Body mass estimates of hominin fossils and the evolution of human body size.

Journal of Human Evolution xxx (2015) 1e19

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Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol

Body mass estimates of hominin fossils and the evolution of human body size Mark Grabowski a, b, *, Kevin G. Hatala a, c, William L. Jungers d, Brian G. Richmond e a

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, 800 22nd St., NW Suite 6000, Washington, DC 20052, USA b Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, 0316 Oslo, Norway c Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103, Leipzig, Germany d Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA e Division of Anthropology, American Museum of Natural History, New York 10024, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 28 July 2014 Accepted 7 May 2015 Available online xxx

Body size directly influences an animal's place in the natural world, including its energy requirements, home range size, relative brain size, locomotion, diet, life history, and behavior. Thus, an understanding of the biology of extinct organisms, including species in our own lineage, requires accurate estimates of body size. Since the last major review of hominin body size based on postcranial morphology over 20 years ago, new fossils have been discovered, species attributions have been clarified, and methods improved. Here, we present the most comprehensive and thoroughly vetted set of individual fossil hominin body mass predictions to date, and estimation equations based on a large (n ¼ 220) sample of modern humans of known body masses. We also present species averages based exclusively on fossils with reliable taxonomic attributions, estimates of species averages by sex, and a metric for levels of sexual dimorphism. Finally, we identify individual traits that appear to be the most reliable for mass estimation for each fossil species, for use when only one measurement is available for a fossil. Our results show that many early hominins were generally smaller-bodied than previously thought, an outcome likely due to larger estimates in previous studies resulting from the use of large-bodied modern human reference samples. Current evidence indicates that modern human-like large size first appeared by at least 3e3.5 Ma in some Australopithecus afarensis individuals. Our results challenge an evolutionary model arguing that body size increased from Australopithecus to early Homo. Instead, we show that there is no reliable evidence that the body size of non-erectus early Homo differed from that of australopiths, and confirm that Homo erectus evolved larger average body size than earlier hominins. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Human evolution Paleoanthropology Australopithecus Homo

1. Introduction An animal's overall body size is directly related to how it interacts with the natural world. Factors such as energy requirements, home-range size, social organization, relative brain size, locomotion, and numerous other morphological, ecological, and life history characteristics are all tied in some way to body size. Thus, interpreting the evolution of any of these factors demands accurate estimates of body size in extinct species. This is true for our own lineage, where almost all of the hows and whys of human

* Corresponding author. E-mail address: [email protected] (M. Grabowski).

evolution are directly tied to estimates of body size at particular points in time. (Note that we define body size as body mass.) The last major review of hominin body size based on postcranial traits was more than 20 years ago e the classic contribution of McHenry (1992), who presented size predictions for individual fossils, species averages, species averages by sex, and a comprehensive set of regression equations that have been used extensively to estimate body size in newly described fossil hominins since its publication. McHenry (1992: 412) presented his results as an “important first step toward establishing the average body size and range of variation of early hominid species” (referring to hominins). It was considered to be a first step because the size estimates required a number of unavoidable assumptions, and the species body mass averages were in many cases based on tentative species

http://dx.doi.org/10.1016/j.jhevol.2015.05.005 0047-2484/© 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Grabowski, M., et al., Body mass estimates of hominin fossils and the evolution of human body size, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.05.005

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M. Grabowski et al. / Journal of Human Evolution xxx (2015) 1e19

attributions that may or may not be valid today. McHenry's (1992) analysis has proven to be a very important step in understanding the evolution of human body size. However, despite McHenry's (1992) caveats about uncertainty regarding some of the estimates, the results of this study have often been used with more confidence than might be warranted in the development of prominent models and hypotheses regarding human evolutionary history. Since then, very few studies have attempted a large review of hominin body size estimation. Ruff et al. (1997) presented a large number of individual fossil body size estimates in their supplementary information, though these estimates were not the focus of this analysis (see also Trinkaus and Ruff, 2012). Hartwig-Scherer (1993) used a slightly different approach than McHenry (1992), though Hartwig-Scherer (1993) provided estimates of a smaller number of individuals. Manger et al. (2012) presented a large number of body size estimates for individual fossils but these were taken from various sources and the focus of that review was on relative brain size. A number of recent articles on the origin of our n, 2012; Anto n and Snodgrass, 2012; Plavcan, 2012; genus (Anto n et al., 2014) used a combination of published and new indiAnto vidual estimates of body mass compiled by Pontzer (2012) that were n, 2012). But most of the then used to calculate species means (Anto early hominin body mass estimates from this compilation (Pontzer, 2012) were taken directly from McHenry (1992), and the majority of the rest were based on regression equations taken from the same source. Therefore, while these represent updated estimates of hominin body size, they rely heavily on McHenry's (1992) analyses. There have also been a number of attempts to estimate fossil hominin body mass based on cranial traits, for example using the regression of orbit size and body mass in modern humans or other primates (Aiello and Wood, 1994; Kappelman, 1996), although Elliott et al. (2014) suggest caution due to the large amount of error present around these estimates, at least within taxa. We argue that, for a number of reasons, it is time for an analysis to build on and update McHenry's (1992: 412) “important first step.” First, many hominin fossils have been discovered since 1992. Second, more taxa have been discovered since that time and, for many species, the taxonomic attributions of postcranial fossils are better understood. Third, more comprehensive comparative samples of known mass, especially smaller-bodied humans, are available to improve estimates of body mass from skeletal remains similar in size to those of early hominins. Finally, methodological advances (e.g.; Brown, 1982; Brown and Sundberg, 1987; Brown, 1993; Konigsberg et al., 1998; Hens et al., 2000; Uhl et al., 2013), including the ability to test for differences in scaling between fossil traits and modern humans (see below), can provide more reliable estimates including prediction and confidence intervals. The objectives of this study are to: 1) Provide body mass predictions, with confidence intervals, for the largest possible current sample of early hominin lower postcranial elements using a combination of multivariate and univariate approaches. For our multivariate estimates, we first determine which traits within a particular fossil shared the same scaling relationship among each other as in modern humans, and only those traits with similar relationships were used in our final body mass estimates. We also include body mass predictions using the same methods for a worldwide sample of smaller-bodied modern human populations and include these in the Supplementary Online Material [SOM]. 2) Present a series of equations for estimating body mass from univariate postcranial trait measurements based on a large sample (n ¼ 220) of modern human skeletons with known body mass.

3) Determine individual traits for each hominin species that produce univariate body mass estimates equivalent to those calculated using our multiple regression approach. 4) Provide body mass species means, species means by sex (both with confidence intervals), and a metric of sexual dimorphism for fossil hominin species. Importantly, these are restricted to fossils with relatively reliable species attributions. 5) Provide all fossil postcranial measurements used in this analysis to aid future researchers.

2. Materials and methods 2.1. Overview of our approach This study follows previous analyses (Brown, 1982; Brown and Sundberg, 1987; Brown, 1993; Konigsberg et al., 1998; Uhl et al., 2013) that use a calibration approach. In the simplest terms, a calibration approach involves using a large training sample (i.e., the sample used to build, or train, the model) with known body mass and multiple trait measurements per individual to construct regression equations that are then used to predict body mass in a sample with an unknown body mass. But this is where the simplicity ends. The questions of what training sample is most appropriate, which traits to use in the analysis, and the particulars of the statistical model employed are all paramount. These are discussed in detail below. In brief, we use a training sample of generally smaller-bodied modern humans of known body mass because modern humans provide the best available model (i.e. better than an all-hominoid sample) for predicting body mass from lower limb size in hominins that are committed bipeds (i.e. those that only travel bipedally on the ground). Traits are limited to dimensions of the lower limb skeleton because of its direct functional role in supporting body mass. We use the “inverse calibration” approach, which has been exclusively used to estimate hominin body mass in most (e.g. McHenry, 1992) but not all (e.g. Nakatsukasa et al., 2007) previous works. We select the inverse calibration approach for theoretical reasons (see below) and because the alternative “classic calibration” approach can produce mass estimates that deviate substantially away from the true mass of the individual (see below). 2.2. Training sample Estimating hominin body mass requires that the training samples comprise individuals from closely related species of known body mass and available skeletal elements. Two possibilities are the living species most closely related to early hominins, modern humans and chimpanzees. Modern humans are the obvious choice here, as there are a number of large collections of individuals with known body mass and matched skeletal elements. Modern human regressions based on lower limb elements are likely to be the most appropriate for early hominins because it appears that some form of bipedal locomotion evolved early in our lineage (Pickford et al., 2002; Richmond and Jungers, 2008; Kimbel and Delezene, 2009; Lovejoy cija et al., 2013), though they may be less approet al., 2009b; Alme priate for fossils argued to be the earliest members of our clade (White et al., 1994; Senut et al., 2001; Brunet et al., 2002). Functional similarity could argue against using a chimpanzee training sample even for early hominins that may have been only facultative bipeds because their lower limbs, while still different from those of humans, appear to possess certain adaptations to some form of bipedal locomotion that are absent in chimpanzees (e.g. Ruff, 1988; Jungers, 1988a). In addition, though skeletal material from chimpanzees is readily available, matched body masses for individuals are extremely



rare. For these reasons, we focus on body mass predictions for hominins using a modern human training sample. Our training sample was 220 modern human skeletons (116 males, 104 females) of known (cadaveric) body mass from the Hamann-Todd (n ¼ 67) and Terry collections (n ¼ 153). Because this study focused on using known body masses for the training sample, it was not possible to use data on smaller-bodied modern human populations that might mirror those of early hominins. As far as could be determined, there are no known body masses for individuals from populations such as Andaman Islanders or other “pygmy” groups that also have skeletal material available. All individuals in our training sample were of European or African descent. While individuals in our Hamann-Todd sample were chosen at random from the collection, our sample from the Terry collection focused on shorter statured individuals of both sexes (to acquire specimens whose skeletal sizes would more closely approximate smaller individuals from the fossil hominin sample). The reasonably strong correlation between stature and mass in this sample (r ¼ 0.66) means that these individuals, on average, also have lower body mass. Both samples excluded individuals with visible or recorded pathologies, as well as causes of death that might impact variation in body masses (e.g. tuberculosis). After combining these two data sets, outliers for the regression between mass and stature were removed to exclude individuals of extreme (large or small) mass and stature. This procedure has the effect of reducing the likelihood of emaciated or substantially overweight individuals biasing the results. The mean body mass for our human sample was 49.2 kg, which is almost 10 kg smaller than that of the worldwide sample of modern humans presented by Ruff et al. (1997) and therefore our regression models should produce less biased body mass estimates for smaller-bodied fossil hominins (see below). 2.3. Trait selection We focus on traits from the lower limb skeleton to estimate hominin body masses. Though some studies have estimated body masses based on both upper and lower limb traits (e.g. McHenry, 1992; Uhl et al., 2013), only the lower limb carries the full weight of the body during bipedal locomotion and thus it has likely adapted to serve this function (Ruff, 1988; Jungers, 1988a, 1990). As bipedalism evolved early in our lineage, early hominins would have shared similar adaptations to weight bearing as we see in modern humans, although some differences may have existed due to possible differences in the relative extents of bipedalism and arboreal climbing in the locomotor repertoires of different early hominin taxa (e.g. Ward, 2002; Green et al., 2007; Richmond and cija et al., 2013). It is Jungers, 2008; Lovejoy et al., 2009b; Alme difficult to know how functional demands on the upper limbs varied among early hominins, and how this might impact the relationship between body size and upper limb morphology. Other researchers have used metrics that quantify external body dimensions such as “stature” (Porter, 1995), or the combination of stature and body breadth (Ruff, 1994, 2002) to estimate body size. While some of these methods have been shown to produce similar estimates as one lower limb trait e femoral head diameter e for a range of modern human populations (Ruff et al., 1997; Auerbach and Ruff, 2004), we do not use this approach here because they require an additional level of prediction (e.g. estimating stature based on preserved elements such as femoral length and then estimating body size based on the relationship between stature and body size) and generally require skeletal elements that have been recovered for only relatively few fossil individuals (e.g. total length of the femur or relatively complete fossil pelvic bones). Traits in fossil species may not follow the same relationship with body mass as in the training sample, which can lead to estimates

