). occurred in heterostracan fishes (Denison. 1983). we see the first extranotochordal skeletal apparatus. as both surviving lines differ markedly in major characteristics. 1950. as well as of elastic recoil. Presumably the earliest ancestors were similar (Barrington. 1986). However. The flow is first divided into a multiplicity of streams. and perichondral bone in ostracoderms (Moy-Thomas & Miles. the supportive apparatus involved a notochord and associated fluid-filled spaces which provided hydrostatic effects due to the tensile components in their epithelioid walls. Stensio. 1971). The resultant addition of tissues. 1981. The latter permitted a unidirectional power stroke to pump water with a two-phase contraction-expansion pharyngeal movement. the skeleton of which is formed of collagenous rods. Ventral to these stiffened axes were supports for a pharyngeal basket. causing particles entrained in the water to impinge onto a mesh of cilia-driven mucus bands which then transport them through the gut.
both grow in parallel permitting points on the original elements and the newly grown positions to remain in relative contact.
d. the requirement for protection and positioning of enlarged and anteriorly placed sense organs. 2). external distance receptors. This appears to have provided the basis for development of new sense organs .paired. Diversity of fish heads
Is it indeed possible to make generalizations about the overall pattern of gnathostome head organization seen in fishes? The adults of both fossil and Recent fishes (a useful term likely to grate the sensibilities of the cladistically inclined) disclose an enormous diversity in cranial structure (Jarvik. Bone grows by apposition and even fibrous and calcified cartilages cannot truly increase in size by interstitial growth. Also. there are certain environmental
. The gnathostome pattern was associated with the posterior extension of the skull past the otic capsules. All in all. (A) Two adjacent skeletal elements grow equivalently. the demand for support of the gill basket and the demand for the placement and support of jaws. sclerification of the jaws was adaptive. Even more far reaching is the development of an articu(A)
b c. In 2 and 3. acting synergistically and requiring fixed sites. This development of jaws would have facilitated the catching and break-up of food objects and their ingestion into the pharynx and the oesophagus. actually conflicting roles in the head during the agnathanearly gnathostome transition. As the several components developed skeletal supports. which here supports the roles of gas exchange and feeding. We may consider this stage to reflect the origin of the cranial component of what will become the craniofacial system. The small arrows show direction of growth and only one linear dimension is shown. noses. Sketches to show the kinds of association that can occur among appositionally growing skeletal elements. In 2. They likely triangulated the position of prey. growth occurs at opposite ends. This postotic portion allowed anchoring of the pharyngo-branchial skeleton to the braincase. Jollie. as it added strength and capacity to cut prey more effectively.Craniofaclal growth. Hence. the demand for encapsulation of the enlarged brain. Much of the facial component derives from the pharyngeal system. we see at least four. (B) Equivalent sketches for allometric growth in which the two elements grow at different rates. whereas in 3 the elements slide past each other precluding fusion during growth.
Fig. the geometry changes markedly. 1980. 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. Presumably.eyes. it remained loosely suspended ventral to the anterior tip of the axial skeleton. 1971). evolutionary questions of calcification along the connective tissue planes of the head that outlined the sensory capsules and braincase. Although the anterior portion acquired a new role in feeding. namely. their association posed problems during growth (Fig. Interestingly enough. 1962). fusion of components could only occur after allometric growth had been completed. although most early gnathostomes displayed ligamentous connections rather than extensive fusion of the jaw and palatal elements (Moy-Thomas & "Miles. In 1. the more posterior portions of the pharyngeal skeleton still supported the gas exchange surfaces. the three potential results reflect growth on different surfaces and retention or shift of the relative position of the initial elements. lated vertebral column leading to the gradual (often ontogenetic) reduction of the notochord. 2. the increased potential for handling and ingestion of larger prey increased the existing advantage for detection of distant prey. in short an apparatus in which the dorsal and ventral portions could be folded and exert pressure one upon the other. ears .
1984) and energetic cost. 1981) have shown that this leads to dissolution of skeletal armour and may provide the explanations for such phenomena as acellular bone. constraints that affect fishes in general. Generally the cephalic shields are larger than those on the trunk. However.
