The development of the trigeminal jaw adductor musculature in the grass snake Natrix natrix

The ontogenetic development of the jaw adductor musculature in Natrix natrix (L.) is described in detail and related to patterns of ossification in the skull. A comparison with the development of the jaw adductors in the lizard Podarcis sicula reveals some interesting differences of dynamics in the developing head. The problem of the establishment of topological relations of similarity (homology) in developing systems is discussed.
The homologies of the external jaw adductor compartments in lizards and snakes are revised. Early ontogenetic divergence explains the reversal of fibre direction in the anterior portion of the external adductor of snakes, and renders the homologization of that fibre bundle with part of the external adductor in lizards impossible.     

Phylogenetic interpretation of ontogenetic change: sorting out the actual and artefactual in an empirical case study of centrarchid fishes

Hypothesized relationships between ontogenetic and phylogenetic change in morphological characters were empirically tested in centrarchid fishes by comparing observed patterns of character development with patterns of character evolution as inferred from a representative phylogenetic hypothesis. This phylogeny was based on 56–61 morphological characters that were polarized by outgroup comparison. Through these comparisons, evolutionary changes in character ontogeny were categorized in one of eight classes (terminal addition, terminal deletion, terminal substitution, non-terminal addition, non-terminal deletion, non-terminal substitution, ontogenetic reversal and substitution). The relative frequencies of each of these classes provided an empirical basis from which assumptions underlying hypothesized relationships between ontogeny and phylogeny were tested. In order to test hypothesized relationships between ontogeny and phylogeny that involve assumptions about the relative frequencies of terminal change (e.g. the use of ontogeny as a homology criterion), two additional phylogenies were generated in which terminal addition and terminal deletion were maximized and minimized for all characters. Character state change interpreted from these phylogenies thus represents the maxima and minima of the frequency range of terminal addition and terminal deletion for the 8.7 × 10³⁶ trees possible for centrarchids. It was found for these data that terminal change accounts for c. 75% of the character state change. This suggests either that early ontogeny is conserved in evolution or that interpretation and classification of evolutionary changes in ontogeny is biased in part by the way that characters are recognized, delimited and coded. It was found that ontogenetic interpretation is influenced by two levels of homology decision: an initial decision involving delimitation of the character (the ontogenetic sequence), and the subsequent recognition of homologous components of developmental sequences. Recognition of phylogenetic homology among individual components of developmental sequences is necessary for interpretation of evolutionary changes in ontogeny as either terminal or non-terminal. If development is the primary criterion applied in recognizing individual homologies among parts of ontogenetic sequences, the only possible interpretation of phylogenetic differences is that of terminal change. If homologies of the components cannot be ascertained, recognition of the homology of the developmental sequence as a whole will result in the interpretation of evolutionary differences as substitutions. Particularly when the objective of a study is to discover how ontogeny has evolved, criteria in addition to ontogeny must be used to recognize homology. Interpretation is also dependent upon delimitation within an ontogenetic sequence. This is in part a function of the way that an investigator ‘sees’ and codes characters. Binary and multistate characters influence interpretation differently and predictably. The use of ontogeny for determining phylogenetic polarity as previously proposed rests on the assumptions that ancestral ontogenies are conserved and that character evolution occurs predominantly through terminal addition. It was found for these data that terminal addition may comprise a maximum of 51.9% of the total character state change. It is concluded that the ontogenetic criterion is not a reliable indicator of phylogenetic polarity. Process and pattern data are collected simultaneously by those engaged in comparative morphological studies of development. The set of alternative explanatory processes is limited in the process of observing development. These form necessary starting points for the research of developmental biologists. Separating ‘empirical’ results from interpretational influences requires awareness of potential biases in the course of character selection, coding and interpretation. Consideration of the interpretational problems involved in identifying and classifying phylogenetic changes in ontogeny leads to a re-evaluation of the purpose, usefulness and information conveyed by the current classification system. It is recommended that alternative classification schemes be pursued.     

