Title of entry: Homo heidelbergensis Author: Laura T. Buck, Research Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores University, Byrom Street, Liverpool, L3 3AF, UK; [email protected] Definition: A controversial Middle Pleistocene (~780-130 ka) hominin species, part of the same genus (Homo) as extant humans. Introduction: The taxonomy and phylogeny of Homo heidelbergensis is much debated (for a review see Stringer, 2012), so much so that this period in human evolution has been dubbed the ‘muddle in the Middle [Pleistocene]’. There is little agreement on which specimens should be included in H. heidelbergensis (that is to say, the group of specimens which constitute what is known as its ‘hypodigm’), nor even whether it constitutes a valid species at all. Many Middle Pleistocene hominins (taxa more closely related to H. sapiens than to chimpanzees) share primitive features with earlier species, such as H. erectus, but also share derived traits with later Pleistocene specimens such as H. sapiens and Neanderthals (e.g., Rightmire, 2013). This mosaic morphology has led researchers to group them together as a single Afro-European species designation: H. heidelbergensis. Some have also suggested that additional Asian Middle Pleistocene fossils may extend the range of H. heidelbergensis (e.g., Stringer, 2012). One reason for the great interest in H. heidelbergensis is that the Middle Pleistocene is the epoch during which the H. sapiens lineage split from our sister taxa, the Neanderthals and Denisovans and H. heidelbergensis has long been considered a possible last common ancestor (LCA) for these two lineages (Buck & Stringer, 2014; Mounier et al., 2009; Rightmire, 2008; Stringer, 2012). Knowing the identity of the LCA would allow us to see which differences between our own species and Neanderthals are derived in which lineage, enabling us to better understand our own evolution and that of our closest relatives. What is H. heidelbergensis? The name H. heidelbergensis comes from the Mauer mandible, a ~600 ka (thousand year old) fossil found near Heidelberg, Germany in 1907. This remarkably robust mandible is the type specimen for H. heidelbergensis, the specimen against which all potential members of the species must be compared. This means that no hypodigm can be called H. heidelbergensis without the inclusion of the Mauer mandible. The size and robusticity of the Mauer mandible are reminiscent of H. erectus, yet it is much younger than any European H. erectus and also displays characteristics linking it to later taxa, such as smaller teeth (Stringer, 2012). There are similarities between the Mauer mandible and a mandible from Arago (France, ~ 400 ka) and a partial cranium from Arago shows affinities with Middle Pleistocene fossils from elsewhere in Europe and Africa, allowing the entire hypodigm to be designated H. heidelbergensis (Mounier et al., 2009; Rightmire, 2008). The use of a mandible for the important role of type specimen has complicated our understanding of H. heidelbergensis (Stringer, 2012). Few mandibular fossils are known from the Middle Pleistocene, making it hard to link specimens from different sites with the Mauer mandible and thus with the species designation H. heidelbergensis. Furthermore, there are fewer diagnostic traits on the hominin mandible than the cranium, making it a less reliable region for dividing taxa. Comparative shape analysis of Mauer and other Middle Pleistocene mandibles supports an Afro-European species diagnosis of H. heidelbergensis (Mounier et al., 2009), but this depends on the hypodigm. If Spanish material from the site of Sima de los Huesos is excluded, based on recent reinterpretations of these fossils as early Neanderthals, there is less evidence for linking the Mauer mandible to the rest of the hypodigm (Stringer, 2012). It has been suggested that the Mauer mandible should be discarded as the type specimen for H. heidelbergensis (Hublin 2009), in which case the name H. rhodesiensis (taken from the fossil Kabwe from Zambia, previously Rhodesia) would probably be applied to an Afro-European taxon combining Middle Pleistocene material such as Bodo, Kabwe and Petralona (Fig. 1) (Buck & Stringer, 