Support of the gas exchange and feeding functions seems initially to have involved skeletal elements associated with the integument and the pharyngeal basket. 1971. The presence of an external armour also involves issues of scaling (Schmidt-Nielsen. Both of these factors also made it advantageous to strengthen the integument against damage upon contact with other objects. 1987). the cost of accelerating an external calcified mass is substantial (particularly in aquatic locomotion: Webb. the medial surface of which provides attachment sites for the jaw adductor muscles. This led to the need for improved mechanisms for transmitting such forces (1) between the mandible and the upper jaw. 3. coincidentally. 0rvig. 1972. (B) In many tetrapods. Northcutt & Gans. 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. Webb & Weihs. and a remarkable number of the specializations we see in the fish head reflects these. The shift to undulant muscular propulsion provided vertebrates with the means for rapid movement. it increased potential for larger body size in agnathans and even more in gnathostomes (thus the placoderms include some spectacularly large fishes). there is a dermal armour. however. 1964. 1977. However. 1986). calcium storage and similar roles were most likely involved in its maintenance (Romer. The relative positions of the two systems are maintained by radial skeletal braces within the soft intermediate tissues. (A) In simple fish skulls. The braincase retains membranous fenestrations. A second energetic consideration is the acidification of the extracellular fluids coincident with increased metabolism during exercise. Ventral to these is an astounding range of diversifications of the pharyngeal skeleton. 3). Gans
Dermal armour Closed braincase Open braincase Muscle Bony brain case (closed) Muscle x-sec. (2) between the jaws
. and sequestration of scales (from the circulation) seen in some fishes. physical protection. this has led to reduction of external ossification in each vertebrate group that developed it (Olson. Ruben & Bennett (1980. perhaps due to fusion or to accretion (Halstead. the forces that could be applied to the prey (and by struggling prey to the predator) became substantial.C. The first is an external dermal armour composed of variously fused and sculptured plates. 1983). Romer. as the anterior pharyngeal arches became modified into articulated jaws (and their supports) that allowed larger prey items to be trapped and partitioned. 1978. The external cephalic skeleton presumably arose initially in association with the developing sensory system (Schaeffer. which may or may not be linked to the central skeletal axis. Sections through schematized vertebrate skulls to show the sites of bone formation. 1966). 1933). the second is the internal braincase. One sees two variably expressed concentric levels of cephalic enclosure (Fig. Richmond.
The second is the distension of the posterior pharynx during the bite. Hence the developmental rates of the jaw-pharyngeal system then change. 1984. and utilization of the intrinsic pharyngeal mobility. The details of these patterns are not important in the present context. it is also seen.Craniofacial growth. Rubinson et al. the growth rates of brain case. From a human perspective. (A spoon is a poor tool for catching fishes in an aquarium. They are often redesigned to a different Bauplan at metamorphosis. The most obvious is the displacement of the jaws out of the streamlined shape of the predator. sensory capsules. 1967). indeed to most aquatic vertebrates (Lauder. although differently. 1987). The opening mouth will furthermore change the streamline pattern. Northcutt & Gans. Also.