Is there a direct ontogenetic criterion in systematics?

Much recent literature focuses on whether ontogenetic information can be used as a direct criterion for determining the polarity of character trasformations in systematic analysis. This paper reviews the relevant literature and concludes that the ontogenetic criterion is dependent on parsimony rather than the sequence observed during ontogeny. It is not, therefore, based on the discredited arguments of recapitulation. From the perspective of phyologenetic systematics the ontogenetic criterion is a valid means of polarizing character transformations that represents a special case of a broader methodology involving parsimony. The alternative perspective perspective of patttern cladistics holds that polarity should be contained within the data and not imposed upon it. Thus, ontogeny is not required to polarize characters, but ontogenetic information can generate unequivocal character interpretations in terms of the relative generality of related attributes, and in the sense that absence precedes presence. Furthermore, ontogeny is central to systematics, providing empirical evidence of character transformation, information on the whole life cycle and an escape from systematics being teleologically related to phylogenetic inference and the theory of evolution.     

Application of the biogenetic law to behavioral ontogeny: a test using nest architecture in paper wasps

General principles derived from studies of morphological ontogeny are useful in ethology. Behavioral ontogeny may be interpreted from an holistic view in which a series of behaviors is treated as an ontogeny toward a larger, complex, behavioral product. If the component behaviors are defined broadly, many taxa may be compared to find general principles that are not evident when behaviors are dissected to their smallest recognizable units. Flow charts can illustrate such general ontogenetic sequences in a manner that shows what sorts of modifications have evolved from the general pattern. Certain changes may illustrate forms of ontogenetic evolution that are well known for morphological development, such as addition or embellishment of terminal ontogenetic steps, or compression of ontogeny by acceleration or deletion of early steps. The major modifications in nest construction behavior of 28 genera of paper wasps are presented to test the predictions of the biogenetic rule with respect to character polarity. Cladistic analyses of separate morphological and behavioral data sets show that polarity is accurately inferred with respect to the five major patterns of nest construction in paper wasps.     

Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades

Middle ear ontogeny in Monodelphis domestica is investigated to understand better both the immediate consequences for suckling in a neonate marsupial and the epigenetic factors that constrain morphogenesis. Neonates of Monodelphis possess neither mammalian (dentarysquamosal) nor reptilian (quadrate-articular) jaw articulations, nor does the contact between the incus and crista parotica offer a joint surface ( contra Maier, 1987). Elasticity in Meckel's cartilage allows minimal deflection of the lower jaw. Observation of the developmental rate of the individual elements reveals that mandibular arch derivatives (malleus, incus and tensor tympani) are on a slightly faster ontogenetic schedule than hyoid arch derivatives (stapes and m. stapedius).     

Size-related changes in cranial morphology affect diet in the catfish Clariallabes longicauda

Within the catfish family Clariidae, species exist with different degrees of jaw adductor hypertrophy. This jaw adductor hypertrophy has been related to bite performance, in turn suggesting a link to dietary specialization. Thus, an increase in the degree of hypertrophy will likely be reflected in an increase in the amount of hard prey in the diet. In the present study, we examine the ontogenetic scaling of cranial structure and diet in a species of catfish with a moderate degree of jaw adductor hypertrophy, Clariallabes longicauda . Additionally, we investigate whether the observed changes in the morphology of the feeding system during growth are linked to changes in diet. The fish examined demonstrate a strong positively allometric growth of the jaw adductors, of head height and of maximal head width, suggesting that larger fish can feed on larger and harder prey. Dietary data confirm these hypotheses and reveal an increase in maximal prey size consumed, the proportion of large prey in the diet, and average prey hardness during ontogeny. Moreover, the observed changes in the proportion of large prey consumed and prey hardness are correlated with an increase in lower jaw width and maximal head width, respectively. An increase in the amount of evasive prey in the diet with fish size is correlated with an increase in hyoid length. In summary, not only size dependent, but also size-independent variation of the feeding system was associated with ontogenetic changes in diet in C. longicauda .  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 323–334.     

