Hierarchical nature of morphological integration and modularity in the human posterior face

Morphological integration and modularity are important points of intersection between evolution and the development of organismal form. Identification and quantification of integration are also of increasing paleoanthropological interest. In this study, the "posterior face," i.e., the mandibular ramus and its integration with the associated midline and lateral basicranium, is analyzed in lateral radiographs of 144 adult humans from three different geographic regions. The null hypothesis of homogenously pervasive morphological integration among "posterior-face" components is tested with Procrustes geometric morphometrics, partial least squares, and singular warps analysis. The results reveal statistically significant differences in integration. Only loose integrative relationships are found between midline and lateral components of the basicranium, which may indicate the presence of at least two different basicranial modules. This modularity can be interpreted in terms of spatiotemporal dissociation in the development of those basicranial structures, and gives support to hypotheses of independent phylogenetic modifications at the lateral and midline basicranium in humans. In addition, morphological integration was statistically significantly stronger between the middle cranial fossa and the mandibular ramus than between the ramus and the midline cranial base. This finding confirms previous hypotheses of a "petroso-mandibular unit," which could be a developmental consequence of well-known phylogenetic modifications in coronal topology of the posterior face and base in hominoid evolution, related to middle cranial fossa expansion. This unit could be involved in later evolutionary tendencies in the hominid craniofacial system.     

The nature and evolution of intelligence in orangutans (Pongo pygmaeus)

Orangutans share many intellectual qualities with African great apes and humans, likely because of their recent common ancestry. They may also show unique intellectual adaptations because of their long evolutionary divergence from the African lineage. This paper assesses orangutan intelligence in light of this evolutionary history. Evidence derives from observations of juvenile ex-captive orangutans reintroduced to free forest life by the Wanariset Orangutan Reintroduction Project, East Kalimantan, Indonesia. The intellectual qualities shared by great apes and humans point to a distinct “great ape” intelligence with hierarchization as a pivotal cognitive mechanism. Evolutionary reconstructions jibe with this view and suggest that technically difficult foods may have been key selection pressures. Orangutans should then show hierarchical intelligence when obtaining difficult foods. Evidence on ex-captive orangutans' techniques for processing difficult foods concurs. Intellectual qualities distinct to orangutans may owe to arboreal travel pressures; in particular arboreality may aggravate foraging problems. Evidence confirms that ex-captive orangutans' techniques for accessing difficult foods located arboreally are intellectually complex—i.e. they show hierarchization. These findings suggest other factors probably important to understanding great ape and orangutan forms of intelligence and their evolutionary origins.     

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.     

Ontogeny of craniofacial sexual dimorphism in the orangutan (Pongo pygmaeus). I: face and palate

The orangutan is widely recognized as a highly dimorphic species. An ontogenetic approach to the study of sexual dimorphism can assist researchers in understanding both where and when these differences develop. In this study, 357 orangutans from Borneo were divided into five developmental stages representing infancy to mature adulthood. Three-dimensional (3D) coordinate data from 16 landmarks representing the face and palate were analyzed by means of a Euclidean distance matrix analysis (EDMA), a quantitative method for the comparison of forms. Three separate analyses (an age-specific static comparison of forms, a sex-specific analysis of growth trajectories, and an intersex comparison of patterns of relative growth) were carried out with the intent to describe the rate, timing, magnitude, and pattern of growth in the orangutan face and palate. The results indicate that generally males and females share a similar, but not identical, pattern of growth or local form change, but differ in growth rate, timing, and magnitude of difference. Dimorphism in the face and palate can be localized in infancy and traced throughout all age intervals. Orangutan females grow slightly faster than males from infancy to adolescence, at which time male growth exceeds female growth. Female growth ceases with the advent of adulthood, while male growth continues (i.e., both the number and magnitude of the dimorphic dimensions increase). Males and females are similar in facial dimensions and growth related to the orbits, upper face, and palate width. They maintain these similarities throughout development. However, they differ in facial and nasal height, palate length, snout projection, depth of the nasopharynx, and hafting of the face onto the skull. The face broadens and the zygomatic bone flares dramatically in adult males, corresponding to the development of cheek pads. While growth patterns are similar between the two sexes, they differ in the lateral orbit, snout projection, and hafting of the face onto the cranium. Adult dimorphism is the result of growth patterns experienced throughout life, and it is not equally expressed across the cranium. An understanding of patterns of dimorphism, along with the magnitude of difference, may be helpful for interpreting dimorphism in the fossil record.     

