Evolutionary Biology

For many species, sexual dimorphism is one of the major sources of intraspecific variation. This is the case in some extant great apes, such as gorillas and orangutans, and to a lesser degree in humans, chimpanzees and bonobos. This variation has been well documented in various aspects of these species skeletal anatomy, including differences in the size and shape of the body, cranium, canines, and cresting of males and females, but less is known about sexually dimorphic variation of great ape mandibles. This is particularly important for building robust analog models to interpreting variation in the early hominin fossil record which preserves a large proportion of isolated mandibles and partial mandibles. Here we describe the phenotypical expression of sexual dimorphism in the mandible of six extant hominoid species, including humans, using geometric morphometrics. Our analyses show that the extent of sexual dimorphism in mandibular size and shape amongst the species studied is not the same, as well as the presence of significant differences in the degree of sexual dimorphism being expressed at different sections of the mandible. Furthermore, we find significant differences in how sexual dimorphism is expressed phenotypically even amongst closely related species with small divergence times. We discuss the potential pathways leading to such variation and the implications for extinct hominin variability.

ObjectiveThe patterning cascade model of crown morphogenesis has been studied extensively in a variety of organisms to elucidate the evolutionary history surrounding postcanine tooth form. The current research examines the degree to which model expectations are reflected in the crown configuration of lower deciduous and permanent molars in a modern human sample. This study has two main goals: 1) to determine if metameric and antimeric pairs significantly differ in size, accessory trait expression, and relative intercusp spacing, and 2) to establish if the relative distance among early-forming cusps accounts for observed variation in accessory cusp expression. MethodsTooth size, intercusp distance, and morphological trait expression data were collected from 3D scans of mandibular dental casts representing 124 individual participants of the Harvard Solomon Islands Project. Paired tests were utilized to compare tooth size, accessory trait expression, and relative intercusp distance between diphyodont metameres and permanent antimeres. Proportional odds logistic regression was implemented to investigate how the likelihood of accessory cusp formation varies as a function of the distance between early-developing cusps. Results/SignificanceFor paired molars, results indicated significant discrepancies in tooth size and cusp 5 expression, but not cusp 6 and cusp 7 expression. Several relative intercusp distances emerged as important predictors of accessory cusp expression. These findings support previous quantitative genetic results and suggest the development of neighboring crown structures represents a zero-sum partitioning of cellular territory and resources. As such, this study contributes to a better understanding of the evolution of deciduous and permanent molar crown configuration in humans.

There is a longstanding interest in whether the loss of complex characters is reversible (so-called "Dollos law"). Reevolution has been suggested for numerous traits but among the first was Kurten (1963), who proposed that the presence of the second lower molar (M2) of the Eurasian lynx (Lynx lynx) was a violation of Dollos law because all other Felids lack M2. While an early and often cited example for the reevolution of a complex trait, Kurten (1963) and Werdelin (1987) used an ad hoc parsimony argument to support their proposition that M2 reevolved in Eurasian lynx. Here I revisit the evidence that M2 reevolved in Eurasian lynx using explicit parsimony and maximum likelihood models of character evolution and find strong evidence that Kurten (1963) and Werdelin (1987) were correct - M2 reevolved in Eurasian lynx. Next, I explore the developmental mechanisms which may explain this violation of Dollos law and suggest that the reevolution of lost complex traits may arise from the reevolution of cis-regulatory elements and protein-protein interactions, which have a longer half-life after silencing that protein coding genes. Finally, I present a model developmental model to explain the reevolution M2 in Eurasian lynx.

Coelacanths, lungfishes, and holosteans represent three emblematic living fossil lineages, thought to be united by similar patterns of phenotypic change through time. While past studies suggest that diverse evolutionary patterns occur within these groups, it is unclear whether these reflect biological differences or arise from contrasting analytical approaches. Here, we examine these lineages under a common framework to assess variation in the evolution of discrete characters, and morphometric shape data, to test whether living fossils show comparable patterns of phenotypic evolution. Our results suggest different evolutionary modes occur, both among and within lineages, as a function of data type. For lungfishes, rates in discrete characters are highest in the Devonian and monotonically decline over time. Coelacanth rates show multiple early peaks followed by a decline toward the recent. Holostean rates show modest peaks but are broadly comparable over time. Patterns of body shape evolution also differ among clades, with strong support for declining rates over time for coelacanths but mixed evidence for similar dynamics in the other groups. Our results imply idiosyncratic processes of evolutionary change among traditional examples of living fossils and indicate a need to explicitly quantify patterns of change rather than apply informal, often qualitative, macroevolutionary classifications.