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that are systematically too big or too small (Ruff, 1988; Jungers, 1990; Hartwig-Scherer, 1993). For example, numerous studies have suggested that femoral head diameter is smaller in australopiths relative to other traits when compared to modern humans (Napier, 1964; Corruccini and McHenry, 1978; Jungers, 1988b; Richmond and Jungers, 2008). Here we follow a number of previous analyses (Konigsberg et al., 1998; Hens et al., 2000; Uhl et al., 2013) that use the methods of Brown and colleagues (Brown and Sundberg, 1987; Brown, 1993) to determine which postcranial traits follow the same scaling relationship as in our training sample and base our final multivariate estimates of body mass on the results of these regressions. Importantly, though this approach can reveal if a set of traits scale in a similar fashion as modern humans among themselves, there is no way to determine if they scale with body mass in a similar fashion as in modern humans. Here, we necessarily assume that traits that scale similarly with each other as in modern humans also scale similarly with body mass. Humans have a derived pattern of scaling between postcranial traits and body mass when compared to other great apes (Ruff, 1988; Jungers, 1990; HartwigScherer, 1993), and as a result, differences in body mass prediction occur when predicting larger body masses (see also Jungers, 1988a; McHenry, 1992). As early hominins appear to be generally smallbodied in size, using a modern human or non-human great ape regression would likely not have a substantial effect on our results. For the largest individuals, a non-human great ape regression would predict larger body masses than those using a modern human regression. Note that this effect would increase the amount of variation in our fossil species versus the level we see here. 2.4. Measurements Metric traits from individuals in our training sample were collected using digital calipers. The traits in this study were chosen based on their significant relationship with body mass in the calibration sample used here, their relative abundance in the hominin fossil record, and their usage in previous hominin body mass analyses (see Table 1). As opposed to some previous studies (e.g. McHenry, 1992), we focused here on individual measurements, not areas produced by the product of two measurements, as this allows for a greater number of fossil individuals to be included and easily shows the relationship between individual traits and body mass. The measurements used in this analysis are presented in Table 1, with full descriptions and references. 2.5. Hominin data Postcranial measurements on fossil hominins (original fossils) matching that of the training sample were taken from the literature, supplemented by measurements on the original fossils taken by MG, BR, and KH. All measurements used in this analysis are included in SOM Excel Sheet 1 with full references (SOM Excel Sheet 2). In addition, we predict body mass for one Akka “pygmy” using data taken from McHenry (1992). This individual has a previously predicted body mass of 28.2 kg using the relationship between body mass and stature in “pygmies” (Jungers and Stern, 1983). Finally, we predict body masses based on skeletal elements for a range of smaller bodied populations worldwide from various museum collections and include these in SOM Excel Sheets 3 (multivariate) and 4 (univariate). 2.6. Statistical model There are two main methods of calibration; using the nomenclature of Konigsberg et al. (1998), these are labeled classical calibration and inverse calibration. Though “classical” would seem to


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Table 1 Measurements taken for this analysis.a Measurement Femoral Head SI Femoral Neck SI Femoral Head AP Femoral Neck AP Subtrochanteric AP Subtrochanteric ML Femoral Midshaft AP Femoral Midshaft ML Femoral Bicondylar Tibial Plateau AP Tibial Plateau ML Tibial Distal End ML Tibial Distal Articular Surface AP Tibial Plafond a

Description Superoinferior diameter of the head Superoinferior height of the neck Anteroposterior diameter of the head Anteroposterior height of the neck Anteroposterior diameter of the shaft just below the lesser trochanter Mediolateral diameter of the shaft just below the lesser trochanter Anteroposterior diameter of the shaft midway along its length Mediolateral diameter of the shaft midway along its length Maximum mediolateral width of the distal end taken perpendicular to the shaft axis Maximum anteroposterior width of proximal tibia taken perpendicular to the shaft axis Maximum mediolateral width of proximal tibia taken perpendicular to the shaft axis Maximum mediolateral width of distal end taken perpendicular to shaft Maximum anteroposterior width of articular surface of distal tibia Maximum mediolateral width of articular surface of distal tibia

Source McHenry and Corruccini, McHenry and Corruccini, e e McHenry and Corruccini, McHenry and Corruccini, McHenry and Corruccini, McHenry and Corruccini, McHenry and Corruccini, McHenry, 1992 McHenry, 1992 e McHenry, 1992 McHenry, 1992

1978 1978

1978 1978 1978 1978 1978

Traits in bold were used in the final body mass analysis, but all traits are included in regression equations in Table 2.

imply that this approach is most commonly taken, Konigsberg et al. (1998) noted this term was given by Krutchkoff (1967) based on the longer history of this method. In prediction, at least in biology and paleoanthropology, inverse calibration is most commonly used (Konigsberg et al., 1998). The technical difference between these two approaches concerns which set of variables is considered the dependent and independent variables and thus regressed on the other (body mass or the traits), but there is a large literature debating which of these methods is more appropriate in calibration analyses, particularly when predicting outside of the range of the training sample (i.e. extrapolation) (e.g. Krutchkoff, 1967; Ott and Myers, 1968; Berkson, 1969; Krutchkoff, 1969; Shukla, 1972; Konigsberg et al., 1998). In the inverse calibration approach, known body masses would be regressed on the traits, and then this equation would be used to predict the fossil body mass from fossil traits (Brown, 1993). This method produces the Bayes estimator for body mass, which combines the likelihood estimator and the distribution of known body masses from the training sample (called the informative prior; Konigsberg et al., 1998). In the classical calibration approach, traits used to predict body mass would be regressed on known body masses in the training sample, solved for body mass, and then this equation would be used with the fossil traits to predict the fossil body mass (Brown, 1993). This method produces the maximum likelihood estimator for body mass, which is an estimate of the parameter (body mass) that maximizes the likelihood of obtaining the observed data (fossil measurements) given a likelihood function (Konigsberg et al., 1998). Uhl et al. (2013) (see also Konigsberg et al., 1998) pointed out that classical calibration only produces the maximum likelihood estimator under certain conditions, including when only one trait is used to predict the unknown quantity (i.e. univariate estimates of body mass). Multivariate estimates calculated only using those traits that scale with each other in a similar fashion as modern humans (see below) are preferable to univariate estimates as they use data from multiple preserved fossil elements and are generally more precise. Uhl et al. (2013) introduced profile likelihood (Brown and Sundberg, 1987; Brown, 1993) into the anthropological literature; this method produces the maximum likelihood estimator given a multivariate regression equation. Konigsberg et al. (1998) (see also Uhl et al., 2013) made the case that in instances where extrapolation is likely to take place (in this case, when the fossil is substantially smaller or larger than the training sample), the classical estimator will produce estimates closer to the true unknown value than the inverse estimator. This suggestion is based on the idea that classical calibration (as well as profile likelihood) produces parameter estimates that are free of

bias, and inverse calibration produces estimates that are biased toward the mean of the training sample (the mean body mass in this case). This bias occurs because inverse calibration uses prior knowledge based on the training sample, while classical calibration and profile likelihood do not. However, bias is the mean difference between the expected value and the true value of the parameter being estimated (i.e., on average, is the estimate larger or smaller than the true value?). Both the classical and profile likelihood approaches, while unbiased (i.e. the average difference given a large number of replications is zero), produce some individual estimates that are far from accurate. This can be observed directly in Figs. 2 and 3 from Uhl et al. (2013) and the results of a simulation using our data (Fig. 1). In this simulation, 10,000 individuals with the same scaling relationship between skeletal measurements and body mass as in our comparative sample were created by drawing from a multivariate random normal distribution. Using both the inverse and profile likelihood approaches, body mass was estimated for each of these individuals and estimated body mass was then plotted against the “true” body mass for each individual (Fig. 1). This figure makes clear that as the difference between the true body mass of the individual and the average body mass of the training sample increases, the profile likelihood estimate of mass will deviate substantially away from the true mass of the individual (see Fig. 1a e black circles). This effect is magnified when the number of traits in the simulation is low (Fig. 1b), such as for most hominin fossils. This is probably the cause of the biologically extremely unlikely estimates of the H. floresiensis skeleton, LB1 (6.9 kg, PI: 2.2e19.4 kg), produced using the profile likelihood approach (Uhl et al., 2013). In contrast, the inverse calibration method has the effect of producing results that are biased towards the mean of the calibration sample as the difference between true body mass of the fossil and the mean body mass of the calibration sample increases (Fig. 1a, b e red circles). This means that predicted body masses of early hominins that are substantially smaller than modern humans would appear bigger than their true mass, and those that are bigger would appear smaller. In other words, this would likely reduce the amount of variation in body mass in our fossil sample. Here, we focus on the results calculated using inverse calibration rather than classical or profile likelihood calibration because inverse calibration minimizes variation in body mass and, therefore, is the conservative approach to comparing the amount of body mass variation across taxa. Because many early hominins were significantly smaller than modern humans, we attempt to minimize the upward bias that is unavoidable when using inverse calibration by including a large sample of smaller-bodied modern humans in our training sample. Choosing a training sample based on what we



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Figure 1. (A) Results of simulations using our data set. The x-axis is the true log body mass, y-axis is the predicted log body mass. Values in red are body mass predictions using the inverse prediction method, values in black are using the profile likelihood method. The diagonal line is the expectation given no difference between the true values and the prediction. The horizontal line is the average known body mass of the simulated data set. While the inverse prediction results (red [lighter] circles) suggest a “regression to the mean” e individuals smaller than the sample mean will have predicted values larger than the true value and individuals larger than the sample mean will have predicted values smaller than the true valueethe profile likelihood results (black circles) show greatly increased variation visible in the increased range of values along the y-axis when compared to the x-axis. (B) Same as A but with a reduced number of traits (Traits 1,2,3,4,5) such as that seen for most of the fossils in our data set and the results are even more striking. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

believe we know about the unknown sample or individual e in this case choosing the training sample of smaller-bodied modern humans e was argued against in Konigsberg et al. (1998) as this practice treats a posteriori information as if it were prior information. In other words, we are choosing a training sample composition based on our belief that early hominins were smallbodied. But there are numerous lines of evidence that many early hominin individuals were small; most notably, many early hominin fossil specimens are smaller than comparable skeletal elements in modern humans, and the inclusion of small-bodied modern populations to compare body mass, morphology and proportions is commonly accepted in the paleoanthropological literature for this reason. Because our training sample was constructed to minimize upward bias in early hominins, it would likely have the opposite effect if used to predict body masses in hominins from the latermiddle to late Pleistocene. Species such as Homo heidelbergensis and Neandertals were apparently as large as or larger than large modern humans (Ruff et al., 1997), and because of this methodological limitation we do not estimate fossil body masses for later fossil hominins here. While there have been a number of other methods suggested for calibration, including major axis regression, reduced major axis regression, and the ratio of the means (Konigsberg et al., 1998), there are issues with all of these. The latter assumes isometric scaling (Konigsberg et al., 1998), which is an unrealistic assumption in both extant and extinct hominins (Gordon et al., 2008). While major axis and reduced major axis regression are methods commonly believed to correct for error in both the dependent and independent variables (see Smith, 2009 for more on this point), Hansen and Bartoszek (2012) made a convincing case based on both statistical and biological issues that these methods should not be used in analyses that approach evolutionary questions. The basis for their argument is that these methods make no differentiation between biological and measurement error in the model and hence can produce biased parameter estimates and resulting predictions.