2014; Stringer, 2012; Thackeray et al., 2020). For clarity, the designation H. heidelbergensis will be used here throughout to describe this general hypodigm. What are the characteristics of H. heidelbergensis? Middle Pleistocene fossils diagnosed as H. heidelbergensis (Fig. 1) exhibit a combination of primitive, H. erectus-like, features with those that are derived compared to H. erectus and are those found in chronologically younger taxa. Primitive characteristics of this group include the occipital morphology, wide interorbital breadth and large browridges, whilst more derived features include greater brain volumes, the basicranial morphology and reduced facial projection (Rightmire, 2008; Rightmire, 2013). There is, however, much variation within the group, even within geographical regions. Many species show considerable variation due to factors such as sexual dimorphism, adaptation to local environments and population history and opinions differ as to whether the levels of variation within the H. heidelbergensis hypodigm exceed those plausible for a single species (Lacruz et al., 2019; Mounier et al., 2009; Rightmire, 2008; Stringer, 2012). [Placement Fig. 1 – H. heidelbergensis fossils] Figure 1 legend: Three of the most iconic potential H. heidelbergensis specimens (left to right): Kabwe (Broken Hill) from Zambia dated to ~ 300ka, Bodo from Ethiopia dated to ~ 600 ka and Petralona from Greece dated to ~400 ka. From top to bottom, images are of front, top and side views of crania. Images are of virtual models created using CT data, courtesy of the Natural History Museum (London), University of Vienna and University of Thessaloniki respectively. The side view of Kabwe has been mirrored horizontally for consistency as the right side of the fossil is better preserved. Images have been approximately scaled to equal size for better comparison. Archaeological sites attributed to H. heidelbergensis, such as Boxgrove (UK, ~500 ka), have yielded rich lithic assemblages including beautiful Acheulian handaxes (Roberts & Parfitt, 1995). Organic remains this ancient are rarely preserved, but extraordinary wooden artefacts, possible spears, from the sties of Clacton (UK, ~400 ka (Allington-Jones, 2015)) and Schöningen (Germany, ~300 ka (Conard et al., 2015)) hint at considerable technological and hunting sophistication during this epoch. The Middle Pleistocene also sees the first good evidence for control of fire, with the remains of clear hearths at sites such as Beeches Pit (UK, ~ 400 ka) (Roebroeks & Villa, 2011). This archaeology provides insights into how these hominins were able to colonize high latitude regions of Europe during the Middle Pleistocene. The role of H. heidelbergensis in human evolution: For some time, H. heidelbergensis has been widely thought of as the possible LCA of H. sapiens and Neanderthals (Fig. 2). H. heidelbergensis is a suitable candidate for this role as the H. sapiens and Neanderthal / Denisovan lineages diverged in the Middle Pleistocene and potential H. heidelbergensis fossils are found in both Africa, the birthplace of H. sapiens, and Europe, the birthplace of Neanderthals. Depending on the hypodigm favored, H. heidelbergensis also shows cranial expansion and facial characteristics that can be argued to foreshadow the morphology of both H. sapiens and Neanderthals (Buck & Stringer, 2014; Mounier et al., 2009; Rightmire, 2008; Stringer, 2012; Thackeray et al., 2020). An alternative viewpoint for many years has been that H. heidelbergensis was limited to Europe, where it was ancestral to the Neanderthals alone (e.g., Dean et al., 1998) (Fig. 2). In this scenario, Middle Pleistocene African fossils formed part of another taxon, most likely H. rhodesiensis. This hypothesis relied heavily on the inclusion in H. heidelbergensis of fossils from the Spanish site of Sima de los Huesos, since these specimens show many Neanderthal characteristics, placing them firmly on the Neanderthal lineage. The re-dating of the Sima de los Huesos fossils from ~600 to ~430 ka (Arsuaga et al., 2014) has convinced many that they are best interpreted as early Neanderthals, rather than H. heidelbergensis, reducing support for exclusively European