Cranial morphology and development: new light on the evolution of language

A hypothesis is presented which may explain within a single framework both the large behavioural differences and the large differences in head morphology between the great apes and humans. All these differences can be parsimoniously explained by a shift of few regulatory genes controlling the onset of the division of late migrating neurons in the human cortex. This simple shift resulted in the following effects: 1) the neurocranium responded to brain enlargement by increasing mineral deposition on its external surface, increasing its overall size and mass. 2) This increase in the braincase was largely achieved by developmental reabsoption of the face bones. 3) The relative shift in growth between these two skull components also induced a rearrangement at the basicranium level. This brought about the facial orthognatism of modernHomo and, as a mechanical by-product, the descent of the larynx into the throat. Brain enlargement led to a large increase in cognitive capacity, and as a developmental byproduct, produced a mechanical organ preadapted for speech, as well as bringing about the reduction of canines and the origin of the chin. In this study, the phylogenetic basis, the selective pressures, and the behavioural consequences of this process during hominization are examined. Cognitiveversus communicative aspects of human language are distinguished and discussed. Cognitive capacities were the first to be selected due to the survival advantage of mapping huge territories during the expansion of the Plio-Pleistocene savanna ecotone. The present hypothesis is then compared with current theories leading to the conclusion that it is a more parsimonious explanation. It integrates data from a wide array of fields of human biology, pathology and clinical medicine, all assessed from evolutionary and ecological perspectives.     

Covariance in human limb joint articular morphology

Objectives

Limb synovial joints exhibit complex shapes that must accommodate often-antagonistic demands of function, mobility, and stability. These demands presumably dictate coordination among joint articular shapes, but the structure of morphological covariance within and among joints is unknown. This study analyzes the human shoulder, elbow, hip, and knee to determine how articular covariance is structured in relation to joint structure, accessory cartilage, and function.

Materials and Methods

Surface models were created from the CT scans of 200 modern skeletons from the University of Tennessee Donated Skeletal Collection. Three-dimensional landmarks were collected on the shoulder, elbow, hip, and knee joints. Two-block partial least squares were conducted to determine associations between surfaces of conarticular shapes, functionally analogous articulations, and articulations belonging to the same bone.

Results

Except for the components of the shoulder, all conarticular pairs exhibit covariance, though the strength of these relationships appears unrelated to the amount of accessory cartilage in the joint. Only the analogous articulations of the humerus and femur exhibit significant covariance, but it is unlikely that this pattern is due to function alone. Stronger covariance within the lower limb than the upper limb is consistent broader primate patterns of within-limb integration.

Discussion

With the exception of the elbow, complementary joint function does not appear to promote strong covariance between articulations. Analogous humeral and femoral surfaces are also serially homologous, which may result in the articular associations observed between these bones. Broadly, these patterns highlight the indirect relationship between joint congruence and covariance.

     

The correspondence between proximal phalanx morphology and locomotion: implications for inferring the locomotor behavior of fossil catarrhines

Phalanges are considered to be highly informative in the reconstruction of extinct primate locomotor behavior since these skeletal elements directly interact with the substrate during locomotion. Variation in shaft curvature and relative phalangeal length has been linked to differences in the degree of suspension and overall arboreal locomotor activities. Building on previous work, this study investigated these two skeletal characters in a comparative context to analyze function, while taking evolutionary relationships into account. This study examined the correspondence between proportions of suspension and overall substrate usage observed in 17 extant taxa and included angle of curvature and relative phalangeal length. Predictive models based on these traits are reported. Published proportions of different locomotor behaviors were regressed against each phalangeal measurement and a size proxy. The relationship between each behavior and skeletal trait was investigated using ordinary least-squares, phylogenetic generalized least-squares (pGLS), and two pGLS transformation methods to determine the model of best-fit. Phalangeal curvature and relative length had significant positive relationships with both suspension and overall arboreal locomotion. Cross-validation analyses demonstrated that relative length and curvature provide accurate predictions of relative suspensory behavior and substrate usage in a range of extant species when used together in predictive models. These regression equations provide a refined method to assess the amount of suspensory and overall arboreal locomotion characterizing species in the catarrhine fossil record.     

