Conserved relative timing of cranial ossification patterns in early mammalian evolution

We analyzed a comprehensive data set of ossification sequences including seven marsupial, 13 placental and seven sauropsid species. Data are provided for the first time for two major mammalian clades, Chiroptera and Soricidae, and for two rodent species; the published sequences of three species were improved with additional sampling. The relative timing of the onset of ossification in 17 cranial elements was recorded, resulting in 136 event pairs, which were treated as characters for each species. Half of these characters are constant across all taxa, 30% are variable but phylogenetically uninformative, and 19% potentially deliver diagnostic features for clades of two or more taxa. Using the conservative estimate of heterochronic changes provided by the program Parsimov, only a few heterochronies were found to diagnose mammals, marsupials, or placentals. A later onset of ossification of the pterygoid with respect to six other cranial bones characterizes therian mammals. This result may relate to the relatively small size of this bone in this clade. One change in relative onset of ossification is hypothesized as a potential human autapomorphy in the context of the sampling made: the earlier onset of the ossification of the periotic with respect to the lacrimal and to three basicranial bones. Using the standard error of scaled ranks across all species as a measure of each element's lability in developmental timing, we found that ossification of early, middle, and late events are similarly labile, with basicranial traits the most labile in timing of onset of ossification. Despite marsupials and placental mammals diverging at least 130 Ma, few heterochronic shifts in cranial ossification diagnose these clades.     

Skeletal development in the African elephant and ossification timing in placental mammals

We provide here unique data on elephant skeletal ontogeny. We focus on the sequence of cranial and post-cranial ossification events during growth in the African elephant (Loxodonta africana). Previous analyses on ossification sequences in mammals have focused on monotremes, marsupials, boreoeutherian and xenarthran placentals. Here, we add data on ossification sequences in an afrotherian. We use two different methods to quantify sequence heterochrony: the sequence method and event-paring/Parsimov. Compared with other placentals, elephants show late ossifications of the basicranium, manual and pedal phalanges, and early ossifications of the ischium and metacarpals. Moreover, ossification in elephants starts very early and progresses rapidly. Specifically, the elephant exhibits the same percentage of bones showing an ossification centre at the end of the first third of its gestation period as the mouse and hamster have close to birth. Elephants show a number of features of their ossification patterns that differ from those of other placental mammals. The pattern of the initiation of the ossification evident in the African elephant underscores a possible correlation between the timing of ossification onset and gestation time throughout mammals.     

The ontogeny of cross‐sex genetic correlations: an analysis of patterns

The independent evolution of males and females is typically constrained by shared genetic variance. Despite substantial research, we still know little about the evolution of cross‐sex genetic covariance and its standardized measure, the cross‐sex genetic correlation (r_MF). In particular, it is unclear if r_MF tend to vary with age. We compiled 28 traits for which ontogenetic trends in r_MF were documented. Decreases in r_MF with age were observed significantly more often than increases and the mean effect size for the relationship between r_MF and age was large and negative. This suggests that sexual dimorphism (SD) may typically evolve more readily for phenotypes expressed later in ontogeny and that evolutionary inferences related to the evolution of SD should be limited to the ontogenetic stage at which r_MF was estimated. Knowledge about ontogenetic variation in r_MF should help improving our understanding of evolutionary patterns related to SD and the resolution of intralocus sexual conflicts.     

The tri-segmented limbs of therian mammals: kinematics, dynamics, and self-stabilization--a review

The evolution of therian mammals is to a large degree marked by changes in their motion systems. One of the decisive transitions has been from the sprawled, bi-segmented to the parasagittal, tri-segmented limb. Here, we review aspects of the tri-segmented limb in locomotion which have been elucidated in our research groups in the last 10 years. First, we report the kinematics of the tri-segmented therian limb from mouse to elephant in order to explore general principles of the therian limb configuration and locomotion. Torques will be reported from a previous paper (Witte et al., 2002. J Exp Biol 205:1339-1353) for a better understanding of the anti-gravity work of all limb joints. The stability of a limb in z-configuration will be explained and its advantage with respect to other potential solutions from modeling will be discussed. Finally, we describe how the emerging concept of self-stability can be explained for a tri-segmented leg template and how it affects the design of the musculoskeletal system and the operation of legs during locomotion. While locomotion has been considered as mainly a control problem in various disciplines, we stress the necessity to reduce control as much as possible. Central control can be cheap if the limbs are "intelligent" by means of their design. Gravity-induced movements and self-stability seem to be energy-saving mechanisms.     