Metamorphosis The preceding account has dealt entirely with adult conditions. although it may rasp the food against the base of the braincase. 1983). 1983. This generates suction which interferes temporarily with the pressure wave in front of the head and pulls the prey into the mouth. all differ profoundly from the simpler rhipidistian amphibian (McCosker & Lagios. the sensory pattern changes at the time of metamorphosis. may be seen as a derivative of this continuing separation of the pharyngeal apparatus from the braincase. such as parrot-fishes. These constraints have been overcome in a variety of ways. Also. the posterior pharynx of many fishes often sees the development of a secondary food grinding mill that is mounted on the branchial skeleton. 1983). it displaces water. there need be no obvious links among the changing functional influences affecting these structures. 1981). the mammalian condition. Even in teleosts that have a short powerful bite. The initial development of jaws in an aquatic environment could not have occurred independent of ancillary behavioural and physiological patterns. evolutionary questions and the units encapsulating the brain and sense organs (neurocranium). Not only must the fish be steered to the prey. Consequently. With this. they occur in side branches of the vertebrate sequence and their mechanical states are not really pertinent to the biting mechanisms of tetrapods (Liem. Furthermore. If these objects were small they would be deflected during the bite. some of which flows out of the mouth and exerts flow pressure onto objects against which fish bite. which is moving in three-dimensional space. As the opening closes. the linkages remain complex. the water displaced by the head of a moving fish would produce similar effects. The first pattern is seen in sharks. gill apparatus and jaws will differ both before and after metamorphosis. 1977) and old ones are remodelled (de Jongh. in this case the jaws. in which the upper jaw and palate are tightly associated with the braincase. because the biting they made possible involved more than the mere act of closure of any oral opening. As the food utilized by an animal almost always changes at metamorphosis (this being a major reason for incorporating metamorphosis in the life cycle. However. referred to as cranial kinesis. becomes a late specialization in the pattern of craniofacial evolution. The second pattern initially utilizing the pharyngeal gill-ventilating mechanism is common to teleosts. but the moving fish must compensate for the effect of its pressure wave which will tend to displace small floating objects. Most of these specializations involve chondrichthians and actinopterygians. The functional bases underlying their allometric growth rates are clearly distinct. juvenile fishes are more than miniature adults. new sense organs then come into play (Kennedy & Rubinson. remodelling of the brain is limited as particular motor neurones then shift function and control the new muscles (Barnes & Alley. the packing of the muscles and the intrinsic elasticity of the system (often constrained by linkage to an external armour). in some abyssal fishes (Tchernavin. 1985). Perhaps the system originated initially by slowly bringing the mouth into contact with attached prey or forcing it against a fixed site and then closing the incipient jaws. The reptilian condition. but also for the manipulation of the food. and (3) (via a head joint) between the anterior head skeleton and the more posterior axial one. The lever systems. Small size allows early larvae to use hydrostatic skeletons (Gutmann & Bonik. However. Fusion of the cranial and (future)
. Hence. It is not only used for the initial prey capture. 1979) and dipnoan patterns (Bemis et al. heterochronies will be unpredictable. However. as witnessed by the protrusion of the palatoquadrate and Meckel's cartilage. The critical thing is that in both cases the constraints of feeding in water establish an advantage for the retention of a loose and flexible connection between the elements of the jaws and other components of the pharyngeal skeleton and the more dorsal elements including both the sensory capsules and the braincase. rigid skeletons involving ossification and chondrifications only form later. 1978). This is similar to the prey attack used by members of both lines of Recent agnathans which force their buccal region into contact with potential prey (and is the method predicted for the evolution of prey engulfment by fossil agnathans.) Additionally. 1953). 1981) so will the feeding mechanism. Just et al. biting at floating prey or biting while the fish was swimming could only have occurred after substantial advances in the sensory and motor coordination pattern.
fusion of the braincase was soon followed by development of a true head joint on the level of the anteriormost vertebrae. also. Recent studies (Condon. The ventral aspect of the quadrate may or may not be anchored by attachment to the pterygoid and/or jugal arch. 1953). 1974). Multiple support schemes occur. 1987). may be protruded. as the majority of models derive from extrapolations from dried skulls rather than observations and measurements on living organisms. palatines and pterygoids may be lifted. de Vree & Gans. widening of the gape. so that they maintain a single cranial configuration after hatching or birth. K. the lower end of which supports the mandible in all nonmammalian vertebrates. movements (of head and jaws) no longer had to act against the resisting effects of a dense medium. It is interesting that the greatest range of skull sizes is shown by animals (turtles and crocodilians) that show secondary palates and nonkinetic skulls. 1970). often modelling the outline of the CNS. 1966). Whereas various fishes could already lift the snout above the axis of the vertebral column (Romer. lead to potentially greater sudden reaction forces on the skeleton). This so-called kinesis was first noted by Versluys (1912) some 75 years ago. Frazetta. The transition also removed the benefits of buoyancy and required muscular effort for support and resisting the effects of gravity. ectopterygoid. in most reptiles the junction of the elements of the upper jaw to the sensory capsules and brain case remains loose. The array of externally placed. More important is the separation of the head and pectoral girdle. and the stage was set for the development of new techniques of prey manipulation. thus kinesis differs among species of reptiles and birds (Fig. permitting attachment of the increasingly large adductor muscles. Transition to terrestrial tetrapody The first stage toward a future invasion of the land presumably occurred in rhipidistian fishes with the shift to aspiration breathing (Gans. 1984). the quadrate. Romer. articulated dermal bones either migrated inward or was replaced functionally by central ossifications. Unfortunately. even though the posterior parts of the tooth row remain separated. The mechanical designs involved often are scaled up in size between one and three orders of magnitude. kinesis facilitates prey manipulation and in others aids in shock absorption during crushing of hard prey. The more anterior brain case may shift vertically relative to the back of the lepidosaurian skull. seen in lepidosaurs. rather than the entire trunk. in preparation) suggest that roles differ and are species-specific. Only allometric. In the latter case. the head. facilitation of the strike. expansion of the throat. suction feeding using air was ineffective. With the transition from water to land. 1968. the exact roles of the multiple kinds of kinesis are still poorly understood.
