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Hlusko, Leslea; Mahaney, Michael
doi: 10.1007/s11692-008-9048-1pmid: 22919117
Variation in the mammalian dentition is highly informative of adaptations and evolutionary relationships, and consequently has been the focus of considerable research. Much of the current research exploring the genetic underpinnings of dental variation can trace its roots to Olson and Miller’s 1958 book Morphological Integration. These authors explored patterns of correlation in the post-canine dentitions of the owl monkey and Hyopsodus, an extinct condylarth from the Eocene. Their results were difficult to interpret, as was even noted by the authors, due to a lack of genetic information through which to view the patterns of correlation. Following in the spirit of Olson and Miller’s research, we present a quantitative genetic analysis of dental variation in a pedigreed population of baboons. We identify patterns of genetic correlations that provide insight to the genetic architecture of the baboon dentition. This genetic architecture indicates the presence of at least three modules: an incisor module that is genetically independent of the post-canine dentition, and a premolar module that demonstrates incomplete pleiotropy with the molar module. We then compare this matrix of genetic correlations to matrices of phenotypic correlations between the same measurements made on museum specimens of another baboon subspecies and the Southeast Asian colobine Presbytis. We observe moderate significant correlations between the matrices from these three primate taxa. From these observations we infer similarity in modularity and hypothesize a common pattern of genetic integration across the dental arcade in the Cercopithecoidea.
Willmore, Katherine; Roseman, Charles; Rogers, Jeffrey; Cheverud, James; Richtsmeier, Joan
doi: 10.1007/s11692-009-9056-9pmid: 22212926
In this study we compare patterns of mandibular integration between mice and baboons using both phenotypic and quantitative genetic data. Specifically, we test how well each species fits with the mosaic model of mandibular integration suggested by Atchley and Hall (Biol Rev Camb Philos Soc 66:101–157, 1991) based on developmental modules. We hypothesize that patterns of integration will be similar for mice and baboons and that both species will show strong integration within developmental modules and weaker integration between modules. Corresponding landmark data were collected from the hemi-mandibles of an advanced intercross mouse sample (N = 1239) and mandibles from a baboon sample of known pedigree from the Southwest Foundation for Biomedical Research (N = 430). We used four methods of analysis to quantify and compare the degree of mandibular integration between species including two methods based on a priori assumptions, and two a posteriori analyses. We found that patterns of integration are broadly similar for baboon and mouse mandibles, with both species displaying a modular pattern of integration. While there is a general trend of similarity in integration patterns between species, there were some marked differences. Mice are strongly correlated among distances within the coronoid process and the incisive alveolar region, whereas baboons are strongly integrated within the condylar process. We discuss the potential evolutionary implications of the similar patterns of integration between these species with an emphasis on the role of modularity.
Martínez-Abadías, Neus; Paschetta, Carolina; Azevedo, Soledad; Esparza, Mireia; González-José, Rolando
doi: 10.1007/s11692-008-9045-4pmid: N/A
Neurocranial globularity is one of the few derived traits defining anatomically modern humans. Variations in this trait derive from multiple and complex interactions between portions of the brain and the size and shape of the cranial base, among other factors. Given their evolutionary and functional importance, neurocranial globularity is expected to present high genetic and developmental constraints on their phenotypic expression. Here we applied two independent approaches to investigate both types of constraints. First, we assessed if patterns of morphological integration are conserved or else disrupted on a series of artificially deformed skulls in comparison to non-deformed (ND) ones. Second, after the estimation of the genetic covariance matrix for human skull shape, we explored how neurocranial globularity would respond to putative selective events disrupting the normal morphological patterns. Simulations on these deviations were explicitly set to replicate the artificial deformation patterns in order to compare developmental and genetic constraints under the same biomechanical conditions. In general terms, our results indicate that putative developmental constraints help to preserve some aspects of normal morphological integration even in the deformed skulls. Moreover, we find that the response to selection in neurocranial globularity is pervasive. In other words, induced changes in the vault generate a global response, indicating that departures from normal patterns of neurocranial globularity are genetically constrained. In summary, our combined results suggest that neurocranial globularity behaves as a highly genetic and developmental constrained trait.
Young, Nathan; Hallgrímsson, Benedikt; Garland, Theodore
doi: 10.1007/s11692-009-9053-zpmid: N/A
Mammals exhibit a similar pattern of integration among homologous limb elements, the strength of which is believed to vary in response to selection for functional coordination or similarity. Although integration is hypothesized to primarily reflect the effect of genes intrinsic to limbs, extrinsic genetic or epigenetic factors may also affect the strength of integration through their impact on the magnitude and direction of skeletal variance or covariance. Such factors as neuromuscular coordination or bone-muscle interactions may therefore play a role in both canalization and the structure or magnitude of limb integration. If this were the case, then increased levels of locomotor activity would be predicted to increase canalization and the magnitude of covariation between limbs. To investigate whether postnatal activity levels can have a significant effect on variance within or covariance among homologous limb elements, we compared four groups of male mice from a long-term selective breeding experiment: (1) mice from lines bred for increased voluntary activity on running wheels and allowed free access to a wheel for 8 weeks beginning at weaning (“active”), (2) selected mice that did not have wheel access (“sedentary”), (3) active mice from non-selected control lines, and (4) sedentary control mice. Mice from selected lines that had wheel access ran significantly more than control-line mice. However, when controlled for activity, linetype, and body mass, results indicate few significant differences in means, variance, or covariation structure, and no significant differences in integration between limbs, suggesting that postnatal activity levels do not significantly affect canalization or integration of limb lengths. A possible explanation for this result is that whereas baseline levels of postnatal activity may help to maintain patterns of variance and integration, increased levels of activity do not further increase these measures. Investigations into disrupted epigenetic processes (e.g., via models in which neuromuscular coordination is impaired) are required to further test hypotheses about how canalization or integration of limb variation is affected by epigenetic factors.
