Body mass evolution in hominoids including fossils

To reconstruct the adaptive landscape for body mass in primates including hominins and test hypotheses on when regime shifts occurred, we used the recently introduced “SURFACE” approach38 that fits a series of evolutionary hypotheses via Ornstein-Uhlenbeck or OU stabilizing selection models37 to phenotypic species data related via a phylogeny and retains the hypotheses that best fits the data (seen in the lowest corrected Akaike Information Criterion or AIC c score). OU models permit the realization of Simpson’s41 adaptive zones by allowing for the placement of selective regimes along different branches of a phylogeny, where species in each regime evolve toward a distinct trait optimum—in this case the optimal body mass for a given regime. In the OU model, species have their own local adaptive optima, the position of which is influenced by numerous selective factors. Species within the same selective regime are also pulled toward a “primary” adaptive optima that is influenced by the selective factor or factors that define that regime (e.g., arboreality as a factor could define a selective regime with a smaller bodied optimal body size). Evolutionary constraints (due to ancestry, genetic correlations, functional constraints, and so on) reduce the rate of adaptation given a change in the selective regime, and can lead to species' trait values that are quite distant from the primary optimum of a given selective regime37. Here, “optima” or “adaptive optima” always refer to primary adaptive optima, not local adaptive optima. OU models differ from the more commonly used Brownian motion (BM)-based models of evolution as they model the evolutionary process as the combination a deterministic pull toward adaptive optima and fluctuations around this optimum that result from unmeasured forces (e.g., other selective factors, genetic drift). As such, OU models are consistent with current views on evolutionary change39, 42, 43. Importantly, this approach also identifies convergence in regimes—whether distantly related species found similar optima. Here, because the selective regimes are not assigned a priori, distantly related species in convergent regimes are not necessarily under the same set of selective factors, though they share the same estimated optima.

Our results show that the earliest putative hominins (O. tugenensis, Ar. ramidus), and the early australopith Au. anamensis shared an selective regime with both species of Pan (Fig. 1a, b; Regime “m” in Table 2), and along with evidence that these fossil taxa were the mass of a chimpanzee (see above and Table 1), argue that the LCA of chimpanzees and humans was indeed chimpanzee-sized. This selective regime begins after the divergence of Hispanopithecus and includes the African hominid LCA—while geographically and temporally distinct, this result suggests that all of these species lived in an environment/or environments that favored the same optimal body size. While a selective regime favoring a slightly smaller body mass shared by Sivapithecus (with both species of Pongo sharing a derived larger body mass regime) and Hispanopithecus (Fig. 1a, b; Regime “b” in Table 2) was present after the divergence of hylobatids until after the LCA of hominids, the LCA of hominoids lived in a regime that was similar to extant hylobatids, stem fossil apes Ekembo heseloni, Proconsul africanus, and Pliobates cataloniae, and was plesiomorphic (primitive) and shared with a large number of Old World Monkey species and converged on by Atelidae (Fig. 1a, b; Regime “h” in Table 2). Focusing on hominins, a regime shift towards a smaller body mass (Fig. 1a, b; Regime “b” in Table 2) occurred with the arrival of Au. afarensis and persisted through all early hominins (Au. africanus, Au. sediba, P. boisei, P. robustus, H. habilis, H. floresiensis), before a regime shift to a larger optimal body mass near the origins of H. erectus shared with modern humans (Fig. 1a, b; Regime “e” in Table 2). There was also evidence that a few hominins and fossil apes converged on selective regimes shared with other hominoids—Pr. africanus converged on the body mass optima shared with both species of Pan and the earliest hominins, Pr. major with the large bodied regime of both Gorilla species, E. nyanzae and D. fontani with the larger bodied regime shared by both species of Pongo, which is also converged on by H. erectus and modern humans (Table 2).

