Journal of Human Evolution 181 (2023) 103395 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Early euprimates already had a diverse locomotor repertoire: Evidence from ankle bone morphology Oriol Monclús-Gonzalo a, 1, David M. Alba a, Anaïs Duhamel b, Anne-Claire Fabre c, d, e, *, 1,  f, a, *, 1 Judit Marigo a  de Paleontologia Miquel Crusafont, Universitat Auto Institut Catala noma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, 08193 Cerdanyola del Vall es, Barcelona, Spain b University of Lyon, ENSL, CNRS, LGL-TPE, Villeurbanne 69622, France c Naturhistorisches Museum Bern, 3005 Bern, Switzerland d Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland e Life Sciences Department, Vertebrates Division, Natural History Museum, London SW7 5BD, UK f Universitat Autonoma de Barcelona, Departament de Geologia, 08193 Cerdanyola del Vall es, Barcelona, Spain a r t i c l e i n f o a b s t r a c t Article history: The morphological adaptations of euprimates have been linked to their origin and early evolution in an Received 9 August 2022 arboreal environment. However, the ancestral and early locomotor repertoire of this group remains Accepted 8 May 2023 contentious. Although some tarsal bones like the astragalus and the calcaneus have been thoroughly Available online xxx studied, the navicular remains poorly studied despite its potential implications for foot mobility. Here, we evaluate early euprimate locomotion by assessing the shape of the naviculardan important Keywords: component of the midtarsal region of the footdusing three-dimensional geometric morphometrics in Early euprimates relation to quantified locomotor repertoire in a wide data set of extant primates. We also reconstruct the Locomotor repertoire Geometric morphometrics locomotor repertoire of representatives of the major early primate lineages with a novel phylogenetically Functional morphology informed discriminant analysis and characterize the changes that occurred in the navicular during the Paleogene archaic primateeeuprimate transition. To do so, we included in our study an extensive sample of na- Navicular viculars (36 specimens) belonging to different species of adapiforms, omomyiforms, and plesiadapiforms. Our results indicate that navicular shape embeds a strong functional signal, allowing us to infer the type of locomotion of extinct primates. We demonstrate that early euprimates displayed a diverse locomotor behavior, although they did not reach the level of specialization of some living forms. Finally, we show that the navicular bone experienced substantial reorganization throughout the archaic primate eeuprimate transition, supporting the major functional role of the tarsus during early primate evolu- tion. This study demonstrates that navicular shape can be used as a reliable proxy for primate locomotor behavior. In addition, it sheds light on the diverse locomotor behavior of early primates as well as on the archaic primateeeuprimate transition, which involved profound morphological changes within the tarsus, including the navicular bone. © 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction and leaping (VCL), climbing and suspensory behaviors, and terrestrial bipedalism, among others (Oxnard et al., 1990; Hunt Extant primates are very diverse in body size (from ~30 g in et al., 1996; Fleagle, 2013). Several evolutionary scenarios have mouse lemurs to 200 kg in male gorillas) and locomotor behavior, been proposed to explain the origin and evolution of primates of including arboreal and terrestrial quadrupedalism, vertical clinging modern aspect (or euprimate, sensu Hoffstetter, 1977) locomotor diversity from an adaptive viewpoint, but they remain highly debated (Napier and Walker, 1967; Walker, 1974; Cartmill, 1974, 1992; Szalay and Dagosto, 1980; Dagosto, 1988, 2007; Rasmussen, * Corresponding authors. E-mail addresses: fabreac@gmail.com (A.-C. Fabre), judit.marigo@uab.cat 1990; Sussman, 1991). The early adaptive radiation of euprimates ). (J. Marigo (adapiforms and omomyiforms) has been extensively investigated 1 O.M.G, A.-C.F., and J.M. contributed equally to this work. based on postcranial remains, especially ankle bones such as the https://doi.org/10.1016/j.jhevol.2023.103395 0047-2484/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 calcaneus, astragalus, and navicular, as they are well represented in comparatively poorly studied despite being important for midfoot the fossil record and considered to be good proxies for locomotor mobility as an intermediate between the astragalus and the distal habits among primates (e.g., Decker and Szalay, 1974; Szalay and tarsals and metatarsals (Lewis, 1980b; Su and Zeiniger, 2022). Only Decker, 1974; Conroy and Rose, 1983; Rose and Walker, 1985; a handful of studies have investigated the functional signal of the Covert, 1988; Gebo et al., 1991, 2015; Moya -Sola et al., 2012; Boyer navicular (Covert, 1988; Dagosto, 1988, 2007; Gebo et al., 1991; et al., 2013, 2015, 2017a; Llera Martín et al., 2022). The morphology Anemone and Covert, 2000; Dunn, 2010; Rose et al., 2011; Marigo  of these bones suggests that the archaic primateeeuprimate tran- et al., 2020), and none have used a geometric morphometrics sition was characterized by a substantial reorganization of the foot approach, quantified locomotor data, or phylogenetic comparative (Dagosto, 1988, 2007). Nonetheless, an integrative study relating methods. Differences in proximodistal elongation as well as in the foot bone morphology with quantified locomotor data in a broad morphology of the navicular facets among extant taxa with varied sample of living and extinct primates is currently missing. locomotor behaviors suggest that this bone may be useful for Among early euprimates, basal omomyiforms have been pro- inferring the locomotor behavior of extinct primates and, hence, posed to be more active and prone to leaping than basal adapiforms might provide additional insight into the reconstruction of the (Walker, 1974; Gebo, 1988; Rose, 1994; Boyer et al., 2013). However, ancestral euprimate morphotype from an adaptive viewpoint. differences in body size between the members of these groups have We aim to investigate the evolution and diversification of the hindered the interpretation of their morphological differences, as locomotor behavior of early euprimates. To do so, we use a three- adapiforms (except for some small forms such as Anchomomys dimensional (3D) geometric morphometric approach focused on frontanyensis) are substantially larger than most omomyiforms the navicular and based on a large sample of extant and extinct (Rose, 1994), although within the latter group there are also larger- species. These include representatives of the plesiadapiforms, as bodied species (Dunn et al., 2006; Dunn, 2010). For this reason, it they are considered an early paraphyletic radiation of stem pri- has been suggested that some morphological differences between mates (Bloch et al., 2007; Silcox et al., 2015, 2017). We generated a these groups might simply reflect size-scaling (allometric) effects novel data set including representatives of living lemuriforms and instead of fundamental differences in locomotor behavior, although noncatarrhine haplorrhines, as well as a large sample of early pri- body mass and locomotor behavior are functionally interwoven mates from the Paleocene and Eocene (plesiadapiforms, adapi- (Walker, 1974). Furthermore, for biomechanical reasons, foot type forms, and omomyiforms). We hypothesize that navicular has also been proposed as an important factor influencing tarsal morphology is functionally linked to the locomotor behavior of morphology (Morton, 1924; Moya -Sola  et al., 2012). Foot types primates. Specifically, we predict that navicular shape (quantified differ with respect to the location of the fulcrum, which is defined by means of a 3D geometric morphometrics approach) is a reliable as the position in which the lever (in this case, the foot) pivots predictor of the locomotor repertoire of extant primates and, thus, (Morton, 1924). Anthropoids and most nonprimate mammals have can be used to infer the locomotion of extinct primate species for a metatarsi-fulcrumating foot, with the fulcrum placed on the which this bone has been recovered. With regards to early eupri- heads of the metatarsals, associated with an increased load arm mates, we hypothesize that their locomotor repertoire was already (Morton, 1924). In contrast, extant strepsirrhines and tarsiers have diverse early on in their evolution as they rapidly diversified in the a tarsi-fulcrumating