facial components of the skull can only occur after growth has ceased and the relative position of adjacent parts will no longer change. However. premaxilla. the external protective cover shows degrees of fenestration. include retention of an ontogenetic state. more anterior portions of the nasal capsules and snout may rotate further about distinct transverse axes. Gans 1966). changes occur during growth. 1986). These animals and certain geckos can thus close the front of the mouth. 1987. The issue is complicated by organismic diversity. This occurs most spectacularly in certain snakes (Cundall & Gans. de Vree & Gans. such as inertial feeding. 1986. could now address the prey. classified by the number and sites of the connections between pharynx and braincase. Certainly the braincase became better defined and composed of more central elements. Smith. 4). 1964 for one list). The maxilla.
. protruded and retruded. Reptiles differ from fishes and amphibians by not displaying metamorphosis. One group of snakes has even subdivided its maxilla into anterior and posterior moieties. in some cases.10
C. The dorsal aspect of the quadrate may articulate and shift about the supratemporal (tabular of some authors) or directly about the surface of the braincase. the ingestion system was no longer constrained by the need for a major adaptive compromise (Gans. and shock absorption (see Bock. that could swell during contraction without pressing against the brain prior to the development of an internal braincase (Fox. comprising palatomaxillary and other branchial derivatives. thus shifting the mandibular articulation. locking prey in place (Cundall & Irish. All of these aspects led to tighter articulations among its skeletal elements (autostyly).e. The purported advantages of the more classical cranial kinesis. with development of cervical flexibility. This restructuring of the gas exchangers permitted changes of integument and kidneys that protoadapted the animals for terrestrial life. In a number of groups. Also. which was reflected in the modification of the locomotor pattern and in the ventilation-movement conflict seen in Recent ectotherms (Carrier. rotated. 1979) and analogously in some deep-sea fishes (Tchernavin. With this change. constraints on the shape of the buccal cavity associated with pulse pumping of air disappeared and the posterior pharyngeal skeleton no longer had to support gills (Hughes. 1987. A given muscular effort now would accelerate parts of the skeleton to higher velocities (i. but no absolute. 1986. With terrestriality there is a tighter association of the axial skeleton with the upper jaw. depressed. 1964.
In birds and mammals. It is generally taught that both of these groups retain the reptilian absence of metamorphosis.Craniofacial growth. trogonophid amphisbaenians. this is only partly correct as they invented a developmental pattern involving prolonged parental care. permitting individual skeletal elements to change proportions according to local demands. Still. is the derived (and perhaps the adaptive) state (de Vree & Gans. Gans. sensory capsules and jaws and the outline of the cranial periphery. However. 4. Also. rather than kinesis. although it may be expressed in different ways. Sketches of the light. but strong. In the snake. kinesis assures that the growth of the brain case need not be constrained by functional demands on the facial system. the high level
. show a clear compromise among the shape and position of brain. and highly kinetic skulls of a pitviper (A) and an owl (B). 1974. the bony elements are connected by ligamentous articulations. it seems to be appropriate to argue that in lepidosaurs akinesis. burrowing squamate reptiles that form tunnels with their head. we see variation of the way in which kinesis may facilitate shock absorption and may permit the maxil-
lary and mandibular tooth rows to move relative to each other. already noted as a key aspect of metamorphosis. Avian adaptations Birds and mammals apparently invented endothermy independently. evolutionary questions
Fig. and flexibility is obtained by allowing some slender elements to bend. Certainly some degree of such flexibility simplifies growth.) The general capacity for interelement flexibility is probably an ancestral (plesiomorphic) condition in squamates. The bird skull is fused. that in some ways incorporates switches of food type. (However.