Fig. 1 Time-calibrated phylogenetic tree with selective regimes and estimated body size optima. a Primate phylogenetic tree including fossils with tips color-coded to denote families, major families noted on the right. Phylogeny showing complete species names shown in Supplementary Fig. 1A Colors along branches showing best-supported selective regimes for body mass evolution including convergence and are consistent between a, b and c. Two major selective regimes for primates and optimal body size for each regime shown on far right correspond to Table 2; b focus on hominoids from a including fossil taxa. Marked nodes correspond to last common ancestors of all hominoids (1), hominids (2), African hominids (3), and chimpanzees and humans (4); c body mass averages (smaller circles) and inferred primary adaptive optima (larger circles) for species in each regime for primates including fossils corresponding to a and b. Numbered LCAs match nodes in b. Also noted is the adaptive optima of chimpanzees, the earliest hominins, later early hominins, and modern humans. Named taxa are outliers to their estimated optima Full size image

Table 2 Selective regimes, estimated body mass optima, and groups assigned to each regime for primates including fossils with fossil families in parentheses Full size table

To test how different estimates of body mass for O. tugenensis and Ar. ramidus 7, 30 affect our results, we reran our analysis using smaller body mass estimates that depend on the fossils sharing a modern human rather than a great ape pattern of scaling (Table 1). Our results (Supplementary Fig. 2A, B) show that a smaller body mass for these two taxa has no major impact on our overall findings—the LCA of chimpanzees and humans now shares a selective regime with the slightly smaller bodied pygmy chimpanzee (Pa. paniscus) as well as two of the earliest putative hominins (O. tugenensis, Ar. ramidus) but this regime now includes the slightly smaller Au. afarensis while Au. anamensis converges on the slightly larger-bodied regime that contains common chimpanzees. As the phylogenetic placement of D. fontani and other European and Asian hominids as closely related to African hominids is debated (reviewed in ref. 26), we tested how including these taxa affected our results by rerunning our analyses after removing these species. Overall results are consistent and robust (Supplementary Fig. 3A, B), with the only major change being that the larger-bodied regime that includes the Pongo lineage now includes both the hominid and the African hominid LCA, from which the smaller-bodied chimpanzee-like and larger bodied gorilla-like optima diverge. To test how inclusion of fossil taxa where average body mass estimates are based on only a few individuals (e.g., n = 1) affects our results, we reran our analyses using only those taxa where average body mass is based on more than two individuals (leading to the exclusion of O. tugenensis, Ar. ramidus, Au. anamensis, Au. sediba, H. habilis, and H. floresiensis) and are well attributed to particular taxa (leading to the exclusion of “probable” P. boisei 3). We also excluded the data from Miocene apes and other fossil primates because of uncertainties about their phylogenetic relatedness. Overall results (Fig. 2a; Supplementary Fig. 4) are extremely similar to the results using the smaller bodied estimates of Ar. ramidus and O. tugenensis—Au. afarensis shares a selective regime with Pan (here both Pa. troglodytes and Pa. paniscus) with a shift to a smaller-bodied regime early in australopiths (encompassing Au. africanus and P. robustus) and increase at the time of H. erectus, but now the Pan-sized selective regime extends back to a shift after the LCA of hominoids (Node “1”). Finally, to test how using species averages for extremely sexually dimorphic species affects our findings, we used only average female body mass for the extant primates and estimated female body mass averages for our well-sampled reliably attributed hominins3, leading to the removal of a number of hominin taxa (O. tugenensis, Ar. ramidus, Au. anamensis, Au. sediba, P. boisei, and H. habilis). Here (Supplementary Fig. 5), the LCA of chimpanzees and humans shares a selective regime with the smaller bodied pygmy chimpanzee (Pa. paniscus), which stretches back to shortly after the LCA of hominoids (Node “1”) and includes Sivapithecus, Hispanopithecus, Pongo pygmaeus, and Au. afarensis. It is important to note that in some lineages, female body masses may have evolved in a different manner than average body mass, as discussed below.

