Studying morphological integration and modularity at multiple levels: concepts and analysis

Although most studies on integration and modularity have focused on variation among individuals within populations or species, this is not the only level of variation for which integration and modularity exist. Multiple levels of biological variation originate from distinct sources: genetic variation, phenotypic plasticity resulting from environmental heterogeneity, fluctuating asymmetry from random developmental variation and, at the interpopulation or interspecific levels, evolutionary change. The processes that produce variation at all these levels can impart integration or modularity on the covariance structure among morphological traits. In turn, studies of the patterns of integration and modularity can inform about the underlying processes. In particular, the methods of geometric morphometrics offer many advantages for such studies because they can characterize the patterns of morphological variation in great detail and maintain the anatomical context of the structures under study. This paper reviews biological concepts and analytical methods for characterizing patterns of variation and for comparing across levels. Because research comparing patterns across level has only just begun, there are relatively few results, generalizations are difficult and many biological and statistical questions remain unanswered. Nevertheless, it is clear that research using this approach can take advantage of an abundance of new possibilities that are so far largely unexplored.     

The evolutionary role of modularity and integration in the hominoid cranium

Patterns of morphological integration and modularity among shape features emerge from genetic and developmental factors with varying pleiotropic effects. Factors or processes affecting morphology only locally may respond to selection more easily than common factors that may lead to deleterious side effects and hence are expected to be more conserved. We briefly review evidence for such global factors in primate cranial development as well as for local factors constrained to either the face or the neurocranium. In a sample comprising 157 crania of Homo sapiens, Pan troglodytes, and Gorilla gorilla, we statistically estimated common and local factors of shape variation from Procrustes coordinates of 347 landmarks and semilandmarks. Common factors with pleiotropic effects on both the face and the neurocranium account for a large amount of shape variation, but mainly by extension or truncation of otherwise conserved developmental pathways. Local factors (modular shape characteristics) have more degrees of freedom for evolutionary change than mere ontogenetic scaling. Cranial shape is similarly integrated during development in all three species, but human evolution involves dissociation among several characteristics. The dissociation has probably been achieved by evolutionary alterations and by the novel emergence of local factors affecting characteristics that are controlled at the same time by the common factors.     

Morphological integration and modularity in the hyperkinetic feeding system of aquatic‐foraging snakes

The kinetic skull is a key innovation that allowed snakes to capture, manipulate, and swallow prey exclusively using their heads using the coordinated movement of eight bones. Despite these unique feeding behaviors, patterns of evolutionary integration and modularity within the feeding bones of snakes in a phylogenetic framework have yet to be addressed. Here, we use a dataset of 60 μCT‐scanned skulls and high‐density geometric morphometric methods to address the origin and patterns of variation and integration in the feeding bones of aquatic‐foraging snakes. By comparing alternate superimposition protocols allowing us to analyze the entire kinetic feeding system simultaneously, we find that the feeding bones are highly integrated, driven predominantly by functional selective pressures. The most supported pattern of modularity contains four modules, each associated with distinct functional roles: the mandible, the palatopterygoid arch, the maxilla, and the suspensorium. Further, the morphological disparity of each bone is not linked to its magnitude of integration, indicating that integration within the feeding system does not strongly constrain morphological evolution, and that adequate biomechanical solutions to a wide range of feeding ecologies and behaviors are readily evolvable within the constraint due to integration in the snake feeding system.     

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 pace of morphological change: historical transformation of skull shape in St Bernard dogs

Owing to the great morphological diversity of domestic dogs (Canis familiaris), the study of historical shape change in dog skulls provides an excellent opportunity for investigating the dynamics of morphological evolution. Breed standards make known which features were selected by breeders. Here we use the methods of geometric morphometrics to study change of skull shape in a series of purebred St Bernard dogs spanning nearly 120 years. A regression of shape on time was highly significant and revealed a consistent trend of shape change that corresponded to the features deemed desirable by the breed standard. Historical shape change in St Bernards involves a broadening of the skull and a tilting of the palate and upper jaw relative to the rest of the skull. This trend appears to be linear throughout the entire period and appears to be continuing. Allometry was ruled out as a contributing factor to this change because there was no consistent trend of historical change in skull size and because neither the patterns of static nor ontogenetic allometry corresponded to the historical shape change. The dramatic modification of the St Bernard skull demonstrates that selection can achieve sustained and substantial change and can completely overcome constraints such as allometry.     

