The meaning of Neandertal skeletal morphology Timothy D. Weaver1 Department of Anthropology, University of California, One Shields Avenue, Davis, CA 95616; and Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved June 26, 2009 (received for review April 9, 2009) A procedure is outlined for distinguishing among competing hypotheses for fossil morphology and then used to evaluate current views on the meaning of Neandertal skeletal morphology. Three explanations have dominated debates about the meaning of Nean- dertal cranial features: climatic adaptation, anterior dental loading, and genetic drift. Neither climatic adaptation nor anterior dental loading are well supported, but genetic drift is consistent with the available evidence. Climatic adaptation and activity patterns are the most discussed explanations for Neandertal postcranial features. Robust empirical relationships between climate and body form in extant humans and other endotherms currently make climatic adaptation the most plausible explanation for the wide bodies and relatively short limbs of Neandertals, and many additional postcranial features are likely secondary consequences of these overall skeletal proportions. Activity patterns may explain certain Neandertal postcranial features, but unlike the situation for climate, rela- tionships in extant humans between morphology and activities are typically not well established. For both the cranium and the post- cranium, changes in diet or activity patterns may underlie why Neandertals and Pleistocene modern humans tend to be more robust than Holocene humans. cranium ͉ human evolution ͉ modern human origins ͉ postcranium ince the discovery of Neandertals ent approaches. I begin by outlining a Lifetime Behavior vs. Evolution. Traits pro- in 1856 at the Kleine Feldhofer procedure for distinguishing among duced by lifetime behaviors should typi- Grotte in the Neander Valley competing hypotheses for fossil mor- cally be found on the skeletons of S near Du¨sseldorf, Germany (1), phology. adults, possibly older subadults, but not deciphering the meaning of Neandertal the skeletons of very young individuals. skeletal morphology has fascinated sci- Distinguishing Among Competing Individuals so young that they have not entists and the public alike. According Explanations yet done certain behaviors would not be to some early proposals, Neandertal The morphology of fossil skeletons, like expected to show traits that result from skeletons were simply pathological mod- any aspect of the phenotype, is the the mechanical loading produced by ac- ern human skeletons, but as more fossils product of genetic influences, environ- tually doing a behavior. This argument accumulated with a consistent set of mental influences, and often interac- is certainly relevant to the foraging, ma- morphological features these explana- tions between the two (14). Genetic in- nipulative, or mobility activities that tions became untenable (2, 3). Although fluences on skeletal morphology are have been proposed to explain certain pathology cannot explain Neandertal ultimately the result of the adaptive Neandertal traits (16, 17). Therefore, if skeletal morphology in general, patho- (i.e., natural selection) or neutral (i.e., a trait is present on the skeletons of logical lesions, particularly healed trau- mutation, gene flow, genetic drift) evo- young Neandertals, it must either have matic injuries, are frequent on Neander- lutionary forces that have shaped allele an evolutionary explanation (i.e., be due tal skeletons (4). frequencies in a population or species to genetic differences shaped by natural Current evidence suggests that Nean- over multiple generations. There are selection or neutral evolutionary forces) dertals last shared a common ancestor many possible environmental influences or result from environmental influences with modern humans Ͼ350,000 years on the phenotype (14), but dietary, lo- unrelated to adult behaviors. An im- ago (5–7), and fossils that are certainly comotor, or manipulative behaviors that proved understanding of development classified as Neandertals are present in shape skeletal form through the me- often cannot help with distinguishing the fossil record by Ϸ130,000 years ago chanical loading patterns they produce among possible evolutionary explana- (8, 9) and persist until Ͻ35,000 years over the lifetime of an individual are of tions, because neutral evolutionary ago (10, 11). Separate Neandertal and particular interest to investigations of forces or different natural selective pres- modern human lineages perhaps ancient skeletons (15). Therefore, the sures can act through similar develop- emerged when geographic barriers pro- task of deciphering the meaning of Ne- mental shifts (18), but it can help with duced by climate fluctuations isolated andertal skeletal morphology can be deciding whether an evolutionary expla- Neandertal populations in Europe from encapsulated as finding ways to infer the nation is warranted or not. modern human populations further evolutionary and lifetime behavioral Controlled experiments on laboratory south (8, 12). Although Neandertals causes of Neandertal skeletal features. animals are another way to distinguish originated in Europe they later extended This task is not straightforward, and, between lifetime behavioral and evolu- their geographic range into western and even when it is possible to determine tionary explanations for morphology central Asia, ranging as far south as Is- whether genetic or environmental influ- (19, 20). Because it is possible in the rael and perhaps as far east as southern ences are primarily responsible for varia- laboratory to control many variables Siberia (8, 13). tion among individuals, populations, or other than the ones of interest, the re- My purpose is to present current species for a particular skeletal trait, it sults of laboratory experiments can of- views on the meaning of Neandertal is still necessary to decide among com- skeletal morphology. Instead of a giving peting evolutionary or lifetime behav- comprehensive review, I concentrate on ioral explanations. With this in mind, I Author contributions: T.D.W. wrote the paper. aspects of Neandertal cranial and post- outline a procedure for going from a The author declares no conflict of interest. cranial morphology that have been stud- description of fossil morphology to its This article is a PNAS Direct Submission. ied extensively using a variety of differ- meaning. 1E-mail: [email protected]. 16028–16033 ͉ PNAS ͉ September 22, 2009 ͉ vol. 106 ͉ no. 38 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903864106 Downloaded by guest on September 26, 2021 SPECIAL FEATURE: PERSPECTIVE Evolutionary Explanations. If an evolution- ary explanation is warranted, the final step is to distinguish among possible hypotheses. One approach is to investi- gate whether there is an empirical rela- tionship between the morphological fea- ture of interest and a potential selective factor (e.g., temperature, humidity, loco- motor behavior, etc.) in one or more extant species. If so, then perhaps the same relationship explains patterns of variation for the feature in the fossil record. This approach implicitly assumes that whatever factors lead to a relation- ship in the extant species are also im- portant for the extinct species, and con- sequently, is most robust when similar relationships are found for multiple pop- ulations or species. A second approach is to evaluate whether the form of the feature, or complex of features, observed in fossil specimens is consistent with its pur- Fig. 1. Neandertal and modern human cranial differences. On the left is a Neandertal (La Chapelle- aux-Saints). On the right is a modern human (Cro-Magnon 1). Anterior (above) and lateral (below) views. ported function. This approach does not Photos courtesy of Chris Stringer and the Muse´e de l’Homme (Paris). attempt to directly model how natural selection would have acted; it simply evaluates the internal consistency of an ten be interpreted unambiguously. How- simply due to shared ancestry, even if the adaptive hypothesis. An internally con- ever, it is important to be cautious when features are genetically, developmentally, sistent adaptive hypothesis is not neces- extending laboratory results outside the and functionally unlinked. sarily correct, but an inconsistent one realm of the experiment. It is well An alternative to directly estimating can be rejected. Depending on the par- known that the sources of variation covariance patterns from fossils is to ticular hypothesis, different approaches within and between groups and for dif- study extant species, with the implicit can be taken to assess consistency, but ferent sets of groups can be quite differ- assumption that they have similar co- biomechanical modeling or laboratory experiments are often used (31). ent (21). This means, for example, that variance patterns to the fossil species of Third, it is sometimes possible to dis- variation in a feature could be mostly interest. Covariance patterns are similar tinguish among different evolutionary due to environmental effects for the across human populations (22), and al- laboratory animals within the context of explanations by explicitly modeling evo- though there are some important differ- lutionary forces with quantitative and the experiment, but genetic effects ences, African apes and humans have