H. heidelbergensis (Buck & Stringer, 2014; Stringer, 2012). The presence of some Middle Pleistocene European fossils lacking Neanderthal characteristics, such as Ceprano (Italy, ~430 ka), and no clear chronological sequence in the development of Neanderthal morphology, may instead indicate taxonomic complexity and the co-existence of multiple lineages (Martinón-Torres et al., 2012, Bermudez e Castro et al., 2016) Changing places – recent developments: The iconic cranium from Kabwe has been pivotal to discussions of H. heidelbergensis, in part due to its similarities with Petralona from Greece, which support the taxon’s Afro-European distribution (e.g., Harvati et al., 2010; Stringer, 2012). Recent work has, however, begun to undermine the status of this fossil as a representative of the LCA of H. sapiens and Neanderthals. Since its discovery in 1921, Kabwe has been difficult to date precisely and it was given an indirect approximation of ~700-300 ka, which made it a reasonable candidate for a member of the LCA (Klein, 1973). After years of reanalysis, Kabwe has now been directly dated to about 300 ka (299 ± 25 ka) (Grün et al., 2020). Recent work shows that some characteristically H. sapiens features are already present at ~300 ka at sites such as Jebel Irhoud in Morocco (Richter et al., 2017) and the same is true of Neanderthal features in European fossils from ~400 ka onwards (e.g., Sima de los Huesos from Spain, Swanscombe from the UK, and Steinheim from Germany (Dean et al., 1998)). This being the case, Kabwe, which displays no clear Neanderthal or H. sapiens derived morphology, is less convincing as a representative of the LCA. Earlier potential H. heidelbergensis, such as Bodo (~600 ka), are chronologically possible representatives of the LCA, but with split times for H. sapiens and Neanderthal lineages based on aDNA modelling at ~600 ka (Meyer et al., 2016), an older taxon is also plausible. An alternative LCA is H. antecessor, a species known only from the Early Pleistocene (~860 ka) site of Gran Dolina, Spain (Bermúdez de Castro et al., 2017; Stringer, 2016). H. sapiens is peculiar amongst hominins in its small, vertically orientated face (Lacruz, 2019; Stringer & Buck, 2014). A fairly complete juvenile face from Gran Dolina appears to have distinctively H. sapiens-like morphology, suggesting it could be part of our lineage, whilst in other characteristics, H. antecessor fossils resemble Neanderthals (Bermúdez de Castro et al., 2017). An H. sapiens-like face in H. antecessor suggests the facial morphology of the LCA was preserved in the human lineage, whilst Neanderthal morphology diverged (Lacruz et al., 2019). The young developmental age of the crucial H. antecessor fossil was initially a concern, but computer modelling, which virtually aged the fossil along different potential growth trajectories, supported the assertion that its diagnostic morphology would have been retained into adulthood (Freidline et al., 2013). Microscopic examination of juvenile fossil bone surfaces is also suggestive. These analyses reveal patterns of areas where bone is either laid down or sculpted away, producing characteristic adult shape over the course of development. Of all the hominin taxa currently investigated, only H. antecessor seems to have a H. sapiens-like facial growth pattern (Lacruz et al., 2013; 2019). The facial evidence thus supports the hypothesis that H. sapiens-like morphology was already present in H. antecessor, the potential LCA, during the Early Pleistocene (~1800 – 780 ka) and was preserved in its descendent, H. sapiens. Those who take this viewpoint do not necessarily discount the validity of H. heidelbergensis as a species, but suggest it is tangential to the evolution of H. sapiens and Neanderthals (Lacruz et al., 2019). [Placement – Figure 2 – Possible position for H. heidelbergensis in the phylogeny of mid-late genus Homo] Figure 2 legend. Three main hypotheses for the taxonomic position of H. heidelbergensis. Time is on the left-hand axis, Ma: millions of years ago, ka: thousands of years ago. (a) European H. heidelbergensis as ancestral to Neanderthals (H. neanderthalensis) and the related Denisovans, whilst African Middle