Quantitative analyses of morphological variation using geometric morphometrics are often performed on 2D photos of 3D structures. It is generally assumed that the error due to the flattening of the third dimension is negligible. However, despite hundreds of 2D studies, few have actually tested this assumption and none has done it on large animals, such as those typically classified as megafauna. We explore this issue in living equids, focusing on ventral cranial variation at both micro- and macro-evolutionary levels. By comparing 2D and 3D data, we found that size is well approximated, whereas shape is more strongly impacted by 2D inaccuracies, as it is especially evident in intra-specific analyses. The 2D approximation improves when shape differences are larger, as in macroevolution, but even at this level precise inter-individual similarity relationships are altered. Despite this, main patterns of sex, species and allometric variation in 2D were the same as in 3D, thus suggesting that 2D may be a source of noise that does not mask the main signal in the data. However, the problem is complex and any generalization premature. Morphometricians should therefore test the appropriateness of 2D using preliminary investigations in relation to the specific study questions in their own samples. We discuss whether this might be feasible using a reduced landmark configuration and smaller samples, which would save time and money. In an exploratory analysis, we found that in equids results seem robust to sampling, but become less precise and, with fewer landmarks, may slightly overestimate 2D inaccuracies.

Morphological covariation within the modern human postcanine dentition remains an open field of study. Analysis of covariation patterns of the three-dimensional (3D) shape between different tooth types has been seldom conducted, but it is relevant for the advancement of human biology and evolution, as well as dental anthropology, phylogeny, and medicine. Here, we analysed 3D shape covariation of the postcanine dentition (excluding third molars), both within and between dental arches using geometric morphometrics (GM). Based on high-resolution ({micro}CT) scans of 526 teeth from 136 individuals we found high pairwise correlation in tooth pairs within the dental arches (lower P3 and P4, r1 = 0.89; upper P3 and P4, r1 = 0.81; upper M1 and M2, r1 = 0.86). The correlation values between antagonists varied notably from the highest value detected between upper and lower M1s (r = 0.9), to the lowest between upper P4s and lower M1s (r = 0.58). Of all analysed tooth types, only the upper M1s showed moderate to high correlation in every pair analysis. Noticeably, unusually high covariation was detected between some of the tooth type pairs that do not articulate in a normal dentition (e.g., lower P3 and upper M2, r1 = 0.88). Furthermore, a relatively high covariation was found in the pairs of lower P4s and M1s (r1 = 0.79), and upper P4s and M1s (r1 = 0.77), which are the only tooth type pairs of the postcanine dentition belonging to different tooth classes (premolars and molars, respectively) and still serving similar masticatory functions. This study points to the fact that higher morphological integration seems to characterize teeth within the same dental arch rather than between antagonistic teeth. With this study, we provided an overview of pairwise correlations and strength of covariation between different tooth types. This information might inform future studies aimed at understanding developmental, phylogenetic, and functional aspects of the human postcanine dentition, including possible phenotype-genotype associations. However, with this study being the first one performed on a 3D sample of this size, we also report on obstacles and peculiarities that have been determined.

In modern humans, facial soft tissue thicknesses have been shown to covary with craniometric dimensions. However, to date it has not been confirmed whether these relationships are shared with non-human apes. In this study, we analyze these relationships in chimpanzees (Pan troglodytes) with the aim of producing regression models for approximating facial soft tissue thicknesses in Plio-Pleistocene hominid individuals. Using CT scans of 19 subjects, 637 soft tissue, and 349 craniometric measurements, statistically significant multiple regression models were established for 26 points on the face and head. Examination of regression model validity resulted in minimal differences between observed and predicted soft tissue thickness values. Assessment of interspecies compatibility using a bonobo (Pan paniscus) and modern human (Homo sapiens) subject resulted in minimal differences for the bonobo but large differences for the modern human. These results clearly show that (1) soft tissue thicknesses covary with craniometric dimensions in P. troglodytes, (2) confirms that such covariation is uniformly present in both extant Homo and Pan species, and (3) suggests that chimp-derived regression models have interspecies compatibility with hominids who have similar craniometric dimensions to P. troglodytes. As the craniometric dimensions of early hominids, such as South African australopithecines, are more similar to P. troglodytes than those of H. sapiens, chimpanzee-derived regression models may be used for approximating their craniofacial anatomy. It is hoped that the results of the present study and the reference dataset for facial soft tissue thicknesses of chimpanzees it provides will encourage further research into this topic.