foot, where the fulcrum is located on the distal arboreal niche, exploring different ecological strategies within the tarsal bones; this provides them increased grasping abilities but arboreal milieu. Notwithstanding, we predict that their locomotor results in a reduced load arm, which is compensated by the elon- adaptations were less specialized than the ones present in some gation of the tarsus, especially the calcaneus and the navicular extant species. Finally, we hypothesize that the locomotor mode (Moy a-Sola et al., 2012). In addition, indriids are specialized VCLs played a critical role during the archaic primateeeuprimate tran- that depart from the tarsi-fulcrumating condition, being described sition, leading to substantial morphological changes in the foot as ‘tarsi-rotators’ because their foot displays a greater range of anatomy that can be traced on the navicular bone. inversioneeversion and acts solely as a force transducer instead of as a propulsive lever (Demes et al., 1996; Ankel-Simons, 2007). Moreover, they possess a derived adductor grasping mode (sensu 2. Materials and methods Gebo, 1985; Gebo and Dagosto, 1988) characterized by an enhanced grasping action of the hallux and the second digit that enables the 2.1. Sample composition, data collection, and phylogenetic tree exploitation of the vertical support niche despite their large body size compared to other vertical clingers and leapers. The analyzed sample is composed of 121 naviculars belonging to The functional morphology of the tarsus has been extensively 46 extant and 17 extinct primate species (alongside one specimen studied for the calcaneus and astragalus of extinct primates (e.g., attributed to Omomyidae indet. [UCMP V 134984]). The extant taxa Decker and Szalay, 1974; Szalay and Decker, 1974; Lewis, 1980a,b; represent nearly the entire genus diversity of strepsirrhines Godinot and Dagosto, 1983; Dagosto, 1988, 2007; Gebo, 1988; Gebo (cheirogaleids: n ¼ 8; galagids: n ¼ 2; indriids: n ¼ 8; lemurids: et al., 2000, 2001, 2012, 2015; Seiffert and Simons, 2001; Dunn n ¼ 15; lorisids: n ¼ 10; daubentoniids: n ¼ 5; and lepilemurids: et al., 2006; Dagosto et al., 2010; Dunn, 2010; Marivaux et al., n ¼ 2) and a representative sample of extant noncatarrhine hap- 2010, 2011; Moya -Sola et al., 2012; Boyer et al., 2013, 2015, 2017a, lorrhines (atelids: n ¼ 10; callitrichids: n ¼ 10; cebids: n ¼ 5; 2019; Gladman et al., 2013; Chester et al., 2015; Seiffert et al., 2015; pitheciids: n ¼ 9; and tarsiids: n ¼ 1). Due to the semi(terrestrial) Marigo  et al., 2016; Yapuncich et al., 2017, 2019). These two bones locomotor behavior of several catarrhine species, which is not account for the 31% and 38% of the fossil primate pedal remains adequate for comparison with early euprimates, this group has not preserved in the fossil record, respectively, indicating a strong bias been included in the sample. The extinct taxa correspond to 13 toward their study compared with other foot elements (Yapuncich omomyiforms, 19 adapiforms, and four plesiadapiforms. The 3D et al., 2022). They have been the most informative for our under- models of all specimens were downloaded from the online re- standing of foot function, as they present several traits related to pository MorphoSource (www.MorphoSource.org; Boyer et al., pedal grasping, load transmission, and degree of movements at the 2017b). The complete list of specimens analyzed is provided in crural, subtalar, and transverse tarsal joints (Su and Zeiniger, 2022), Supplementary Online Material (SOM) Table S1, the list of living allowing us to produce strong inferences about the locomotor species and their locomotor data in SOM Table S2, and the list of behavior of extinct species. In contrast, the navicular remains extinct species in SOM Table S3. 2 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 A phylogenetic tree (SOM Fig. S1) comprising all extant primates regularization/shrinkage approaches, which are commonly used to in our study was downloaded from the 10kTrees Project v. 3 (Arnold constrain the estimates of parameters such as the maximum like- et al., 2010). The criteria used to place the extinct taxa are explained lihood error, to address analyses in which the number of variables in SOM S1. Unless otherwise stated, all analyses were performed in exceed the sample number (Clavel et al., 2019). Next, we tested for R v. 4.2.2 (R Core Team, 2022), and the alpha level of significance significant correlation between shape and centroid size using the was set at p < 0.05. function ‘manova.gls’. Navicular shape variation To assess navicular shape variation across 2.2. Quantification of shape, impact of size, and navicular shape the sample, a principal component analysis (PCA) was performed variation using the species-mean Procrustes shape coordinates. The phy- logeny was plotted along with the results of the PCA, building a Quantification of shape using three-dimensional geometric mor- phylomorphospace using the function ‘phylomorphospace’ of the phometrics To accurately depict navicular shape, a series of 16 package phytools v. 0.7e20 (Revell, 2012). homologous anatomical landmarks (Fig. 1; Table 1) was placed on the 3D surface of each specimen using the software Landmark v. 2.3. Covariation between navicular shape and locomotion in extant 3.0.0.6 (Wiley, 2006). For those specimens belonging to the left euprimate species foot, a mirroring of the mesh was performed before placing the landmarks in order to have the same orientation for all specimens. To test the correlation between navicular shape and locomotor A generalized Procrustes analysis was carried out with the function behavior, a quantified locomotor data set was compiled from the ‘gpagen’ of the package geomorph v. 4.0.3 (Adams and Ota rola- available literature. To assemble this data set, six different loco- Castillo, 2013) to obtain the Procrustes shape coordinates (Rohlf motor categories were used, following several field studies as well and Slice, 1990; Mitteroecker and Gunz, 2009). A mean shape was as the descriptions for standardized primate locomotor and calculated for each species, and species means were used as input postural modes presented by Hunt et al. (1996): quadrupedalism in all further analyses. (Q), leaping (L), climbing (C), suspension (S), bridging (B), and Impact of size on navicular shape To assess the impact of navicular scrambling/clambering (S/C; see SOM S1 for further details). We size on navicular shape in the analyzed sample, we first examined next performed a PCA to assess if the locomotor categories the correlation between navicular size and body mass (SOM described in SOM Table S2 were suitable for describing the loco- Fig. S2). After that, we computed a series of allometric re- motor repertoire described in the field studies from which the lo- gressions of species-mean Procrustes shape coordinates vs. log10- comotor percentages were retrieved (SOM Fig. S3). transformed centroid size (CS; Goodall, 1991) in the entire sample A two-block partial least squares (2B-PLS) analysis (Rohlf and and two subsets: only euprimates (excluding plesiadapiforms) and Corti, 2000) was performed to study the covariation between euprimates except for the small vertical clingers and leapers (Tar- navicular shape and quantified locomotor data (SOM Table S2) in sius spectrum, Galago moholi, and Sciurocheirus alleni). We fitted a extant taxa. To do so, the function ‘two.b.pls’ from the package multivariate phylogenetic linear model with a Pagel's lambda by geomorph v. 4.0.3 (Adams and Ota rola-Castillo, 2013) was used. penalized likelihood using the ‘mvgls’ function of the package This method uses 3D landmark data and performs a singular value mvMORPH v. 1.1.6 (Clavel et al., 2015; Clavel and Morlon, 2020). A decomposition, which decomposes the covariance matrix of the penalized-likelihood approach is a modern formulation of the two blocks of variables into two matrices of eigenvectors (each one Figure 1. Landmark configuration and anatomy of the navicular bone. Plantar, proximal, and distal views of the navicular of Eulemur fulvus (USNM 542489, https://doi.org/10.17602/ M2/M15828). McCuLength (mesocuneiform-cuboid contact length), depicting the contact between the McFA (mesocuneiform facet area) and CFA (cuboid facet area), is shown as an orange dotted line (between landmarks 8 and 14). Abbreviations: AFA ¼ astragalar facet area; EnFA ¼ entocuneiform facet area; EcFA ¼ ectocuneiform facet area. See Table 1 for landmark definitions. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 3 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Table 1 and locomotor categories, we used a type II phylogenetic multi- Definition of the anatomical landmarks used in this study. To visualize placement of variate analysis of variance (MANOVA) with the function ‘man- the landmarks on the navicular bone, see Figure 1. ova.gls’ of the package mvMORPH v 1.1.6 (Clavel et al., 2015). The Landmark Definition multivariate phylogenetic linear models were fitted with a Pagel's 1 Most proximomedial point of the AFA lambda by penalized likelihood using the ‘mvgls’ function of the 2 Most proximolateral point of the AFA package mvMORPH v1.1.6 (Clavel et al., 2015). In comparison to 3 Plantarmost point of maximum curvature between LM1 and other modes, the advantage of using Pagel's lambda is that it pro- LM2 vides more flexibility in estimating the error structure, as if we 4 Dorsalmost point of maximum concavity between LM1 and LM2 5 Dorsolateralmost point of the EcFA were fitting a phylogenetic mixed model while accounting for de- 6 Plantarlateralmost point of the EcFA parture from Brownian motion (Clavel and Morlon, 2020). Signifi- 7 Dorsalmost point of the contact between the EcFA and the McFA cance was assessed using a Pillai statistic and 1000 permutations. 8 Plantarmost point of the contact between the EcFA and the McFA Phylogenetic discriminant function analysis To predict the loco- 9 Dorsalmost point of the contact between the McFA and the EnFA motor category of fossil euprimates, we carried out a recently 10 Plantarmost point of the contact between the McFA and the developed phylogenetic discriminant analysis. This consists of EnFA 11 Dorsomedialmost point of the EnFA fitting a generalized least-squares model on the extant species 12 Plantarmedialmost point of the EnFA data (training data set) to predict the locomotor category of each 13 Distolateralmost point of the CFA extinct euprimate species using both its Procrustes shape co- 14 Distomedialmost point of the CFA ordinates and its phylogenetic position. This new method is the 15 Proximolateralmost point of the CFA 16 Proximomedialmost point of the CFA first linear discriminant analysis which is both phylogeny- informed and applicable to high dimensional data sets (i.e., data Abbreviations: AFA ¼ astragalar facet area; LM ¼ landmark; EcFA ¼ ectocuneiform sets containing more traits than individuals). The fitting of the facet area; McFA ¼ mesocuneiform facet area; EnFA ¼ entocuneiform facet area; CFA ¼ cuboid facet area. model on the training data set was performed using the function ‘mvgls.dfa’ from the package mvMORPH v. 1.1.6 (Clavel et al., 2015), and the performance (misclassification rate) of the phylogenetic for one block of data) and a matrix of eigenvalues (the square-roots discriminant function analysis (pDFA) was assessed by performing of eigenvectors; Rohlf and Corti, 2000; Bookstein et al., 2003). The a LOOCV on the training set. It consists of removing each indi- significance of each linear combination is assessed by comparing vidual one by one from the training set, performing the pDFA only the singular value to those obtained after resampling. If the partial on the remaining individuals, and checking if the locomotor least squares (PLS) covariation coefficient (r-PLS) is higher than the category of the removed individual is well predicted. Then, we ones obtained from permutated blocks, its associated p-value is compared it to 1000 randomized predictions on the training set significant. (SOM Fig. S6). Group membership to a locomotor class and pos- terior probabilities for fossil taxa were calculated using the func- 2.4. Reconstruction of early euprimate locomotor behavior tion ‘predict.mvgls.dfa’ of the package mvMORPH v. 1.1.6 (Clavel et al., 2015). The predictions were made assuming an equal prior Prediction of the locomotor percentages To reconstruct the loco- probability of belonging to the different locomotor categories since motor repertoire of early euprimates, we used the two sets of ei- we do not have a priori knowledge of the prevalence of those genvectors generated by the singular warp analysis performed on categories in the geological period in which the extinct primates the previous covariance analysis (which was exclusively carried out lived. Posterior probabilities are not necessarily a good estimate of on extant species). Similar approaches have previously been the classification uncertainty because they may suffer from over- applied to reconstruct one block of shape variables from another fitting and do not accurately reflect out-of-sample prediction un- block (e.g., Torres-Tamayo et al., 2020). We projected the species- certainty (Qiao et al., 2009). As we previously did to evaluate the means Procrustes shape coordinates belonging to the early eupri- discriminant model performances, we assessed the classification mate species into the latent space generated after the singular warp uncertainty by using resampling techniques. For each fossil, we analysis. We then used the coefficients obtained from the linear repeated the class prediction several times from models trained on regression of the original latent variables to estimate the latent different subsamples of the training set, and we computed the variables corresponding to the second block (derived from the proportions in which the fossil was assigned to each locomotor quantified locomotor behavior data). The resulting variables can be class. Each training set was obtained using two different sub- projected back to obtain the quantified locomotor behavior of the sampling approaches inspired from leave-one-out and K-fold early euprimate species. Finally, the locomotor percentages were cross-validation. The leave-one-out subsampling approach con- predicted after reversing the arcsin square-root transformation and sisted in removing one by one each extant individual from the normalization (to ensure that their total sum was equal to 100). training set and predicting the fossils' classes from a model trained To check the accuracy of this method, we performed a leave- on the remaining extant individuals. The K-fold subsampling one-out cross-validation (LOOCV) on the extant species set to approach consisted in randomly removing one-third of each lo- predict their quantified locomotor behavior and compare it with comotor class from the training setdsince the smaller class con- their actual quantified locomotor behavior. We calculated the mean tains three individualsdand predicting the fossils' classes from a absolute error (MAE; Willmott and Matsuura, 2005) and plotted model trained on the remaining extant individuals. The three-fold the estimated values against the original ones in a bivariate plot for random subsampling was repeated 200 times. The K-fold each locomotor variable to compare them and assess if the pre- approach tends to highlight more uncertainty in the predictions dictive performance of this method varied depending on the esti- because it destabilizes more consequently the training set. mated locomotor variable or the degree of locomotor Convergence analyses To identify morphological convergence specializations of some species (SOM Figs. S4 and S5; SOM depending on similar locomotor behaviors, we utilized a phyloge- Table S4). netic ridge regression method of the package RRPhylo v. 2.5.8 Phylogenetic multivariate analysis of variance To assess the differ- (Castiglione et al., 2019). First, a phylogenetic ridge regression was ences between navicular shape and foot type, taxonomic groups, performed on the tree with the species-means Procrustes shape 4 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 coordinates of the navicular, using the ‘RRPhylo’ function to obtain sampling every 10,000 iterations, and the first 25,000,000 iterations the branch-wise evolutionary rates and the ancestral character were discarded as burn-in (SOM Table S5). Trace plots were exam- estimates at each node. After that, morphological convergence was ined, and the 10 independent chains that were stationary after burn- tested using the function ‘search.conv’ of the package RRPhylo v. in were kept (SOM Fig. S7). The effective sample size (ESS) of the 2.5.8. Finally, the mean angle and the p-value of the mean angle posterior samples (ESS < 100) as well as the convergence of the were retrieved. chains were assessed with a Gelman and Rubin's convergence diagnostic (SOM Tables S5 and S6), with the functions ‘effectiveSize’ 2.5. Navicular morphological evolution and ‘Gelman.diag’ implemented in the package coda v. 0.19e4 (Plummer et al., 2005). Assessing the