Pleistocene specimens are placed in H. rhodesiensis; (b) H. heidelbergensis as the last common ancestor of H. sapiens, Neanderthals and the related Denisovans; (c) H. heidelbergensis as not directly ancestral to either H. sapiens or Neanderthals. Conclusion: Recent years have to some extent clarified the ‘muddle in the Middle’ and evidence is building that H. heidelbergensis may not be the LCA of H. sapiens and Neanderthals. Whether it is a valid species and what constitutes its hypodigm if so, however, is still an open question. Indeed, there is growing recognition in Paleoanthropology that strict species designations are human constructs that only approximate biological reality and can be particularly problematic when applied to the fossil record (Thackeray et al., 2020). There is strong morphological evidence that at least some African and European Middle Pleistocene fossils can be combined in a hypodigm, which in the absence of mandibular evidence for the key specimens is probably best referred to as H. rhodesiensis (Stringer, 2012). Asian Middle Pleistocene fossil material has been to some-extent overlooked during this discussion and the addition of Asian fossils to this hypodigm is also still possible. One key example is the newly announced cranium from Harbin, China. This specimen appears to have similarities to the Afro-European hypodigm, but it has yet to be formally described (Lacruz et al., 2019). A number of other new discoveries, or new dates, of crania from sites such as Harbin, Aoerira (Portugal; Daura et al., 2017) and Apidima (Greece; Harvati et al., 2019), show increasing evidence of taxonomic complexity in the genus Homo during the Middle Pleistocene and multiple taxa seem likely in several regions (Martinón-Torres et al., 2012; Rak et al., 2011). Advances in aDNA research may help to unpick the relationships between Middle Pleistocene taxa. Genetic material has been sequenced from the ~430 ka Sima de los Huesos fossils, supporting their close relationship with Neanderthals and showing that Middle Pleistocene DNA can be successfully retrieved and analyzed (Meyer et al., 2016). Recent work shows the introgression of DNA from ‘ghost’ taxa (hominins of unknown taxonomic designation, perhaps those for which there is no known fossil evidence as yet) into both H. sapiens and extinct species, such as the Denisovans (Wolf & Akey, 2018). Perhaps better understanding of these ghosts, as well as additional aDNA recovery from fossils, will illuminate the true nature of H. heidelbergensis. Cross-References: Denisovans; Homo antecessor; Homo erectus; Homo ergaster; Homo neanderthalensis; phylogeny References: Allington-Jones, L. (2015). The Clacton spear: The last one hundred years. Archaeological Journal, 172(2), 273-296. Arsuaga, J. L., Martínez, I., Arnold, L. J., Aranburu, A., Gracia-Téllez, A., Sharp, W. D., Quam, R. M., Falguères, C., Pantoja-Pérez, A., Bischoff, J. & Poza-Rey, E. (2014). Neandertal roots: Cranial and chronological evidence from Sima de los Huesos. Science, 344(6190), 1358-1363. Bermúdez-de-Castro, J. M., Martinón-Torres, M., Rosell, J., Blasco, R., Arsuaga, J. L., & Carbonell, E. (2016). Continuity versus discontinuity of the human settlement of Europe between the late Early Pleistocene and the early Middle Pleistocene. The mandibular evidence. Quaternary Science Reviews, 153, 51-62. Bermúdez-de-Castro, J. M., Martinón-Torres, M., Martín-Francés, L., Modesto-Mata, M., Martínez-de-Pinillos, M., García, C., & Carbonell, E. (2017). Homo antecessor: The state of the art eighteen years later. Quaternary International, 433, 22-31. Buck, L. T., & Stringer, C. B. (2014). Homo heidelbergensis. Current Biology, 24(6), R214-5. Conard, N. J., Serangeli, J., Böhner, U., Starkovich, B. M., Miller, C. E., Urban, B., & Van Kolfschoten, T. (2015). Excavations at Schöningen and paradigm shifts in human evolution. Journal of Human Evolution, 89, 1-17. Daura, J., Sanz, M., Arsuaga, J. L., Hoffmann, D. L., Quam, R. M., Ortega, M. C., ... & Souto, P. (2017). New Middle Pleistocene hominin cranium from Gruta da Aroeira (Portugal). Proceedings of the National Academy of Sciences, 114(13), 3397-3402. Dean, D., Hublin, J. J., Holloway, R., & Ziegler, R. (1998). On