The scaling pattern of the forelimb in Carnivora was determined using a sample of 30 variables measured on the scapula, humerus, radius, ulna, and third metacarpal, of 429 specimens belonging to 137 species of Carnivora. Standardized major axis regressions on body mass were calculated for all variables, using both traditional regression methods and phylogenetically independent contrasts (PIC). In agreement with previous studies on the scaling of the appendicular skeleton, conformity to either the geometric similarity hypothesis or the elastic similarity hypothesis was low. The scaling pattern of several phyletic lines and locomotor types within Carnivora was also determined, and significant deviations from the scaling pattern of the order were found in some of these subsamples. Furthermore, significant evidence for differential scaling was found for several variables, both in the whole sample and in various phylogenetic and locomotor subsamples. Contrary to previous studies, significant differences were found between the allometric exponents obtained with traditional and PIC regression methods, emphasizing the need to take into account phylogenetic relatedness in scaling studies. In light of these and previous results, we conclude that similarity hypotheses are too simplistic to describe scaling patterns in the carnivoran appendicular skeleton, and thus we propose that scaling hypotheses should be built from similarities in the scaling patterns of phylogenetically narrow samples of species with similar locomotor requirements. The present work is a first step in the study of those samples.

INTRODUCTIONThe original brain lag hypothesis proposed that primate brain evolution depended on spare energy derivative of savings of scale enabled by increasing body size. Deaner & Nunn [1] concluded that, in fact, there was no evidence for a brain lag. However, their result may have been due to a number of possible confounds in their analysis. METHODSI revisit their analysis to test for potential confounds using updated datasets. I also ask how primates paid for the energy costs incurred by changes in brain and body mass, and whether the impetus for these changes was predation risk. Finally, I ask whether the observed patterns explain the brain/body size ratio trajectory observed in fossil hominins. RESULTSI show that using statistically more appropriate statistics and updated data yields a significant brain lag effect. However, contrary to the original brain lag hypothesis, the brain/body ratio does not converge back on the allometric regression line, but continues to evolve beyond it. Increases in brain size are correlated with exploiting large group size rather than body size as the principal defence against predation risk, with significant growth in brain size (but not body size) only being possible if species adopted a more frugivorous diet. Finally, I show that hominins followed a similar trajectory from an australopithecine baseline that fell on the relevant allometric regression. CONCLUSIONThe brain lag effect is much more complicated than the original hypothesis proposed, with a distinctive switch from body to brain over evolutionary time.

This paper is concerned with rank deficiency in phenotypic covariance matrices: first to establish it is a problem by measuring it, and then proposing methods to treat for it. Significant rank deficiency can mislead current measures of whole-shape phenotypic integration, because they rely on eigenvalues of the covariance matrix, and highly rank deficient matrices will have a large percentage of meaningless eigenvalues. This paper has three goals. The first is to examine a typical geometric morphometric data set and establish that its covariance matrix is rank deficient. We employ the concept of information, or Shannon, entropy to demonstrate that a sample of dire wolf jaws is highly rank deficient. The different sources of rank deficiency are identified, and include the Generalized Procrustes analysis itself, use of the correlation matrix, insufficient sample size, and phenotypic covariance. Only the last of these is of biological interest. Our second goal is to examine a test case where a change in integration is known, allowing us to document how rank deficiency affects two measures of whole shape integration (eigenvalue standard deviation and standardized generalized variance). This test case utilizes the dire wolf data set from Part 1, and introduces another population that is 5000 years older. Modularity models are generated and tested for both populations, showing that one population is more integrated than the other. We demonstrate that eigenvalue variance characterizes the integration change incorrectly, while the standardized generalized variance lacks sensitivity. Both metrics are impacted by the inclusion of many small eigenvalues arising from rank deficiency of the covariance matrix. We propose a modification of the standardized generalized variance, again based on information entropy, that considers only the eigenvalues carrying non-redundant information. We demonstrate that this metric is successful in identifying the integration change in the test case. The third goal of this paper is to generalize the new metric to the case of arbitrary sample size. This is done by normalizing the new metric to the amount of information present in a permuted covariance matrix. We term the resulting metric the relative dispersion, and it is sample size corrected. As a proof of concept we us the new metric to compare the dire wolf data set from the first part of this paper to a third data set comprising jaws of Smilodon fatalis. We demonstrate that the Smilodon jaw is much more integrated than the dire wolf jaw. Finally, this information entropy-based measures of integration allows comparison of whole shape integration in dense semilandmark environments, allowing characterization of the information content of any given shape, a quantity we term latent dispersion.