Whatever its role. 1988). Note the relative sizes of orbits as one indication of different modification of these animals.
The shift to birds involved a series of supplementary cranial specializations presumably associated with the evolution of flight. Pond. 1960). at least into a lactation (reprocessing of food by the adults) and a freely feeding stage. they always subdivide the life cycle. The constraints of development within a hard egg shell may keep the bill short and the greatest allometric growth takes place here (and perhaps in the legs of waders). 1984). note that three herbivores (weighing approximately 24 g). avian kinesis involves localized bending of bones. The eye of the starling represents 15 % of the weight of the head. However. Bennett & Harvey. There is emphasis on vision. (The special conditions seen in monotremes and marsupials are omitted here. they remain to be studied for cranial dimensions (Rickleffs. 1983). Precocial (nidifugous) species tend to be born larger and generally show linear scaling over less than one order of magnitude (Quiring. The first is the use of thermoregulation for cooling the brain. the 'wisdom tooth' prob-
of parental care may have led to complex social systems. The increase in relative brain size was apparently coupled with an early development of determinate neuronal arrangement. Mammals have reinvented metamorphosis even more completely than birds. some achieve relative brain size values larger than those in any other vertebrates (Jerison. each have brain weights equivalent respectively to 0-55. 1981. thus the face of a tarsier with primarily visual orientation is markedly different from that of a canid with a primarily olfactory one. Hence. 1980). This phenomenon does not seem to involve changes of overall brain volume or of that of the braincase. the elements of the old jaw joint having been incorporated into the middle ear (Van de Water. Jerison. Rickleffs. but the relation is far from clear (Bennett & Harvey. 1973. only the lagomorphs show a condition analogous to cranial kinesis (Bramble. reflected in large eyes. lizard. 1950. Lactation also required modification of the ossification sequence. 1964. 1985). 1984). this involves use of the heat exchange capacity of the nasal passages. and unlike ectotherms (but see Andrews. the dentary ossifies much earlier than do elements of the braincase and upper jaw (Bellairs & Kamal. whereas that of an ostrich is the largest in any terrestrial vertebrate (Pumphrey. The snout is also relatively short during the suckling period. 1985). Zusi.) The feeding specializations have been refined by allowing dentition and general cranial arrangement to maintain an adult feeding pattern over a linear range of only twoor three-to-one. This effect is even greater for the visual organs. In mammals. Various species of birds show cranial kinesis (Bock. crocodilians and some turtles which have secondary palates are the only Recent reptiles with rigid and reinforced skulls. Other major avian specializations are the substantial increase of the volume of the sense organs and certainly of the brain (Quiring. 1950. Lactation is associated with an ability to suck and this involved development of a bony secondary palate deriving from extension and modification of the dentigerous bones. Two physiological processes may markedly influence the shape of various mammalian faces. Even the milk dentition is large and tooth size and length of tooth row are apparently determined by cues independent of the length of the jaws. Also. 1983). Substantial allometric changes occur in the proportions of the growing skull. Birds annually generate new neurones during the restructuring of centres involved in vocal control (Paton & Notteboom. Some birds even have a mandibular pseudarthrosis. The second is the selection of different primary sensory modalities. The mammalian condition Mammals are unique among vertebrates in having only the dentary bone in the mandible. the size of the brain increases only a fraction as much as that of the body. The early determination of the anterior region of the mandible and determinate growth have presumably provided the basis for the mammalian pattern of allowing only a single replacement wave for the dentition which becomes functional only as the lactation period is completed. Three major ones are a general lightening of the skull. as their body size changes through an order of magnitude. Development of a secondary palate presumably required relative immobility of the facial region. It is well known that during post-term ontogeny. altricial (nidicolous) birds need not rely on a single feeding pattern. 1984).12
C. 1973). For example. Gans whereas such changes have been documented for legs and wings. Among mammals. however. 1982). 2-8 and 4-4% of body weight. such as those connecting the top of the beak and the eye capsules.