the phylogenetic position of the pre-Neandertal specimen from Reilingen, Germany. Journal of Human Evolution, 34(5), 485-508. Freidline, S. E., Gunz, P., Harvati, K., & Hublin, J. J. (2013). Evaluating developmental shape changes in Homo antecessor subadult facial morphology. Journal of Human Evolution, 65(4), 404–423. Grün, R., Pike, A., McDermott, F., Eggins, S., Mortimer, G., Aubert, M., Kinsley, L., Joannes-Boyau, R., Rumsey, M., Denys, C., Brink, J., Clark, T., & Stringer, C. (2020). Dating the skull from Broken Hill, Zambia, and its position in human evolution. Nature, 580(7803), 372–375. Harvati, K., Hublin, J. J., & Gunz, P. (2010). Evolution of middle-late Pleistocene human cranio-facial form: A 3-D approach. Journal of Human Evolution, 59(5), 445-464. Harvati, K., Röding, C., Bosman, A. M., Karakostis, F. A., Grün, R., Stringer, C., Karkanas, P., Thompson, N. C., Koutoulidis, V., Moulopoulos, L. A., Gorgoulis, V. G. & Kouloukoussa, M. (2019). Apidima Cave fossils provide earliest evidence of Homo sapiens in Eurasia. Nature, 571(7766), 500-504. Klein, R. G. (1973). Geological antiquity of Rhodesian Man. Nature 244, 311–312. Lacruz, R. S., Bermúdez-de-Castro, J. M., Martinón-Torres, M., O’Higgins, P., Paine, M. L., Carbonell, E., Arsuaga, J. L. & Bromage, T. G. (2013). Facial morphogenesis of the earliest Europeans. PloS one, 8(6), e65199. Lacruz, R. S., Stringer, C. B., Kimbel, W. H., Wood, B., Harvati, K., O’Higgins, P., Bromage, T. G., & Arsuaga, J. L. (2019). The evolutionary history of the human face. Nature Ecology and Evolution, 3(5), 726–736. Martinón-Torres, M., de Castro, J. M. B., Gómez-Robles, A., Prado-Simón, L., & Arsuaga, J. L. (2012). Morphological description and comparison of the dental remains from Atapuerca-Sima de los Huesos site (Spain). Journal of Human Evolution, 62(1), 7-58. Meyer, M., Arsuaga, J. L., De Filippo, C., Nagel, S., Aximu-Petri, A., Nickel, B., Martínez, I., Gracia, A., De Castro, J. M. B., Carbonell, E., Viola, B., Kelso, J., Prüfer, K., & Pääbo, S. (2016). Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature, 531(7595), 504–507. Mounier, A., Marchal, F., & Condemi, S. (2009). Is Homo heidelbergensis a distinct species? New insight on the Mauer mandible. Journal of Human Evolution, 56(3), 219–246. Rak, Y., Hylander, W., Quam, R., Martinez, I., Gracia, A., & Arsuaga, J. L. (2011). The problematic hypodigm of Homo heidelbergensis. American Journal of Physical Anthropology 144(S52), 247 Richter, D., Grün, R., Joannes-Boyau, R., Steele, T. E., Amani, F., Rué, M., Fernandes, P., Raynal, J. P., Geraads, D., Ben-Ncer, A., Hublin, J. J., & McPherron, S. P. (2017). The age of the hominin fossils from Jebel Irhoud, Morocco, and the origins of the Middle Stone Age. Nature, 546(7657), 293–296. Rightmire, G. P. (2008). Homo in the middle pleistocene: Hypodigms, variation, and species recognition. Evolutionary Anthropology: Issues, News, and Reviews, 17(1), 8–21. Rightmire, G. P. (2013). Homo erectus and Middle Pleistocene hominins: brain size, skull form, and species recognition. Journal of Human Evolution, 65(3), 223-252. Roberts, M. B., Parfitt, S. A., & Austin, L. A. (1999). Boxgrove: a middle pleistocene hominid site at Eartham Quarry, Boxgrove, West Sussex (pp. 1-456). London: English Heritage. Roebroeks, W., & Villa, P. (2011). On the earliest evidence for habitual use of fire in Europe. Proceedings of the National Academy of Sciences, 108(13), 5209-5214. Stringer, C. (2012). The status of Homo heidelbergensis (Schoetensack 1908). Evolutionary Anthropology, 21(3), 101–107. Stringer, C. (2016). The origin and evolution of Homo sapiens. Philosophical Transactions of the Royal Society B, 371(1698), 20150237. Stringer, C. B., & Buck, L. T. (2014). Diagnosing Homo sapiens in the fossil record. Annals of Human Biology, 41(4), 312-322. Thackeray, F., Albessard-ball, L., & Balzeau, A. (2020). Comments on the Zambian Kabwe cranium (BH1) in the context of Pleistocene specimens of Homo and the need for species definitions. PaleoAnthropology, March, 29–33. Wolf, A. B., & Akey, J. M. (2018). Outstanding questions in the study of archaic hominin admixture. PLoS Genetics, 14(5), e1007349.