A preliminary analysis of correlations between chewing motor patterns and mandibular morphology across mammals

The establishment of a publicly-accessible repository of physiological data on feeding in mammals, the Feeding Experiments End-user Database (FEED), along with improvements in reconstruction of mammalian phylogeny, significantly improves our ability to address long-standing questions about the evolution of mammalian feeding. In this study, we use comparative phylogenetic methods to examine correlations between jaw robusticity and both the relative recruitment and the relative time of peak activity for the superficial masseter, deep masseter, and temporalis muscles across 19 mammalian species from six orders. We find little evidence for a relationship between jaw robusticity and electromyographic (EMG) activity for either the superficial masseter or temporalis muscles across mammals. We hypothesize that future analyses may identify significant associations between these physiological and morphological variables within subgroups of mammals that share similar diets, feeding behaviors, and/or phylogenetic histories. Alternatively, the relative peak recruitment and timing of the balancing-side (i.e., non-chewing-side) deep masseter muscle (BDM) is significantly negatively correlated with the relative area of the mandibular symphysis across our mammalian sample. This relationship exists despite BDM activity being associated with different loading regimes in the symphyses of primates compared to ungulates, suggesting a basic association between magnitude of symphyseal loads and symphyseal area among these mammals. Because our sample primarily represents mammals that use significant transverse movements during chewing, future research should address whether the correlations between BDM activity and symphyseal morphology characterize all mammals or should be restricted to this "transverse chewing" group. Finally, the significant correlations observed in this study suggest that physiological parameters are an integrated and evolving component of feeding across mammals.     

Cephalic muscle development in the Australian lungfish,Neoceratodus forsteri

Lungfishes are the extant sister group of tetrapods. As such, they are important for the study of evolutionary processes involved in the water to land transition of vertebrates. The evolution of a true neck, that is, the complete separation of the pectoral girdle from the cranium, is one of the most intriguing morphological transitions known among vertebrates. Other salient changes involve new adaptations for terrestrial feeding, which involves both the cranium and its associated musculature. Historically, the cranium has been extensively investigated, but the development of the cranial muscles much less so. Here, we present a detailed study of cephalic muscle development in the Australian lungfish, Neoceratodus forsteri, which is considered to be the sister taxon to all other extant lungfishes. Neoceratodus shows several developmental patterns previously described in other taxa; the tendency of muscles to develop from anterior to posterior, from their region of origin toward insertion, and from lateral to ventral/medial (outside‐in), at least in the branchial arches. The m.protractor pectoralis appears to develop as an extension of the most posterior m.levatores arcuum branchialium, supporting the hypothesis that the m.cucullaris and its derivatives (protractor pectoralis, levatores arcuum branchialium) are branchial muscles. We present a new hypothesis regarding the homology of the ventral branchial arch muscles (subarcualis recti and obliqui, transversi ventrales) in lungfishes and amphibians. Moreover, the morphology and development of the cephalic muscles confirms that extant lungfishes are neotenic and have been strongly influenced via paedomorphosis during their evolutionary history.     

Overview of FEED, the feeding experiments end-user database

The Feeding Experiments End-user Database (FEED) is a research tool developed by the Mammalian Feeding Working Group at the National Evolutionary Synthesis Center that permits synthetic, evolutionary analyses of the physiology of mammalian feeding. The tasks of the Working Group are to compile physiologic data sets into a uniform digital format stored at a central source, develop a standardized terminology for describing and organizing the data, and carry out a set of novel analyses using FEED. FEED contains raw physiologic data linked to extensive metadata. It serves as an archive for a large number of existing data sets and a repository for future data sets. The metadata are stored as text and images that describe experimental protocols, research subjects, and anatomical information. The metadata incorporate controlled vocabularies to allow consistent use of the terms used to describe and organize the physiologic data. The planned analyses address long-standing questions concerning the phylogenetic distribution of phenotypes involving muscle anatomy and feeding physiology among mammals, the presence and nature of motor pattern conservation in the mammalian feeding muscles, and the extent to which suckling constrains the evolution of feeding behavior in adult mammals. We expect FEED to be a growing digital archive that will facilitate new research into understanding the evolution of feeding anatomy.     