Fig. 2 Alternative hypotheses for primates focused on hominoids. a Best-supported selective regimes with only well-sampled reliably attributed early hominins and without other fossil primates; complete data set with b Brownian motion; c single regime model (OU1); d chimpanzee-sized ancestor all hominoids. Colors reflect regime assignment within each figure and are not comparable between figures Full size image

We tested the relative support of our results for each iteration of our data set compared to three other alternative evolutionary hypotheses (Fig. 2b–d) using relative AIC c values including a hypothesis of evolution by genetic drift (a Brownian motion model of evolution), a model where adaptive evolution is toward one body mass optimum (a single-peak OU model), and a (multi-peak) model based on the SURFACE model where the LCA of all hominoids was chimpanzee-sized and the hylobatid lineage evolved by dwarfism. This last hypothesis assumes that the increase in body mass occurred prior to the divergence of the hylobatids and proconsuloids. Our results suggest that the adaptive landscape shown above (Fig. 1) and returned by SURFACE is the most likely model as seen in its smallest AIC c values, regardless of the data set used (Table 3; Supplementary Table 2).

Table 3 AIC c results and comparison between models for different evolutionary hypotheses including Brownian motion (BM), a single regime OU model (OU1), a chimpanzee-sized ancestor of all hominoids (Anc_Pan), and the best-supported model (Surface fit) for different subsets of body mass data Full size table

Patterns of body mass evolution in primates

One main goal of the OU model of evolution is to infer details of evolutionary processes such as estimating adaptive optima for each selective regime and quantifying the rate of adaptation, measured by the phylogenetic half-life (t 1/2 )—the average time it takes for the trait to evolve half of the distance from its ancestral state to the new optima after a regime shift37. Half-lives provide an estimate of the time it takes before adaptation to the new selective regime is expected to be more influential than constraints from the ancestral regime, thus providing a metric quantifying the effects of phylogenetic inertia (resistance or slowness in adaptation to the optima). Combined with half-lives greater than zero, divergence of individual species means from their optimum can be an indication of constraints on adaptation from any source (e.g., genetic, selective, and so on). Our best-fit model shows that all non-hominid (and non-proconsuloid) primates are evolving towards only two body mass optima (regime “a” and regime “h” Fig. 1a)—with some groups converging on these optima even when separated by deep time (e.g., the Atelidae with Hylobatidae and the majority of Cercopithecidae, separated by about 43 Ma44). All species within these regimes appear relatively close to their optima—shown in the distance of the smaller circles (species means) from the larger circles (body mass optima) in Fig. 1c. Included extant strepsirrhine species from the families Cheirogaleidae, Daubentoniidae, Galagidae, Indriidae, Lemuridae, Lorisidae, and species of the New World Monkey group Cebidae, as well as extant taxa Aotus trivirgatus, Tarsius bancanus, and Cacajao calvus and fossil taxa Archicebus achilles (Family: Archicebidae), Karanisia clarki (Galagidae), Komba robustus (Galagidae), Carlocebus carmenensis (Pitheciidae), Nycticeboides simpsoni (Lorisidae), Branisella boliviana (incertae sedis), are all evolving toward an optimal body mass of around 1.4 kg (Regime “a” in Fig 1a, c; Table 2); extant species from the families Atelidae, Hylobatidae, and almost all Cercopithecidae, as well as fossil taxa Victoriapithecus macinnesi (Cercopithecidae), Epipliopithecus vindobonensi (Pliopithecidae), Ekembo heseloni (Proconsulidae), Proconsul africanus (Proconsulidae), and Pliobates cataloniae (Pliobatidae) are evolving toward an optimal mass of around 7.0 kg (Regime “h” in Fig 1a, c; Table 2). Undoubtedly, inclusion of large-bodied extinct species for some clades (e.g., subfossil “giant” lemurs and huge Pleistocene atelids) would impact some of these results, but including these groups would likely merely add side branches where body mass independently increased (such as seen in the Gorilla lineage) and have no effect on our overall results. Hominids and proconsuloids are evolving to five unique optima out of the eight estimated optima for primates (Fig. 1; Table 2) despite the relatively small number of species in this clade. Hominids also appear to show the greatest difference between species averages and the estimated optima, which, combined with half-lives around 1 Ma (see below), suggest body mass evolution is constrained in our clade and/or not enough time has passed for lineages to adapt