Speciation mirrors geomorphology and palaeoclimatic history in African laminate-toothed rats (Muridae: Otomyini) of the Otomys denti and Otomys lacustris species-complexes in the 'Montane Circle' of East Africa

We adopted an integrated systematic approach to delimit evolutionary species and describe phylogeographic, morphometric and ecological relationships in Otomys denti (from the Albertine Rift, Southern Rift in Malawi and the northern Eastern Arc Mountains) and Otomys lacustris (from the Southern Rift in Tanzania and Zambia, and the southern Eastern Arc Mountains). Molecular [cytochrome (cyt) b sequences, 1143 bp, N  = 18], craniometric (classical, N  = 100 and geometric, N  = 60) and ecological (Partial Least Squares regression of shape and ecogeographic variables) approaches show a profound, parallel disjunction between two groups: (1) Eastern Arc and Southern Rift (including the Malawi Rift) ( O. lacustris and Otomys denti sungae ) and (2) Albertine Rift ( Otomys denti denti and Otomys denti kempi ) taxa. Within both groups, cyt b sequences or craniometric analysis provided evidence for the differentiation of both southern and northern Eastern Arc from Southern Rift lineages (across the so-called Makambako Gap). Within the Albertine Rift ( denti – kempi ) lineage, populations from individual mountain ranges differed significantly in skull shape (but not size), but were similar genetically. Over-reliance in the past on very few morphological characters (e.g. number of molar laminae) and a polytypic species concept has obscured phylogenetic relationships and species discrimination in this group. We recognize at least three species in this group, and distinct lineages within two of these species. Each species or lineage was endemic to one of three regions: the Albertine Rift, the Malawi Rift or the Eastern Arc. Our result echo conclusions of recent studies of other mammalian and bird taxa and reflect the geomorphology and palaeoclimatic history of the region.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 913–941.     

Phenotypic integration in feliform carnivores: Covariation patterns and disparity in hypercarnivores versus generalists

The skeleton is a complex arrangement of anatomical structures that covary to various degrees depending on both intrinsic and extrinsic factors. Among the Feliformia, many species are characterized by predator lifestyles providing a unique opportunity to investigate the impact of highly specialized hypercarnivorous diet on phenotypic integration and shape diversity. To do so, we compared the shape of the skull, mandible, humerus, and femur of species in relation to their feeding strategies (hypercarnivorous vs. generalist species) and prey preference (predators of small vs. large prey) using three-dimensional geometric morphometric techniques. Our results highlight different degrees of morphological integration in the Feliformia depending on the functional implication of the anatomical structure, with an overall higher covariation of structures in hypercarnivorous species. The skull and the forelimb are not integrated in generalist species, whereas they are integrated in hypercarnivores. These results can potentially be explained by the different feeding strategies of these species. Contrary to our expectations, hypercarnivores display a higher disparity for the skull than generalist species. This is probably due to the fact that a specialization toward high-meat diet could be achieved through various phenotypes. Finally, humeri and femora display shape variations depending on relative prey size preference. Large species feeding on large prey tend to have robust long bones due to higher biomechanical constraints.     

Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution

This study addresses some enduring issues of ontogenetic and evolutionary integration in the form of the hominid cranium. Our sample consists of 38 crania: 20 modern adult Homo sapiens, 14 sub-adult H. sapiens, and four archaic Homo. All specimens were CT-scanned except for two infant H. sapiens, who were imaged by MR instead. For each specimen 84 landmarks and semi-landmarks were located on the midsagittal plane and converted to Procrustes shape coordinates. Integration was quantified by the method of singular warps, a new geometric-statistical approach to visualizing correlations among regions. The two classic patterns of integration, evolutionary and ontogenetic, were jointly explored by comparing analyses of overlapping subsamples that span ranges of different hypothetical factors. Evolutionary integration is expressed in the subsample of 24 adult Homo, and ontogenetic integration in the subsample of 34 H. sapiens. In this data set, vault, cranial base, and face show striking and localized patterns of covariation over ontogeny, similar but not identical to the patterns seen over evolution. The principal differences between ontogeny and phylogeny pertain to the cranial base. There is also a component of cranial length to height ratio not reducible to either process. Our methodology allows a separation of these independent processes (and their impact on cranial shape) that conventional methods have not found.     