convergence of chains is critical Ancestral state reconstruction To assess the evolutionary model to detect large deviations among the different chains (non- that best depicts the evolution of the first two principal compo- convergence) and ensure similar between-chain variances (Gelman nents (PCs) of the PCA performed on the species-means Procrustes and Rubin, 1992). The results were plotted on the tree using the shape coordinates (Fig. 2), a maximum-likelihood approach was function ‘mytreebybranch’ (https://github.com/anjgoswami/salam used with the functions ‘mvBM,’ ‘mvOU,’ ‘mvEB,’ and ‘aicw’ of the anders/blob/master/mytreerateplotter.R). Branch-specific average package mvMORPH v. 1.1.6 (Clavel et al., 2015). The ancestral rates and the posterior probability of rate shifts (the mean of all ten morphotype for each node of the phylogenetic tree was estimated independent chains) were summarized using the ‘rjpp’ and ‘plot- with the function ‘estim’ of the package mvMORPH v. 1.1.6 (Clavel Shift’ functions of the package btrtools v. 0.0.0.9000 (https://github. et al., 2015). Finally, a phenogram plot, a projection of the phylo- com/hferg/btrtools/tree/master/R). genetic tree in a space defined by a shape variable (y axis) and time (x axis), was performed using the function ‘pheno’ of the 2.6. Shape visualization package phytools v. 0.7e20 (Revell, 2012) for each PC. Rates of morphological evolution To test the morphological evolution To visualize shape differences in navicular shape between the of the navicular, we estimated the branch-specific evolutionary rates extremes of the axes of the different analyses carried out, a thin- and rate shifts using the variable rates model applied in BayesTraits v. plate spline deformation of the 3D model of a navicular bone was 3 (http://www.evolution.rdg.ac.uk/). The shifts in the rate of carried out. Shape visualization of the effects of PCs, PLS, and continuous trait evolution, which was modeled using a Brownian discriminant function values was performed using the functions motion model, were detected with a reversible-jump Monte Carlo ‘shape.predictor’ and ‘plotRefToTarget’ of the package geomorph v. algorithm. The first 10 PCs of the phylogenetic PCA on the species- 4.0.3 (Adams and Ota rola-Castillo, 2013) and ‘shade3d’ of the mean Procrustes shape coordinates, computed using the function package rgl v. 0.100.47 (Adler and Murdoch, 2020). The specimen ‘phyl.pca’ of the package phytools v. 0.7e20 (Revell, 2012) accounting used as the reference was the navicular bone of Eulemur fulvus for >99% of the overall variation in navicular shape, were used as an (USNM 542489), which is adequate to represent the mean shape of input. Ten independent chains were run for 200,000,000 iterations, the sample. Figure 2. Phylomorphospace based on the first and second principal components (PCs of the principal component analysis carried out on the species-mean adjusted shape co- ordinates). Data points are color-coded by taxonomic group. The amount of variance explained by each PC is depicted below the axis in parenthesis. Navicular shapes associated with minimum (blue) and maximum (red) values along each PC (plantar, proximal, and distal views are shown from left to right and from top to bottom, as shown in Fig. 1). Thin plate splines correspond to the specimen of Eulemur fulvus USNM 542489. Abbreviations: EuLCA ¼ euprimate last common ancestor; Th ¼ Tetonius homunculus; Ag ¼ Arapahovius gazini; Oi ¼ Omomyidae indet.; Oc ¼ Omomys carteri; Ou ¼ Ourayia uintensis; Cl ¼ Chipetaia lamporea; Tb ¼ Teilhardina brandti; Afr ¼ Anchomomys frontanyensis; Nr ¼ Notharctus robustior; Nt ¼ Notharctus tenebrosus; Ct ¼ Copelemur tutus; Sg ¼ Smilodectes gracilis; Smc ¼ Smilodectes mcgrewi; Cr ¼ Cantius ralstoni; Ic ¼ Ignacius clarforkensis; Cs ¼ Carpolestes simpsoni; Ds ¼ Dryomomys szalayi; Tg ¼ Tinimomys graybulliensis. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 5 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 3. Results shape and locomotion (r-PLS ¼ 0.435, p ¼ 0.041). Proximodistally elongated naviculars with a more proximally projecting medial side 3.1. Navicular shape variation among primates at the astragalar facet are correlated with leaping, whereas prox- imodistally short and mediolaterally wide naviculars are associated No significant correlation is found between navicular shape and with preference for scrambling and clambering, bridging, and log10-transformed centroid size in the entire sample (Pillai's quadrupedal behaviors. However, among large VCL species, indriids trace ¼ 0.470, p ¼ 0.756) or among euprimates alone (Pillai's (indicated in the figure) depart from the general trend and display trace ¼ 0.561, p ¼ 0.415). Although navicular centroid size and body proximodistally shortened naviculars despite their proclivity for mass are significantly correlated (r2 ¼ 0.299, p < 0.001; see SOM leaping, thus indicating that proximodistal elongation is indicative Fig. S2), three species of vertical clingers and leapers (T. spectrum, of leaping behavior in tarsi-fulcrumating species but not in tarsi- G. moholi, and S. alleni) are clear outliers of the linear regression, rotator ones. Because of the importance of taking the type of foot displaying larger navicular centroid sizes than expected given their posture into account, we repeated the analysis, including only the body masses. Thus, we repeated the allometric analysis on eupri- tarsi-fulcrumating species. When tarsi-fulcrumators are considered mates excluding these three species and found a significant cor- alone (Fig. 3B), a stronger correlation is found between navicular relation between navicular shape and log10-transformed centroid shape and locomotion. Again, proximodistal elongation of the size, indicating intrinsic allometric effects (smaller naviculars are navicular is related to leaping proclivity, whereas a proximodistally relatively proximodistally longer compared to larger ones) in most short and mediolaterally broader navicular is characteristic of more euprimates (Pillai's trace ¼ 0.594, p ¼ 0.031). suspensory, bridging, and quadrupedal animals (r-PLS ¼ 0.824, The phylomorphospace of the first two PCs of a PCA based on the p < 0.001). species-mean Procrustes shape coordinates differentiates species by locomotor behavior and foot type (Fig. 2). PC 1 (63.44% of the 3.3. Reconstruction of the locomotor repertoire of early primates total variance) separates species depending on the degree of proximodistal elongation of the navicular, hence denoting a much The estimated locomotor percentages (Fig. 3A, B; Table 2) for wider distribution in tarsi-fulcrumating species (comprising extant early euprimate species depict two main patterns of locomotor strepsirrhines, tarsiers, and the extinct adapiforms and omomyi- repertoires. Omomyiforms as well as A. frontanyensis are charac- forms) than in metatarsi-fulcrumating ones (extant platyrrhines terized by intermediate to high reliance on leaping (34e65%), and plesiadapiforms). Slow climbers (SC, lorisids), large vertical moderate degrees of quadrupedalism and climbing (13e32%), and clingers and leapers (LVCL, indriids), suspensors/clamberers (SUS/ more modest values for the other locomotor variables (<10%, most CLA, atelids), clawed-leapers (CL, callitrichids), and many arboreal of them <5%). Among extant species, the locomotor repertoires of quadrupeds/large leapers (AQ/LL, cebids, pitheciids, and Dau- Microcebus and Mirza are the ones that more closely resemble the bentonia madagascariensis) display negative scores with a prox- reconstructed ones for these taxa. Except for A. frontanyensis, the imodistally short navicular. In contrast, the small-sized vertical other adapiforms display higher percentages of quadrupedalism clingers and leapers (tarsiids and galagids), which possess a very (30e50%) and climbing (21e40%) and variable reliance on leaping proximodistally elongated navicular, display positive scores. Spe- (7e33%), although always below the percentages displayed by cies with a moderate proximodistal elongation, such as the cheir- omomyiforms. Some species, like Notharctus robustior, also display ogaleids, the lemurids, and the large VCL Lepilemur mustelinus, moderate percentages of suspension (17%), whereas bridging and display intermediate scores. Extinct species are distributed along scrambling/clambering percentages are very low for all species the first axis, forming three differentiated clusters: omomyiforms (less than 6%). These species are reconstructed as above-branch overlap with cheirogaleids, displaying moderate proximodistal