This holds true for intraspecific as well as interspecific analyses (Hansen, pers. comm.). 2.7. Prediction and confidence intervals As Smith et al. (1996) noted, there is a tendency to ignore the implications of confidence and/or prediction intervals in estimations of hominin body mass. Predictions are often taken as the “true” value of the individual, with little heed paid to uncertainty around this estimate. But around each estimate is a 95% prediction interval, the result of both variation in the location of the distribution of the body mass because of error in estimating the slope of the regression, and variation in the location of the individual within that distribution. That prediction interval, like the confidence interval, shows the reliability of the estimate, and in our case states a 95% probability that our interval contains the parameter value. For some fossils included here, prediction intervals could be very wide due to a small number of traits used in constructing the estimate and/or a weak relationship between body mass and the traits (see also Elliott et al., 2014). Similarly, accurate species averages should not be merely the result of averaging point estimates of predictions because each of these has its own prediction intervals. Here, our species averages take into account the uncertainty of individual fossil predictions. Including multiple individuals reduces the size of the confidence intervals, which in turn helps to uncover how hominin species differed from one another, or not. Along with our estimates of body mass, prediction intervals can be inaccurate when the sample to be predicted comes from a different population than the training sample, or differs in the scaling relationship between the traits of interest and body mass. As mentioned above, the relationship between body mass and postcranial traits can never be known with certainty for early hominins and our predictions and prediction intervals assume that a modern human-like pattern of scaling was present at least by the time of the australopiths.


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2.8. Overview of analysis All analyses were performed using natural log-transformed data to improve model fit (Jungers, 1988a) and to correct for any heteroscedasticity in the residuals that may exist. Using natural logtransformed data also makes univariate coefficients roughly interpretable as proportional differences that may be useful for future researchers. For example, given the regression of log body mass on log femoral length, a coefficient of 1.57 can be interpreted as approximately an increase in 1% of femoral length corresponds to a 1.57% increase in body mass. 2.9. Univariate regression equations First, a series of regression equations was calculated using the modern human training sample to estimate the relationship between known body masses and the traits of interest. The final 12 traits used for this analysis were chosen based on their use in previous analyses to estimate body mass (see references in Table 1) and their significant relationship with body mass (significant slope), which is also reflected in their relatively high correlations with body mass. The 12 traits included in this analysis had correlations ranging from 0.20 to 0.69 in our modern human training sample. Though our correlations appear to be dramatically lower than those of McHenry (1992), the results of that analysis were based on body mass regressions using sex-specific hominoid species means (n ¼ 16) or partially sex-specific population means (n ¼ 4) for their intra-Homo regressions. Besides the extra error that is the result of estimating means and then using these mean estimates to estimate hominin body mass (Smith et al., 1996), using means removes much of the variation in body masses that is inherent in populations, leading to higher correlations and R2 values. Variation within populations also needs to be included to produce prediction intervals for individual fossil body mass predictions. The one analysis to which our regression results are directly comparable is that of Uhl et al. (2013), who based their analysis on a modern human calibration sample of 600 individuals. In that analysis, the slope of the regression between log body mass and log superoinferior femoral head diameter was 1.45 and the R2 was 0.21, which does not differ substantially from the results of this study (Table 2). The regression equations, standard errors for the parameter estimates, p-values for the intercept and slope, R2, standard error of the estimate (SEE), and root mean square error (RMSE) are included in Table 2 and SOM Excel Sheet 5. Because of the multitude of different multivariate equations used here (which depend on the traits present in the fossil individual), we only report parameter

estimates for univariate equations, but the multivariate equations were constructed from different combinations of those traits. In the SOM we include the p-values for the individual traits that contribute to each fossil body mass estimate. 2.10. Fossil body mass prediction Using multivariate trait data from relatively more complete fossil individuals, we tested which fossil traits followed the same scaling relationship among each other as in the training sample, following Brown (1993) (see also Konigsberg et al., 1998; Uhl et al., 2013). If individual fossil traits were found to differ from this relationship, we used an iterative procedure described in Uhl et al. (2013) (see also Brown and Sundberg, 1987) to drop them from the model and refit the model using the remaining traits. We repeated this procedure until the traits that remained were found to no longer be significantly different in terms of scaling from the training sample. The final multivariate estimate of the body mass of a fossil is the result of the traits that had the same scaling relationship among each other as in the training sample. To test for difference in scaling, fossil body mass was first predicted using a classical calibration approach (Brown, 1993; Konigsberg et al., 1998) and all preserved traits at once. We then calculated the R statistic (Brown, 1993), which allowed us to test if the individual fossil traits in the multiple regression followed the same scaling relationship among each other as the training sample (modern humans). R is defined as:

R ¼ ðy0 b y Þ0 Qðy0 b y

Where y0 is the vector of observed traits in the fossil, b y is the vector of predicted traits estimated by using classical calibration to estimate body mass and the regression of the traits on body mass to obtain trait values. Q is defined as the inverse of the prediction covariance matrix (Brown, 1993):

Q¼

1 1 b G b b þ bT vx byx G G yx

b is the variance-covariance matrix for the traits after Where G regressing out the effects of body mass, byx is the vector of regression slopes for the traits on body mass in the training sample, and vx is the variance in body mass. Increasing values of R mean that there are increasing differences between the scaling relationship among the traits in the fossil compared to the calibration

Table 2 Regression equations for logged body mass on logged traits from Table 1 including standard errors, p-values, R2, correlation (R), percent standard error of the estimate (%SEE), and expected error in kg (root mean square error; RMSE) for modern humans. Traits

Intercept

SE

p-value

Slope

SE

p-value

R-squared

R

%SEE

RMSE

Femoral Head SI Femoral Neck SI Femoral Head AP Femoral Neck AP Subtrochanteric AP Subtrochanteric ML Femoral Midshaft AP Femoral Midshaft ML Femoral Bicondylar Tibial Plateau AP Tibial Plateau ML Tibial Distal End ML Tibial Distal Articular Surface AP Tibial Plafond

2.10269 0.86668 1.91619 1.67760 1.29964 0.56999 1.76031 0.24989 3.34842 1.03562 0.18975 2.81334 0.40691 1.01948

0.852 0.620 0.855 0.525 0.723 0.751 0.714 0.658 1.151 1.053 1.347 0.498 0.695 0.730

0.014 0.163 0.026 0.002 0.074 0.449 0.014 0.705 0.004 0.327 0.888 0.000 0.559 0.164

1.574 0.873 1.528 0.659 0.778 1.290 0.636 1.100 1.658 1.252 0.954 1.748 1.002 0.858

0.225 0.180 0.226 0.158 0.219 0.219 0.216 0.200 0.264 0.268 0.314 0.130 0.201 0.220

0.000 0.000 0.000 0.000 0.000 0.000 0.004 0.000 0.000 0.000 0.003 0.000 0.000 0.000

0.191 0.101 0.180 0.077 0.058 0.145 0.040 0.126 0.160 0.108 0.062 0.473 0.109 0.071

0.437 0.318 0.424 0.277 0.240 0.380 0.200 0.355 0.399 0.328 0.250 0.688 0.331 0.267

0.065 0.068 0.065 0.069 0.070 0.067 0.070 0.067 0.066 0.066 0.066 0.052 0.068 0.068

0.249 0.262 0.250 0.266 0.268 0.256 0.270 0.258 0.252 0.254 0.254 0.199 0.261 0.262



sample. As R is distributed as a chi-square with the number of traits 1 degrees of freedom, this allows testing if the estimate of R is significantly different from the expectation and thus if traits in the fossil were scaled significantly differently from those of the training sample. To determine which traits cause a significant difference in R, we calculated the elements of the vector:

b 1 2 ðz b z cla Þ G =

b 1 2 is the inverse square root of G b Where G Positive values of this vector indicate traits that are larger than expected if the fossil followed the same scaling relationship as the training sample, and negative values indicate the reverse (Brown and Sundberg, 1987). Recursively dropping the largest elements b 1 2 one at a time and recalculating R until it becomes nonof G significant allows one to reduce the trait set to those that follow a similar scaling relationship as in the training sample. Because inverse calibration biases predicted fossil body masses towards the mean of the training sample, it might be preferable to determine if predicted fossil body masses were actually significantly lower or higher than that of modern humans. To test for extrapolation e in this case significant differences between the fossil's predicted body mass and that of the training sample e we calculated the Rx statistic (Brown, 1993). Rx is defined as: =

=

^

^

Rx ¼ ð b y y Þ0 Qð b y yÞ

7

based on a similarity in scaling alone to allow for the inclusion of earlier hominins but include predictions for individuals that meet the requirements of both scaling and size in the SOM. 2.11. Univariate versus multivariate prediction Though it might seem that individual traits from our multivariate set that scale the same as our training sample could then be used to produce univariate estimates of body size, this is an incorrect assumption. These traits share a similar scaling relationship as the training sample only in this particular multivariate combination e in other words, given the traits present in this particular fossil. Because of correlations between the traits, multivariate regression parameters will not be the same as univariate parameters (Sokal and Rohlf, 1995) and therefore using univariate regression equations made up of the traits in the multiple regression will not necessarily produce equivalent body mass estimates. To provide a useful guide to which traits individually produced comparable body mass estimates as those using our multiple regression approach, we compared our multivariate estimates to our univariate estimates. McHenry (1992) followed a similar approach, though his comparisons were based on individual traits that produced body mass estimates that were consistent with each other. In this analysis, individual traits that produced univariate regression body mass estimates ± 5 kg to the multiple regression estimates on the same individuals were identified and recorded. From these results, we constructed a table (Table 3) showing which traits in each fossil hominin species produced a comparable body mass estimate as the multivariate estimate.