Post-weaning maternal effects and the evolution of female dominance in the spotted hyena

Mammalian societies in which females dominate males are rare, and the factors favouring the evolution of female dominance have yet to be clearly identified. We propose a new hypothesis for the evolution of female dominance and test its predictions with empirical data from the spotted hyena (Crocuta crocuta), a well-studied species characterized by female dominance. We suggest that constraints imposed by the development of a feeding apparatus specialized for bone cracking, in combination with the intensive feeding competition characteristic of spotted hyenas, led to the evolution of female dominance. Specifically, we propose that protracted development of the feeding apparatus in young hyenas led to selection for increased aggressiveness in females as a compensatory mechanism for mothers to secure food access for their young after weaning. Our analyses yielded results consistent with this hypothesis. Morphological and behavioural measurements indicate that skull development is indeed protracted in this species; spotted hyenas do not achieve adult skull size or feeding performance capabilities until after sexual maturity. The period between weaning and completed skull development is particularly challenging, as indicated by high mortality. Finally, maternal presence between weaning and full skull maturity, as well as the relative ability of females to aggressively displace conspecifics from food, are important determinants of offspring survival.     

Social organization in Eulipotyphla: evidence for a social shrew

Shrews and their close relatives (order Eulipotyphla) are typically considered to be solitary. This impacts our understanding of mammalian social evolution: (i) the ancestor of mammals is believed to have been shrew-like, and even though Eulipotyphla are not more basal than other mammalian orders, this might have been one reason why the first mammals have been assumed to be solitary-living; (ii) Eulipotyphla are the third largest mammalian order, with hundreds of species entering comparative analyses. We review primary field studies reporting the social organization of Eulipotyphla, doing a literature research on 445 species. Primary literature was only available for 16 of the 445 species. We found 56% of the studied species to be social (38% were living in pairs), which is in sharp contrast to the 0.5 and 8% reported in other databases. We conclude that the available information indicates that shrews are more sociable than generally believed. An interesting alternative hypothesis is that the mammalian ancestor might have been pair-living. To understand the social evolution of mammals, comparative studies must be based on reliable and specific information, and more species of all orders must be studied in the field.     

Encephalization and the evolution of longevity in mammals

Allometric principles account for most of the observed variation in maximum life span among mammals. When body-size effects are controlled for, most of the residual variance in mammalian life span can be explained by variations in brain size, metabolic rate and body temperature. It is shown that species with large brains for a given body size and metabolic rate, such as anthropoid primates, also have long maximum life spans. Conversely, mammals with relatively high metabolic rates and low levels of encephalization, as in most insectivores and rodents, tend to have short life spans. The hypothesis is put forward that encephalization and metabolic rate, which may govern other life history traits, such as growth and reproduction, are the primary determinants directing the evolution of mammalian longevity.     

Comparative Aspects of Proinsulin and Insulin Structure and Biosynthesis

This review summarizes currently available information on thecomposition and structure of vertebrate insulins and proinsulins.Consideration is given to the important structural featuresof insulin and its precursor that are involved in the functionand formation of the active hormone. Studies on the biosynthesisof insulin in teleost fishes indicate the existence of largersingle chain precursor forms similar to the mammalian proinsulins.Preliminary results of experiments on insulin biosynthesis inthe hagfish (Myxine glutinosa), which has the most primitiveislet parenchyma of all vertebrates, indicate the existenceof a similar biosynthetic mechanism. The major storage productin the B-cells in all the vertebrate species studies thus faris insulin rather than proinsulin. In fishes an intracellulartryspin-like enzyme may suffice to convert proinsulin to insulin,while in mammals a more complex mechanism involving both anendopeptidase and an exopeptidase is probably required. Conversionoccurs within the Golgi apparatus and newly formed secretorygranules in the B-cells. The similarity to the higher vertebrates in the biosynthesisand molecular structure of insulin in the primitive hagfishindicates that the properties and biological role of this hormonehave remained fairly constant throughout several hundred millionyears, or that its evolution has followed the same pattern inmost extant organisms despite considerable differences in theirorigin and living conditions. A hypothesis for the evolutionof insulin and of the B-cells based on the biosynthetic mechanisminvolving proinsulin and its conversion to insulin is brieflyconsidered.     

Neuromuscular control of prey capture in frogs.

While retaining a feeding apparatus that is surprisingly conservative morphologically, frogs as a group exhibit great variability in the biomechanics of tongue protraction during prey capture, which in turn is related to differences in neuromuscular control. In this paper, I address the following three questions. (1) How do frog tongues differ biomechanically? (2) What anatomical and physiological differences are responsible? (3) How is biomechanics related to mechanisms of neuromuscular control? Frog species use three non-exclusive mechanisms to protract their tongues during feeding: (i) mechanical pulling, in which the tongue shortens as its muscles contract during protraction; (ii) inertial elongation, in which the tongue lengthens under inertial and muscular loading; and (iii) hydrostatic elongation, in which the tongue lengthens under constraints imposed by the constant volume of a muscular hydrostat. Major differences among these functional types include (i) the amount and orientation of collagen fibres associated with the tongue muscles and the mechanical properties that this connective tissue confers to the tongue as a whole; and (ii) the transfer of intertia from the opening jaws to the tongue, which probably involves a catch mechanism that increases the acceleration achieved during mouth opening. The mechanisms of tongue protraction differ in the types of neural mechanisms that are used to control tongue movements, particularly in the relative importance of feed-forward versus feedback control, in requirements for precise interjoint coordination, in the size and number of motor units, and in the afferent pathways that are involved in coordinating tongue and jaw movements. Evolution of biomechanics and neuromuscular control of frog tongues provides an example in which neuromuscular control is finely tuned to the biomechanical constraints and opportunities provided by differences in morphological design among species.     