Origin of the tooth-replacement pattern in therian mammals: evidence from a 110 Myr old fossil

Living placental and marsupial mammals (therians) use distinctive tooth-replacement patterns that have not yet been traced back fully to their time of divergence in the Early Cretaceous (>100 Myr ago). Slaughteria eruptens, a small 110 Myr old fossil mammal from Texas, USA, is near the base of that divergence. Using ultra-high-resolution X-ray CT analysis we demonstrate that Slaughteria preserves an unrecognized pattern of tooth replacement with simple posterior premolars replacing molariform precursors. Differing from both placentals that have a more complex posterior adult premolar, and from marsupials, in which only one premolar is replaced, Slaughteria provides the first direct evidence of a tooth-replacement pattern that is plausible for the common ancestor of all therians. By our interpretation Slaughteria has only one adult molar in place and contains two mental foramina in the jaw, thus changing characters that are critical to reconstruction of mammalian relationships and to species discrimination and interpretations of diversity for Early Cretaceous mammals.     

Hunter-gatherer postcranial robusticity relative to patterns of mobility, climatic adaptation, and selection for tissue economy

Human skeletal robusticity is influenced by a number of factors, including habitual behavior, climate, and physique. Conflicting evidence as to the relative importance of these factors complicates our ability to interpret variation in robusticity in the past. It remains unclear how the pattern of robusticity in the skeleton relates to adaptive constraints on skeletal morphology. This study investigates variation in robusticity in claviculae, humeri, ulnae, femora, and tibiae among human foragers, relative to climate and habitual behavior. Cross-sectional geometric properties of the diaphyses are compared among hunter-gatherers from southern Africa (n = 83), the Andaman Islands (n = 32), Tierra del Fuego (n = 34), and the Great Lakes region (n = 15). The robusticity of both proximal and distal limb segments correlates negatively with climate and positively with patterns of terrestrial and marine mobility among these groups. However, the relative correspondence between robusticity and these factors varies throughout the body. In the lower limb, partial correlations between polar second moment of area (J(0.73)) and climate decrease from proximal to distal section locations, while this relationship increases from proximal to distal in the upper limb. Patterns of correlation between robusticity and mobility, either terrestrial or marine, generally increase from proximal to distal in the lower and upper limbs, respectively. This suggests that there may be a stronger relationship between observed patterns of diaphyseal hypertrophy and behavioral differences between populations in distal elements. Despite this trend, strength circularity indices at the femoral midshaft show the strongest correspondence with terrestrial mobility, particularly among males.     

Morphology of the inner ear of mammals in ontogeny

In both phylogenesis and ontogenesis, the inner ear is formed first as a core, which, phylogenetically, is the most ancient part of the peripheral region of the auditory system. Along with the development of the inner ear, other links of different evolutionary ages (the auricle is a phylogenetically young link) begin to form in the peripheral auditory system.     

Comparative analysis of the peroxidase activity of myoglobins in mammals

Studies have been made on the peroxidase activity of metmyoglobins in animals from various ecological groups--the horse Equus caballus, cattle Bos taurus, beaver Castor fiber, otter Lutra lutra, mink Mustela vison and dog Canis familiaris. It was found that the level of this activity in diving animals depends on the duration of their diving, whereas in terrestrial species--on the strength of muscular contraction.     

Maturation of the retinal structures in the ontogeny of mammals

Using various neurohistological, electronmicroscopic, cytochemical and electrophysiological techniques, studies have been made on the development of peripheral visual pathways in human subjects and some homoiotherm animals (pigeon Columba livia, cats, rabbits). Heterochronous maturation of the conducting pathways in the retina was observed. The data obtained on rabbits suggest that heterochronous maturation of the receptors accounts for heterochronous differentiation of various elements within the system retina--visual cortex.     

The relative timing of the origin of flight and endothermy: evidence from the comparative biology of birds and mammals.