Repeat proliferation and partial endoreplication jointly shape the patterns of genome size evolution in orchids

Although the evolutionary drivers of genome size change are known, the general patterns and mechanisms of plant genome size evolution are yet to be established. Here we aim to assess the relative importance of proliferation of repetitive DNA, chromosomal variation (including polyploidy), and the type of endoreplication for genome size evolution of the Pleurothallidinae, the most species-rich orchid lineage. Phylogenetic relationships between 341 Pleurothallidinae representatives were refined using a target enrichment hybrid capture combined with high-throughput sequencing approach. Genome size and the type of endoreplication were assessed using flow cytometry supplemented with karyological analysis and low-coverage Illumina sequencing for repeatome analysis on a subset of samples. Data were analyzed using phylogeny-based models. Genome size diversity (0.2–5.1 Gbp) was mostly independent of profound chromosome count variation (2n = 12–90) but tightly linked with the overall content of repetitive DNA elements. Species with partial endoreplication (PE) had significantly greater genome sizes, and genomic repeat content was tightly correlated with the size of the non-endoreplicated part of the genome. In PE species, repetitive DNA is preferentially accumulated in the non-endoreplicated parts of their genomes. Our results demonstrate that proliferation of repetitive DNA elements and PE together shape the patterns of genome size diversity in orchids.     

Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo

Orangutans are amongst the most craniometrically variable of the extant great apes, yet there has been no attempt to explicitly link this morphological variation with observed differences in behavioral ecology. This study explores the relationship between feeding behavior, diet, and mandibular morphology in orangutans. All orangutans prefer ripe, pulpy fruit when available. However, some populations of Bornean orangutans (Pongo pygmaeus morio and P. p. wurmbii) rely more heavily on bark and relatively tough vegetation during periods of low fruit yield than do Sumatran orangutans (Pongo abelii). I tested the hypothesis that Bornean orangutans exhibit structural features of the mandible that provide greater load resistance abilities to masticatory and incisal forces. Compared to P. abelii, P. p. morio exhibits greater load resistance abilities as reflected in a relatively deeper mandibular corpus, deeper and wider mandibular symphysis, and relatively greater condylar area. P. p. wurmbii exhibits most of these same morphologies, and in all comparisons is either comparable in jaw proportions to P. p. morio, or intermediate between P. p. morio and P. abelii. These data indicate that P. p. morio and P. p. wurmbii are better suited to resisting large and/or frequent jaw loads than P. abelii. Using these results, I evaluated mandibular morphology in P. p. pygmaeus, a Bornean orangutan population whose behavioral ecology is poorly known. Pongo p. pygmaeus generally exhibits relatively greater load resistance capabilities than P. abelii, but less than P. p. morio. These results suggest that P. p. pygmaeus may consume greater amounts of tougher and/or more obdurate foods than P. abelii, and that consumption of such foods may intensify amongst Bornean orangutan populations. Finally, data from this study are used to evaluate variation in craniomandibular morphology in Khoratpithecus piriyai, possibly the earliest relative of Pongo from the late Miocene of Thailand, and the late Pleistocene Hoa Binh subfossil orangutan recovered from Vietnam. With the exception of a relatively thicker M(3) mandibular corpus, K. piriyai has jaw proportions that would be expected for an extant orangutan of comparable jaw size. Likewise, the Hoa Binh subfossil does not differ in skull proportions from extant Pongo, independent of the effects of increase in jaw size. These results indicate that differences in skull and mandibular proportions between these fossil and subfossil orangutans and extant Pongo are allometric. Furthermore, the ability of K. piriyai to resist jaw loads appears to have been comparable to that of extant orangutans. However, the similarity in jaw proportions between P. abelii and K. piriyai suggest the latter may have been dietarily more similar to Sumatran orangutans.     