Variation in growth form and precocity at birth in eutherian mammals.

Using the flexible Chapman-Richards model for describing the growth curves from birth to adulthood of 69 species of eutherian mammals, we demonstrate that growth form differs among eutherian mammals. Thereby the commonly used Gompertz model can no longer be considered as the general model for describing mammalian growth. Precocial mammals have their peak growth rate earlier in the growth process than altricial mammals. However, the position on the altricial-precocial continuum accounts for most growth-form differences only between mammalian lineages. Within mammalian genera differences in growth form are not related to precocity at birth. This indicates that growth form may have been associated with precocity at birth early in mammalian evolution, when broad patterns of body development radiated. We discuss four non-exclusive interpretations to account for the role of precocity at birth on the observed variation in growth form among mammals. Precocial and altricial mammals could differ according to (i) the distribution of energy output by the mother, (ii) the ability of the young to assimilate the milk yield, (iii) the allocation of energy by the young between competing functions and (iv) the position of birth between conception and attainment of physical maturity.     

Evolution of sarcomeric myosin heavy chain genes: evidence from fish

Myosin heavy chain (MYH) is a major structural protein, integral to the function of sarcomeric muscles. We investigated both exon-intron organization and amino acid sequence of sarcomeric MYH genes to infer their evolutionary history in vertebrates. Our results were consistent with the hypothesis that a multigene family encoded MYH proteins in the ancestral chordate, one gene ancestral to human MYH16 and its homologues and another ancestral to all other vertebrate sarcomeric MYH genes. We identified teleost homologues of mammalian skeletal and cardiac MYH genes, indicating that the ancestors of those genes were present before the divergence of actinopterygians and sarcopterygians. Indeed, the ancestral skeletal genes probably duplicated at least once before the divergence of teleosts and tetrapods. Fish homologues of mammalian skeletal MYH are expressed in skeletal tissue and homologues of mammalian cardiac genes are expressed in the heart but, unlike mammals, there is overlap between these expression domains. Our analyses inferred two other ancestral vertebrate MYH genes, giving rise to human MYH14 and MYH15 and their homologues. Relative to the skeletal and cardiac genes, MYH14 and MYH15 homologues are characterized by evolution of intron position, differences in evolutionary rate between the functionally differentiated head and rod of the myosin protein, and possible evolution of function among vertebrate classes. Tandem duplication and gene conversion appear to have played major roles in the evolution of at least cardiac and skeletal MYH genes in fish. One outcome of this high level of concerted evolution is that different fish taxa have different suites of MYH genes, i.e., true orthologs do not exist.     

Morphological constraints in the digging apparatus of pocket gophers (Mammalia: Geomyidae)

The digging apparatus of pocket gophers offers a unique opportunity to examine morphological constraints within a historical context because relationships among extant taxa are well resolved and the features enhancing digging performance are relatively well understood. Structural and functional considerations suggest that the muscles associated with tooth- and claw-digging in pocket gophers are subjected to contrasting levels of morphological constraints. To assess this hypothesis, we analysed the bones and muscles of the jaws and forelimbs in four genera comprising five species of pocket gophers. Morphometric analyses were performed on 12 osteological measurements selected to reflect overall skull size, variation in rostral shape and procumbency, differences in overall length of the forelimbs and processes relating to the function of lever systems used in claw-digging. In addition, dissections were made of the jaw, hyoid, neck and all of the forelimb muscles excluding the intrinsic muscles of the manus. Results of our morphometric analyses corroborate the recent suggestion that pocket gophers encompass a wide range of morphological variation extending from claw-diggers to tooth-diggers. Myologically, however, we found structural variation only in the forelimb muscles, some of which may be advantageous for digging. No changes in jaw, neck and hyoid muscles, other than differences in muscle mass or those concordant with differences in rostral shape, were noted. These results support our hypothesis that constrasting levels of morphological constraint exist between the jaw and forelimb muscles of pocket gophers. We present a discussion of the structural and functional constraints on jaws and forelimbs in gophers as well as an analysis of historical constraints acting on this group, and perhaps on mammals in general.     