Felidae, a family of the order Carnivora, includes extinct and extant species of cats spread across a wide ecological and geographical landscape. Cats are well-suited for predation due to various physical and behavioral characteristics, such as optimized limb length, skull shape, as well as enhanced hearing and vision. Morphological changes across Felidae species, particularly changes in skull shape, are likely explained by differences in predatory and feeding behaviors. Toward that end, cranial shape was analyzed across six different extant and extinct Felidae species using two-dimensional geometric morphometrics. From the lateral cranial view, we discovered that the cheetah (Acinonyx jubatus) and the North American Sabretooth (Smilodon) had the most significant shape divergence, specifically at the frontal bone and post orbital regions of the skull. Specifically, we found that the Sabretooth had a significantly shorter coronoid process compared to other Felids. We also observed a significant difference in post orbital shape in the cheetah dorsal cranium. Interestingly, we found that both the cheetah and the extinct North American Lion demonstrate significant shape asymmetry in the postorbital region from a ventral view of the skull. Shape divergence and asymmetry in select Felid skulls may arise from decreased genetic diversity. Taken together, we reasoned that morphological changes in skull shape likely evolved to support differences in predatory behavior across Felidae.

The modern human foot is a complex structure thought to play an important role in our ability to walk and run efficiently. Comparisons of our feet to those of our evolutionary ancestors and closest living relatives have linked the shape of several foot components (e.g., the longitudinal and transverse arches, size of the heel and length of the toes) to specific mechanical functions. But since foot shape varies widely across the modern human population, this study aimed to investigate how closely foot shape, deformation and joint mechanics during various locomotor tasks are actually linked. And whether the latter can be accurately predicted based entirely on the former two. A statistical shape-function model (SFM) was constructed by performing a principal component analysis on 100 participants three-dimensional foot scans, and joint angles and moments captured during level, uphill, and downhill walking and running. This SFM revealed that the main sources of variation were the longitudinal and transverse arches, relative foot proportions and toe shape along with their associated joint mechanics. However, each of these only accounted for a small proportion of the overall variation in foot shape, deformation and joint mechanics, most likely due to the high structural complexity and variability of the foot. Nevertheless, a leave-one-out analysis showed that the SFM can be used to accurately predict the joint angles and moments of a new foot based only on its shape. These results have implications and potential applicability across numerous fields, such as evolutionary anthropology, podiatry, orthopaedics and footwear design.

AbstractAccounting for phylogenetic relatedness in the analysis of shape has become a common practice, deemed necessary to factor in the non-independence between species because of common ancestry. However, when adjusting error distributions to account for relatedness, the phylogenetic-generalised-least-squares (PGLS) test can obscure an important component of variation called conservative trait correlation (CTC). This is the amount of variation in a response variable that is both attributable to a predictor variable and phylogenetically structured. If CTC represents a large amount of correlated variation, true biological associations with strong phylogenetic signal (from unrepeated evolutionary events for example) might not be supported using a PGLS. We demonstrate this effect using geometric morphometric shape analysis on 370 crania from the speciose Australian rock- wallabies (genus Petrogale). In this clade, well-recognised allometric patterns such as scaling of the braincase (Hallers rule) and snout length (craniofacial evolutionary allometry) are supported using ordinary least squares (OLS) regression, but not PGLS, indicating that important between-species shape variation is lost. We then apply two methods capable of quantifying aspects of the missing variation: variation partitioning (VARPART), which estimates the proportion of variation shared between the predictor and phylogeny, and multi- response phylogenetic mixed models (MR-PMM), which identify the strength of correlation within the phylogenetic component of trait variance. Both methods show that CTC dominates the allometric shape variation in our sample, highlighting its importance in assessing phylogenetically informed models. We suggest approaches that can consider CTC become more widely used to better understand morphology and its predictors.