^

Where y is the vector of traits predicted by regressing body mass on traits to estimate body mass in the fossil and then regressing traits on body mass to estimate traits in the fossil. As Rx is distributed as a chi-square with one degree of freedom, this allows testing if the estimate of Rx is significantly different from the expectation and thus if the estimate of the fossil body mass is significantly different in terms of size from the calibration sample. Although body mass predictions produced by the inverse calibration approach are likely to be more accurate using traits that do not differ in scaling (R) and size (Rx) from our training sample, early hominins were generally smaller than modern humans, and this requirement dramatically reduces the number of fossils for which we can predict body masses. Here, we concentrate on predictions

2.12. Estimating species means Uhl et al. (2013) presented a reasonable approach for species means based on the work of Brown (1993); however, this method is only useful in cases where there are individuals from the same species with the same preserved traits e an unlikely scenario in most hominin fossils. Mean estimates for each species, with confidence intervals, were calculated following Borenstein et al. (2010) using an approach originally intended to be used with metaanalyses. In this case, a random effect meta-analysis model was used. Here, body mass estimates of individual fossils within each species were considered akin to the results of individual studies,

Table 3 Individual traits for each species that appear to produce comparable body mass estimates as our multivariate estimates.a Species O. tugenensis Au. anamensis Au. afarensisb Au. africanusb Possible P. boisei H. erectus H. floresiensis Early Homo

African and Georgian H. erectus Possible African and Georgian H. erectus

H. sapiens (“pygmy”) a b

Traits Femoral Head SI (BAR 10020 00, BAR 10030 00) Tibial Plateau AP, Tibial Plateau ML, Tibial Distal End ML, Tibial Plafond (KNM-KP 29285) Femoral Head SI, Femoral Neck SI, Subtrochanteric AP, Subtrochanteric ML, Femoral Bicondylar, Tibial Plateau AP, Tibial Distal End ML, Tibial Distal Articular AP (AL 152-2, AL 288-1, AL 333-142, AL 827-1) Femoral Head SI (Sts 14) Femoral Neck SI, Subtrochanteric ML (OH 20) Femoral Head SI, Femoral Midshaft ML, Tibial Plateau AP, Tibial Distal Articular Surface AP, Tibial Plafond (Dmanisi large adult (D4167, D3901)) Femoral Head SI, Tibial Plateau AP (LB1) Femoral Head SI, Femoral Neck SI, Subtrochanteric AP, Subtrochanteric ML, Femoral Midshaft AP, Femoral Midshaft ML, Femoral Bicondylar, Tibial Plateau AP, Tibial Plateau ML, Tibial Distal End ML, Tibial Distal Articular Surface AP, Tibial Plafond (Dmanisi large adult (D4167, D3901), KNM-ER 1472, KNM-ER 1481) Femoral Head SI, Femoral Midshaft ML, Tibial Plateau AP, Tibial Distal Articular Surface AP, Tibial Plafond (Dmanisi large adult (D4167, D3901)) Femoral Head SI, Femoral Neck SI, Subtrochanteric AP, Subtrochanteric ML, Femoral Midshaft AP, Femoral Midshaft ML, Femoral Bicondylar, Tibial Plateau AP, Tibial Plateau ML, Tibial Distal End ML, Tibial Distal Articular Surface AP, Tibial Plafond (Dmanisi large adult (D4167, D3901), KNM-ER 1472, KNM-ER 1481) Femoral Head W, Subtrochanteric ML, Tibial Plateau AP (Akka “pygmy”)

Comparison is based on the more complete fossil hominins for each species e shown in parentheses e and one “pygmy” individual. Femoral Head SI appears to scale the same as in modern humans in AL 152-2, AL 827-1, and Sts 14, though not AL 288-1.


8


and the random-effects model allowed for determination of the species mean and the pooled confidence interval around this mean. In this model, each individual has its own “true” best estimate and prediction interval, and we are estimating the species mean of these “true” best estimates and the confidence interval weighted by the precision of the individual estimates. Because the approach used here is based on the individual fossil body mass estimates and their prediction intervals, rather than particular traits across all fossils within a species, it does not have the same issue found in Uhl et al. (2013). We also applied the same approach to estimate species means by sex. Means by sex for each taxon were calculated by splitting the individuals into two groups depending on whether they were larger or smaller than the mean of that taxon (the mean method; Plavcan, 1994). In addition, we calculated the degree of sexual dimorphism for each species, which was the ratio of the mean male body mass to mean female body mass following Plavcan (1994; see also McHenry, 1992). This technique is the most accurate when there are large differences between the sexes and can overestimate dimorphism when there are slight differences between them. No approach for estimating sexual dimorphism appears to work well in all conditions (Plavcan, 1994), but the mean method has been found to be the most accurate of a number of possible methods and as it has been used previously in discussions of dimorphism in hominin body mass (McHenry, 1992), our estimates will be comparable. Note that while we are cognizant that back-transforming our predictions from log space into standard linear space may result in negative bias (Smith, 1993), prediction intervals around individual estimates and confidence intervals around species should dwarf this bias (which tends to be small for intraspecific data sets; Hayes and Shonkwiler, 2006; Uhl et al., 2013). 3. Results For the univariate regression equations, the relationship between body mass and all traits was significant (Table 2), with slopes

ranging from 0.636 (Femoral Midshaft Anteroposterior e AP) to 1.748 (Tibial Distal End Mediolateral e ML). R-squared values ranged from 0.040 (Femoral Midshaft AP) to 0.473 (Tibial Distal End ML). Table 3 lists the individual traits for each species that were found to produce a comparable body mass estimate as the multivariate prediction (see also SOM Excel Sheet 6). These traits should thus provide reasonable estimates of body mass for fragmentary fossil individuals. While univariate estimates should be avoided when possible because of the reduction in precision when compared to multivariate estimates, these traits (Table 3) are relatively unbiased by differences in scaling relationships and can be used to estimate body mass of future fossil discoveries. Table 4 gives the species means, the 95% confidence intervals around those means, and the number of individuals used to calculate each mean using both the multivariate and univariate approach where applicable. The individual fossil body mass predictions that make up the multivariate sample are all based on traits that follow the same scaling pattern among themselves as in the modern humans (see also SOM Excel Sheet 7). Except where noted, the univariate means are based on Femoral Head Superoinferior (SI) Diameter. Average body masses for each species for the other traits in this analysis are included in SOM Excel Sheet 8. Table 5 compares our species averages to estimates from previous studies. Our univariate estimates are substituted when multivariate estimates are unavailable and are the same as in Table 4. Table 6 presents the multivariate sex-specific species means, the 95% confidence intervals, the number of individuals used to calculate sex-specific means, and an estimate of the amount of sexual dimorphism (see also SOM Excel Sheet 9; Sheet 10 has the univariate sex specific species means for individual traits). The individual body mass estimates making up these multivariate means are all based on traits that follow the same scaling pattern among themselves as in the modern human training sample. Table 7 presents body mass predictions for 90 individual early hominin fossils using the multivariate (bolded) and/or univariate approach (see also SOM Excel Sheets 11e13). All traits used in the

Figure 2. Multivariate and univariate estimates of predicted body mass for fossil hominin individuals over time and known body mass averages from a worldwide sample of modern human populations. Multivariate estimates are based on those traits that share a similar scaling relationship among themselves as modern humans, univariate estimates are based on Femoral Head ML and are for those individuals for which multivariate estimates could not be calculated.



9

Figure 3. Multivariate and univariate estimates of predicted body mass for fossil hominin individuals as in Fig. 1 by species over time and known body mass averages from a worldwide sample of modern human populations.

Table 4 Species means and 95% confidence intervals based on multivariate estimates (MV Mass) given the same pattern of scaling among the traits as modern humans and univariate estimates (Uni Mass) based on Femoral Head SI except where noted.a MV Mass

CI.L

CI.U

MV n ¼

Uni Mass

Uni n ¼

O. tugenensis Ar. ramidus Au. anamensis Au. afarensis Au. africanus Au. sediba P. boisei Possible P. boiseie P. robustus H. habilis H. erectus H. floresiensis Early Homof African and Georgian H. erectusg Possible African and Georgian H. erectush

35.8 e 46.3 39.1 30.5 25.8 e 35.3 30.1 32.6 51.4 27.5 43.8 50.0 51.0

25.0 e 31.5 32.9 24.3 19.3 e 29.7 23.4 22.5 43.4 16.4 37.9 33.0 42.4

51.3 e 68.1 46.4 38.4 34.4 e 42.0 38.9 47.5 60.9 46.1 50.5 75.8 61.3

2 e 1 12 5 2 e 8 4 2 9 1 12 2 7

30.2 32.1b 43.0c 34 30 29.5 46.4d 31.5 31.7 27.1d 44.1 27.1 44.3 44.1 43.8

1 1 1 5 18 1 1 3 9 1 6 1 7 6 8

Known Body Mass H. sapiens (this study) Worldwide H. sapiensi P. troglodytesj

49.2 58.2 52.8

CI.L 47.5 56.2 e

CI.U 50.9 60.1 e

220 51 9

Species

a

Multivariate estimates in bold. All masses in kilograms. Point estimates based on the central value (39 mm) of the range of acetabular values provided by Lovejoy et al. (2009b). See SI for upper and lower bound results. based on Tibial Distal End ML. d based on Subtrochanteric ML. e All possible adult P. boisei individuals. Multivariate estimate based on: KNM-ER 1500d, KNM-ER 1465, KNM-ER 1476b, KNM-ER 1503, KNM-ER 738, KNM-ER 815, KNM-ER 993, OH 20. Univariate estimate based on: KNM-ER 1503, KNM-ER 1505, KNM-ER 738. f All adult Homo individuals between 1.95 and 1.5 Ma. Multivariate estimate based on: Dmanisi large adult (D4167, D3901), KNM-ER 736, KNM-ER 737, KNM-ER 803A, KNM-ER 3735, OH 62, KNM-ER 1472, KNM-ER 1481, KNM-ER 1475, KNM-ER 1810, KNM-ER 5880A, KNM-ER 5881. Univariate estimate based on: KNM-ER 1472, KNM-ER 1481, KNM-ER 3228, Dmanisi large adult (D4167, D3901), KNM-ER 1808, adult projection of KNM-WT 15000 (see text), KNM-ER 5881. g African and Georgian adult H. erectus individuals. Multivariate estimate based on: Dmanisi large adult (D4167, D3901), OH 28. Univariate estimates based on: BSN49/P27, Dmanisi large adult (D4167, D3901), KNM-ER 1808, KNM-ER 3228, adult projection of KNM-WT 15000, OH 28. h All possible African and Georgian adult H. erectus individuals. Multivariate estimate based on: Dmanisi large adult (D4167, D3901), OH 28, KNM-ER 736, KNM-ER 737, KNM-ER 803A, KNM-ER 1472, KNM-ER 1481. Univariate estimates based on: BSN49/P27, Dmanisi large adult (D4167, D3901), KNM-ER 1808, KNM-ER 3228, adult projection of KNM-WT 15000, OH 28, KNM-ER 1472, KNM-ER 1481. i From Ruff et al. (1997). Based on population means. j From Smith and Jungers (1997). b c


10


Table 5 Species average from a selection of previous studies compared to estimates from the current study taken from Table 4.a Species

This study

McHenry, 1992

Wolpoff, 1973

Steudel, 1980

McHenry, 1988

Holliday, 2012

O. tugenensis Ar. ramidus Au. anamensis Au. afarensis Au. africanus Au. sediba P. boisei j Possible P. robustus H. habilis H. erectus H. floresiensis Early Homo African and Georgian H. erectus j Possible