Complementation hypothesis: the necessity of a monoallelic gene expression mechanism in mammalian development

Gene expression from both parental alleles (biallelic expression) is beneficial in minimizing the occurrence of recessive genetic disorders in diploid organisms. However, imprinted genes in mammals display parent of origin-specific monoallelic expression. As some imprinted genes play essential roles in mammalian development, the reason why mammals adopted the genomic imprinting mechanism has been a mystery since its discovery. In this review, based on the recent studies on imprinted gene regulation we discuss several advantageous features of a monoallelic expression mechanism and the necessity of genomic imprinting in the current mammalian developmental system. We further speculate how the present genomic imprinting system has been established during mammalian evolution by the mechanism of complementation between paternal and maternal genomes under evolutionary pressure predicted by the genetic conflict hypothesis.     

Prey size and ingestion rate in raptors: importance for sex roles and reversed sexual size dimorphism

Compared to other birds, most raptors take large prey for their size, and feeding bouts are extended. However, ingestion rate has largely been overlooked as a constraint in raptors' foraging and breeding ecology. We measured ingestion rate by offering avian and mammalian prey to eighteen wild raptors temporarily kept in captivity, representing seven species and three orders. Ingestion rate was higher for small than for large prey, higher for mammalian than for avian prey, higher for large than for small raptors, and higher for wide-gaped than for narrow-gaped raptors. Mammalian prey were ingested faster by raptors belonging to species with mainly mammals in their diet than by raptors with mainly birds in their diet, but the drop in ingestion rate with increasing prey size was more rapid for the former than for the latter. We argue that the separate sex roles found in raptors, i.e. the male hunting and the female feeding the young, is a solution of the conflict between the prolonged feeding bouts at the nest, and the benefit of rapid resumption of hunting in general, and rapid return to the previous capture site in particular (the prey size hypothesis). Thus, the sex roles differ more when prey takes longer to feed, i.e. from insects to mammals to birds. We then argue that the reversed sexual size dimorphism in raptors, i.e. smaller males than females, results from a conflict between the benefit of being small during breeding to capture the smallest items with the highest ingestion rate among these agile prey types (mammals and bird), and the benefit of being large outside the breeding season to ensure survival by being able to include large items in the diet when small items are scarce (the ingestion rate hypothesis). This hypothesis explains the observed variation in reversed sexual size dimorphism among raptors in relation to size and type of prey, i.e. increasing RSD from insects to mammals to birds as prey.     

Limbs vs. Jaws: Can They Be Compared?

Current experimental research on mammalian limb muscle structureand function is compared to that on mammalian jaw muscles. Twomajor areas of comparison are stressed: structural and functional.Comparisons of limbs and jaws are made from the point of viewof the impact of recent studies on simple mechanical modelsof limb/jaw muscle function. Limb muscle structure is comparedto jaw muscles at the level of muscle architecture, muscle histochemicaland motor unit properties, and the organization of motor unitsinto neuromuscular compartments. Such comparisons reveal thatalthough limb muscles and jaw muscles might be organized insimilar ways, fundamental differences exist, both in terms ofmuscle structure and the functional conclusions which have beenbased on studies of muscle structure. The comparisons also demonstratethat much recent evidence from structural studies have had littledirect impact on simple models of muscle function but a muchlarger influence on the assumptions of the models. Comparisonsof limb/jaw muscle function from kinematic and EMG studies,indicate that many masticatory strategies are used by differentmammals but the basic problems of posture and locomotion havebeen met with essentially similar solutions, even among diversemammalian groups. The results of such comparisons demonstratethat both limb and jaw muscle function are sufficiently complexthat new or re-vitalized models are needed if the relationshipbetween structure and function are ever to be understood.     

Avian Jaw Function: Adaptation of the Seven–Muscle System and a Review

Avian jaw function is the most interesting part of the feeding apparatus, and essential in the life of birds. The usual seven jaw muscles in birds are highly adapted for diverse food-getting devices through muscular modifications as well as changes in kinesis of the skeletal components of the skull. In the first part I have described from an introspection of my earlier works, the functional morphology of the seven jaw muscles in different birds in four functional groups such as, adductors of the lower jaw, depressor of the lower jaw, protractors of the upper jaw and retractors-cum-adductors of the upper and lower jaws. Emphasis has been laid on the differential force production by these muscles, depending on the nature of their connective tissue attachments on the skeletal parts and changes in the kinesis of the skeletal parts. The contraction of the muscles and movements of the skeletal parts are rhythmically synchronized in such a way that their concerted action performs adaptively in different feeding adaptations. The differential force production by the one-joint and two-joint muscles in terms of ‘torque’ analysis is important in jaw kinesis. The second part of the text is a historical review of some notable works centred around the avian jaw muscles, jaw kinesis, tongue muscles, synchronization with the movements of the tongue apparatus and adaptational as well as evolutionary significance of the feeding apparatus in different feeding strategies.