Developmental systems may preferentially produce certain types of variation and, thereby, bias phenotypic evolution. This is a central issue in evolutionary developmental biology, albeit somewhat understudied. Here we focus on the shape of the first upper molar which shows a clear, repeated tendency for anterior elongation at different scales from within mouse populations to between species of the Mus genus. In contrast, the lower molar displays more evolutionary stability. We compared upper and lower molar development of mouse strains representative of this fine variation (DUHi: elongated molars and FVB: short molars). Using a novel quantitative approach to examine small-scale developmental variation, we identified temporal, spatial and functional differences in tooth signaling centers between the two strains, likely due to different tuning of the activation-inhibition mechanisms ruling signaling center patterning. Based on the spatio-temporal dynamics of signaling centers and their lineage tracing, we show an intrinsic difference in the fate of signaling centers between lower and upper jaw of both strains. This can explain why variations in activation-inhibition parameters between strains are turned into anterior elongation in the upper molar only. Finally, although the \"elongated\" DUHi strain was inbred, first molar elongation was variable in adults, and we found high levels of intra-strain developmental variation in upper molar development. This is consistent with the inherent developmental instability of the upper molar system enabling the morphological variability of the tooth phenotype.\n\nIn conclusion, we have uncovered developmental properties that underlie the molars capacity for repeated phenotypic change, or said differently, that underlie a \"line of least resistance\". By focusing on the developmental basis of fine phenotypic variation, our study also challenges some common assumptions and practices in developmental and evolutionary developmental biology.

Domestic dogs (Canis familiaris) display more morphological variation than any other mammal. Cranial morphology has been extensively studied, as have the relationships with function, development, genetics, veterinary medicine, and breed welfare. Postcrania remain comparatively understudied, despite well-documented breed-specific predispositions to musculoskeletal disease. Here, we apply three-dimensional landmark-free morphometrics to quantify the shape of 743 elements from 213 dogs, including the scapula, humerus, radius, ulna, pelvic girdle, femur, tibia, and fibula. We assess integration among limb elements and investigate drivers of shape variation within and between breeds. Across most breeds, limb bone shape is strikingly similar. Dachshunds, however, exhibit distinct morphology across all elements and one to two orders of magnitude greater variation than any other breed. Despite this disparity, integration remains high between all element pairs. Remarkably, we find no significant relationship between bone shape and body mass, age, or pathology, but comparison with historic specimens reveals marked changes in dachshund long bone shape over the past [~]150 years. These extreme differences are not shared by other sampled chondrodysplastic breeds, underscoring the need to understand morphological diversity beyond simple categorisation. These findings provide a quantitative framework for linking postcranial morphology with function, disease risk, and evidence-based improvements to canine welfare.

In order to understand the energy implications of primate limb conformation, the biomechanics of swing phase and the vertical movements of limb center of gravity were examined in the arboreal rhesus macaque (Macaca mulatta) and the semi-terrestrial long-tailed macaque (Macaca fascicularis). The objective was to better understand the potential variation in locomotor adaptations in these two macaque species within different ecological environments. In particular, the objective of this study was to identify the implications that these movements have on the internal energy costs of locomotion. I show that the biomechanics of swing phase for these two species have important effects on their limb center of gravity, although they may have similar limb segment mass distributions. This study suggests that mechanical energy conservation during swing phase is important in mammalian locomotion.

