Morphological evolution of the mammalian jaw adductor complex

The evolution of the mammalian jaw during the transition from non‐mammalian synapsids to crown mammals is a key event in vertebrate history and characterised by the gradual reduction of its individual bones into a single element and the concomitant transformation of the jaw joint and its incorporation into the middle ear complex. This osteological transformation is accompanied by a rearrangement and modification of the jaw adductor musculature, which is thought to have allowed the evolution of a more‐efficient masticatory system in comparison to the plesiomorphic synapsid condition. While osteological characters relating to this transition are well documented in the fossil record, the exact arrangement and modifications of the individual adductor muscles during the cynodont–mammaliaform transition have been debated for nearly a century. We review the existing knowledge about the musculoskeletal evolution of the mammalian jaw adductor complex and evaluate previous hypotheses in the light of recently documented fossils that represent new specimens of existing species, which are of central importance to the mammalian origins debate. By employing computed tomography (CT) and digital reconstruction techniques to create three‐dimensional models of the jaw adductor musculature in a number of representative non‐mammalian cynodonts and mammaliaforms, we provide an updated perspective on mammalian jaw muscle evolution. As an emerging consensus, current evidence suggests that the mammal‐like division of the jaw adductor musculature (into deep and superficial components of the m. masseter, the m. temporalis and the m. pterygoideus) was completed in Eucynodontia. The arrangement of the jaw adductor musculature in a mammalian fashion, with the m. pterygoideus group inserting on the dentary was completed in basal Mammaliaformes as suggested by the muscle reconstruction of Morganucodon oehleri. Consequently, transformation of the jaw adductor musculature from the ancestral (‘reptilian’) to the mammalian condition must have preceded the emergence of Mammalia and the full formation of the mammalian jaw joint. This suggests that the modification of the jaw adductor system played a pivotal role in the functional morphology and biomechanical stability of the jaw joint.     

Morphological analysis of tendinous structure in the American alligator jaw muscles

In the American alligator, the jaw muscles show seven bundles of tendinous structure: cranial adductor tendon, mandibular adductor tendon, lamina anterior inferior, trap-shaped lamina lateralis, lamina intramandibularis, lamina posterior, and depressor mandibular tendon (originating from the musculus depressor mandibulae, m. pseudotemporalis, m. adductor mandibulae posterior, m. adductor mandibulae externus, m. intramandibularis, m. pterygoideus anterior, and m. pterygoideus posterior). These tendinous structures are composed of many collagen fibrils and elastic fibers; however, the distributions and sizes of the fibers in these tendinous components differ in comparison with those of other masticatory muscles. The differences of these properties reflect the kinetic forces or the stretch applied to each tendon by the muscle during jaw movements in spite of the simple tendon-muscle junctions. © 1993 Wiley-Liss, Inc.     

Morphological convergence of pharyngeal jaw structure in durophagous perciform fish

This study investigated the ecomorphology of pharyngeal jaw structure and durophagy in three families of marine teleosts: the Sciaenidae, Haemulidae and Carangidae. Regressions of the bone and muscle mass of pharyngeal jaws were generated to elucidate the differences associated with eating hard-bodied and soft-bodied prey; within-family comparisons revealed significant differences in masses of bones and muscles involved with processing the former. Generally, the durophagous species − Trachinotus carolinus (Carangidae), Pogonias cromis (Sciaenidae) and Anisotremus surinamensis (Haemulidae) − had heavier and stronger pharyngeal toothplates and larger protractor pectoralis muscles, with masses of these musculoskeletal elements ranging from five times to nearly an order of magnitude larger than those of their soft-prey feeding relatives. Pogonias cromis and T. carolinus demonstrate convergence in the ontogeny and morphological modification of the pharyngeal toothplates and protractor pectoralis muscles that enhance crushing ability. In the Haemulidae, moderate size increases in a few pharyngeal jaw elements (and larger overall body size in A. surinamensis ) are sufficient for durophagy. Morphospace analysis of six species from the three families illustrates the strong functional association between the biomechanical properties of prey and the relative sizes of biting and transport mechanisms.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 147−165.     