Common features of sexual dimorphism in the cranial airways of different human populations

Sexual dimorphism in the human craniofacial system is an important feature of intraspecific variation in recent and fossil humans. Although several studies have reported different morphological patterns of sexual dimorphism in different populations, this study searches for common morphological aspects related to functional anatomy of the respiratory apparatus. 3D geometric morphometrics were used to test the hypothesis that due to higher daily energy expenditure and associated greater respiratory air consumption as well as differences in body composition, males should have absolutely and relatively greater air passages in the bony cranial airways than females. We measured 25 3D landmarks in five populations (N = 212) of adult humans from different geographic regions. Male average cranial airways were larger in centroid sizes than female ones. Males tended to show relatively taller piriform apertures and, more consistently, relatively taller internal nasal cavities and choanae than females. Multivariate regressions and residual analysis further indicated that after standardizing to the same size, males still show relatively larger airway passages than females. Because the dimensions of the choanae are limiting factors for air transmission towards the noncranial part of the respiratory system, the identified sex-specific differences in cranial airways, possibly shared among human populations, may be linked with sex-specific differences in body size, composition, and energetics. These findings may be important to understanding trends in hominin facial evolution.     

Mosaic heterochrony and evolutionary modularity: the trilobite genus Zacanthopsis as a case study

Logical connections exist between evolutionary modularity and heterochrony, two unifying and structuring themes in the expanding field of evolutionary developmental biology. The former sees complex phenotypes as being made up of semi-independent units of evolutionary transformation; the latter requires such a modular organization of phenotypes to occur in a localized or mosaic fashion. This conceptual relationship is illustrated here by analyzing the evolutionary changes in the cranidial ontogeny of two related species of Cambrian trilobites. With arguments from comparative developmental genetics and functional morphology, we delineate putative evolutionary modules within the cranidium and examine patterns of evolutionary changes in ontogeny at both global and local scales. Results support a case of mosaic heterochrony, that is, a combination of local heterochronies affecting the different parts individuated in the cranidium, leading to the complex pattern of allometric repatterning observed at the global scale. Through this example, we show that recasting morphological analyses of complex phenotypes with a priori knowledge or hypotheses about their organizational and variational properties can significantly improve our interpretation and understanding of evolutionary changes among related taxa, fossil and extant. Such considerations open avenues to investigate the large-scale dynamics of modularity and its role in phenotypic evolution.     

Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves

The structure of compound leaves provides flexibility for morphological change by variation in the shapes, sizes and arrangement of leaflets. Here, we conduct a multilevel analysis of shape variation in compound leaves to explore the developmental plasticity and evolutionary potential that are the basis of diversification in leaf shape. We use the methods of geometric morphometrics to study the shapes of individual leaflets and whole leaves in 20 taxa of Potentilla (sensu lato). A newly developed test based on the bootstrap approach suggests that uncertainty in the molecular phylogeny precludes firm conclusions whether there is a phylogenetic signal in the data on leaf shape. For variation among taxa, variation within taxa, as well as fluctuating asymmetry, there is evidence of strong morphological integration. The patterns of variation are similar across all three levels, suggesting that integration within taxa may act as a constraint on evolutionary change.     

Geometric morphometrics: recent applications to the study of evolution and development

The field of morphometrics is developing quickly and recent advances allow for geometric techniques to be applied easily to many zoological problems. This paper briefly introduces geometric morphometric techniques and then reviews selected areas where those techniques have been applied to questions of general interest. This paper is relevant to non-specialists looking for an entry into geometric morphometric methods and for ideas of how to incorporate them into the study of variation within and between species, the measurement of developmental stability, the role of development in shaping evolution and the special problem of measuring the shape of fossil specimens that are deformed from their original shape.     

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.