quadrupeds and climbers, and the better analogues for their loco- elongation without reaching the extreme shown by tarsiids and motor repertoire are the lemurids, especially the larger forms such galagids; adapiforms occupy the same range as lemurids and as Lemur catta or Varecia variegata. There are no important differ- L. mustelinus; and plesiadapiforms fall apart of the other species, ences between the predictions obtained from the analysis carried exhibiting a proximodistally short navicular outside the euprimate out on the entire extant sample and the sample comprised only by morphospace. tarsi-fulcrumators, although the latter are slightly less scattered Principal component 2 (8.83% of the total variance) reflects across the fossil sample (omomyiforms and A. frontanyensis on the changes in the shape of the astragalar facet as well as the one hand, and the other adapiforms on the other, show more arrangement of the cuneiform facets. Plesiadapiforms differ from consistent within-group percentages) and yielded smaller MAEs for the other species in displaying a more transversely elongated all locomotor variables (SOM Table S4). astragalar facet on the medial side and having a medially and The phylogenetically informed discriminant analysis has a plantarly extended entocuneiform facet. In contrast, all euprimates misclassification rate of 0.152 after performing a LOOCV on the display an ovoid astragalar facet and more aligned cuneiform fac- training set (extant ones). Two estimates of group membership ets, though some small leapers like tarsiers possess a small classification confidence for each extinct species (comparing two and plantarly compressed mesocuneiform facet, and others, such subsampling techniques: leave-one-out and K-fold cross- as several anthropoids, display an L-shaped arrangement of the validation) are presented in Table 3. Figure 4 is the graphical facets. result of the pDFA (the plot of the species on the principal discriminant axes, which are those that better discriminate among 3.2. Navicular shape as a proxy for locomotion the different locomotor categories). Omomyiforms are classified as cheirogaleid generalists (Omomys carteri, Ourayia uintensis, Chipe- Phylogenetic MANOVA results indicate that among living taia lamporea, and Omomyidae indet.), arboreal quadrupeds/large euprimate species, there are significant shape differences between leapers (Tetonius homunculus), or small VCL (Teilhardina brandti and locomotor categories (Pillai's trace ¼ 3.732, p ¼ 0.003) and foot type Arapahovius gazini). Conversely, all adapiforms fall into the arboreal (Pillai's trace ¼ 1.246, p ¼ 0.046), thus indicating that both loco- quadrupeds/large leapers category except for A. frontanyensis, motor behavior and type of foot posture impact navicular shape. which is classified as a large VCL. The first two blocks of the 2B-PLS analysis for the entire extant Convergence analyses (Table 4) confirmed the similarities be- sample (Fig. 3A) show significant covariation between navicular tween adapiforms and extant arboreal quadrupeds/large leapers 6 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Figure 3. Results of the two-block partial least squares (2B-PLS) between the species-mean Procrustes shape coordinates and quantified locomotor data for all extant species included in this study (A) and tarsi-fulcrumating ones (B). Data points are color coded by taxonomic group and shape is coded by locomotor category. The vectors of the first PLS axis of the locomotor variables are plotted in the right side of the figure. The predicted locomotor percentages for the fossil species are presented in a bar chart located next to the vectors for the first PLS axis for each condition. Navicular shapes associated with minimum (blue) and maximum (red) values of covariation are plotted below each scatterplot (plantar, proximal, and distal views are shown, from left to right and from top to bottom, as shown in Fig. 1). Thin plate splines correspond to the specimen of Eulemur fulvus USNM 542489. Abbreviations: Q ¼ quadrupedalism; B ¼ bridging; C ¼ climbing; L ¼ leaping; S ¼ suspension; S/C ¼ scrambling/clambering; Th ¼ Tetonius homunculus; Ag ¼ Arapahovius gazini; Oi ¼ Omomyidae indet.; Oc ¼ Omomys carteri; Ou ¼ Ourayia uintensis; Cl ¼ Chipetaia lamporea; Tb ¼ Teilhardina brandti; Afr ¼ Anchomomys frontanyensis; Nr ¼ Notharctus robustior; Nt ¼ Notharctus tenebrosus; Ct ¼ Copelemur tutus; Sg ¼ Smilodectes gracilis; Smc ¼ Smilodectes mcgrewi; Cr ¼ Cantius ralstoni; Al ¼ Avahi laniger; Ii ¼ Indri indri; Pd ¼ Propithecus diadema; Pv ¼ Propithecus verreauxi. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) and indicated a greater degree of convergence with lemurids than 3.4. Navicular evolution across the archaic primate–euprimate with platyrrhines. In contrast, no convergence was found between transition adapiforms (excluding A. frontanyensis) and cheirogaleids. Among adapiforms, the middle Eocene notharctid genera (Smilodectes and An ‘Early Burst’ model is the one that best explains the evolution Notharctus) also presented significant convergence with the group of PC1, showing a diversification of the proximodistal elongation of of specialized large VCL (indriids, Hapalemur griseus, and the navicular early in euprimate evolutionary history (Fig. 5A; L. mustelinus). Conversely, A. frontanyensis is classified as a large VCL Table 5). By contrast, PC2 evolution is best described by an ‘Orn- in the previous pDFA but shows no convergence with this group. steineUhlenbeck’ model, depicting stabilizing selection toward an Omomyiforms show convergence with the small VCL (T. spectrum euprimate-like navicular, with more ovoid astragalar facet and and the galagids), with the cheirogaleids, and with A. frontanyensis. straighter arrangement of the cuneiform facets (Fig. 5B; Table 5). No convergence was found between omomyiforms and either the Important shifts in rates of navicular evolution occur early in pri- extant arboreal quadrupeds/large leapers or the adapiforms mate evolution (Fig. 6; SOM Fig. S7). Remarkably, mean evolu- excluding A. frontanyensis. Lastly, no convergence was found be- tionary rates are extremely high in the branch leading to the tween the plesiadapiforms and the callitrichids (clawed leapers) euprimate ancestor. Other significant shifts occur earlier, during the and the lorisids (slow climbers). radiation of plesiadapiforms, and across the clade composed of the 7 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Table 2 Predicted locomotor repertoire for each extinct euprimate species. Locomotor percentages were calculated after normalization and reversion of the arcsin square root transformation on the estimated quantified locomotor behavior (see Materials and methods). Species Q L C S B S/C Entire sample Tf Entire sample Tf Entire sample Tf Entire sample Tf Entire sample Tf Entire sample Tf Tetonius homunculus 23.221 30.124 36.652 48.074 24.660 17.220 6.793 3.765 2.359 0.816 6.315 0.000 Arapahovius gazini 22.171 19.091 64.924 57.098 12.728 19.130 0.077 3.464 0.009 1.217 0.091 0.000 Omomyidae indet. 29.220 27.367 34.317 44.136 31.738 22.899 2.723 3.829 1.714 1.769 0.289 0.000 Omomys carteri 19.860 25.412 56.697 50.419 20.832 19.552 1.401 3.537 0.434 1.080 0.776 0.000 Ourayia uintensis 18.866 15.187 35.114 60.949 29.972 20.677 8.752 1.133 3.850 2.046 3.447 0.008 Chipetaia lamporea 16.930 13.006 45.972 58.101 26.900 22.981 4.923 3.858 3.283 2.053 1.992 0.001 Teilhardina brandti 19.444 23.082 59.632 59.353 15.167 15.456 0.792 1.823 0.314 0.285 4.651 0.000 Anchomomys 28.382 25.683 37.752 48.149 24.857 21.311 6.372 3.192 1.796 1.660 0.842 0.004 frontanyensis Notharctus robustior 31.520 41.483 13.308 17.143 31.011 24.745 17.279 11.622 6.010 5.003 0.872 0.003 Notharctus tenebrosus 34.429 38.204 23.614 32.606 32.127 22.408 6.809 4.899 2.699 1.880 0.323 0.003 Copelemur tutus 46.422 49.954 11.553 14.285 35.858 24.122 3.597 10.889 2.554 0.747 0.016 0.004 Smilodectes gracilis 29.627 36.695 12.842 31.928 39.545 25.238 12.076 4.470 5.456 1.665 0.455 0.004 Smilodectes mcgrewi 38.388 39.151 7.067 31.088 40.396 24.539 8.793 2.028 4.595 3.181 0.761 0.014 Cantius ralstoni 40.079 41.644 20.684 32.194 34.811 21.307 1.979 4.621 1.774 0.233 0.673 0.001 Abbreviations: Tf ¼ tarsi-fulcrumators; Q ¼ quadrupedalism; L ¼ leaping; C ¼ climbing; S ¼ suspension; B ¼ bridging; S/C ¼ scrambling/clambering. Table 3 Results of the phylogenetic discriminant analysis. Locomotor category predicted for each species and two estimates of group membership classification confidence (LOOCV and K-fold) are