Evidence from the comparative biology of living birds and mammals is used to address the question ‘which came first, flight or endothermy?’. Birds and mammals have evolved different solutions to the problems of high energy flow demanded by endothermy. The heavy apparatus needed for processing food to allow the rapid assimilation of energy is housed in the head of mammals, but low down in the bird's body. The primitive inefficient tidal-flow system of ventilation is simply enlarged in mammals, but is replaced in birds by a lighter uni-flow system through air sacs and parabronchi. Birds avoid the weight problems associated with the mammalian systems of viviparity and lactation by nourishing their young with large quantities of yolk within the egg and an unprocessed diet after hatching. The apparent adaptedness for flight of the avian systems suggests that in the animals ancestral to birds the adaptations for high energy flow were constrained from the start by the need for aerodynamic stability, i.e. flight was initiated before endothermy. The implications of this conclusion for the origin of flight and feathers are discussed.     

Metabolic profile of the perivertebral muscles in small therian mammals: implications for the evolution of the mammalian trunk musculature

In order to gain a better understanding of the ancestral properties of the perivertebral muscles of mammals, this study investigated the fiber type composition of these muscles in six small, extant therians (two metatherians and four eutherians) similar in body shape to early mammals. Despite a few species-specific differences, the investigated species were very similar in their overall distribution of fiber types indicating similar functional demands on the back muscles in mammals of this body size and shape. Deep and short, mono- or multisegmental muscles (i.e., mm. interspinales, intermammillares, rotatores et intertransversarii) consistently showed the highest percentage of slow, oxidative fibers implying a function as local stabilizers of the vertebral column. Superficial and large, polysegmental muscles (i.e., mm. multifidus, sacrospinalis, iliopsoas et psoas minor) were predominantly composed of fast, glycolytic fibers suggesting they function to both globally stabilize and mobilize the spine during rapid non-locomotor and locomotor activities. Some muscles contained striking accumulations of oxidative fibers in specific regions (mm. longissimus et quadratus lumborum). These regions are hypothesized to function independently from the rest of the muscle belly and may be comparable in their functionality to regionalized limb muscles. The deep, central oxidative region in the m. longissimus lumborum appears to be a general feature of mammals and likely serves a proprioceptive function to control the postural equilibrium of the pelvic girdle and lumbar spine. The potential functions of the m. quadratus lumborum during ventilation and ventral stabilization of the vertebral column are discussed. Because representatives of the stem lineage of mammals were comparable in their body proportions and probably also locomotor parameters to the species investigated here, I suggest that the described fiber type distribution is representative of the ancestral condition in mammals. The origin of mammals was associated with a substantial enlargement of the epaxial muscles and the addition of subvertebral muscle mass. Because this novel muscle mass is mainly composed of fast, glycolytic fibers in extant species, it is plausible that these changes were associated with the evolution of increased sagittal mobility in the posterior trunk region in the therapsid ancestors of mammals. The caudally increasing role of sagittal bending in body propulsion is consistent with the overall increase in the percentage of glycolytic fibers in the cranio-caudal direction. The evolution of mammals was also associated with a loss of ribs in the posterior region of the trunk. This loss of ribs is thought to have decreased the stability of the posterior trunk, which may explain the observed greater oxidative capacity of the caudal local stabilizers. The increased need for postural feedback in the more mobile lumbar region may also explain the evolution of the proprioceptive system in the m. longissimus lumborum. Furthermore, the anatomical subdivision of the transversospinal muscle into several smaller muscle entities is suggested to facilitate their functional specialization.     

Mechanobiological modeling of endochondral ossification: an experimental and computational analysis

Long bone formation starts early during embryonic development through a process known as endochondral ossification. This is a highly regulated mechanism that involves several mechanical and biochemical factors. Because long bone development is an extremely complex process, it is unclear how biochemical regulation is affected when dynamic loads are applied, and also how the combination of mechanical and biochemical factors affect the shape acquired by the bone during early development. In this study, we develop a mechanobiological model combining: (1) a reaction–diffusion system to describe the biochemical process and (2) a poroelastic model to determine the stresses and fluid flow due to loading. We simulate endochondral ossification and the change in long bone shapes during embryonic stages. The mathematical model is based on a multiscale framework, which consisted in computing the evolution of the negative feedback loop between Ihh/PTHrP and the diffusion of VEGF molecule (on the order of days) and dynamic loading (on the order of seconds). We compare our morphological predictions with the femurs of embryonic mice. The results obtained from the model demonstrate that pattern formation of Ihh, PTHrP and VEGF predict the development of the main structures within long bones such as the primary ossification center, the bone collar, the growth fronts and the cartilaginous epiphysis. Additionally, our results suggest high load pressures and frequencies alter biochemical diffusion and cartilage formation. Our model incorporates the biochemical and mechanical stimuli and their interaction that influence endochondral ossification during embryonic growth. The mechanobiochemical framework allows us to probe the effects of molecular events and mechanical loading on development of bone.     