The symphyseal anatomy of extant and fossil cercopithecids has not yet been demonstrated as a useful tool for taxonomic discrimination, and the source of variation in cercopithecid symphysis has not been addressed on a broad taxonomic scale. Here, we used linear and angular dimensions to quantify symphysis shape. Using univariate, multivariate data and allometric regressions (partial least squares and phylogenetic generalized least square regressions), we addressed the hypothesis that extant cercopithecids can be distinguished by symphysis shape. Significant differences in univariate and multivariate data and allometric regressions permitted to distinguish cercopithecids at the subfamilial, tribal, and genus levels. We showed that multivariate data followed the distribution expected under Brownian Motion and significantly discriminates taxa at different taxonomic levels. Colobine symphysis are characterized by developed inferior transverse tori, short planum alveolare, and short symphysis, whereas cercopithecine symphysis are characterized by developed superior transverse tori, long planum alveolare, and long symphysis. Exceptions to this pattern exist within each subfamily, and this study underlines the particular anatomy of Colobus and Presbytis among the colobines, Allenopithecus among the Cercopithecini, and Theropithecus and Lophocebus among the Papionini. We also demonstrate that the relative development of the transverse tori, the relative length of the planum alveolare and symphyseal inclination are dimorphic traits. Specifically, we show that the symphysis of Procolobus verus, Nasalis larvatus, and Papio anubis is strongly dimorphic.

Morphological integration and modularity are concepts that refer to the covariation level between the components of a structure. Species of the opossums, genus Didelphis, have been the object of several taxonomic and morphometric analyses but no study has so far analysed mandibular morphological integration and modularity at a species-level. The aim of this work was to check whether the body (corpus mandibulae, mandibular corpus) and the ramus (ramus mandibulae, ascending mandibular ramus) are separate modules in Didelphis pernigra using a two-dimensional geometric morphometric approach. For this purpose, a sample of hemimandibles from 36 D. pernigra (13 males and 23 females) was analysed using 17 landmarks in lateral view. The modularity hypothesis based on different developmental origins was tested, by using the RV coefficient. Later, the integration level was assessed applying a partial least-squares analysis (PLS). The underlying aim was to know whether the traditional division between mandibular body and ramus has a modular basis, as well as the morphological integration level between these two structures. Results reflected that landmarks integration was not uniform throughout the mandible but structured into two distinct modules: ramus and body. Results allow to conclude that allometry plays an important role in shape variation in this species, and that the hypotheses of two-module organization in males cannot be confirmed. Models that accurately represent the biting mechanics will strengthen our understanding of which variables are functionally relevant and how they are relevant to performances, not only masticatories.

The extent to which evolutionary transitions are shaped by developmental bias remains poorly understood. Classically, morphological variation is assumed to be abundant and continuous, but if morphogenesis biases how traits vary than evolutionary transitions might follow somewhat predictable steps. Compared to other anatomical structures, teeth have an exceptional fossil record which documents striking evolutionary trajectories toward complexity. Using computer simulations of tooth morphogenesis, we examined how varying developmental parameters influenced transitions from morphologically simple to complex teeth. We find that as tooth complexity increases, development tends to generate progressively more discontinuous variation which could make the fine-tuning of dietary adaptation difficult. Transitions from simple to complex teeth required an early shift from mesiodistal to lateral cusp patterning which is congruent with patterns of dental complexification in early mammals. We infer that the contributions of primary enamel knot cells to secondary enamel knots which are responsible for patterning lateral cusps may have been an important developmental innovation in tribosphenic mammals. Our results provide evidence that development can bias evolutionary transitions and highlights how morphogenetic modelling can play an important role in building more realistic models of morphological character evolution.

Increasing variability down serially segmented structures, such as mammalian molar teeth and vertebrate limb segments, is a much-replicated pattern. The same phenotypic pattern has conflicting interpretations at different evolutionary scales. Macroevolutionary patterns are thought to reflect greater evolutionary potential in later-forming segments, but microevolutionary patterns are thought to reflect less evolutionary potential and greater phenotypic plasticity. We address this conflict by recalculating evolutionary potential (evolvability) from a systematic review of published mammalian molar sizes, then directly measure phenotypic plasticity from a controlled feeding experiment. Effects on lengths and widths are discordant in a way that suggests general growth pathways have a role in phenotypically plastic dental responses to nutrition. Effects on successive trait means do not necessarily increase downstream, contrary to long-standing hypotheses. We confirm prior findings of increasing non-inherited variance downstream, showing decoupling between effects on trait mean and variance. These patterns can be explained by a cascading model of tooth development compounding the effect of developmental instability as an influence separate from general environmental effects on the developing embryo. When evaluated in terms of evolvability, later-developing molars are equally or more evolvable than earlier-developing molars, aligning their microevolutionary potential with macroevolutionary patterns in other serially segmented structures.