35.8 32.1 46.3 39.1 30.5 25.8 46.4 j 35.3 30.1 32.6 51.4 27.5 43.8 50.0j 51.0

e e e

e e e e

e e e e

e e e

e e e

37 35.5

37.3

e

e e

36.1 41.3 41.6

e e 40

e e e e e

e e e e

50.6 45.5

36

e e e e e

n, 2012/2014 Anto

38.5 37

e e e e e

e e e

e e e

54.5 e

Other 35e50d ~50e 47e55f e e e e e e e 28.7e36g 61.8h, 62.1i e

40 34 33

e 46.1 47.7 40.5 58.6

c

e e e 41 37.3

e 59

b

52

a

Multivariate estimates in bold. All masses in kilograms. Based on regression equations from McHenry (1992). c Based on data from Pontzer (2012). d From Nakatsukasa et al. (2007). e From White et al. (2009). f From Leakey et al. (1995). g From Brown et al. (2004). h From Ruff et al. (1997). Based on Homo between 1.8 and 1.2 Ma e expanding this range to our 1.95e1.5 range produces a new body mass estimate of 60.7 based on data in their SI. i From Ruff (2010). b

multivariate calculations here followed the same scaling pattern among themselves as in the modern human training sample. This table also gives the result for the Akka “pygmy”, which has the previously mentioned body mass estimate of 28.2 kg. Here, based on the four traits out of five originally measured that have the same pattern of scaling as our training sample, our multivariate estimate of body mass was 27.6 kg (95% prediction interval (PI) of 16.5e46.0 kg). Species means and individual fossil predictions using those traits that did not differ in either scaling or size (nonsignificant p-values for R and Rx statistics) were also calculated and results are shown on SOM Excel Sheets 14 and 15. To aid future researchers, we combined trait measurements, multivariate and univariate body mass predictions for individuals, and multivariate and univariate species means for our early Homo (all Homo between 1.95 and 1.5 Ma) and African and Georgian Homo erectus samples on one SOM Excel Sheet for each group (SOM Excel Sheets 16 and 17). Here we also provide species means using a combination of multivariate and univariate individual predictions to present an estimate based on the largest possible sample. Finally, we include multivariate and univariate body masses predicted by the same methods as used for the fossil hominins for a sample of smallerbodied modern humans (see SOM Excel Sheets 3 and 4 for

individual estimates). The SOM Excel file gives the fossil measurements, ages, previous estimates, references, complete body mass predictions for all fossils (n ¼ 122) for both the multivariate (where applicable) and the univariate regressions, and complete results for all analyses discussed here. Results show that the earliest hominins tend to have small body size, with the notable exception of greater size, and size variation, in the australopiths with the addition of the Hadar hominins at 3e3.5 Ma (Fig. 2; see SOM Fig. 1 for size with 95% confidence intervals). Furthermore, around 2 Ma, average body size increases (Fig. 2; SOM Fig. 1). This is corroborated by evidence from large footprints at Ileret, Kenya, dated to 1.52 Ma, of a number of largebodied hominin individuals, attributable to H. erectus or Paranthropus boisei (Dingwall et al., 2013). When species designations are included (Fig. 3), the large individuals before 2 Ma are all attributed to Au. afarensis, and the large individuals after 2 Ma are attributed to H. erectus and P. boisei. All data for both plots were a combination of the multivariate predictions first together with Femoral Head SI predictions. This latter trait was used in cases where individual fossils either lacked multiple traits on which the multivariate approach can be used, the multiple traits that could be measured significantly differed from the scaling relationship found

Table 6 Sex-specific multivariate species means and 95% confidence intervals.a Species

Male Mass

CI.L

CI.U

Au. afarensis Au. africanus Possible P. boisei P. robustus H. habilis H. erectus Early Homo African and Georgian H. erectus Possible African and Georgian H. erectus

49.5 38.9 45.1 32.3 38.4 54.3 54.1 62.2 61.5

40.2 27.2 33.6 24.1 22.9 44.1 43.0 37.3 47.5

61.0 55.7 60.4 43.2 64.3 66.8 68.0 103.5 79.5

Known Body Mass H. sapiens (this study) Worldwide H. sapiens P. troglodytes

51.8 61.0 59.7

CI.L 49.5 58.4 e

CI.U 54.1 63.7 e

a

Male n ¼

Female n ¼

Female Mass

CI.L

CI.U

SD

6 2 3 3 1 6 5 1 4

31.2 25.8 30.9 24.0 27.3 46.3 38.1 40.7 42.0

25.5 19.1 24.8 14.2 15.8 34.7 31.7 24.9 32.3

38.1 34.8 38.3 40.6 46.9 61.9 45.8 66.5 54.6

6 3 5 1 1 3 7 1 3

1.6 1.5 1.5 1.4 1.4 1.2 1.4 1.5 1.5

116 28 5

46.2 54.7 45.8

CI.L 43.7 52.2 e

CI.U 48.7 57.1 e

104 23 4

1.1 1.1 1.3

All masses in kilograms.



11

Table 7 Multivariate body mass prediction for individual fossil hominins (MV Mass) given the same pattern of scaling among the traits as modern humans and univariate predictions based on Femoral Head SI (Uni Mass) unless otherwise noted. Also shown are 95% prediction intervals.a Number 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72

Specimen

Species

Age (Ma)

Prev. Est.

MV Mass

Uni Mass

PI.L

PI.U

Traits

ARA-VP-6/500 AL 152-2 AL 211-1 AL 288-1 AL 330-6 AL 333-131 AL 333-142 AL 333-3 AL 333-95 AL 333w-40 AL 333w-43 AL 333x-26 AL 827-1 KSD-VP-1/1 MLD 17 MLD 25 MLD 46 Sts 14 StW 121 Stw 25 Stw 300 Stw 31 Stw 311 Stw 361 Stw 392 Stw 403 Stw 431 Stw 443 Stw 479 Stw 501 Stw 522 Stw 527 Stw 598 Stw 99 KNM-KP 29285 MH2 MH4 MH1 BSN49/P27 Dmanisi large adult (D4167, D3901) KNM-ER 1808 KNM-ER 3228 KNM-WT 15000 (projected adult) OH 28 Trinil I Trinil II Trinil III Trinil IV Zhoukoudian I Zhoukoudian IV Zhoukoudian VI Dmanisi subadult (D3160) KNM-WT 15000 KNM-ER 736 KNM-ER 737 KNM-ER 803A LB1 KNM-ER 3735 OH 62 Akka pygmy KNM-ER 1471 OH 35 KNM-ER 1472 KNM-ER 1481 KNM-ER 5881 KNM-ER 1475 KNM-ER 1810 KNM-ER 5880A OH 34 BAR 10020 00 BAR 10030 00 EP1000/98

Ar. ramidus Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. afarensis Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus Au. africanus/Homo sp.? Au. anamensis Au. sediba Au. sediba Au. sediba (juv) H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus H. erectus (juv) H. erectus (juv) H. erectus? H. erectus? H. erectus? H. floresiensis H. habilis H. habilis H. sapiens Hominini gen. et sp. indet. Hominini gen. et sp. indet. Homo sp. Homo sp. Homo sp. Homo sp.? Homo sp.? Homo sp.? Homo sp.? O. tugenensis O. tugenensis P. aethiopicus?

4.4 3.4 3.3 3.2 3.2 3.2 3.2 3.2 3.2 3.2 3.2 3.2 3.1 3.6 2.7 2.7 2.7 2.4 e 2.4 e 2.4 2.4 2.4 2.4 2.4 2.4 e 2.4 2.4 2.4 2.4 2.2 2.4 4.1 2.0 2.0 2.0 1.2 1.8 1.7 1.9 1.5 0.7 0.9 0.9 0.9 0.9 0.8 0.8 0.8 1.8 1.5 1.7 1.6 1.5 0.0 1.9 1.8 0.0 1.9 1.8 2.0 2.0 1.9 1.9 1.9 1.9 1.0 6.0 6.0 2.7

51.0 e 59.7 27.9 e e e 51.5 62.9 e e 48.2 45.6 45.4 e e e 30.3 e 34.6 e e 40.8 e 33.0 e 41.3 41.4 20.5 34.0 29.5 34.0 32.2 45.4 47e55 35.7 e 31.5 33.2 47.6e50 63.4 67.1 80.0 54.0 e e e e e e e 40e42.5 48.0 68.3 70.9 67.1 28.7 e 33.2 28.2 39.1 32.1 52.1 61.2 e 53.6 47.9 55.9 51.0 35e50 35e50 e

e 28.6 52.8 26.0 40.7 63.6 35.2 38.5 49.7 55.2 24.5 39.5 38.2 e e e 35.2 22.8 43.3 e e e e e 28.5 e e e e e 26.3 e e 36.3 46.3 29.1 22.7 29.7 e 40.7 e e e 62.2 51.7 50.0 49.3 51.8 54.8 54.3 51.6 35.6 53.3 65.5 64.1 54.8 27.5 38.4 27.3 27.6 37.2 35.5 45.4 40.9 35.5 42.7 40.5 45.1 28.3 30.0 42.5 31.7

32.1 30.1 e 23.8 e e e 39.7 e e e e 37.4 40.9 36.8 33.9 36.0 25.0 e 29.1 30.2 26.3 33.9 24.6 27.8 27.3 34.5 34.3 27.1 29.9 26.5 29.9 28.8 37.4 e 29.5 e 29.9 29.4 40.9 38.5 50.0 64.4 48.4 e e e e e e e e 50.3 e e e 27.1 e e 28.8 e e 40.9 45.4 35.9 e e e e 30.2 e e

19.4 17.2 31.7 17.2 24.3 37.6 21.0 23.4 29.9 33.1 13.8 23.5 23.3 24.9 22.3 20.5 21.3 13.4 25.8 17.4 18.2 15.6 20.5 14.5 17.0 16.2 20.9 20.8 16.2 18.0 15.6 18.0 17.2 21.9 31.4 19.4 15.0 17.8 17.6 24.8 23.4 30.5 39.0 37.2 31.0 30.0 29.6 30.9 32.9 32.5 30.8 21.2 32.1 39.0 38.0 32.7 16.4 22.9 15.8 16.5 22.0 21.0 27.4 27.4 21.5 25.6 24.2 27.1 16.6 17.9 25.5 18.2

53.3 47.6 87.9 39.2 68.0 107.4 59.0 63.5 82.7 92.0 43.6 66.5 62.5 67.1 60.6 56.1 58.1 38.6 72.8 48.6 50.4 44.3 56.1 41.7 47.8 45.8 57.0 56.8 45.6 49.9 44.2 49.9 48.2 60.2 68.4 43.7 34.5 49.4 49.0 66.9 63.3 81.9 106.3 103.8 86.0 83.2 82.3 86.7 91.2 90.7 86.4 59.9 88.2 110.2 108.1 91.9 46.2 64.5 47.1 46.0 62.8 60.0 75.2 60.9 58.9 71.1 67.7 75.1 48.5 50.2 70.9 55.3

e 2 2 2 2 3 2 2 2 2 2 2 3 e e e 2 3 2 e e e e e 2 e e e e e 2 e e 4 4 2 2 2 e 6 e e e 2 4 4 4 4 3 3 2 2 7 2 4 4 5 2 4 4 2 2 7 7 4 2 2 2 3 4 2 2

(continued on next page)


12


Table 7 (continued ) Number 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 a b

Specimen OH 80-12 KNM-ER 1465 KNM-ER 1476b KNM-ER 1500d KNM-ER 1503 KNM-ER 1505 KNM-ER 738 KNM-ER 815 KNM-ER 993 OH 20 SK 14024 SK 3121 SK 3155B SK 50 SK 82 SK 97 SKW 19 SWT1/LB-2 TM 1605

Species P. P. P. P. P. P. P. P. P. P. P. P. P. P. P. P. P. P. P.

boisei boisei? boisei? boisei? boisei? boisei? boisei? boisei? boisei? boisei? robustus robustus robustus robustus robustus robustus robustus robustus robustus