to their new optima after a regime shift (Fig 1c). The largest differences between the estimated adaptive optima for a given regime and the species placed within that regime are E. nyanzae evolving toward the larger body mass optimum shared with modern humans (Regime “e” in Fig. 1c, Table 2), Pr. major evolving toward the regime shared by both species of Gorilla with an optimal value of 126 kg (Regime “c” in Fig. 1c; Table 2), and H. heidelbergensis and H. neanderthalensis (Regime “j” in Fig. 1c; Table 2), evolving towards a substantially larger body mass optimum of 95 kg. Extreme optima estimates could mean that evolution in a particular lineage is not well modeled by the current OU process, which assumes a constant rate of adaptation and constant magnitude of stochastic fluctuations (e.g., the lineage could be evolving via a Brownian-motion process), or the lineage was indeed experiencing directional selection to a distant optimum45. While an optimal body mass for either hominin species and the larger Proconsul taxon slightly below or approaching that of gorillas might seem unlikely, optima are the average trait values species within a regime would reach given enough time and free of constraints37. These results suggest that these large-bodied hominoids would have eventually evolved even larger body masses, and overall patterns are repeated using the data set with the smaller-bodied estimates of Orrorin and Ardipithecus (Supplementary Fig. 2). Importantly, species means fall extremely close to the estimated optima for the chimpanzee–human LCA (Node “4” in Fig. 1 and Regime “m” in Fig. 1c) and hominoid LCA (Node “1”, Regime “h”), providing good evidence that the body mass of the LCA in these regimes would be quite similar to the other species in the regime and close to the estimated optima. The half-life for all data sets of species averages including fossils is between 0.82 and 1.62 Ma (Table 3; Supplementary Table 2), meaning that it takes around a million years for the average primate to evolve half-way toward a new body mass optimum, which is extremely rapid evolution with only some influence from past history. Notably, when using only average female body mass for the extant primates and well-sampled female body mass averages for hominins from above, the half-life increases to 6.52 Ma (Supplementary Table 2). Relatively long half-lives could suggest that female body mass may be more constrained than average species body mass, likely because of a closer link between females and ecology46,47,48,49. Another possibility is that female body mass evolution on individual branches of the phylogenetic tree adapted at different rates than the majority of other lineages (see above and ref. 45). Support for this latter contention is suggested when comparing the estimated adaptive optima to the female averages, where some optima are quite distant from the taxa within their selective regime (Supplementary Fig. 5). It is of note that the AICc score of the current best fit SURFACE model is still substantially better (a difference of more than 200 units) than a Brownian-motion-based model or a model with only one adaptive peak (Supplementary Table 2), suggesting that neither other evolutionary model is more appropriate for modeling female body mass evolution.

To test how including fossil data affects our results, we reran the analysis with a phylogeny and data from only extant species (Supplementary Fig. 6). Though there are now only seven hominid species, this group again shows high variation in the number of body mass regimes, evolving towards four optima, or more than half of the total number of regimes for primates. One important change is that the LCA for hominids and African hominids as well as chimpanzees and humans now shares a selective regime with Po. pygmaeus, a regime that appears constant at nodes within the phylogeny up to both Po. pygmaeus and modern humans (Nodes “2”–“4”). Notably, the LCA of all hominoids (Node “1”) remains in a regime shared with hylobatids and a large number of other primates, suggesting that this body mass was optimal at this time period, though this could be driven by the presence of the deeply rooted hylobatids. Another important change is the half-life is now 0.21 Ma (Table 3), a significant decrease from previous runs and suggests that the addition of fossil data could provide a more accurate estimate of evolutionary parameters than analyses based purely on extant data (see ref. 50 for more on this point). Additionally, comparing exceedingly long half-lives of the extant females-only data set to the extant species averages data set (Supplementary Fig. 7), 10.13 vs. 0.21 Ma (Supplementary Table 2 vs. Table 3), provides further support that average female primate body mass may be evolving in a substantially different fashion than species averages.