1. Eberle Pls 508

Abstract Researchers often attempt to use limb proportions to ascertain the locomotor repertoires of fossil hominins. This can be problematic as there are few skeletons in the fossil record that preserve both a full forelimb and hindlimb; therefore, estimates of full limb lengths are typically associated with substantial error. In this study, two-block partial least squares analyses were used to examine covariation between forelimb and hindlimb elements in extant hominoids and fossil hominins. This has the benefit of including both forelimb and hindlimb in a type of functional analysis without necessitating an accurate length estimate.

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There is a high degree of covariation between forelimb and hindlimb segments in the mixed species sample, particularly in the proximal ulna, distal humerus, and proximal/distal femur and that shape covariation is significantly correlated with intermembral indices in the extant taxa. Overall, the fossil hominins most closely resembled modern humans with the exception of analyses utilizing the distal femur where some occupied a unique morphological position; thus, some fossil hominins likely possessed locomotor capabilities similar to modern humans, whereas others likely represent a unique morphological compromise between terrestrial bipedality and other positional behaviors not present among extant hominoids. Anat Rec, 2013.

© 2012 Wiley Periodicals, Inc. The most common way to examine the postcranium as a complex is to use body proportions. Numerous studies have been done on the partially complete skeletons of fossil hominins to quantify forelimb-to-hindlimb length and joint proportions with the aim of comparing these proportions to those seen in modern taxa in order to make inferences about locomotor patterns. Limb proportions are an important tool in determining possible locomotor repertoires in the fossil record as they are tightly correlated with positional behavior. Species that practice more suspensory, upper limb-dominated modes of locomotion tend to have longer forelimbs (both segment and total length) than hindlimbs. Species that practice hindlimb-dominated locomotor patterns, such as vertical clinging and leaping or bipedalism, have longer hindlimbs in proportion to the forelimb.

All of the extant apes have high intermembral indices with Pongo and Hylobates achieving the greatest forelimb-to-hindlimb lengths, whereas modern Homo sapiens has a quite low intermembral index reflecting the lengthening of the hindlimb as an adaptation to obligate bipedalism (Jungers,; Fleagle, ). Studies of fossil limb and joint proportions in the Plio-Pleistocene record have yielded complicated and sometimes contradictory results because of the fragmentary nature of the fossil record and the necessity of estimating limb lengths from incomplete specimens such as OH 62, KNM-ER 3735, and BOU-VP-12/1 (Johanson et al., 1987; Korey,; Hartwig-Scherer and Martin,; McHenry and Berger,; Asfaw et al.,; Richmond et al.,; Degusta,; Dobson,; Reno et al.,; Green et al.,; Haeusler and McHenry, ). Another potential way to examine patterns of postcranial variation to make inferences about locomotor patterns and morphological affinity to modern taxa is through the lens of morphological covariation between the forelimb and hindlimb. The forelimb and the hindlimb are functionally related and their morphology should be constrained by locomotor requirements; so, specific traits in the forelimb and hindlimb could be selected as a unit to meet the requirements of some locomotor activity (Cheverud, ). If the forelimb and hindlimb shapes covary, then it should be possible to examine patterns of covariation between regions of the appendicular skeleton and compare those patterns to those seen in extant reference taxa to make inferences about potential locomotor capabilities of fossil hominins. In other words, it should be possible to try and “match” the morphological pattern in the forelimb and hindlimb of fossil hominins to what is seen in the extant radiation. Although this sort of analysis relies on comparisons with extant taxa for functional conclusions and lacks the biomechanical information present in limb proportion studies, it does side-step the necessity of having complete bones and allows for the use of the more fragmentary material that is more frequently found in the hominin fossil record.

There have been only a few studies that have examined covariation in forelimb and hindlimb structures in adult primates. Rolian et al. (2010) compared the length and shape of manual and pedal phalanges in hominoids and found that they covaried strongly.

These authors have suggested that manual phalanx morphology is a byproduct of strong selection on the pedal morphology for efficient bipedality and not necessarily from selection for manual dexterity. tested covariance in length in serially homologous limb modules in humans, great apes, and some Old World monkeys. These authors found that forelimb and hindlimb integration was more relaxed in apes than in quadrupedal monkeys because of the difference in functional roles of the forelimb and hindlimb. This study seeks to examine the postcranium as an integrative unit in a way that avoids the necessity of estimating limb proportions. Instead of using indices such as limb or joint proportions, shape covariation is used to answer questions about the way that multiple bones of the postcranium could function as a unit and to address questions about potential morphological shape covariation and mosaic evolution. This study will address three research questions:.