provided.a Species Classification AQ/LL CG CL LVCL SC SVCL SUS/CLA LOOCV K-fold LOOCV K-fold LOOCV K-fold LOOCV K-fold LOOCV K-fold LOOCV K-fold LOOCV K-fold Tetonius homunculus AQ/LL 0.891 0.447 0.109 0.478 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.075 0.000 0.000 Arapahovius gazini SVCL 0.000 0.000 0.022 0.433 0.000 0.000 0.000 0.000 0.000 0.000 0.978 0.567 0.000 0.000 Omomyidae indet. CG 0.022 0.190 0.978 0.752 0.000 0.000 0.000 0.007 0.000 0.000 0.000 0.052 0.000 0.000 Omomys carteri CG 0.000 0.000 0.978 0.842 0.000 0.000 0.000 0.000 0.000 0.000 0.022 0.158 0.000 0.000 Ourayia uintensis CG 0.000 0.000 0.978 0.877 0.000 0.000 0.000 0.000 0.000 0.000 0.022 0.123 0.000 0.000 Chipetaia lamporea CG 0.000 0.000 0.870 0.395 0.000 0.000 0.000 0.000 0.000 0.000 0.130 0.605 0.000 0.000 Teilhardina brandti SVCL 0.000 0.107 0.435 0.563 0.000 0.000 0.000 0.010 0.000 0.000 0.565 0.320 0.000 0.000 Anchomomys LVCL 0.065 0.357 0.000 0.222 0.000 0.000 0.935 0.422 0.000 0.000 0.000 0.000 0.000 0.000 frontanyensis Notharctus robustior AQ/LL 0.978 0.702 0.000 0.000 0.000 0.007 0.022 0.278 0.000 0.000 0.000 0.000 0.000 0.013 Notharctus tenebrosus AQ/LL 1.000 0.988 0.000 0.000 0.000 0.000 0.000 0.012 0.000 0.000 0.000 0.000 0.000 0.000 Copelemur tutus AQ/LL 1.000 0.982 0.000 0.000 0.000 0.018 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 Smilodectes gracilis AQ/LL 1.000 0.875 0.000 0.000 0.000 0.000 0.000 0.125 0.000 0.000 0.000 0.000 0.000 0.000 Smilodectes mcgrewi AQ/LL 1.000 0.985 0.000 0.000 0.000 0.008 0.000 0.007 0.000 0.000 0.000 0.000 0.000 0.000 Cantius ralstoni AQ/LL 1.000 0.995 0.000 0.000 0.000 0.000 0.000 0.005 0.000 0.000 0.000 0.000 0.000 0.000 Abbreviations: LOOCV ¼ leave-one-out cross-validation; K-fold ¼ K-fold cross-validation; AQ/LL ¼ arboreal quadrupeds/large leapers; CG ¼ cheirogaleid generalists; CL ¼ clawed leapers; LVCL ¼ large vertical clingers and leapers; SC ¼ slow climbers; SVCL ¼ small vertical clingers and leapers; SUS/CLA ¼ suspensors/clamberers. a The highest estimate for each method is marked in bold. early to middle Eocene notharctid species and within groups and Szalay, 1974; Gebo, 1988; Dagosto, 1988, 2007; Moy a-Sol a characterized by a particular locomotor behavior, such as the et al., 2012; Boyer et al., 2013). However, the functional associa- indriids, the lorisids, and the atelids. tion between tarsal elongation and leaping does not hold for some groups, such as indriids, which are highly committed leapers 4. Discussion despite possessing a proximodistally short navicular (Gebo and Dagosto, 1988). Other taxa, such as lemurids and anthropoids, The study of early euprimate locomotor diversity is essential to display a wide variation in leaping frequency among taxa with understand the factors that led to their origin and early diversifi- similar navicular shape, thus hampering locomotor inferences cation. A substantial reorganization of the postcranial skeleton, solely on this basis (Crompton et al., 1987; Gebo, 1987a; Oxnard including the tarsus, has been observed during the archaic et al., 1990). Biomechanical studies of leaping have shown there primateeeuprimate transition (Dagosto, 1988, 2007). Our study are various constraints related to the size of the animal (Demes and provides new clues on such a transition, shedding light on the Günther, 1989; Demes et al., 1996, 1999), leading to different remarkably diverse locomotor behavior of early euprimates on the anatomical solutions (Alfaro et al., 2005; Wainwright et al., 2005). basis of navicular shape, which emerges as a reliable proxy for Small-bodied leapers like tarsiers or small galagids must accelerate primate locomotor behavior. over small distances and hence need to maximize the time and distance required to generate enough impulse during takeoff. For 4.1. Understanding variation in navicular shape among primates this reason, small leapers possess very elongated feet, including the navicular in the midtarsal region (Hall-Crags, 1965; Demes and The elongation of different tarsal elements, such as the talar Günther, 1989). In contrast, large VCL species are constrained by neck, the cuboid, the navicular, or the distal part of the calcaneus, is the more limited force available to accelerate (muscle force in- informative about the locomotor behavior of extinct taxa (Decker creases as a function of area, whereas weight increases as a function 8 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Figure 4. Phylogenetic discriminant analysis based on the species mean-adjusted shape coordinates and locomotor categories. Data points are color coded by locomotor category (extant species) or taxonomic group (extinct species). Navicular shapes associated with minimum (blue) and maximum (red) values of each discriminant function (DF; plantar, proximal, and distal views are shown, from left to right and from top to bottom, as shown in Fig. 1). Thin plate splines correspond to the specimen of Eulemur fulvus USNM 542489. Abbreviations: Th ¼ Tetonius homunculus; Ag ¼ Arapahovius gazini; Oi ¼ Omomyidae indet.; Oc ¼ Omomys carteri; Ou ¼ Ourayia uintensis; Cl ¼ Chipetaia lamporea; Tb ¼ Teilhardina brandti; Afr ¼ Anchomomys frontanyensis; Nr ¼ Notharctus robustior; Nt ¼ Notharctus tenebrosus; Ct ¼ Copelemur tutus; Sg ¼ Smilodectes gracilis; Smc ¼ Smilodectes mcgrewi; Cr ¼ Cantius ralstoni. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) Table 4 distribution along PC1 of the phylomorphospace (Fig. 2), and sig- Results of the convergence analyses performed on species-mean adjusted shape nificant shape differences are found between groups. This distinc- coordinates between extinct and living primate species.a tion is linked to the loss of available load arm, that tarsi- Comparison Mean angle p-value fulcrumators compensate for by means of a greater elongation of Adapiforms and arboreal quadrupeds/ 13.332 0.001 the tarsal region (Morton, 1924; Moya -Sola  et al., 2012). large leapers Covariation analyses confirm the relationship between navic- Adapiforms and arboreal quadrupeds/ 9.494 0.009 ular shape and locomotor behavior, as well as the importance of large leapers (Lemuridae) considering foot-type posture. Both 2B-PLS analyses (Fig. 3) relate Adapiforms and arboreal quadrupeds/ 12.396 0.049 large leapers (Cebidae and proximodistal elongation of the navicular with leaping proclivity, Pitheciidae) whereas proximodistally short naviculars are associated with Adapiforms and cheirogaleid 15.643 0.162 quadrupedalism, bridging, and scrambling and clambering (Gebo, generalists 1988). However, proximodistal elongation is only correlated with Middle Eocene notharctids (Smilodectes 8.532 0.002 and Notharctus) and large vertical locomotor behavior among tarsi-fulcrumating species (Fig. 3B). For clingers and leapers example, indriids display a very proximodistally short navicular Anchomomys frontanyensis and large 18.470 0.32 despite their high proclivity toward leaping, with broad and vertical clingers and leapers shallow astragalar and cuneiform facets, as well as a more sellar- Omomyiforms and small vertical 11.429 0.011 shaped cuboid facet, features more related to climbing rather clingers and leapers Omomyiforms and cheirogaleid 9.103 0.006 than leaping behavior (Gebo and Dagosto, 1988). This set of features generalists is likely related to their particular foot type, in which the foot does Omomyiforms and arboreal 15.683 0.172 not act as a propulsor but as a force transducer (Demes et al., 1996). quadrupeds/large leapers Among metatarsi-fulcrumators, suspensors, scramblers, and Omomyiforms and North American 15.475 0.162 notharctids (Cantius, Copelemur, clamberers also display broader naviculars with wide and shallow Smilodectes and Notharctus) astragalar and cuneiform facets, whereas more quadrupedal and Omomyiforms and Anchomomys 8.330 0.002 leaping species possess narrow naviculars with deeper facets that frontanyensis enhance the stability of the astragalonavicular joint (Decker and Plesiadapiforms and clawed leapers 20.396 0.518 Szalay, 1974). Cuneiform facets (in particular the entocuneiform Plesiadapiforms and small climbers 22.371 0.687 facet) are also broader and shallower in more suspensory or a Significant results are indicated in bold for p < 0.05. climbing primates like lorisids (Gebo, 1989), compared to the nar- rower and more protuberant facets displayed by more quadrupedal or leaping species, such as galagids, in which the arrangement and of volume) and hence do not show such an elongation of the tarsal shape of the facets limit rotational movements (Hall-Craggs, 1966; elements (Gebo and Dagosto, 1988; Demes and Günther, 1989; Gebo, 1987b). Tarsiers are an exception to this trend, as they possess Demes et al., 1996). a navicular capable of rotating in both its proximal and distal ends Foot-type posture also impacts the degree of proximodistal to achieve foot inversion (Gebo, 1987b). Differences in the shape of elongation of the navicular. Tarsi-fulcrumating species display a the cuboid facet also exist between saltatory or more suspensory broader range of navicular elongation, as shown by their species as well as climbing taxa, the latter presenting broader and 9 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 and high proclivity for leaping (Gebo, 1988; Anemone and Covert, 2000; Rose et al., 2011; Gebo et al., 2012, 2015; Boyer et al., 2013). This is revealed in the phylomorphospace (Fig. 2), in which omo- myiforms display relatively similar scores to some extant small- bodied leapers (such as Microcebus or Mirza), although they do not overlap with any extant species and do not reach the extreme values displayed by specialized small VCL forms like T. spectrum or the galagids, suggesting that they lacked a specialized VCL locomotion. Moreover, the results from the prediction of their locomotor reper- toire (Fig. 3; Table 2) indicate a moderate to high proclivity for leaping, combined with lower percentages of quadrupedalism and climbing. Phylogenetic discriminant analysis classifies omomyiform species either as cheirogaleid generalists (C. lamporea, O. uintensis, Omomys carteri, and Omomyidae indet. [UCMP V 134984]) or small VCL (T. brandti and A. gazini), apart from T. homunculus, which falls in the arboreal quadrupeds/large leapers category (Table 3). The scat- terplot of the discriminant analysis (Fig. 4) and the results of the convergence analyses (Table 4) illustrate overall similarities between omomyiforms and both small VCL species and cheirogaleid gener- alists, indicating an active (yet not specialized for VCL) locomotor behavior for these species (Gebo, 1988). Interestingly, when the robustness of each classification is assessed by means of a sub- sampling technique (LOOCV and K-fold cross-validation), we find that the locomotor category that better suits to all omomyiforms is cheirogaleid generalists, whereas some specimens (belonging to T. homunculus and Omomyidae indet.) show moderate propensity for the arboreal quadrupeds/large leapers category, and others (including A. gazini, T. brandti, or C. lamporea) are more frequently classified as small VCL. The relatively elongated navicular of omo- myiforms, which falls within the cheirogaleid range, is the most important feature related with increased leaping behavior (Gebo, Figure 5. Phenogram based on the (A) first and (B) second principal components 1988; Boyer et al., 2013). In addition, the proximal protrusion of (Fig. 2) for all extant and fossil species and the reconstructed internal nodes following the proximomedial side of the astragalar facet and the shallower and an ‘Early Burst’ (A) or an ‘Ornstein-Uhlenbeck’ (B) evolutionary model (see also reduced cuneiform facets without a contact between the meso- Table 5). Tree branches are color-coded by taxonomic group. The euprimate last common ancestor is indicated by a black triangle in its corresponding node. Adapiform, cuneiform and the cuboid facets likely limit the degree in which omomyiform, and plesiadapiform ranges and their overlap with the other groups are rotational movements were accomplished along these articulations indicated by blue, green, and yellow shades, respectively. (For interpretation of the (Dagosto, 1988; Marigo  et al., 2020). The smaller estimated body size references to color in this figure legend, the reader is referred to the Web version of for most omomyiforms is also an important feature that has been this article.) related to a more agile locomotor repertoire (Rose, 1994). However, larger-sized omomyiforms such as O. uintensis and C. lamporea are Table 5 still classified in our analyses as relatively agile unspecialized leapers. Results of the evolutionary model comparison for the first and second principal This agrees with previous studies (Dunn et al., 2006; Dunn, 2010) components (PC) of the principal component analysis performed on the species- and indicates that an increased leaping behavior was a shared mean adjusted shape coordinates. The highest AICw for each PC is in bold. feature within the omomyiform locomotor repertoire. Tetonius Axis Evolutionary Loglikelihood AIC AICw homunculus, which compared to other omomyiforms shows in our model analyses more propensity for quadrupedal and climbing locomotion, PC1 BM 47.210 90.224 0.026 is also the one displaying less navicular proximodistal elongation, in OU 47.867 87.056 0.007 accordance with other features in the calcaneus and the astragalus, EB 51.849 ¡97.297 0.968 such a slightly shorter distal calcaneus and a mediolaterally broader PC2 BM 103.954 203.712 0.001 OU 113.198 ¡217.718 0.996 astragalar head (Gebo, 1988). One omomyiform genus, Necrolemur, EB 106.559 206.718 0.004 for which the navicular is unknown, displays similar tarsier-like Abbreviations: AICc ¼ Akaike Information Criterion corrected; AICw ¼ weighted morphological specialization in its hindlimbs, and likely had a AIC; BM ¼ Brownian motion; OU ¼ Ornstein-Uhlenbeck; EB ¼ Early Burst. different locomotor repertoire than the species present in our study. This would add more locomotor diversity to this group, which likely mediolaterally extended cuboid facets. This last feature is also included from active arboreal quadrupeds to specialized VCL in the relevant from a phylogenetic viewpoint, as the contact between the case of some later forms (Dagosto, 1985; Gebo, 1987b). cuboid and mesocuneiform facets is a strepsirrhine synapomorphy Adapiforms are considered basal strepsirrhines by most cladistic that has been related to increased midtarsal folding of the foot, an analyses (Seiffert et al., 2005; Williams et al., 2010). Moreover, adaptation toward the use of vertical supports (Beard et al., 1988; adapiforms share derived pedal traits with extant strepsirrhines, Dagosto, 1988). whereas omomyiforms usually retain a more primitive condition (Decker and Szalay, 1974; Gebo, 1986, 1988; Dagosto, 1988, 2007). 4.2. The diverse locomotion of early euprimates Adapiforms are generally larger than omomyiforms and charac- terized by less elongated tarsal bones, indicating that they were Among early euprimates, omomyiforms have been described as predominantly above branch arboreal quadrupeds with less pro- agile climbing and running animals, with active arboreal locomotion clivity for leaping (Rose and Walker, 1985; Covert, 1988; Gebo, 10 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Figure 6. Evolutionary rates and rate shifts for navicular shape in extant and extinct primates. Branch rates are color-coded (warmer colors indicate faster evolutionary rates while cooler colors represent slower evolutionary rates). High probability shifts in evolutionary rates are indicated by blue triangles. The relative size of the triangles represents the posterior probabilities (PP) of the rate shifts (see SOM Fig. S7 to visualize the PP of rate shifts). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 1988; Gebo et al., 1991; Boyer et al., 2013), as supported by our (Fig. 3; Table 2), and the results from the convergence analyses results (Figs. 3e5; Tables 2e4). The only exception is the small- (Table 4) also highlight the similarities in navicular shape between bodied adapiform A. frontanyensis, which possesses an A. frontanyensis and omomyiforms. Nevertheless, the more bulbous omomyiform-like tarsal elongation (Marigo  et al., 2016, 2020). This cuneiform facets and the contact between the mesocuneiform and is indicated in the phylomorphospace (Fig. 2), in which cuboid facets in A. frontanyensis are likely related to a more inverted A. frontanyensis falls very close to the omomyiform cluster. Despite foot posture than in omomyiforms, which some authors have these morphological similarities, there is no doubt that interpreted as an adaptation for the small branch niche (Marigo  A. frontanyensis is a basal strepsirrhine instead of an omomyiform. et al., 2020). Considering this, an active arboreal locomotion for Apart from the dental characters that identify A. frontanyensis as a A. frontanyensis, similar to that of Cheirogaleus or Mirza, is the best strepsirrhine (Marigo  et al., 2011), its navicular displays an unam- interpretation for its locomotor behavior. Interestingly, conver- biguous