Heterochronic patterns in primate evolution: evidence from endochondral ossification

Heterochrony (evolutionary modifications in developmental timing and/or rates) is widely recognized as an important agent of morphological change. The adaptive significance of heterochronic changes might lie either in the advantages of the derived morphologies (organ size and shape) or the derived growth parameters themselves (rate and duration of growth). We have tested these hypotheses by comparing the growth rate, the duration of growth and the relative length of the adult tibia in Primates in a phylogenetic context. We report an evolutionary decrease in growth rates (paedochronocline) and an increase in the duration of growth (perachronocline), lying in the cline from the last common ancestor of Primates, passing through the last common ancestor of Haplorhini, that of Catarrhini, to the last common ancestor of the Hominidae. However, the variation in the relative length of the adult tibia does not show any phylogenetic pattern. The derived growth parameters in themselves (slower rate, longer duration) would be of adaptive significance and they would have been selected because a prolonged learning period prior to maturity conferred advantage. The proximate (developmental) causation of differences in bone growth rate were also investigated and it was found that cell production rate in the growth plates rather than the chondrocyte size, underlies the variation in bone growth rate.     

Comparative lectin histochemical analysis of the duodenal glands in various mammals

Composition and histotopography of lectin receptors have been studied in 12 species of mammals with various nutritional specialization: carnivorous, phytophagous and omnivorous. In cells of the duodenal glands of the carnivorous and omnivorous receptors to concanavalin A and lentil lectin (D-mannosoglycans ) are absent and they are present in the glands of the phytophagous animals. In cells of some parts of the glands presence of receptors to soya bean lectin (N-acetyl-D-galactosamine++) is the most characteristic sign of the duodenal glands in the carnivorous and phytophagous animals. Together with certain differences, depending on the nutritional way of the animals, specific peculiarities of lectins binding with glandulocytes of the duodenal glands are demonstrated. The data on rearrangement of the lectin receptors are obtained during the process of cellular differentiation. Presence of N-acetyl-D-galactosamine++ remnants-biding soya bean lectin in composition of oligosaccharide++ chains of glycoconjugates is a sign of low differential degree of the glandular cells. In more differentiated cells concealment in oligosaccharide chains of D-galactose remnants (peanut and castor-oil lectins receptors) by L-fucose, N-acetil-D-glucosamin remnants and sialic acid can have place; this is demonstrated as accumulation of receptors to wheat germ and Laburnum anagyroides lectins in the glandular cells.     

Comparative functional analysis of aquaporins/glyceroporins in mammals and anurans

Maintenance of fluid homeostasis is critical to establishing and maintaining normal physiology. The landmark discovery of membrane water channels (aquaporins; AQPs) ushered in a new area in osmoregulatory biology that has drawn from and contributed to diverse branches of biology, from molecular biology and genomics to systems biology and evolution, and from microbial and plant biology to animal and translational physiology. As a result, the study of AQPs provides a unique and integrated backdrop for exploring the relationships between genes and genome systems, the regulation of gene expression, and the physiologic consequences of genetic variation. The wide species distribution of AQP family members and the evolutionary conservation of the family indicate that the control of membrane water flux is a critical biological process. AQP function and regulation is proving to be central to many of the pathways involved in individual physiologic systems in both mammals and anurans. In mammals, AQPs are essential to normal secretory and absorptive functions of the eye, lung, salivary gland, sweat glands, gastrointestinal tract, and kidney. In urinary, respiratory, and gastrointestinal systems, AQPs are required for proper urine concentration, fluid reabsorption, and glandular secretions. In anurans, AQPs are important in mediating physiologic responses to changes in the external environment, including those that occur during metamorphosis and adaptation from an aquatic to terrestrial environment and thermal acclimation in anticipation of freezing. Therefore, an understanding of AQP function and regulation is an important aspect of an integrated approach to basic biological research.