South Amerindian craniofacial morphology: diversity and implications for Amerindian evolution

The most compelling models concerning the peopling of the Americas consider that modern Amerindians share a common biological pattern, showing affinities with populations of the Asian Northeast. The aim of the present study was to assess the degree of variation of craniofacial morphology of South American Amerindians in a worldwide context. Forty-three linear variables were analyzed on crania derived from American, Asian, Australo-Melanesian, European, South-Saharan African, and Polynesian regions. South America was represented by seven Amerindian samples. In order to understand morphologic diversity among Amerindians of South America, variation was estimated using regions and local populations as units of analysis. Variances and F(ST) values were calculated for each unit, respectively. Both analyses indicated that morphologic variation in Southern Amerindians is extremely high: an F(ST) of 0.01531 was obtained for Southern Amerindians, and values from 0.0371-0.1205 for other world regions. Some aspects linked to the time and mode of the peopling of the Americas and various microevolutionary processes undergone by Amerindians are discussed. Some of the alternatives proposed to explain this high variation include: a greater antiquity of the peopling than what is mostly accepted, a peopling by several highly differentiated waves, an important effect of genetic drift, and gene flow with Paleoamericans. A combination of some of these alternatives explains at least some of the variation.     

Feasibility study on the potential of visible and near infrared reflectance spectroscopy to measure alpaca fibre characteristics

Visible (Vis) and near infrared (NIR) reflectance spectroscopy is a rapid and non-destructive technique that has found many applications in assessing the quality of agricultural commodities, including wool. In this study, Vis and NIR spectroscopy combined with multivariate data analysis was investigated regarding its feasibility in predicting a range of fibre characteristics in raw alpaca wool samples. Mid-side samples (n = 149) were taken from alpacas from a range of colours and ages at shearing time over 4 years (2000 to 2004) and subsequently analysed for fibre characteristics such as mean fibre diameter (MFD) and standard deviation (and coefficient of variation), spin fineness, curvature degree (and standard deviation), comfort factor, medullation percentage (by weight and number in white samples only) using traditional reference laboratory testing methods. Samples were scanned in a large cuvette using a FOSS NIRSystems 6500 monochromator instrument in reflectance mode in the Vis and NIR regions (400 to 2500 nm). Partial least squares (PLS) regression was used to develop a number of calibration models between the spectral and reference data. Mathematical pre-treatment of the spectra (second derivative) as well as various combinations of wavelength range were used in model development. The best calibration model was found when using the NIR region (1100 to 2500 nm) for the prediction of MFD, which had a coefficient of determination in cross-validation (R2) of 0.88 with a root mean square standard error of cross validation (RMSECV) of 2.62 μm. The results show the NIR technique to have promise as a semi-quantitative method for screening purposes. The lack of grease in alpaca wool samples suggests that the technique might find ready application as a rapid measurement technique for preliminary classing of shorn fleeces or, if used directly on the animal, the technology might offer an objective tool to assist in the selection of animals in breeding programmes or shows.     

Covariation between forelimb muscle anatomy and bone shape in an Australian scratch-digging marsupial: Comparison of morphometric methods

The close association between muscle and bone is broadly intuitive; however, details of the covariation between the two has not been comprehensively studied. Without quantitative understanding of how muscle anatomy influences bone shape, it is difficult to draw conclusions of the significance of many morphological traits of the skeleton. In this study, we investigated these relationships in the Quenda (Isoodon fusciventer), a scratch-digging marsupial. We quantified the relationships between forelimb muscle anatomy and bone shape for animals representing a range of body masses (124–1,952 g) using two-block partial least square analyses. Muscle anatomy was quantified as muscle mass and physiological cross-sectional area (PCSA), and we used two morphometric methods to characterize bone shape: seven indices of linear bone proportions, and landmarks analysis. Bone shape was significantly correlated with body mass, reflecting allometric bone growth. Of the seven bone indices, only shoulder moment index (SMI) and ulna robustness index (URI) showed a significant covariation with muscle anatomy. Stronger relationships between muscle anatomy and forelimb bone shape were found using the landmark coordinates: muscle mass and PCSA were correlated with the geometric shape of the scapula, humerus, and third metacarpal, but to a lesser extent with shape of the ulna. Overall, our data show that landmark coordinates are more sensitive than bone indices to capturing shape changes evident throughout ontogeny, and is therefore a more appropriate method to investigate covariation with forelimb muscle anatomy. Single-species studies investigating ontogeny require refined methods to accurately develop understanding of the important relationships between muscle force generation and bone shape remodeling. Landmark analyses provide such a method.     