Age (Ma) 1.3 1.5 1.9 1.9 1.9 1.9 1.9 1.8 1.5 1.8 e e 1.9 1.9 1.9 1.9 1.9 1.9 e

Prev. Est. 50 57.4 36.0 42.2 38.0 e 35.1 41.6 39.4 49.3 e 24.6 28.4 31.1 36.7 43.4 28.8 e e

MV Mass

Uni Mass

PI.L

PI.U

Traits

e 43.4 34.7 28.4 30.5 e 29.4 40.9 33.5 51.6 e 24.0 e e 30.8 35.3 e 30.9 e

46.4b e e e 32.1 32.4 29.9 e e e 27.6 23.9 29.1 42.6 32.1 35.7 26.0 32.0 39.0

27.9b 26.1 20.2 18.9 18.2 19.5 17.7 24.5 20.0 31.0 16.4 14.1 17.4 26.0 18.5 21.4 15.4 18.6 23.7

77.2b 72.2 59.3 42.8 51.2 53.7 48.8 68.1 56.3 85.8 46.2 40.8 48.6 69.9 51.4 58.3 43.9 51.4 64.0

e 2 2 3 3 e 4 2 2 3 e 2 e e 3 3 e 2 e

Multivariate body mass predictions and prediction intervals are in bold. Last column shows number of traits used in multivariate calculation. All masses in kilograms. Based on Subtrochanteric ML.

in modern humans, or only head width was measured. On both plots we added known body mass averages for modern human populations worldwide from Ruff (1994). The potential effects of using multivariate-versus univariatebased (Femoral Head SI) estimates were assessed for those individuals with the requisite combination of traits to calculate multivariate estimates (SOM Fig. 2). It appears that the results using femoral head diameter are generally quite close to those calculated using the multivariate approach, with no systematic bias and suggests that both methods produce consistent results. Differences such as in OH 28, with a multivariate estimate of 62.2 kg and a univariate estimate of 48.4 kg, are due to scaling differences between traits used in the final multivariate body mass estimate and Femoral Head SI. 4. Discussion The hominin body mass estimates in this study differ in three important ways from those of previous studies, through the inclusion of more recently discovered fossils (especially since McHenry, 1992), basing species means on much more conservative fossil attributions, and combining significantly larger comparative samples and improved methods. Taken together, these differences lead to a picture of hominin body mass (Fig. 2) that is distinct from n those of other analyses (e.g. Holliday, 2012; Pontzer, 2012; Anto et al., 2014) in several important ways. First, many of our species averages are slightly smaller (Table 5), based on generally slightly smaller individual fossil body mass estimates (Table 7). The difference is likely due to larger estimates in previous studies resulting from the use of large-bodied modern human reference samples and other factors (see 'Comparisons with previous studies e species averages and overall trends', below). Second, marked increases in body mass variation are observed multiple times in the known hominin fossil record, with these increases in variation apparently taking place in certain taxa, including Au. afarensis and H. erectus. This contrasts with recent n et al., 2014) that increased size variation first views (e.g. Anto appeared in H. erectus and represents a novel ability to adapt to varying selective regimes and led to the cardinal characteristics we associate with Homo. Furthermore, some taxa (e.g. P. boisei) may have greater average size (e.g. Aiello and Wood, 1994; Kappelman, 1996; Domínguez-Rodrigo et al., 2013) and size variation (Silverman et al., 2001) than currently appreciated due to sampling

and difficulties with reliable attributions of many postcranial remains. Finally, the magnitude of sexual dimorphism appears to have been only slightly lower in early H. erectus (African and Georgian individuals) compared to earlier hominins such as Au. afarensis. It should be noted that the sparseness of the fossil record makes spatial and temporal averaging unavoidable. For geographically dispersed taxa like H. erectus, it is difficult to tease apart the effects of geography, time, and dimorphism. Furthermore, the sparseness of the fossil record currently limits the sample, such that more accurate measures of size variation will require additional fossils. However, based on current data, our results suggest it is very unlikely that early H. erectus had a level of dimorphism comparable to n, 2012; Anto n et al., that seen in modern humans (see also Anto 2014). Low levels of dimorphism in early H. erectus are also unlikely given the presence of large and small cranial remains in the Turkana Basin (Spoor et al., 2007). Thus, evolutionary models based on a significant reduction in dimorphism in this taxon should be reevaluated. It is worth noting that this improved picture of hominin body mass evolution confirms previous work in important respects. Most notably, early H. erectus is characterized by larger average size than n, that of any known earlier hominin taxon (Fig. 3; Table 5; see Anto n et al., 2014; Ruff and 2012; Holliday, 2012; Pontzer, 2012; Anto Burgess, 2015). 4.1. Comparisons with previous studies e individual specimens Our results include new body mass estimates for certain fossil specimens that have figured prominently in previous analyses of trends in hominin body mass over time. These include some of the earliest possible hominins, as well as key specimens that tend to be seen as particularly “representative” of certain taxa. In some cases our results confirm previous estimates but in others there are important differences. Here, BAR 10020 00 and 10030 00, assigned to Orrorin tugenensis, have multivariate body mass estimates of 30.0 and 42.5 kg, respectively (PI: 17.9e50.2 and 25.5e70.8). These estimates are based on 3e4 traits, but equivalent results are produced using Femoral Head SI diameter alone for BAR 10020 00 (Table 3; SOM Excel Sheet 6). These estimates are slightly lower than or in the range given for previous estimates e 35e50 kg (Nakatsukasa et al., 2007), with the lower end of that range based on a modern human sample.



There is only one individual, ARA-VP-6/500, of the species Ardipithecus ramidus from which body mass can be estimated (White et al., 2009). The published body mass estimate of this fossil individual was ~50 kg, based on the relationship between the mean of the geometric mean of the talus and capitate and the mean body mass of a large number of primate species (Lovejoy et al., 2009a). This was noted as a “large female body mass” by White and colleagues (2009: 80). Here, we used the range of acetabular diameters presented in Lovejoy et al. (2009b; 36e42 mm) and regressions between acetabular diameter and Femoral Head SI from Plavcan et al. (2014) for modern humans to predict Femoral Head SI in this fossil. Using this range of estimates of Femoral Head SI and our univariate regressions, body mass was calculated as between 28.1 and 36.0 kg (PI: 16.8e47.1, 21.8e59.4). Using the central value of the range of acetabular dimensions (39 mm), we predicted a body mass of 32.1 kg (PI: 19.4e53.3), and report this in Tables 4 and 5 and the use the central value in the SOM Excel Sheet calculations. As no additional postcranial measurements for ARA-VP-6/500 are readily available, we cannot determine if femoral head diameter in this species scales with other traits in a similar fashion as modern humans. As discussed above, these and all body mass predictions included here depend on the assumption that a modern humanlike pattern of scaling between our final set of traits and body mass was present in all hominins. Very early hominins such as Orrorin and Ardipithecus may instead scale more like Pan or other great apes, which based on previous findings (e.g. Nakatsukasa et al., 2007) would likely lead to greater body mass estimates. The evidence that Orrorin (Richmond and Jungers, 2008) and ARAVP-6/500 (Lovejoy et al., 2009b) had adaptations for bipedalism could mean that the human regression is most appropriate (see also Russo and Kirk, 2013). However, ARA-VP-6/500 lacks some of the derived bipedal adaptations seen in all known Australopithecus and Homo species (Lovejoy et al., 2009b), and Orrorin also lacks some derived bipedal traits (Kuperavage et al., 2010) and retains cija et al., 2013) in the femur. These issues primitive features (Alme raise doubts about whether the human regression would be more appropriate than one based on Pan or other non-human great apes. We note that unless there was a change in scaling during the time period that separated these two taxa, the O. tugenensis specimens and ARA-VP-6/500 suggest broadly similar body sizes for these early hominins. AL 288-1 has often been assigned a body mass around 27e29 kg (e.g. McHenry, 1992; Lovejoy et al., 2009a). In this study the best estimate of body mass was 26.0 kg (PI: 17.2e39.2), calculated using the multivariate approach, and two traits that share the same scaling relationship with body mass as in modern humans (Subtrochanteric ML and Tibial Distal End ML). In comparison, the univariate best estimate from Femoral Head SI was 23.8 (PI: 14.0e40.4). Our results therefore support previous estimates of body mass in AL 288-1. Here, we tentatively place BSN49/P27 (Simpson et al., 2008) in H. erectus, though we note that there is debate on this attribution (Ruff, 2010; Simpson et al., 2014). While we do not wish to be drawn into this debate, we note that by necessity our multivariate estimates of H. erectus do not include this individual as no other relevant measurements were available. Our univariate estimate of BSN49/P27 was 29.4 kg (PI: 17.6e49.0), while the previous estimate was 33.2 kg (Ruff, 2010). Our estimate would qualify BSN49/P27 as a very small H. erectus individual, small even compared with the average for Au. afarensis, though it is closer to that average than that of H. erectus. KNM-ER 1472 and ER 1481, attributed to Homo sp. had previous estimates of 52.1 and 61.2 kg, respectively. Here, our predicted body masses are smaller, 45.4 and 40.9 kg. While KNM-ER 1481 is generally larger than ER 1472, the former has a number of

13

measurements from the tibia that are not present in the other fossil. These measurements, when combined with traits from the femur, drive the multivariate body mass estimate down from what would likely be predicted using femur traits alone. This is the nature of multivariate scaling analysis e given a combination of different traits, some will contribute more to the final body mass estimate, and estimates will change somewhat depending on which traits are included. We feel it is better to use as much data as possible when estimating fossil body masses (given that the traits have the same scaling relationships as modern humans). We also note that the prediction intervals for our body mass predictions dwarf small differences between these two fossils. We also estimated the body mass of an Akka “pygmy” individual (Flower, 1889), which is often presented in stature and body mass analyses of early hominins as a comparative sample (e.g. Jungers, 1988c). Using the multivariate approach and four traits found to follow the modern human scaling pattern (Femoral Head SI, Subtrochanteric ML, Tibial Distal Articular Surface AP and ML), body mass was estimated at 27.6 kg (PI: 16.5e46.0 kg). Our results were consistent with Jungers and Stern (1983) who placed this individual's body mass at 28.2 kg using the relationship between mass and stature in a sample of Efe “pygmies”. 4.2. Comparisons with previous studies e species averages and overall trends Many of our species mean estimates are slightly smaller than estimates from previous studies (Table 5). This pattern results from slightly smaller body mass estimates of individual fossils when compared to previous estimates (Table 7). There are a number of likely causes of this disparity. First, a large amount of this difference is probably due to the fact that most previous estimates either come from or are based on McHenry (1992), which used four means in his intra-hominin regression e Khoisan, “Pygmy”, and sex-separated male and female North Americans e an extremely small number of data points for prediction using regression. Here, our training sample comprised modern human individuals rather than means (n ¼ 220) and our multivariate estimates focused on fossil traits that followed the same scaling relationship among each other as in modern humans. Using a data set comprising individuals rather than means allows us to calculate prediction intervals around the individual fossil body mass estimates. These intervals can then be included in our final estimate of the species means, which are weighted by the precision of the individual fossil body mass estimates and allow for creation of confidence intervals around those means. Second, our modern human training sample is made up of generally smaller-bodied individuals; it is ~10 kg smaller than that of a worldwide population sample from Ruff et al. (1997; see our Table 4). As almost all previous body mass estimates have been calculated using the inverse calibration approach, their results have likely been biased towards the mean body mass of their modern human training sample. A lowered average body mass for the training sample, as we use here, would thus reduce this bias and produce lower estimates for small-bodied fossil hominins (see also Konigsberg et al., 1998; Uhl et al., 2013). It should be noted that body mass predictions are lower for fossil individuals even if they do not differ in size from our training sample (i.e. non-significant Rx values e see SOM Excel Sheet 15), meaning there would be little bias due to our method of calibration for these individuals, and this further supports the suggestion that previous results may indeed have been upwardly biased by larger bodied training samples. Third, many earlier average body mass estimates (Table 5) were also based on McHenry's (1992) femoral head diameter regression, which was also calculated using population means. McHenry's


