Short-term challenges resulting from colder temperature experienced by hominins were apparently countered via phenotypic adaptation toward larger bodies as a buffer mechanism; no such association of temperature with brain size

Different environmental variables predict body and brain size evolution in Homo. Manuel Will, Mario Krapp, Jay T. Stock & Andrea Manica. Nature Communications volume 12, Article number: 4116, Jul 8 2021. https://www.nature.com/articles/s41467-021-24290-7

Abstract: Increasing body and brain size constitutes a key macro-evolutionary pattern in the hominin lineage, yet the mechanisms behind these changes remain debated. Hypothesized drivers include environmental, demographic, social, dietary, and technological factors. Here we test the influence of environmental factors on the evolution of body and brain size in the genus Homo over the last one million years using a large fossil dataset combined with global paleoclimatic reconstructions and formalized hypotheses tested in a quantitative statistical framework. We identify temperature as a major predictor of body size variation within Homo, in accordance with Bergmann’s rule. In contrast, net primary productivity of environments and long-term variability in precipitation correlate with brain size but explain low amounts of the observed variation. These associations are likely due to an indirect environmental influence on cognitive abilities and extinction probabilities. Most environmental factors that we test do not correspond with body and brain size evolution, pointing towards complex scenarios which underlie the evolution of key biological characteristics in later Homo.

Discussion

Climatic fluctuations and ecological factors have frequently been proposed as potential drivers of brain and body size evolution within the hominin lineage8,9,10,11,12,23. This study presents the first systematic attempt to quantitatively test different environmental effects on body and brain size variation for the genus Homo during the past ~1 Ma. The climate variables we investigated are representative of the climatological mean (30-year averages) for each 1000-year period of the past ~1 Ma. Hence, climate oscillations on sub-millennial time scales, which might have had some impact on human body and brain size evolution, are not resolved, but such a finer resolution is also precluded by the inherently larger dating uncertainty of Pleistocene human fossils.

We found that MAT is uniformly associated with body size across Mid-Pleistocene Homo, Neanderthals, and Pleistocene H. sapiens. The extent of this relationship is greater than that estimated for modern humans in a recent study31. The direction of this association supports some of the predictions of the Environmental Stress Hypothesis, with temperature (i.e., thermal stress) being the key driver: larger body sizes are consistently found in colder regions, where both annual mean and mean coldest quarter temperature are lower. These findings fit the general expectations of Bergmann’s rule and are consistent with some—though not all33,38—previous studies on humans, hominins, and other animals8,10,22,31. Following this interpretation, short-term challenges resulting from colder temperature experienced by hominin populations (thermal stress) were apparently countered via phenotypic adaptation toward larger bodies as a buffer mechanism, either through natural selection, plasticity, or a combination of both. We failed to detect any effect of low rainfall or nutrient-poor environments as determinants of stress in our analyses.

Our analyses detected no such association of temperature with brain size. We did find relationships with the 10 ka-sigma of mean annual precipitation (MAP) and NPP, but the variance in brain size explained by these variables was small compared to the effect of MAT on body size. These results suggest that brain size within Homo is less influenced by environmental variables than body size during the past 1.0 Ma. Apart from other drivers being likely more relevant (see below), one factor contributing to the difficulty of detecting environmental effects lies in the strong performance of the null model (LM-T) based on taxonomic differences in brain size variations that explained much more variance (R2 = 0.47) compared to body size (R2 = 0.05). This being said, our analyses suggest that brain sizes tend to be higher in regions of low NPP and smaller in more productive regions, although this only holds for Mid-Pleistocene Homo but not for Neanderthals or Pleistocene H. sapiens. This negative correlation is not necessarily a direct effect of environments on human phenotype but can rather be interpreted as an indirect interaction of behavioral changes with environmental variables: regions with lower NPP feature more open steppe and grassland habitats with more frequent large mammals and particularly bovids (“productivity paradox”; ref. 39). As such, our findings can be related to changes in subsistence strategies toward more frequent and systematic hunting of larger-sized bovids in these environments, in association with cognitive changes toward more complex weapons and coordinated group activity. The lithic, faunal, and isotopic records show an increase of such behaviors and ecosystems inhabited by Homo throughout the Middle Pleistocene that supports this interpretation40,41,42,43. The divergent pattern in Neanderthals and Pleistocene H. sapiens might be due to an already higher established brain size close to the physiological maximum during colonization of more northern latitudes (>40°; H. sapiens: mean = 1505 cm3, n = 37; Neanderthals: mean = 1398 cm3; n = 25), while the other taxon either evolved in situ in these areas or had higher growth potential. More early African H. sapiens fossils are required to adequately test this interpretation.

Our fossil data show a relationship between long-term variation in rainfall (MAPvar10) and brain size that is of opposite sign than expected from the Environmental Variability Hypothesis11,36. Instead, this prediction is consistent with the Environmental Consistency Hypothesis: larger brain sizes occur in more stable environments across all studied Homo taxa. This result is likely an effect of brain growth being constrained by reduced resource availability and predictability over multi-millennial scales, acting as an extinction filter.