. rather than movement among elements. and a minimal olfactory system. birds and mammals show determinate growth so that developmental instructions for interelement fusion may more easily be specified at a particular size. an analogue of the new jaw joint of mammals (Bock. 1977). this in turn involves substantial allometric growth for species in which adults have an elongate snout. as noted above. the loss of teeth and the use of air-filled spaces surrounded by bony struts so that the external shape of the head may be maintained with minimal expenditure of mass. 1961). Brain weight is related to metabolic rate. mouse and sparrow.
J. 273-320. (1972). H. evolutionary questions lem. development and metabolism in birds and mammals. 11. D ' A & KAMAL. It has been demonstrated that their roles often demanded retention and even redevelopment of a mechanically loose association. & KEMP. 67-84. comparative studies considering history and function (role) retain the promise of providing answers to developmental questions. Edinburgh: Oliver and Boyd. Miss Lucy Alejandro inked the sketches. A byproduct of the requirement for allometric changes among adjacent elements has been relative flexibility among the mechanical components throughout much of ontogeny.. however. The several parts have each passed through repeated functional changes in phylogeny. may be involved in this phenomenon. Lampreys in the
fossil record. The early determination of brain size furthermore assures that between term and sexual maturity the cranium grows relatively more slowly than does the mandibular system. Liss. London: Academic Press. S. London: Academic Press. New York: A.
BARNES. N. Maturation and
recycling of trigeminal motoneurons in anuran larvae. Parsons). it seems as if the potential of the pattern for generating substantially distinct phenotypes by minor changes on a theme may have been one reason for the ability of the vertebrates to radiate successfully into most major environments. (1985). impacting of the posterior end of the tooth row into the mandibular ramus. I am beholden to David Carrier. 406-414.. Gans & T. Previously we have referred to the increased brain size. C. (1983). Hardisty & I. hyoid and posthyoid structures may have facilitated phenotypic shifts. History has generated the basis for allometric growth within any one species and we see evidence of heterochrony in comparing interspecific change. Furthermore. & ZANGERL. These circumstances presumably established advantages to a developmental pattern in which the fate of some several craniofacial subunits could be independently controlled. Mammals show a substantial further increase over the condition disclosed by Recent reptiles. comp. The trend to ontogenetic fusion among the elements of the braincase. What is perhaps most interesting in evaluating the cephalic array is the amazing constancy of the portions of the developmental patterns already disclosed for diverse vertebrates. we as yet lack detailed understanding of the developmental pathways in enough organisms to see which of the changes reflect current role and which reflect history and at what level. (1965). pp. the several craniofacial components have been shown to have a long independent history. E.Craniofacial growth. & ALLEY. M. In hindsight. C. Gans & H.
BELLAIRS. pp. 218. M. vol. the formerly anterior sensory capsules and the dorsal elements of the pharyngeal skeleton may then be considered as involving relatively late developmental events modifying the results of processes that arose in history. Patterns of growth in reptiles. W. vol. M. deriving from at least four disjunct portions in early vertebrates. post-term growth leads to relatively late closure of cranial sutures. & HARVEY. answers that may well be complementary to those furnished by the recent elegant studies about the detailed mechanisms utilized in the development of particular forms. E. In Biology of the Lampreys. they encounter changing demands during ontogeny. Morph. Neurol. (eds)
ANDREWS. the issue of brain size and mental capacity is one best avoided here.
The preceding summary should have documented that the mammalian craniofacial system is truly compound. P. Utilization of neural crest tissues as a source of preotic mesenchyme
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