A quantitative approach to the cranial ontogeny of the puma

The cranial ontogeny of specialized mammals is relevant to the understanding of the connection of form and function in a developmental, ecological, and evolutionary context. As highly specialized carnivores, felids are of especial interest. We studied the postnatal ontogeny of the skull in Puma concolor (Mammalia: Carnivora: Felidae) using a quantitative approach. We interpreted our results in the light of a previous qualitative assessment of ontogenetic changes in the species. This represents one of the few integrative studies of skull development in any extant species of wild felids. We report patterns of multivariate allometry of 19 linear skull dimensions measured in 48 Argentine specimens. We examined the (jackknife resampled) departures from isometry as well as the interplay of isometric and allometric trends in shaping the puma skull. Both the qualitative and quantitative results indicate that the major ontogenetic changes are directly linked to cranial structures that support a developing masticatory apparatus and its associated jaw and neck musculature, which are essential for the action of canines and carnassials during the killing bite and slicing flesh. Sexual differences suggest allometric scaling (hypo- or hyper-morphosis) as key processes in the development of the puma skull.     

Stiffening the stingray skeleton - an investigation of durophagy in myliobatid stingrays (Chondrichthyes, batoidea, myliobatidae)

The stingray family Myliobatidae contains five durophagous (hard prey specialist) genera and two planktivorous genera. A suite of morphological features makes it possible for the hard prey specialists to crush mollusks and crustaceans in their cartilaginous jaws. These include: 1) flat, pavement-like tooth plates set in an elastic dental ligament; 2) multiple layers of calcified cartilage on the surface of the jaws; 3) calcified struts running through the jaws; and 4) a lever system that amplifies the force of the jaw adductors. Examination of a range of taxa reveals that the presence of multiple layers of calcified cartilage, previously described from just a few species, is a plesiomorphy of Chondrichthyes. Calcified struts within the jaw, called "trabecular cartilage," are found only in the myliobatid genera, including the planktivorous Manta birostris. In the durophagous taxa, the struts are concentrated under the area where prey is crushed, thereby preventing local buckling of the jaws. Trabecular cartilage develops early in ontogeny, and does not appear to develop as a direct result of the stresses associated with feeding on hard prey. A "nutcracker" model of jaw function is proposed. In this model, the restricted gape, fused mandibular and palatoquadrate symphyses, and asynchronous contraction of the jaw adductors function to amplify the closing force by 2-4 times.     

The early anomodont Venjukovia and the evolution of the anomodont skull

The skull morphology and function of the anomodont mammal-like reptile Venjukovia is described and compared with that of Patranomodon, Eodicynodon, Galeops and Diictodon. Changes in osteology and functional anatomy of these forms are noted.
It is concluded that the acquisition of herbivorous adaptations in the anomodonts may have occurred in the following sequence: division of the external adductor muscles of the jaw into a medial and lateral component, propalinal jaw movement, increased Moment Arm of the external adductors by raising the level of the jaw hinge, anterior migration of the adductor insertions, reduction of the size and number of teeth and acquisition of a horn covering to the jaws, elaboration of the external adductors and reduction of the internal adductors (pterygoideus muscles), and elaboration of palatal areas for mastication of food.
The first (in the morphological sense) committed herbivorous anomodont is identified as the South African form, Galeops. As far as anomodonts are concerned, the major correlate of successful herbivorous feeding is the acquisition of propaliny.
A chronology of character acquisition in the anomodonts cannot yet be drawn up since the stratigraphic correlation of Russian and South African sequences is uncertain. However, it appears that the transition from a generalized carnivore to a committed herbivore took place very rapidly compared to the species longevity of anomodonts.     