Ontogenetic relationships between cranium and mandible in coyotes and hyenas

Developing animals must resolve the conflicting demands of survival and growth, ensuring that they can function as infants or juveniles while developing toward their adult form. In the case of the mammalian skull, the cranium and mandible must maintain functional integrity to meet the feeding needs of a juvenile even as the relationship between parts must change to meet the demands imposed on adults. We examine growth and development of the cranium and mandible, using a unique ontogenetic series of known‐age coyotes (Canis latrans), analyzing ontogenetic changes in the shapes of each part, and the relationship between them, relative to key life‐history events. Both cranial and mandibular development conform to general mammalian patterns, but each also exhibits temporally and spatially localized maturational transformations, yielding a complex relationship between growth and development of each part as well as complex patterns of synchronous growth and asynchronous development between parts. One major difference between cranium and mandible is that the cranium changes dramatically in both size and shape over ontogeny, whereas the mandible undergoes only modest shape change. Cranium and mandible are synchronous in growth, reaching adult size at the same life‐history stage; growth and development are synchronous for the cranium but not for the mandible. This synchrony of growth between cranium and mandible, and asynchrony of mandibular development, is also characteristic of a highly specialized carnivore, the spotted hyena (Crocuta crocuta), but coyotes have a much less protracted development, being handicapped relative to adults for a much shorter time. Morphological development does not predict life‐history events in these two carnivores, which is contrary to what has been reported for two rodent species. The changes seen in skull shape in successive life‐history stages suggest that adult functional demands cannot be satisfied by the morphology characterizing earlier life‐history stages. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

The influence of feeding on the evolution of sensory signals: a comparative test of an evolutionary trade‐off between masticatory and sensory functions of skulls in southern African Horseshoe bats (Rhinolophidae)

The skulls of animals have to perform many functions. Optimization for one function may mean another function is less optimized, resulting in evolutionary trade‐offs. Here, we investigate whether a trade‐off exists between the masticatory and sensory functions of animal skulls using echolocating bats as model species. Several species of rhinolophid bats deviate from the allometric relationship between body size and echolocation frequency. Such deviation may be the result of selection for increased bite force, resulting in a decrease in snout length which could in turn lead to higher echolocation frequencies. If so, there should be a positive relationship between bite force and echolocation frequency. We investigated this relationship in several species of southern African rhinolophids using phylogenetically informed analyses of the allometry of their bite force and echolocation frequency and of the three‐dimensional shape of their skulls. As predicted, echolocation frequency was positively correlated with bite force, suggesting that its evolution is influenced by a trade‐off between the masticatory and sensory functions of the skull. In support of this, variation in skull shape was explained by both echolocation frequency (80%) and bite force (20%). Furthermore, it appears that selection has acted on the nasal capsules, which have a frequency‐specific impedance matching function during vocalization. There was a negative correlation between echolocation frequency and capsule volume across species. Optimization of the masticatory function of the skull may have been achieved through changes in the shape of the mandible and associated musculature, elements not considered in this study.     

Individual variation in nest size and nest site features of the Bornean orangutans (Pongo pygmaeus)

Nest construction is a daily habit of independent orangutans for sleeping or resting. Data on their nests have been used in various ecological studies (e.g., density estimation, ranging behavior, evolution of material culture) because they are the most observable field signs. We investigated nest size and nest site features of Bornean orangutans in the wild during 10 months' fieldwork at three sites in East Kalimantan, Indonesia: Kutai National Park, Birawa, and Meratus. To examine individual variation, we followed 31 individual orangutans and recorded the 92 nests they made for nest size (diameter) and nest site features (height of nest above ground, tree species used for the nest site, the diameter and height of the tree, whether the nest was new or reused, and nest location within the tree). Analyses taking age–sex classes of the focal individuals into consideration showed significant age–sex differences in nest size and location, but not in nest height or nest tree features (diameter, height of tree, and height of lowest branch). Mature orangutans (adult females, unflanged and flanged males) made larger nests than immatures (juveniles and adolescents). Flanged male orangutans with larger nests used stable locations for nesting sites and reused old nests more frequently than immatures. The overall proportion of nests in open (exposed) locations was higher than in closed (sheltered) locations. Flanged males and immatures frequently made open nests, whereas adult females with an infant preferred closed locations. The good correspondence between nest size and age–sex classes indicates that nest size variation may reflect body size and therefore age–sex variation in the population. Am. J. Primatol. 71:393–399, 2009. © 2009 Wiley‐Liss, Inc.