Morphological functions of gibberellins in leptosporangiate fern gametophytes: insights into the evolution of form and gender expression

In addition to genetic load, the induction of maleness in leptosporangiate gametophytes by the pheromone antheridiogen may facilitate rates of outcrossing similar to those found in angiosperms. The antheridiogens that have been chemically identified are similar to gibberellins and probably evolved from this common plant hormone. The purposes of this study were to determine the functions of endogenous gibberellins in morphological development and gender expression in leptosporangiate fern gametophytes and to elucidate how antheridiogens may have evolved from gibberellin precursors. We grew gametophytes of Osmunda regalis and Athyrium filix‐femina on nutrient agar enriched with APOGEE, which blocks gibberellin synthesis. Osmunda regalis is a member of Osmundaceae, the only family in Osmundales, the sister group of all remaining extant leptosporangiate ferns. This family possesses a male‐first gender in isolation and lacks any known antheridiogen systems. In contrast, A. filix‐femina is a member of a derived family, Woodsiaceae, which possesses antheridiogen systems. Disruption of gibberellin synthesis retarded notch development and expression of both maleness and femaleness (i.e. gender status) in both species. On the basis of these results, we offer a simple model of gametophyte evolution driven by gender‐based fitness gain curves and the influence of exogenous gibberellins. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159 , 599–615.     

The evolution of encephalization in caniform carnivorans

A weighted-average model, which reliably estimates endocranial volume from three external measurements of the neurocranium of extant taxa in the mammalian order Carnivora, was tested for its applicability to fossil taxa by comparing model-estimated endocranial volumes to known endocast volumes. The model accurately reproduces endocast volumes for a wide array of fossil taxa across the crown radiation of the Carnivora, three stem carnivoramorphan taxa, and Pleistocene fossils of two extant species. Applying this model to fossil taxa without known endocast volumes expanded the sample of fossil taxa with estimated brain volumes in the carnivoran suborder Caniformia from 11 to 60 taxa. This then allowed a comprehensive assessment of the evolution of relative brain size across this clade. An allometry of brain volume to body mass was calculated on phylogenetically independent contrasts for the set of extant taxa, and from this, log-transformed encephalization quotients (logEQs) were calculated for all taxa, extant, and fossil. A series of Mann-Whitney tests demonstrated that the distributions of logEQs for taxa early in caniform evolutionary history possessed significantly lower median logEQs than extant taxa. Median logEQ showed a pronounced shift around the Miocene-Pliocene transition. Support tests, based on likelihood ratios, demonstrated that the variances of these distributions also were significantly lower than among modern taxa, but logEQ variance increased gradually through the history of the clade, not abruptly. Reconstructions of ancestral logEQs using weighted squared-change parsimony demonstrate that increased encephalization is observed across all major caniform clades (with the possible exception of skunks) and that these increases were achieved in parallel, although an "ancestor-descendant differencing" method could not rule out drift as a hypothesis. Peculiarities in the estimated logEQs for the extinct caniform family Amphicyonidae were also investigated; these unusual patterns are likely due to a unique allometry in scaling brain to body size in this single clade.     

Modeling the occupancy of sympatric carnivorans in a Mediterranean ecosystem

Site occupancy provides a reasonable estimate of population status and trends, and it also provides an unbiased, cost-effective alternative method for large-scale, multispecies monitoring programs. In this study, we used camera-trapping data to determine carnivoran occupancy and associated environmental factors in Serra da Malcata Nature Reserve, Portugal. The study was intended as a precursor of further long-term multispecies monitoring programs. We estimated carnivoran species occupancy using a likelihood-based method, using the software PRESENCE. The major conclusions of the study were (1) fox occupancy tends to be independent of environmental factors; (2) stone marten occupancy is related with habitat variables, landscape structure, and preys; (3) common genet occupancy is related to broad leaf formations and preys; and (4) mongoose occupancy is higher in extensive areas of shrub habitats. Methodologically, we demonstrated the importance of modeling detection probabilities for species with low or variable detection rates. In the future, monitoring programs could benefit from incorporating estimates of detection probabilities into their design and analysis.     