strepsirrhine synapomorphy: a contact between the mes- gence analyses also yielded significant convergence between ada- ocuneiform and the cuboid facets (Dagosto, 1988). Interestingly, the piforms and extant large VCL species. This is at odds with our contact between these facets in A. frontanyensis is more restricted prediction of the notharctid locomotor repertoire, which is domi- than in most extant strepsirrhines, probably a primitive retention nated by quadrupedalism and climbing (Table 4), and thus is closer from the ancestral euprimate, given that Cantius ralstoni, the most to that of above-branch quadrupeds than specialized VCL. In basal adapiform of our sample, also displays a very short contact addition, some authors have noted that the foot of notharctids (Beard et al., 1988; Marigo  et al., 2020). The prediction of its loco- lacked some morphological adaptations required to engage in VCL motor repertoire, similar to that of some omomyiform species locomotion, such as a derived adductor grasping mode (sensu 11 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 Gebo, 1985; Gebo and Dagosto, 1988), thus strengthening our view 5. Conclusions that these animals were more likely non-specialized arboreal quadrupeds, like the ringtail (Lemur catta) and ruffed lemurs Our study demonstrates that navicular shape is a reliable indi- (V. variegata). Similarly, the phylogenetic discriminant analysis cator of the locomotor behavior in primates and can be used as a classifies A. frontanyensis as a large VCL, in disagreement with the predictor to infer the locomotor adaptations of extinct species. results of other analyses for this taxon. We hypothesize that some Most notably, proximodistal elongation of this bone is related to similarities in navicular shape and elongation between leaping proclivity, although type of foot posture needs to be A. frontanyensis and the non-indriid large VCL (H. griseus and considered, as it can influence navicular morphology. Our research L. mustelinus) might have led to this result. In addition, when also shows that early euprimates displayed a diverse array of lo- resampling techniques (LOOCV and K-fold CV) are performed to comotor adaptations early on their evolution, although they did not assess the classification uncertainty of the pDFA, A. frontanyensis reach the level of specialization displayed by some living groups. shows moderate propensity for the AQ/LL and CG categories, thus Finally, we have assessed the archaic primateeeuprimate transition indicating a more agile arboreal locomotor behavior. by studying the morphological changes occurred in the navicular bone. Initial increases in navicular elongation, as well as other 4.3. The archaic primate–euprimate transition morphological features such as an ovoid astragalar facet, might be related to the acquisition of a tarsi-fulcrumating foot type and a Our results support that early euprimates underwent a rapid euprimate-like hallucal grasping, indicating a shift toward a more adaptive diversification very early in their evolutionary history, active locomotor behavior. Collectively, our results provide evi- which allowed them to occupy different arboreal niches (Figs. 5 dence that early euprimates emerged from a small and unspecial- and 6; Table 5). The postcranial remains of plesiadapiforms are ized grasp-leaper animal, but soon diversified into a broad range of scarce and usually belong to derived species, such as Carpolestes locomotor behaviors that allowed the occupation of different simpsoni, Plesiadapis cookei, or Ignacius clarkforkensis (Bloch and arboreal niches. Boyer, 2002; Bloch et al., 2007; Boyer and Gingerich, 2019), that are not representative of the early evolution of this group. How- Acknowledgments ever, a recent study carried out on the astragalus and calcaneus of the most basal plesiadapiform, Purgatorius, confirms that these This work has been supported by CERCA Programme/General- animals were arboreal but did not possess a euprimate-like grasp- itat de Catalunya, research projects PID2020-116908GB-I00 and leaping behavior (Chester et al., 2015). Instead, they are viewed as PID2020-117289GB-I00 financed by MCIN/AEI/10.13039/501100 arboreal clawed-climbers similar to the living scandentian Ptilo- 011033, and project CLT_2022_EXP_ARQ001SOLC_00000197 cercus lowi, which is also regarded as a good analogue for the financed by the Culture Department of the Generalitat de Cata- ancestral euarchontan (Szalay and Dagosto, 1988; Sargis, 2002, lunya, as well as the consolidated research groups 2022 SGR 01188 2004; Nyakatura, 2019). A remarkable exception is C. simpsoni, and 2022 SGR 00620 (Generalitat de Catalunya), Ramo n y Cajal whose partial skeleton displays euprimate-like hallucal grasping grant (RYC2021-034366-I to J.M.) funded by MCIN/AEI/10.13039/ features (Bloch and Boyer, 2002). The transition from an archaic 501100011033 and by the European Union NextGenerationEU/ primate to the ancestral euprimate is marked by a substantial PRTR, FI AGAUR fellowship (2021 FI_B 00524 and 2022 FI_B1 00131 increase in the proximodistal elongation of the navicular bone to O.M.G.) funded by the Secretaria d'Universitats i Recerca de la (extensive to the whole midtarsal region), together with the Generalitat de Catalunya and the European Social Fund. We want to acquisition of a more ovoid proximal facet as well as the rear- thank our colleagues Doug M. Boyer and Stephen G. B. Chester for rangement of the cuneiform and cuboid facets, allowing the foot providing insightful comments and suggestions that greatly to engage in more complex rotational movements at the astra- improved an earlier version of the manuscript. We thank Julien galonavicular joint and reducing the mediolateral translation of Clavel for providing the script for the discriminant analysis. We the foot (Szalay and Decker, 1974; Szalay and Drawhorn, 1980; thank the team of the online repository Morphosource and the Dagosto, 1988, 2007). These profound morphological changes following US institutions for providing access to specimens: explain the major shifts that occurred early in primate evolution, Museum of Natural History (NY), Duke Lemur Center Division of during the radiation of plesiadapiforms and in the branch leading Fossil Primates (NC), National Museum of Natural History (Wash- to the ancestral euprimate (Fig. 6; SOM Fig. S7). ington DC), University of California, Berkeley Museum of Paleon- The acquisition of a tarsi-fulcrumating foot by the ancestral tology (CA), University of Michigan Museum of Paleontology (MI), euprimate, presumably as an adaptation to access the fine-branch University of Wyoming (WY), and Stony Brook University (NY). We milieu, would have led to proximodistal elongation of the mid- also thank the Leakey Foundation General Research Grant (to Ste- tarsal region to compensate for the decreased load arm, followed by phen G. B. Chester). This article is part of the Ph.D. dissertation of a rapid diversification of locomotor behaviors (Morton, 1924). O.M.G. within the Geology Ph.D. program of the Universitat Omomyiforms retained a small body size and an active arboreal Auto noma de Barcelona. locomotor behavior for which cheirogaleids, particularly the agile Microcebus and Mirza rather than the more cautious Cheirogaleus, might be good analogues (Gebo et al., 1991, 2012, 2015; Anemone Author contributions and Covert, 2000; Rose et al., 2011). Omomyiforms show lower evolutionary rates than adapiforms, which experienced a body size O.M.G., A.-C.F., and J.M. designed the research; O.M.G., A. D., A.- increase that led to the acquisition of a different type of locomotion C.F., and J.M. carried out the research; O.M.G. and J.M. performed than the ancestral euprimate, arguably emphasizing above-branch data collection; O.M.G., A.-C.F., and J.M. analyzed the data; and quadrupedalism, as in extant lemurids (Rose and Walker, 1985; O.M.G., D.M.A., A.-C.F., and J.M. wrote the paper. Covert, 1988; Gebo et al., 1991). Some adapiforms, such as the small-bodied A. frontanyensis, converged toward the omomyiform Supplementary Online Material condition by displaying a more proximodistally elongated navicular as a result of more active arboreal locomotor behaviors (Marigo  Supplementary Online Material to this article can be found et al., 2016, 2020). online at https://doi.org/10.1016/j.jhevol.2023.103395. 12 O. Monclús-Gonzalo, D.M. Alba, A. Duhamel et al. Journal of Human Evolution 181 (2023) 103395 References Dagosto, M., 2007. The postcranial morphotype of primates. 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