1Is there strong shape covariation between the forelimb and hindlimb bones in extant hominoids and, if so, what are the correlated aspects of shape in the forelimb and hindlimb among the extant taxa?. 2Is the morphological pattern of covariance in forelimb and hindlimb elements correlated with intermembral indices in the extant hominoids?. 3Does the pattern of forelimb and hindlimb covariance differ among associated skeletons of earlier hominins and to what extent do their morphological patterns match those of the extant taxa? This information could potentially be used to make inferences about their locomotor capabilities.

MATERIALS AND METHODS Three-dimensional geometric morphometrics (3D-GM) is a morphometric approach that allows for the retention of shape information. This information is preserved in most statistical analyses, which allows for the visualization of shape changes among the original specimens (Rohlf and Slice, ). Twenty-five landmarks on the humerus, 16 landmarks on the radius, 23 landmarks on the ulna, 32 landmarks on the femur, and 20 landmarks on the tibia were collected as a series of x,y,z, coordinates (Figs., see Supporting Information Table S1 for a description of the points) using a Microscribe 3DX digitizer. Diagram illustrating the landmark and wireframe configuration on a elements from Homo sapiens. ( A) Humerus in posterior (left) and anterior (right) view. ( B) Radius in medial (left) and distal (right) view.

( C) Ulna in anterior (right), lateral (middle) view, and distal (left) view. ( D) Proximal femur in posterior (top left) and anterior (top right) view and distal femur in anterior (left), posterior (center), and distal (right) views. ( E) Tibia in proximal (top) and distal (bottom) views.

First axes (top) and second axes (bottom) from a singular value decomposition (SVD) of the cross-covariance (CCV) matrix of the data for the distal humerus and proximal femur as part of a 2BPLS. Homo is represented by open squares, Pan by squares, Gorilla by crosses, and Pongo by Xes. Fossils are labeled in the graph. Lines are convex hulls drawn around each extant group.

Wireframes are in an anterior view for the humerus and a posterior view for the femur, and are located by their respective axes. First axes (top) and second axes (bottom) from a SVD of the CCV matrix from the proximal ulna and distal femur as part of a 2BPLS. Homo is represented by open squares, Pan by squares, Gorilla by crosses, and Pongo by Xes. Fossils are labeled in the graph.

Lines are convex hulls drawn around each extant group. Wireframes are in a medial view for the ulna and distal view for the femur, and are located by their respective axes. The specimens were stabilized and oriented using modeling clay and points were taken in the same orientation on each individual. Data were collected on a modern comparative sample of Homo, Gorilla, Pan, and Pongo (Table ) as well as original fossils (Table ).

No casts were used in these analyses. Table 1. List of extant specimens used for this study by species, subspecies, and sex Males Females Unknown Total.

a Virunga isolates; RMCA. b Cameroon (and some gorilla males from Republic of Congo); PCM. c DRC; RMCA, AMNH-M. dBorneo, Sumatra; AMNH-M, NHM-M. Gorilla (N = 77) Gorilla gorilla beringei 2 3 0 5 Gorilla gorilla gorilla 24 26 0 50 Gorilla gorilla graueri 13 9 0 22 Homo sapiens (N = 76) Andaman Islanders 11 10 8 29 Australian Aborigines 3 3 8 14 Late Stone Age South Africans 8 4 1 13 Point Hope Ipiutak 15 15 0 30 Pan (N = 88) Pan paniscus 7 9 0 16 Pan troglodytes schweinfurthii 7 7 14 28 Pan troglodytes troglodytes 19 25 0 44 Pongo (N = 16) Pongo pygmaeus 9 6 1 16. Table 2. List of fossil individuals and elements used Accession # Taxon Elements A.L.

Afarensis Humerus, ulna A.L. Afarensis Femur KNM-ER 1500 P. Boisei Ulna, femur KNM-ER 1503/1504 Homo sp. Humerus, femur Omo (Kibish) 1 H.

Sapiens Humerus, ulna, femur KNM-WT 15000 H. Erectus Humerus, ulna, femur In the extant sample, all individuals were adults and displayed full epiphyseal closure at all joints. Where sex was not indicated on the specimen, it was determined using the pelvis in H.