14


(1992) slope of body mass on Femoral Head SI (1.7125; for four modern human population means) is higher than ours (1.57; modern human individuals), and combined with the difference in the intercepts (1.048 in McHenry vs. -0.913 in this study after our data are transformed into log base 10 rather than the natural log we use here), implies that predicted body masses for fossil hominins over the range of our training sample will be larger (see SOM Fig. 3). In comparison, Uhl et al. (2013) used a larger comparative sample but also with larger-bodied individuals (mean body mass in that study was 57.2 kg) and found a slope of ~1.45. This brings an interesting subject to light: what to make of the differences in scaling between populations compared to scaling within populations. Though we do not pursue this point here, what these results mean for biology is a subject of great interest that appears to mirror intraspecific versus interspecific differences in brain-body regressions (e.g. Gould, 1975). By following the approach of Brown and colleagues (Brown and Sundberg, 1987; Brown, 1993), Uhl et al. (2013; Uhl, 2014) provided estimates of fossil body mass that not only included prediction intervals but also an approach that tested if individual traits followed the same scaling relationship among each other as in the training sample (i.e. modern humans). But, following Konigsberg et al. (1998), Uhl et al. (2013) presented the classical calibration (and its equivalent, profile likelihood calibration) as being most appropriate when extrapolation is likely as inverse calibration estimates are biased. But bias is the average difference between the estimate and the true value. As we showed here, while classical calibration may not be biased e i.e. the average body mass given a large number of replicates is the “true” body mass e estimates predicted from traits that are significantly smaller or larger than the mean of the training sample tend to be pushed towards the extreme (Fig 1). While estimates based on the inverse calibration approach we use here are biased towards the mean body mass of the training sample (in this case modern humans), these estimates may lead to a reduction in the amount of interspecific variation in body mass, rather than a drastic increase (Fig. 1). We therefore consider these estimates conservative and might even underestimate the amount of variation in hominin body mass (see below).

With regards to individual traits, the most surprising result was that femoral head diameter for australopiths may not always be relatively smaller when compared to other postcranial traits than modern humans (Table 3). A number of australopith individuals for which R could be calculated based on at least the Femoral Head SI and Subtrochanteric ML (Au. afarensis: AL 152-2, AL 827-1; Australopithecus africanus: Sts 14; see SOM Excel Sheet 13) do not appear to have relatively smaller femoral heads when compared to their shafts. In addition, these traits give roughly equivalent estimates of body mass when used in the univariate case in all of these individuals save Sts 14 (SOM Excel Sheet 6). To explore femoral head size further, we reproduced a figure from Napier (1964) showing differences in the ratio of Femoral Head SI and Subtrochanteric ML among fossil species and a worldwide sample of modern humans (Fig. 4). While the results of Napier (1964) were used to point out that australopiths possessed relatively small femoral heads, the picture appears to be more complex. For example, while Au. afarensis has a smaller average value for this ratio than in our current sample or other modern human populations, it is not significantly different when compared to our current sample (t-test p-value ¼ 0.074), with some fossil individuals overlapping with our modern human samples. While australopiths on average have relatively small femoral heads (Fig. 4), the overlap between australopiths and modern humans in this morphology facilitates body mass estimation using modern human regressions. Another deviation from previous studies is the dramatic increase in the “average” mass of P. boisei e 46.4 kg here when compared to 36.1 kg (McHenry, 1992). Average is in quotes here because the univariate average is based on Subtrochanteric ML diameter for the only P. boisei postcranial fossil with associated craniodental remains e OH 80-12. On the other hand, the multivariate average for “possible” P. boisei fossils (see Table 4 and SOM Excel Sheet 1 for included fossils) is 35.3 kg based on eight individuals, and both this value and the level of sexual dimorphism (1.5), is consistent with the range seen in other australopith taxa. As the predicted body mass of OH 80-12 is only slightly smaller than

Figure 4. Ratio of Femoral Head SI to Subtrochanteric ML for each species in this analysis compared to a sample of modern human populations and the sample of individuals used in this study (Current Sample).



the multivariate body mass of “possible” P. boisei OH 20 (51.6 kg), it may be that the OH 80-12 is simply a large male individual (Domínguez-Rodrigo et al., 2013). Size variation in a large sample of P. boisei mandibles also indicates substantial size variation similar to that seen in Au. afarensis (Silverman et al., 2001). McHenry (1992) suggested that using femoral shafts to estimate body mass in australopiths produced estimates that were biased upward and suggested multiplying by a correction factor of 0.74 to correct for this upward bias. But McHenry's (1992) suggestion was based on seeming incongruities between body mass estimates produced via shafts versus other measures of joint size from the same individuals. Chief among these was AL 288-1. Here we found a similar result, where Subtrochanteric AP and ML predict body masses of 34.3 kg and 34.8 kg for AL 288-1, which are larger than our multivariate estimate (26.0 kg) or univariate estimates using other measurements included here (see SOM Excel Sheet 11). Similar results are seen for AL 333-3, with a multivariate estimate of 38.5 kg and univariate body mass estimates based on Femoral Head SI of 39.7 kg, Femoral Neck SI of 46.1 kg, Subtrochanteric AP of 52.6 kg, and Subtrochanteric ML of 54.6 kg (SOM Excel Sheet 11). On the other hand, this was not the case for AL 152-2, AL 827-1, or Sts 14. The multivariate body mass estimates for these three individuals are based on similar scaling as in modern humans between the Femoral Head SI and Subtrochanteric ML (and Femoral Neck SI in the latter two fossils). These multivariate estimates are also roughly equivalent to the univariate predictions using the Femoral Head SI and Subtrochanteric AP and ML for AL 152-2 and Femoral Head SI and Subtrochanteric AP for AL 827-1 (see SOM Excel Sheet 6). These findings argue against femoral shafts being relatively large in early australopiths in all cases. As both femoral shafts and heads give equivalent results in some australopiths, either heads and shafts are generally relatively small in these individuals, or both are relatively large. In addition, the difference does not seem to be the result of any “size effect” e when compared to the others, AL 288-1 and AL 152-2, and AL 333-3 and AL 827-1, are similar in size (relatively smaller versus larger) but show contrasting patterns of scaling between femoral head diameter and shaft width. Not applying a correction factor to other australopiths with large femoral shafts leads to a number of individuals (AL 333-131, AL 2111, and AL 333w-40) with body masses estimated as above 50 kg, which when compared to other members of this species is quite large. In fact, AL 333-131 has a multivariate body mass of 63.6 kg. While this might seem high at this early a time period, this specimen has the largest Subtrochanteric ML diameter until H. ergaster and we believe evidence discussed above removes the need for a correction factor as in McHenry (1992). We also note that this body mass is not substantially higher than the average male body mass for wild-caught Pan troglodytes (59.7 kg) based on the reliable estimates from Smith and Jungers (1997). In addition, OH 20 has a multivariate body mass prediction that is only slightly smaller than other members of this group e 49.3 kg e and this prediction is based on Femoral Neck SI, as well as Subtrochanteric AP and ML. 4.3. The potential influence of taxonomic attribution Here we took a very conservative approach and only used the individual fossils with the most reliable attributions in calculating the species means because species designation is a critical issue when determining characteristics of a species and differences between species. For example, McHenry's (1992) estimate of Homo habilis body mass was based on five individuals: KNM-ER 1472 and KNM-ER 1481 (relatively complete femora), KNM-ER 3228 (a fairly complete hip bone), OH 8 (a foot) and OH 35 (a distal tibia; see also Pontzer, 2012). But major issues have been raised with all of these designations, leading us to exclude them from our H. habilis group of

15

taxonomically secure fossils when calculating the species mean. KNM-ER 1472 and KNM-ER 1481 were initially allocated to Homo sp. indet. by Leakey (1973). Later analyses suggested that these c.1.982.09 and 1.95e1.98 Ma (Joordens et al., 2013) femora are more similar in morphology to individuals firmly assigned to Homo such as KNM-WT 15000 than to australopiths (Richmond and Jungers, 2008). Further, they differ from the OH 62 femur (Ruff, 1995), which is reliably assigned to H. habilis (Johanson et al., 1987). Wood and Leakey (2011) assigned KNM-ER 1481 to H. erectus and KNM-ER 1472 to Homo sp. We tentatively attribute them to Homo sp. for these reasons, acknowledging the possibility that they could belong to H. rudolfensis (Wood, 1992), a taxon that currently has no associated postcrania. One note is that if KNM-ER 1481 was indeed H. erectus, its predicted body mass (40.9 kg) is either not substantially different or slightly larger than the smaller current members of this group e Dmanisi subadult (D3160), Dmanisi large adult (D4167, D3901) e but below the group average for African and Georgian H. erectus (50.0 kg). KNM-ER 3228 was initially allocated to Homo sp. indet. by Leakey (1976) while in the detailed anatomical description Rose (1984) noted that the fossil was either from H. erectus or an individual “indistinguishable from H. erectus in pelvic morphology and function” (Rose, 1984: 377), and if it was assigned to Homo habilis this would “necessitate … a considerable reappraisal of other specimens attributed to this and the other hominid species” (Rose, 1984: 377). Based on its close affinities with the hip bone of OH 28, a 0.5 Ma fossil assigned to H. erectus (Rose, 1984) and KNM-ER 15000 (Walker and Ruff, 1993), we have assigned this fossil to H. erectus (in agreement with Wood and Leakey, 2011). Wood and Constantino (2007) suggested that the 1971 discovery of a KNM-ER 813, a more human-like talus from Koobi Fora, lessened the chance that OH 8 belonged to H. habilis because OH 8 includes a talus that appears more like TM 1517 (see Gebo and Schwartz, 2006), the holotype of Paranthropus robustus. On the other hand, Susman (2008) found characteristics linking OH 8 with OH 7, the holotype of H. habilis. OH 35 was suggested to be possibly a part of the holotype of H. habilis by the same authors (Susman, 2008), but Wood and Constantino (2007) pointed out if the OH 35 and OH 8 are part of the same individual then it stands to reason they could both also belong to P. boisei by the reasoning discussed -Sola et al., 2008). OH 35 clearly for OH 8 above (see also Moya cannot belong to OH 8 based on stratigraphic criteria (Njau and Blumenschine, 2012). To complicate matters even more, the OH 8 talus has gorilla shape affinities (WLJ, unpublished), and the OH 7 hand is primitive in most respects (Susman and Creel, 1979; Tocheri et al., 2007). Taken together, this suggests an australopith-like postcranium for H. habilis (see Wood and Collard, 1999; Ruff, 2009; Richmond and Hatala, 2013), complicating taxonomic attributions of isolated postcrania. Thus, none of the postcranial fossils that originally made up the H. habilis group in McHenry (1992) can be reliably attributed to this taxon. The only two lower-body postcranial fossils that can be reliably attributed to H. habilis due to their association with craniodental material are OH 62 and KNM-ER 3735. We estimate the body mass of OH 62 at 27.3 kg (PI: 15.8e47.1) and KNM-ER 3735 at 38.5 (PI: 22.9e64.5). This latter estimate is based on anteroposterior and mediolateral measurements near to, but likely slightly below, the midshaft of the incomplete femur. But, as discussed in Haeusler and McHenry (2004), differences in either dimension appear to be negligible several cm above or below the midshaft. We also note that the univariate body mass predictions of OH 62 using Femoral Midshaft AP and ML (37.4 kg and 33.5 kg) are higher than our multivariate estimate, though they and Subtrochanteric AP and ML scale with each other in this fossil as in our modern human comparative sample (SOM Excel Sheet 13). This result raises the possibility that our body mass estimate for KNM-ER 3735, and thus