doi: 10.1007/s11692-009-9049-8pmid: N/A
Morphological integration theory predicts that sets of phenotypic traits that covary strongly due to developmental and/or functional connections between them eventually co-evolve because of a coordinated response to selection, and accordingly become less independently evolvable. This process is not irreversible, however, and phenotypic traits can become less integrated, and hence more independently evolvable, in the context of selection for divergent functions and morphologies. This study examines the reciprocal relationship between shared function, integration and evolvability by comparing integration patterns among serially homologous skeletal elements in the hands and feet of a functionally diverse sample of catarrhine primates. Two hypotheses are tested: (1) species in which the autopods are functionally more similar (e.g. quadrupedal monkeys) have more strongly integrated autopods than species in which the autopods are functionally divergent (e.g. gibbons, humans) and (2) the latter have autopods that are more evolvable, collectively and independently. Morphometric data from selected hand and foot digital rays were used to derive phenotypic variance/covariance matrices. The strength of integration among autopods was quantified using eigenanalysis and a measure of trait variational autonomy. Evolvability was estimated by subjecting phenotypic variance/covariance matrices to simulated random selection gradients, and comparing evolutionary responses among species. Results indicate that integration decreases as hands and feet become functionally divergent, and that the strongly integrated hand and foot skeletons of quadrupedal monkeys respond to selection in a highly collinear manner, even when simulated selective pressures acting on each autopod are in opposite directions in phenotypic space. Results confirm that the evolvability of morphological traits depends largely on how strongly they covary with other traits, but also with body size. The role of pleiotropy as a developmental mechanism underlying integration and evolvability is also discussed.
Marroig, Gabriel; Shirai, Leila; Porto, Arthur; Oliveira, Felipe; Conto, Valderes
doi: 10.1007/s11692-009-9051-1pmid: N/A
Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.
doi: 10.1007/s11692-009-9050-2pmid: N/A
The fossil record of primate and human evolution cannot provide accurate estimates of within species variation and integration. This means that we cannot directly observe how patterns of integration have evolved over time in this lineage. And yet, our interpretations of fossil diversity are awash with assumptions about variation patterning in precisely these fossil taxa. Most commonly, researchers rely on extant models of variation for interpreting past diversity, by assuming equality of variation (and occasionally covariation) among extant and fossil populations. Yet one of the things we know from studies of integration in primates is that patterns of morphological covariation can differ among even closely related taxa, indicating that they have diverged over evolutionary time, either in response to selection or as the result of neutral evolution. At the same time, overall patterns of integration remain remarkably similar, meaning that in many respects they are highly conserved evolutionarily. Taken together, these seemingly contradictory observations offer an important conceptual framework for interpreting patterns that we observe in the fossil past. This framework dictates that while we can use patterns of covariation in extant taxa as proxies for extinct diversity, and indeed their conserved nature makes them superior to approaches that rely on variation alone, we also need to account for the fact that such patterns change over time, and incorporate that into our models. Here I provide examples using covariation patterns estimated from modern humans and African great apes to demonstrate the extent to which divergence in covariance structure might affect our interpretations of hominin diversity.
Pavlicev, Mihaela; Cheverud, James; Wagner, Günter
doi: 10.1007/s11692-008-9042-7pmid: N/A
The concept of morphological integration describes the pattern and the amount of correlation between morphological traits. Integration is relevant in evolutionary biology as it imposes constraint on the variation that is exposed to selection, and is at the same time often based on heritable genetic correlations. Several measures have been proposed to assess the amount of integration, many using the distribution of eigenvalues of the correlation matrix. In this paper, we analyze the properties of eigenvalue variance as a much applied measure. We show that eigenvalue variance scales linearly with the square of the mean correlation and propose the standard deviation of the eigenvalues as a suitable alternative that scales linearly with the correlation. We furthermore develop a relative measure that is independent of the number of traits and can thus be readily compared across datasets. We apply this measure to examples of phenotypic correlation matrices and compare our measure to several other methods. The relative standard deviation of the eigenvalues gives similar results as the mean absolute correlation (W.P. Cane, Evol Int J Org Evol 47:844–854, 1993) but is only identical to this measure if the correlation matrix is homogenous. For heterogeneous correlation matrices the mean absolute correlation is consistently smaller than the relative standard deviation of eigenvalues and may thus underestimate integration. Unequal allocation of variance due to variation among correlation coefficients is captured by the relative standard deviation of eigenvalues. We thus suggest that this measure is a better reflection of the overall morphological integration than the average correlation.
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