Sapiens and using size for Pongo and Gorilla. If the sex was not given for Pan, or if the pelvis was missing for H. Sapiens, specimens were listed as unknown. No zoo specimens were sampled. Sapiens sample was chosen from maximally different populations to encompass a range of modern human variability. No modern morphological collections were sampled for modern humans as they presumably exhibit a high degree of genetic admixture; instead, archaeological and more isolated populations were sampled.

Previous studies have noted that covariation in elements of two different individuals within a single species does not differ greatly from matched elements (Harcourt-Smith et al., ). Thus, KNM-ER 1503 and KNM-ER 1504 were combined as some researchers believe these represent a single individual (McHenry, ) and the distal femur of A.L. 129-1 was analyzed with the forelimb elements of A.L. 288-1 as they are both from the same taxon (Johanson et al., ) and are of a similar size.

Each postcranial landmark configuration (humerus, radius, ulna, femur, and tibia) was subdivided into proximal and distal subsets and was separately subjected to a generalized Procrustes analysis (GPA). The GPA rotates, translates, and size scales all of the configurations by minimizing the sum of squares distance between each set of landmarks and the mean configuration; this places all of the landmark configurations in the same shape space. After they have been subjected to GPA, the coordinates can be used in standard multivariate analyses (Rohlf and Slice, ). To assess the degree of shape covariation present in this data set, two-block partial least squares analyses (2B-PLS) were conducted using MorphoJ v. (Klingenberg, ).

2B-PLS is a way of assessing the covariance between two separate blocks of data. A 2B-PLS generates pairs of linear variables (one for each block) that function to explain the maximum covariance between the blocks. These new variables are useful in that they only describe the covariation between the two blocks, not any covariation within a single block. Mathematically, this is achieved by a singular value decomposition (SVD) of a cross-covariance matrix. This generates scores for each individual along each axis (similar to the PC scores in a principal components analysis), loadings of each variable (eigenvectors), and singular values (eigenvalues) (Rohlf and Corti, ). 2B-PLS analyses including the fossils and all extant individuals were run to examine patterns of shape covariance across phylogeny in the modern and fossil taxa.

Computing a 2B-PLS of all extant hominoids emphasizes species-specific differences in order to make inferences about overall patterns of morphological covariance among hominoids. This analysis can be used to infer patterns of correlated evolutionary change in morphology (e.g., Bastir et al., for changes in the cranium). For each analysis, the degree of covariation and correlation on the first axes was recorded, as well as the RV coefficient.

The degree of covariation is the amount of variance of the sample that is explained by the first axes of each block, whereas the correlation coefficient (r) is a measure of how well the two blocks covary on the first axis. The first axis will explain the greatest proportion of the covariance in the sample and is not constrained by being orthogonal to the previous axis (Rohlf and Corti,; Bastir and Rosas, 2005). The RV coefficient is analogous to the Pearson's correlation coefficient, but for high-dimensional data sets, and it can be interpreted in the same was as any coefficient of correlation.

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It is different from the correlation coefficient of each axis in that it takes into account all axes (Escoufier, ). Although there is no specific significance value that can be derived from a 2B-PLS, permutation tests can be used to determine whether or not the relationship between blocks is greater than what would be expected in a random sample. In this case, permutation tests of 10,000 replicates were performed to assess the significance of the relationship between the two blocks. These permutation tests compute RV and correlation coefficients in random blocks of data and compare those results to those of the real data (Rohlf and Corti,; Klingenberg, ).

The shape changes along the first axes were visualized in Morpheus et al. (Slice, ) by generating new landmark configurations representing the change from the maximum and minimum of those axes. This was done by multiplying the eigenvectors by the position along each axis and adding it to the consensus configuration (Polly, ). Finally, a multiple regression was performed in PAST (Hammer et al., ) to test whether forelimb and hindlimb shape covariance can predict intermembral index.

In this analysis, average intermembral indices for males and females of each species or subspecies were taken from the literature (Table ) and were used as the dependent variable, and average PLS scores for males and females of each species or subspecies on the first two pairs of axes were used as the independent variables. Individuals of unknown sex were not included in the species or subspecies means for the PLS scores. In this analysis, an r 2 value of 1.0 would indicate that the PLS scores perfectly predict intermembral indices in extant hominoids, whereas a 0 would indicate that there is no correlation whatsoever (Cohen, ).