Repeated loss of frontal sinuses in arctoid carnivorans

Many mammal skulls contain air spaces inside the bones surrounding the nasal chamber including the frontal, maxilla, ethmoid, and sphenoid, all of which are called paranasal sinuses. Within the Carnivora, frontal sinuses are usually present, but vary widely in size and shape. The causes of this variation are unclear, although there are some functional associations, such as a correlation between expanded frontal sinuses and a durophagous diet in some species (e.g., hyenas) or between absent sinuses and semiaquatic lifestyle (e.g., pinnipeds). To better understand disparity in frontal sinus morphology within Carnivora, we quantified frontal sinus size in relationship to skull size and shape in 23 species within Arctoidea, a clade that is ecologically diverse including three independent invasions of aquatic habitats, by bears, otters, and pinnipeds, respectively. Our sampled species range in behavior from terrestrial (rarely or never forage in water), to semiterrestrial (forage in water and on land), to semiaquatic (forage only in water). Results show that sinuses are either lost or reduced in both semiterrestrial and semiaquatic species, and that sinus size is related to skull size and shape. Among terrestrial species, frontal sinus size was positively allometric overall, but several terrestrial species completely lacked sinuses, including two fossorial badgers, the kinkajou (a nocturnal, arboreal frugivore), and several species with small body size, indicating that factors other than aquatic habits, such as space limitations due to constraints on skull size and shape, can limit sinus size and presence. J. Morphol. 276:22–32, 2015. © 2014 Wiley Periodicals, Inc.     

Morphological investigation of the deep pineal of the rat

Summary The results presented here reveal that in adult Sprague-Dawley and Wistar rats the pineal gland represents a complex rather than a single organ. Regularly one can distinguish (i) pineal tissue in the intercommissural region as a deep pineal, (ii) a superficial pineal, which represents the major part of the pineal complex, and (iii) nearly always a parenchymal stalk of variable length. The volume of the deep pineal with the adjacent parenchymal stalk exhibits great interindividual variation. It amounts to 127±39×10⁵ m³ (mean ±standard deviation). The histological appearance of the deep and superficial pineal tissue is fairly similar. The intrinsic cells of the deep and superficial pineal differ in nuances only. Karyometry reveals that the nuclear volumes of the intrinsic cells of the deep pineal are very variable ranging from 90–450 m³, with a mean value of 207 m³. The changes over a period of 24 h reach statistical significance.Supported by the Deutsche Forschungsgemeinschaft (Grant Vo 135/4) within the Schwerpunktprogramm NeuroendokrinologieThis paper is an abridged version of a thesis submitted for obtaining the degree of Dr. med., Fachbereich Medizin, University of Mainz     

Influence of body mass on the shape of forelimb in musteloid carnivorans

In the majority of mammals, the limbs are positioned under the body and play an important role in gravitational support, allowing the transfer of the load and providing stability to the animal. For this reason, an animal's body mass likely has a significant effect on the shape of its limb bones. In the present study, we investigate the influence of body mass variation on the shape of the three long bones of the forelimb in a group of closely‐related species of mammals: the musteloid carnivorans. We use geometric morphometric techniques to quantify forelimb shape; then estimate phylogenetic signal in the shape of each long bone; and, finally, we apply an independent contrasts approach to assess evolutionary associations between forelimb shape and body mass. The results obtained show that body mass evolution is tightly coordinated with the evolution of forelimb shape, although not equally in all elements. In particular, the humeral and radial shapes of heavier species appear better suited for load bearing and load transmission than the ulna. Nevertheless, our results also show that body mass influences only part of forelimb long bone shape and that other factors, such as locomotor ecology, must be considered to fully understand forelimb evolution. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 91–103.     

Locomotor correlates of the scapholunar of living and extinct carnivorans

The relationship of carpal morphology to ecology and habitat is under studied in carnivorans and more generally in mammals. Here, we use 3D-scanning techniques to assess the usefulness of a carpal bone, the scapholunar, in carnivorans to reflect ecology and habitat, and to reconstruct the ecology of five extinct carnivorans from two fossil sites: Rancho La Brea and Natural Trap Cave. We 3D-scanned scapholunars and measured articular surface areas and angles between articular facets using GeoMagic and Rhino 3D-software. We analyzed the difference in these metrics using multivariate analysis of variance and discriminant function analysis. Results show that the scapholunar reflects ecological signal, with clear groupings of cursorial carnivorans and grappling/climbing carnivorans; however, phylogenetic signal was also present in the results with hyaenids, canids, and large felids in distinct morphospaces. Extinct species Miracinonyx trumani (American cheetah) and Smilodon fatalis (sabertooth cat) showed surprising results with M. trumani grouping with pantherines instead of Acinonyx or Puma, suggesting it runs but still retains the ability to grapple prey. S. fatalis groups with pantherines, but also shows some unique adaptations, suggesting it had a different range of wrist motion than living cats. Overall, the scapholunar is a good indicator of ecology and functional morphology and can be another tool to use in modern and fossil carnivorans to reconstruct extinct ecologies and locomotor behaviors.     