Our linear models did not find associations with 10-ka variability measures for other environmental variables in either body or brain size. We also failed to find support for the Environmental Constraints Hypothesis (Table 1). However, we need to be careful in interpreting these negative results. The fossil hominin record is scarce and patchy in space and time, confounding the ability to find patterns in our data26. We thus modeled and analyzed synthetic datasets to assess the degree to which the intrinsic nature of the fossil record biases and distorts associations of body and brain size with environmental variables. The power analysis shows that we should have been able to detect at least medium to strong associations between brain size and MAT, MAP, mean temperature of the coldest quarter, and mean precipitation of the driest quarter (Fig. 2). The synthetic data thus suggest that our negative results for these variables, and the lack of support for the Environmental Stress and the Environmental Constraints Hypothesis, are either “true negative” findings or that true effect sizes are relatively small. On the other hand, we had little power to detect associations of body and brain size with long-term climate variability (i.e., the consequences of the Environmental Variability and the Environmental Consistency Hypotheses), leaving them as potential targets for future analyses with even larger sample sizes.

There are several implications from our study for human evolution that point toward future analyses. Many standard models and recent accounts of the origins, bio-cultural evolution, and dispersal of our genus and species have invoked environmental drivers as prime movers9,44,45,46. Yet, necessary temporal correlations of paleoanthropological and archeological data with environmental information have been plagued by issues of resolution, scale, and data availability47. Using emulated global climate model data27, this study shows that different climatic variables predict human brain and body size evolution over the past 1 Ma. These findings have implications beyond human evolution. The scaling between body size and brain size is remarkably consistent across vertebrates, but increased variability in brain growth appears to underpin observed patterns of encephalization among birds and mammals48. Consistency in the observed patterns of encephalization within lineages is often attributed to developmental constraints that link the ontogenetic trajectories of brain and body size, although there is emerging evidence that deviations from the patterns found in mammals and primates may be driven by functional variation and different selective pressures49. Such adaptive mechanisms likely underpin the variation in brain development observed in Pleistocene hominins50. The demonstration that brain and body size evolution were influenced by different environmental factors supports this broader interpretation of unique selective pressures driving phenotypic diversification in the hominin lineage.

We also note that many of the environmental variables provided no detectable correlations and explained variance is often low, raising doubts about an unquestioned a priori reliance on environmental factors in explaining macro-processes in human evolution. There is a need for more quantitative tests of such hypotheses in explicitly formulated theoretical frameworks. Future work on these questions could (i) expand analyses on environmental drivers into the entire Pleistocene and Pliocene and (ii) examine other proposed drivers that are not tested here (see below). There are ample changes in the size of endocranial volumes and body mass between ~5 and 1 Ma among taxa of Ardipithecus, Australopithecus Paranthropus, and Homo that could be the result of climatic forcing and ecological adaptations, or yet other factors. This period also constitutes the focus of the original variability hypothesis11,36; however, the fossil record ~5–1 Ma has lower sample sizes per taxon and is patchier in time and space. While we gathered datasets for body and brain size back to 4.4 Ma6, we refrained from extending our analyses to this period as the current quality of the fossil data with the added uncertainty of climate models >1 Ma renders such studies more speculative. Improved paleoclimate models and new discoveries with good chronometric ages and taxonomic information will eventually allow for such studies.

In the meantime, testing other proposed drivers of human body and particularly brain size could be more fruitful. Inter-species competition and niche exclusion likely drove some of the observed significant differences in brain and body size between (sympatric) species of Homo (e.g., refs. 2,4,18), including shifts to larger social groups or communication networks driving further encephalization16. Archeologically established changes in subsistence patterns likely played a role as the nutritional basis allowing for the evolution of larger bodies and the maintenance of energetically costly brains14,15,51,52, and we have found indirect evidence to support this in our study. Yet the spatio-temporal trajectories and taxonomic associations of these behaviors in the archeological record are not well resolved. Finally, there is a long-standing debate about a feedback process between culture, cognition, and encephalization. Increased reliance on technology and material culture might have started a long-term directed evolutionary process selecting for advanced cognition and larger brains19,20,21, with greater detachment from direct environmental effects, particularly in H. sapiens. In parallel with brain size increases, stone tool technology showed major changes over the past 2 million years53 with an accelerated pace of cultural change by ~300 ka and again with the onset of the Upper Paleolithic and Later Stone Age17,54,55,56.

While many of these factors might have played a key role in body and/or brain size evolution, future models should include interacting components57,58 such as the co-evolution of changing environments, subsistence, and technology in driving brain evolution14,18,51,52,59. Such potential influences on hominin brain and body size need to be tested by formulating and testing explicit hypotheses with statistical analyses. This strategy requires innovative ways to translate the often qualitative archeological information into comparable quantitative data, potentially via machine learning methods. In this study, the support or falsification of certain environmental hypotheses to explain body and brain size changes among Homo in the past million years exemplify the usefulness of this approach.