Comparative ontogeny of the feeding apparatus of sympatric drums (Perciformes: Sciaenidae) in the Chesapeake Bay

The anatomy of the feeding apparatus in fishes, including both oral and pharyngeal jaw elements, is closely related to the ecology of a species. During ontogeny, the oral and pharyngeal jaws undergo dramatic changes. To better understand how such ontogenetic changes occur and relate to the feeding ecology of a species, ontogenetic series of four closely related members of the family Sciaenidae (Cynoscion nebulosus, Cynoscion regalis, Micropogonias undulatus, and Leiostomus xanthurus) were examined. Sciaenids were selected because as adults they exhibit considerable specialization of the feeding apparatus correlated with differences in foraging habitats. However, it is not clear when during ontogeny the structural specializations of the feeding apparatus develop, and thereby enable early life history stage (ELHS) sciaenids to partition their foraging habitats. A regression tree was recovered from the analysis and three divergences were identified during ontogeny. There are no measurable differences in elements of the feeding apparatus until the first divergence at 8.4 mm head length (HL), which was attributed to differences in average gill filament length on the second ceratobranchial. The second divergence occurred at 14.1 mm HL and was associated with premaxilla length. The final divergence occurred at 19.8 mm HL and was associated with differences in the toothed area of the fifth certatobranchial. These morphological divergences suggest that ELHS sciaenids may be structurally able to partition their foraging habitats as early as 8.4 mm HL. J. Morphol. 277:183–195, 2016. © 2015 Wiley Periodicals, Inc.     

Bite performance in clariid fishes with hypertrophied jaw adductors as deduced by bite modeling

Within clariid fishes several cranial morphologies can be discerned. Especially within anguilliform representatives an increase in the degree of hypertrophy of the jaw adductors occurs. The hypertrophy of the jaw adductors and skeletal modifications in the cranial elements have been linked to increased bite force. The functional significance of this supposed increase in bite force remains obscure. In this study, biomechanical modeling of the cranial apparatus in four clariid representatives showing a gradual increase in the hypertrophy of the jaw adductors (Clarias gariepinus, Clariallabes melas, Channallabes apus, and Gymnallabes typus) is used to investigate whether bite force actually increased. Static bite modeling shows that the apparent hypertrophy results in an increase in bite force. For a given head size, the largest bite forces are predicted for C. apus, the lowest ones for C. gariepinus, and intermediate values are calculated for the other species. In addition, also in absolute measures differences in bite force remain, with C. apus biting distinctly harder than C. gariepinus despite its smaller head size. This indicates that the hypertrophy of the jaw adductors is more than just a correlated response to the decrease in absolute head size. Further studies investigating the ecological relevance of this performance difference are needed.     

ONTOGENY AND CHARACTER PHYLOGENY

Abstract— The doctrine of recapitulation was long ago exchanged for a view that ontogeny is orderly and recapitulates ancestral ontogenies. Only recently has the pattern of ontogeny, as a means for determining individual character phylogenies (polarities), been explicitly explored by Gareth Nelson and other cladists. Constraints on outgroup comparisons are suggested to apply to Nelson's rule equally, and the supposed distinction between "direct" and "indirect" methods is suggested to be nonexistent. Nelson's rule is concluded to measure character adjacency directly, but polarity indirectly. Nelson's (ontogenetic) rule is compared to the Outgroup Rule of Watrous and Wheeler, based on 60 postembryonic larval characters of three species of slime-mold beetles of the genus Agathidium ( onisemdes Palisot de Beauvois, pulchrum LeConte, aristerium Wheeler), and reference to larvae of Amsotoma basalts (Le Conte) as an outgroup. Polarities were hypothesized based on each rule and cladograms constructed with the microcomputer programs Henning86 (J. S. Farris) and CLADOS (K. C. Nixon). With levels of analytical error, or homoplasy, measured as the consistency index, the results were compared and the least homoplastic solutions preferred. It is concluded that the outgroup rule and Nelson's rule arc of about the same efficacy as criteria for polarity, and that each is ultimately justified on the basis of parsimony. The following hypothesis of relationships is accepted for the species studied: ( Anisotoma basalts + ( Agathidium oniscoides + ( Agathidium pulchrum + Agathidium arislerium ))).     