Costs of carnivory: tooth fracture in Pleistocene and Recent carnivorans

Large, carnivorous mammals often break their teeth, probably as a result of tooth to bone contact that occurs when carcasses are consumed more fully, a behaviour likely to occur under conditions of food stress. Recent studies of Pleistocene predators revealed high numbers of teeth broken in life, suggesting that carcass utilization and, consequently, food competition was more intense in the past than at present. However, the putative association between diet and tooth fracture frequency was based on a small sample of large, highly carnivorous species. In the present study, a greater diversity of extant carnivorans is sampled, including insectivorous, omnivorous, and carnivorous forms, ranging in size from weasels to tigers. Species that habitually consume hard foods (bones, shells) had the highest fracture frequencies, followed by carnivores, and then insectivorous and/or omnivorous species. Predator and prey sizes were not associated with tooth fracture frequency, but more aggressive species did break their teeth more often. Comparison of the modern sample with five Pleistocene species confirms the previous finding of higher tooth breakage in the past, although some extant species have fracture frequencies that approach those of extinct species. Thus, the Pleistocene predator guild appears to have been characterized by relatively high levels of competition that are rarely observed today.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 68–81.     

Morphological aspects of the development of swimming and feeding functions in the milkfishChanos chanos

Development of swimming and feeding abilities based on morphological development of larval and early juvenileChanos chanos was investigated. In larvae smaller than about 6.5 mm SL, mechanical supports of fins and branchial arches were in a primordial stage of development. Supports and rays of the vertical fins and branchial arches rapidly developed from 6.5 mm SL, and all components appeared by about 10.5 mm SL. Thereafter body depth proportion changed and the supports and rays of the paired fins and gill-rakers developed. These developmental events were nearly or totally completed by about 17 mm SL, and we concluded that the larvae transformed to juveniles at this size. By this time, the mode of swimming of the fish shifted from undulating locomotion to caudal propulsion and that of feeding from swallowing paniculate food to filtering and concentrating substrate food matters using gill-rakers and the epibranchial organ. One of the most characteristic, and well-known, phenomena in the life history ofChanos chanos is the mass occurrence in the surf zone of postlarvae of a limited size range. In view of the scheme of the development of mechanical supports of the body and fins, they may acquire a swimming ability strong enough to move against the current only upon reaching about 10.5 mm SL, and if active shoreward migration of the larvae occurs, it is only during the late period of their journey from the spawning grounds to the shore. The sudden disappearance from the surf zone of larvae larger than 15–16 mm SL is obviously related to a change in food habit.     

Morphological study of nerve endings in jaw muscles of post-hatching American alligators (Alligator mississippiensis)

Two months after hatching, the fibers of the jaw muscles of the American alligator are associated with three types of nerve terminals namely, plates, simple plates, and grape endings. Simple plate endings are mainly observed on the small muscle fibers. Grape-type endings are found on muscle fibers that resemble the tonic fibers of garter snakes (Hess, Am. J. Anat., '63). Most terminals are plate endings and account for 53.7–74.7% of terminals per muscle. Fibers with grape-type endings were found in all the jaw muscles studied; they lack well organized T-systems, M-lines, and post-junctional sarcolemmal folds, as well as irregularly distributed small of fibrils, and zigzag Z-lines. The properties of nerve endings of the American alligator indicate that M. depressor mandibulae, M. pseudotemporalis, and M. pterygoideus posterior have primary roles in jaw movements. M. pterygoideus anterior and M. intramandibularis contribute mainly to postural adjustments of the jaws. The multiplicity of nerve terminals in the jaw muscles of American alligators contrasts with the simple movements of their jaws. © 1994 Wiley-Liss, Inc.