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the species average for H. habilis, may actually be a bit higher than the true value. On the other hand, if OH 62 was a female and KNMER 3735 was a male of the same species, the magnitude of sexual dimorphism between these two individuals (1.4) is consistent with other early Homo individuals (1.4 e Table 6). This smaller than previously suggested average body mass of H. habilis (Table 5) suggests that if this species, or one of similar mass, was ancestral to Homo floresiensis, little reduction in size would be required to produce the body mass of this small-bodied hominin. Another issue in McHenry (1992) and later articles that use his estimates is the assignment of partial femur StW 99 to Au. africanus. The original catalog of Alan Hughes states that it comes from Sterkfontein member 5 (1.6e1.1 Ma) from grid W/45 at a depth of 6010e70 1000 . Based on the date of this member and our visual inspection of the morphology, this fossil is much more likely to be early Homo. Here we assign it to Homo sp. In addition, we estimate the body mass for this individual was 36.3 kg (PI: 21.9e60.2 kg) based on the multivariate approach and 37.4 kg (PI: 22.7e61.6 kg) using just Femoral Head SI, smaller than the previous estimate (45.4 kg; McHenry, 1992; Pontzer, 2012). Because of these issues, none of the individuals with questionable taxonomic attributions is included in our species mean estimates or sex by species mean estimates with the exception of KNM-ER 3228. When species averages are based on five (McHenry, 1992) or six n, 2012; Anto n et al., 2014) individuals such as is the case for (Anto H. habilis, uncertain attributions can have a major effect on what we think we know about the evolution of hominin body size. Assignment of KNM-ER 1472, KNM-ER 1481, and KNM-ER 3228 to H. habilis, with previous estimates of body mass of 49.6, 57.0, and n, 2012; Anto n et al., 2014), 63.5 kg (Pontzer, 2012; see also; Anto increases the body mass estimates of this species dramatically when compared with a species average (32.6 kg) composed solely of the only two well attributed lower body postcranial fossils, OH 62 and KNM-ER 3735. While species averages based on so few individuals will require re-evaluation with the discovery of new fossils, we argue that it is important to restrict conclusions to what is reliably known about the fossil record. In this case, based on the postcranial fossils with reasonable attribution, the body mass of H. habilis is likely substantially lower than presented in most other analyses. Small body mass is consistent with the small sizes of the known skull remains attributable to H. habilis s.s. (Aiello and Wood, 1994; Kappelman, 1996). This n, conclusion also holds for “non-erectus early Homo” (see also Anto n et al., 2014), where the average postcranial body 2012; sensu Anto mass estimate for this group followed the species designation and estimates for individuals attributed to H. habilis (Pontzer, 2012). Taken alone, taxonomic issues with H. habilis (or non-erectus early Homo) mentioned here lead to a smaller body mass for this taxon based on postcrania (32.6 kg) than the reasonably well sampled Au. afarensis (39.1 kg; Table 4). n et al. (2014) also include body mass predictions based on Anto orbit size for non-erectus early Homo (37 kg and 39 kg; taken from Aiello and Wood, 1994; Kappelman, 1996), and these are almost exactly the same as either McHenry's (1992) or our Au. afarensis species averages. Taken together, these results challenge an evolutionary model with an increase in average body size from n et al., 2014). The Australopithecus to early Homo to H. erectus (Anto increase in average species body mass appears to occur with early H. erectus, but not with other taxa suggested to lie at the origins of our genus (Table 4; see also Wood and Collard, 1999). Indeed, the degree to which body size increases in H. erectus depends on the body size of its ancestor. Currently, body size in H. habilis s.s. appears to be no larger than in australopiths, and too little is known about H. rudolfensis to make any conclusions about size. Further indirect evidence suggests a small body size for non-erectus early

Homo. The very early Homo mandible at c.2.8 Ma at Ledi-Geraru is only slightly larger than the AL 288-1 mandible (Villmoare et al., 2015), and at 35.4 kg (PI: 21.4e58.7; Table 7) the body mass of recently described c.1.9 Ma Homo sp. partial skeleton KNM-ER 5881 (identified as non-erectus early Homo; Ward et al., 2015) is slightly below that of KNM-ER 3735. 4.4. The pattern of hominin body mass evolution When hominin body mass is plotted against time, it is apparent that levels of variation seen later in hominin evolution are present by about 3.5 Ma (Fig. 2). Although the fossil record of Au. anamensis is too sparse to provide a robust size estimate, large body sizes are present in Au. afarensis (Fig. 3), with the largest individual body masses approaching our largest estimates for H. erectus. This result supports arguments that Au. afarensis had substantial size dimorphism (Richmond and Jungers, 1995; Plavcan et al., 2005; Gordon et al., 2008; Gordon, 2013; contra Reno et al., 2003, 2005, 2010), leading to a large amount of variation in body size within this taxon. Between 3.0 and 2.0 Ma there is a dramatic drop in observed variation coinciding with the extinction of Au. afarensis and/or poor sampling of the postcranial fossil record in eastern Africa, and with the fossil record represented by apparently smaller-bodied South African Au. africanus during this time period. This sequence is followed by another spike after 2.0 Ma, coinciding with the arrival of early H. erectus. With the global expansion of modern humans, body size variation appears consistent with levels present prior to 1 Ma (seen in the worldwide sample of body masses on the far right of Fig. 3), but all within one species. Note that because inverse calibration results in body mass estimate bias toward the mean of the training sample (~49 kg for our modern human sample), the size of larger-bodied H. erectus and amount of variation in hominin body mass is probably even greater than shown here. This effect may be the source of the divergent results between our largest H. erectus body masses (~65 kg) and recent suggestions of some extremely large H. erectus individuals e 80 kg for an adult KNM-WT 15000 (Ruff and Burgess, 2015), and more than 90 kg for the KNMER-5428 fossil talus (Boyle and DeSilva, 2015). We also note that the attribution of the latter fossil to H. erectus is tentative as discussed in Boyle and DeSilva (2015), and its mass estimate was calculating using equations from McHenry (1992). While the dramatic increase in body mass variation by 3.5 Ma does not easily fit in the context of most hypotheses on the origin of our genus, our results support previous studies arguing that body size increased with the advent of H. erectus (see also McHenry, n 1992; Holliday, 2012; Pontzer, 2012; Dingwall et al., 2013; Anto et al., 2014). The average body mass in early H. erectus is estimated to be at least 10 kg larger than the average body size of Au. afarensis and almost 20 kg larger than H. habilis s.s. The exact change in body size will depend on what species gave rise to H. erectus. Currently, too little is known about the fossil record to be confident about the exact pattern of body mass evolution prior to H. erectus, but it appears that H. erectus marks a major increase in average body size relative to earlier hominins. Thus, scenarios invoking body mass increase as a major factor in the evolution of Homo are consistent with the evidence for H. erectus but not earlier members of Homo. There are many possible non-exclusive causes for this marked increase in average body mass at c. 2 Ma. Possibilities include a shift to a high quality diet (Aiello and Wheeler, 1995), the advent of cooking (Wrangham et al., 1999; Fonseca-Azevedo and HerculanoHouzel, 2012), a shift to intensive carnivory (Domínguez-Rodrigo, 1997; Braun et al., 2010; Ferraro et al., 2013), or new behavioral responses to deal with changing environments in, or possibly outside, Africa (Gabunia et al., 2000; DeMenocal, 2004). But this



increase concerns average body mass. Our results suggest that large body size in some individuals and high levels of body size variation appeared early, at least with Au. afarensis. In addition to longer lower limbs in some australopiths (Pontzer, 2012; Richmond et al., in prep), these findings contrast with current adaptive models on the origins of Homo that rely on the assumption that these features are unique to our genus. Based on currently described fossils, the picture of hominin body mass painted here (Fig. 2) is distinct from those of other ann et al., 2014). There are no clear temporal trends in alyses (e.g. Anto hominin body mass variation (e.g., from Australopithecus to H. habilis to H. erectus). Rather, body mass increases (and variation in body mass) appears to have evolved in specific hominin taxa, with relatively larger size in some (Au. afarensis, H. erectus) and smaller size in others (Au. africanus, H. habilis s.s., H. floresiensis). Species estimates based on so few individuals will require reevaluation as additional fossils are recovered, but evolutionary n et al., 2014) that suggest a significant increase scenarios (e.g. Anto in hominin body size occurred at the time of the earliest evidence for Homo are not consistent with the best data currently available. As Johanson et al. (1987: 209) wrote in their description of the OH 62 Homo habilis skeleton, “the very small body size of [this individual] … suggests that views of human evolution positing a incremental body size increase through time may be rooted in gradualistic preconceptions rather than fact”. Whatever factors led our genus down its unique evolutionary path, the fossil evidence we can rely on is not consistent with the hypothesis that the origin of Homo coincided with, and thus was driven by, an increase in body mass. Acknowledgments We thank Sarah Elton, the Associate Editor, Adam Gordon, and two anonymous reviewers for comments that greatly improved both the methodology and content of this manuscript. We are grateful to Dave Hunt, Lyman Jellema, Doug Owsley, and Kari Bruwelheide for comparative material used in this analysis. We thank Ashley Hammond for providing supplemental measurements of some of the hominin fossils at the National Museums of Kenya. We thank Ozzie Pearson and Fred Grine for compiling the worldwide sample of modern human skeletal data, along with WLJ. Funding for this research was provided by NSF DGE-0801634, NSF BCS-1128170, NSF BCS-1028699, NSF BCS-1515054, NSF SMA1409612, The George Washington University's Selective Excellence Program, and the Fulbright U.S. Scholar Program. Supplementary Online Material Supplementary online material related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2015.05.005. References Aiello, L.C., Wheeler, P., 1995. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199e221. Aiello, L.C., Wood, B.A., 1994. Cranial variables as predictors of hominine body mass. Am. J. Phys. Anthropol. 95, 409e426. cija, S., Tallman, M., Alba, D.M., Pina, M., Moya -Sola , S., Jungers, W.L., 2013. The Alme femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins. Nat. Comm. 4, 2888. n, S.C., 2012. Early Homo: Who, When, and Where. Curr. Anthropol. 53, Anto S278eS298. n, S.C., Potts, R., Aiello, L.C., 2014. Evolution of early Homo: An integrated Anto biological perspective. Science 345, 1236828-1e1236828-13. n, S.C., Snodgrass, J.J., 2012. Origins and Evolution of Genus Homo. Curr. Anto Anthropol. 53, S479eS496.

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