Ontogenetic scaling of bite force in lizards and turtles

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.     

The mixosaurid ichthyosaur Contectopalatus from the Middle Triassic of the German Basin

The skull of the mixosaurid species Contectopalatus atavus (Quenstedt, 1851-52) is the most bizarre of any known ichthyosaur. It possesses a very high sagittal crest formed by the nasal, frontal and parietal bones which grows higher during ontogeny. This skull structure - found to a lesser extent in the other mixosaurid genera Mixosaurus and Phalarodon - is a synapomorphy of the family Mixosauridae. It is here interpreted as correlated with a unique arrangement of the jaw adductor musculature among tetrapods, with the internal jaw adductors extending over most of the skull roof up to the external narial opening. This reconstruction would increase the biting force considerably and the hypothesis is supported by peculiarities of the dentition and jaws of Contectopalatus. Contectopalatus probably reached a length of about 5 meters. It is therefore the largest known mixosaurid and one of the largest Triassic ichthyosaurs. The general text-book picture of mixosaurs as small, rather unspecialized, primitive ichthyosaurs is incorrect. Mixosaurs were a highly specialized, uniquely adapted and very diverse ichthyosaur family, some members of which rank among the marine top predators of their time.     

Allometry and evolution in the galago skull

To probe the ontogenetic bases of morphological diversity across galagos, we performed the first clade-wide analyses of growth allometries in 564 adult and non-adult crania from 12 galagid taxa. In addition to evaluating if variation in galago skull form results from the differential extension/truncation of common ontogenetic patterns, scaling trajectories were employed as a criterion of subtraction to identify putative morphological adaptations in the feeding complex. A pervasive pattern of ontogenetic scaling is observed for facial dimensions across galagids, with 2 genera also sharing relative growth trajectories for masticatory proportions (Galago, Galagoides). As the facial growth series and adult data are largely coincidental, interspecific variation may result from character displacement and consequent selection for size differentiation among sister taxa. Derived configurations of the jaw joint and jaw muscle mechanical advantage in Otolemur and Euoticus appear to facilitate increased gape during scraping behaviors. Differences in aspects of masticatory growth and form characterizing these 2 genera highlight selection to uncouple shared ontogenetic patterns, which occurred via transpositions that retained ancestral scaling patterns. Due to the lack of increased robusticity of load-resisting mandibular elements in Otolemur and Euoticus, there is little evidence to suggest that exudativory in galagos results in correspondingly higher masticatory stresses.     

Testing the ontogenetic base for the transient model of inflorescence development

Backgrounds and Aims

Current research in plant science has concentrated on revealing ontogenetic processes of key attributes in plant evolution. One recently discussed model is the ‘transient model’ successful in explaining some types of inflorescence architectures based on two main principles: the decline of the so called ‘vegetativeness’ (veg) factor and the transient nature of apical meristems in developing inflorescences. This study examines whether both principles find a concrete ontogenetic correlate in inflorescence development.

Methods

To test the ontogenetic base of veg decline and the transient character of apical meristems the ontogeny of meristematic size in developing inflorescences was investigated under scanning electron microscopy. Early and late inflorescence meristems were measured and compared during inflorescence development in 13 eudicot species from 11 families.

Key Results

The initial size of the inflorescence meristem in closed inflorescences correlates with the number of nodes in the mature inflorescence. Conjunct compound inflorescences (panicles) show a constant decrease of meristematic size from early to late inflorescence meristems, while disjunct compound inflorescences present an enlargement by merging from early inflorescence meristems to late inflorescence meristems, implying a qualitative change of the apical meristems during ontogeny.