Eberle Pls 508

Both r 2 and an adjusted r 2 that takes into account the number of variables and observations in the model are presented, as well as which independent variables were most significant in the regression model. Overall significance of the model was tested using an ANOVA (Hammer et al., ). Table 3. Average intermembral index for males and females by species or subspecies Taxon Males Females. a Jabbour,. b Data are a mean of published values for Point Hope (Auerbach, ), Andaman Islander (Rivet, ), Australian (Rivet, ), and Khoe-San (Jungers, ) populations. Gorilla beringei beringei 116.5 116.9 Gorilla beringei graueri 115.7 116.9 Gorilla gorilla gorilla 116.4 117 Homo sapiens 69.2 68.3 Pongo pygmaeus 139 135 Pan paniscus 101.8 103.7 Pan troglodytes troglodytes 106.4 105.8 Pan troglodytes schweinfurthii 105.5 103.7 RESULTS 2B-PLS analyses for all possible pairs of forelimb and hindlimb segments—including fossil individuals that preserved the relevant portions—were completed, and the results of which are presented in Table. All pairings were significantly different from the null hypothesis of independence in permutation tests.

There were four pairings with relatively high RV scores and strong covariance ( P. Table 4. Percent covariance (% cov) and correlation (corr) along the first and second common axes and RV coefficients for pairs of forelimb/hindlimb segments% cov 1% cov 2 r (1) r (2) RV. Bolded entries indicate comparatively high RV values.

Table 7. Morphological pattern present for each fossil included in these analyses Taxon Distal humerus/ Proximal femur Distal humerus/ Distal femur Proximal ulna/ Proximal femur Proximal ulna/ Distal femur. “Human” indicates a morphological most similar to modern humans, “Ape” indicates that the morphological pattern is most similar to extant great apes, and “Unique” indicates that the morphological pattern is outside the range of the extant taxon, with those that have an asterisk being close to the human distribution. Afarensis (A.L.

129-1) Human Unique. Human Unique. P. Boisei (KNM-ER 1500) N/A N/A N/A Unique. H. Erectus (KNM-WT 15000) Unique. Unique Human Human Early H.

Sapiens (Omo Kibish 1) N/A Human N/A Unique Homo sp. (KNM-ER 1503/1504) Human N/A N/A N/A DISCUSSION Is the Morphological Pattern of Covariance in Forelimb and Hindlimb Elements Correlated With Intermembral Indices in the Extant Hominoids? For the elements examined here, there is a strong correlation between shape covariance in the forelimb and hindlimb and intermembral indices (Table ). Intermembral indices are often used to model locomotor capabilities in hominoids and fossil hominins (Jungers and Stern,; Crompton et al.,; Kramer,; Kramer and Eck,; Wang et al., ) but these studies are generally limited to the few specimens that have a complete forelimb and hindlimb. Although shape covariance data do not allow for true biomechanical analyses, the correlation between these data and intermembral index indicates that they are a valuable proxy for inferring locomotor pattern in the less complete specimens commonly found in the fossil record. In all cases, multiple axes representing elements in the forelimb and hindlimb had higher correlation coefficients with intermembral index than a single axis, indicating that for the anatomical regions tested here, interlimb covariance is a better proxy for locomotion than any single element.

Table 5. Results from multiple regression analyses r 2 F-statistic P value. For each analysis, the r 2 and adjusted r 2 ( ) are given to assess how well the PLS scores can predict intermembral index. The F-statistic and associated P value demonstrate the significance of the model. Below each analysis, the r 2 for each individual axis and its significance to the model as a whole is recorded.

Distal humerus/proximal femur 0.58 0.43 3.77 0.04 Distal humerus axis 1 0.50 0.20 Distal humerus axis 2 0.08 0.6 Proximal femur axis 1 0.25 0.95 Proximal femur axis 2 0.07 0.44 Distal humerus/distal femur 0.84 0.78 14.311 0.0002 Distal humerus axis 1 0.56 0.83 Distal humerus axis 2 0.02 0.01 Distal femur axis 1 0.57 0.003 Distal femur axis 2 0.10 0.01 Proximal ulna/proximal femur 0.90 0.86 24.062. 1 Thomas R. Rein, Terry Harrison, Kristian J.

Carlson, Katerina Harvati, Adaptation to suspensory locomotion in Australopithecus sediba, Journal of Human Evolution, 2017, 104, 1. 2 Melissa Tallman, David Caramelli, Shape Ontogeny of the Distal Femur in the Hominidae with Implications for the Evolution of Bipedality, PLOS ONE, 2016, 11, 2, e0148371. 3 Thomas R. Rein, Katerina Harvati, Terry Harrison, Inferring the use of forelimb suspensory locomotion by extinct primate species via shape exploration of the ulna, Journal of Human Evolution, 2015, 78, 70.

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