Conclusions

Partial confirmation was found for the transient model for inflorescence architecture in the ontogeny: the initial size of the apical meristem in closed inflorescences is consistent with the postulated veg decline mechanism regulating the size of the inflorescence. However, the observed biphasic kinetics of the development of the apical meristem in compound racemes offers the primary explanation for their disjunct morphology, contrary to the putative exclusive transient mechanism in lateral axes as expected by the model.     

Patterns of growth of the mandibular corpus in spotted hyenas (Crocuta crocuta) and cougars (Puma concolor)

Differences in jaw morphology among adult carnivorans are well established, but the ontogenetic mechanisms by which these differences arise are largely unexplored. Mandibular ontogeny in Crocuta crocuta and Puma concolor is analysed biomechanically using principles of beam theory. In each species, the development of cross-sectional properties of the mandibular corpus associated with rigidity under loading follows a biphasic pattern of growth. In early postnatal growth, deposition of cortical bone appears to be constrained by the overall weaker tissue with which juvenile skeletons are constructed and by the need to volumelrically accommodate the developing teeth within their bony crypts. Thus, this stage of growth is characterized by a net periosteal deposition of bone and a swelling of the medullary cavity. In late postnatal growth, the constraints on endosteal deposition of bone are relieved as the permanent teeth erupt; thus, cortical thicknesses increase sharply by periosteal expansion as well as medullary contraction. Finally, it is noted that basic differences in jaw construction between Crocuta and Puma appear to develop prenatally as they are largely in place at birth. Hence, postnatal development enhances, but does not soley contribute to, the biomechanical differences in the jaws of these species.     

The morphology and post-hatching development of the skull of Bolitoglossa nicefori (Caudata: Plethodontidae): developmental implications of recapitulation and repatterning

The cranial morphology of the direct-developing salamander Bolitoglossa nicefori and its post-hatching development are described and compared with that of other urodeles. Four stages of cranial development are defined on the basis of conspicuous events that occur during post-hatching ontogeny. The adult skull morphology of B. nicefori is similar to that of other plethodontids; however, some regions show interspecific variation. The post-hatching ontogeny of the skull and the stage of ossification observed in the hatchlings of B. nicefori show two important ontogenetic features: (1) a mosaic of early larval, metamorphic and post-metamorphic skull features in hatchlings, and (2) absence of characteristic larval elements in skull and hyoid apparatus. The distinctive stage of ossification in the hatchlings of B. nicefori could be caused by heterochronic changes in the ossification sequence, compared to the ontogeny of metamorphic salamanders. The possible heterochronic changes and the absence of larval traits are perhaps due to ontogenetic repatterning, yet without an obvious impact on the adult skull morphology (absence of morphological novelties). This might indicate a compartmentalized development. Further studies should be performed in order to establish the possible occurrence of recapitulatory patterns or ontogenetic repatterning in the skull morphogenesis of B. nicefori during its embryonic development.     

The trigeminal jaw adductors of primitive snakes and their homologies with the lacertilian jaw adductors

The trigeminal jaw adductor musculature of anilioid snakes is analysed. The group is characterised by primitive characters, viz. the presence of an extensive bodenaponeurosis and of a quadrate aponeurosis. A temporal tendon gives rise to superficial (lb) fibres which are not observed in other snakes: this may be a primitive or a derived feature.
Jaw adductor muscles in snakes are usually subdivided following their relative position in an antero–posterior direction. Lacertilian jaw adductors are subdivided in a transverse plane. A detailed comparison of the anilioid and primitive lacertilian jaw adductors establishes correspondences (homologies) of parts in the transverse plane in both groups. These homologies are corroborated by innervational patterns.
Platynotan lizards are widely accepted as potential snake ancestors. A comparison of homologue jaw adductors shows different evolutionary trends to characterise platynotan lizards and snakes. Theoretically, these findings do not rule out primitive platynotan lizards as snake ancestors. On the basis of the structure of jaw adductors, snakes are to be derived from a primitive lacertilian pattern, be it platynotan or not.