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system Simon et al. report that Xist The findings that Xist RNA 3. Engreitz, J.M., Pandya-Jones, A., McDonel, P., Shishkin, A., Sirokman, K., Surka, C., Kadri, S., RNA accumulates first on gene-rich preferentially associates with Xing, J., Goren, A., Lander, E.S., et al. (2013). regions followed by gene-poor gene-dense regions, and that within The Xist lncRNA exploits three-dimensional regions. When Xist RNA is depleted, these gene-dense regions it genome architecture to spread across the X chromosome. Science 341, 1237973. the gene-poor regions lose Xist RNA accumulates first on silent and then on 4. Simon, M.D., Pinter, S.F., Fang, R., Sarma, K., association first, suggesting that these active genes, indicate that underlying Rutenberg-Schoenberg, M., Bowman, S.K., Kesner, B.A., Maier, V.K., Kingston, R.E., and regions have lower affinity for Xist chromatin features associated with Lee, J.T. (2013). High-resolution Xist binding RNA. In the inducible system, Engreitz gene density and activity may affect maps reveal two-step spreading during et al. provide additional resolution of Xist RNA affinity. These characteristics X-chromosome inactivation. Nature 504, 465–469. gene-dense regions. Comparison of suggest two broad classes of models 5. Dietzel, S., Schiebel, K., Little, G., Edelmann, P., the one hour and three hour time that may explain Xist RNA spread Rappold, G.A., Eils, R., Cremer, C., and Cremer, T. (1999). The 3D positioning of ANT2 points revealed that Xist RNA (Figure 1). One possibility is that while and ANT3 genes within female X chromosome accumulates first at silent gene-dense the Xic spends the most time at 3D territories correlates with gene activity. Exp. regions and then progresses to contact sites, it samples the entire X Cell Res. 252, 363–375. 6. Filippova, G.N., Cheng, M.K., Moore, J.M., active gene-dense regions. Together over time, and that affinity of Xist RNA Truong, J.P., Hu, Y.J., Nguyen, D.K., these studies suggest that Xist RNA for chromatin features at each region Tsuchiya, K.D., and Disteche, C.M. (2005). Boundaries between chromosomal domains of coating is a multi-step process that determines how much Xist RNA X inactivation and escape bind CTCF and lack depends on 3D chromosomal accumulates at each region. CpG methylation during early development. organization, gene density, and gene Alternatively, it may be that once Xist Dev. Cell 8, 31–42. 7. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., activity. RNA has moved from the Xic to a Cao, R., Worringer, K.A., Wang, H., de la To determine whether any steps in distal site it makes an alteration at the Cruz, C.C., Otte, A.P., Panning, B., and Zhang, Y. (2003). Role of histone H3 lysine 27 Xist RNA spread are important for distal site to increase the affinity methylation in X inactivation. Science 300, silencing, Engreitz et al. employed a for and promote local cis-spread of 131–135. male ESC line that inducibly expresses Xist RNA. 8. Silva, J., Mak, W., Zvetkova, I., Appanah, R., Nesterova, T.B., Webster, Z., Peters, A.H., a mutant Xist defective in silencing Together, Engreitz et al. and Simon Jenuwein, T., Otte, A.P., and Brockdorff, N. due to deletion of a conserved et al. offer a new view of how Xist RNA (2003). Establishment of histone h3 D methylation on the inactive X chromosome element, the A-repeat ( AXist) [9]. coats the X. This lncRNA exploits the requires transient recruitment of Eed-Enx1 DAXist RNA accumulated at 3D 3D contacts between the Xic and other polycomb group complexes. Dev. Cell 4, contacts and silent gene-dense regions of the X to access distal sites. 481–495. 9. Wutz, A., Rasmussen, T.P., and Jaenisch, R. regions but failed to efficiently This mode of spread contrasts with fly (2002). Chromosomal silencing and localization accumulate over active gene-dense and worm dosage compensation are mediated by different domains of Xist RNA. Nat. Genet. 30, 167–174. regions. Thus, Xist RNA interacts with complexes, in which defined sequence 10. Chaumeil, J., Le Baccon, P., Wutz, A., and active chromatin in a different manner elements recruit the complexes to their Heard, E. (2006). A novel role for Xist RNA in the than inactive chromatin. In earlier sites of action. These new insights into formation of a repressive nuclear compartment into which genes are recruited when silenced. cytological studies DAXist RNA did Xist RNA spread will likely inform our Genes Dev. 20, 2223–2237. not co-localize with active genes, understanding of how other lncRNAs though it still coated the X [10]. can act at a distance. 1Department of Biochemistry and Together the high resolution and Biophysics, 2Department of Anatomy, cytological studies highlight that silent University of California, San Francisco, and active regions of the X are References 600 16th Street, San Francisco, CA 94158, 1. Disteche, C.M. (2012). Dosage compensation of USA. sequestered in 3D space. the sex chromosomes. Annu. Rev. Genet. 46, *E-mail: [email protected] What is the relationship between 537–560. 2. Gendrel, A.V., and Heard, E. (2011). Fifty nucleation at 3D contact points and years of X-inactivation research. Development the spread to encompass the entire X? 138, 5049–5055. http://dx.doi.org/10.1016/j.cub.2013.11.052

Homo erectus : found so far. Only a few years later, now cleaned, it graced and the Limits of a Paleontological the cover of a recent issue of Science magazine. In their article, its discoverer and colleagues [1] describe the spectacular fossil (D 4500) and compare it to its The bushy nature of the evolutionary tree in the past 3 million years is conspecifics from the same site as widely accepted. Yet, a spectacular new fossil of early Homo has prompted as earlier African forms. This some paleoanthropologists to prune our family tree. has led them to lump three early Homo taxa into a single species, Homo Jean-Jacques Hublin the summer of 2005, on a short visit erectus. to the site of in , I To date, the oldest fossil assigned to The last time I had seen this face, it was able to witness the unearthing the genus Homo is a maxilla found in was still covered with ash. One day in of the best-preserved skull of early Hadar (Ethiopia). It derives from a stone Dispatch R83 tool bearing horizon dated to 2.33 million years ago [2] and was tentatively determined as Homo ‘aff. habilis’, a small-brained hominin documented in East and South Africa until 1.44 million years ago [3] (Figure 1). Another group of African hominins that displays distinctive facial and dental features was called . H. rudolfensis is well represented around 2.06–1.78 million years ago [4] but might date back to as early as 2.4–2.5 million years ago [5]. H. erectus is believed to be a quite distinct species. Although exhibiting a broad size variation, it generally has a larger brain than the two previous forms and displays a suite of characteristic cranial features, including extremely protruding bony brow-ridges and a strong thickening across the occipital bone (Figure 1). Importantly, H. erectus is the first hominin that occupied substantial portions of . Its latest representatives lived in the Far East at least as recently as ca. 300,000 years Figure 1. Early Homo head to head. ago. Reconstructions of the best preserved skulls of Javan ( 17) [14] ca. H. erectus is usually thought to 1–1.3 million years old and East African from Koobi Fora, Kenya (KNM-ER have originated in Africa before 1.89 1813) [15], ca. 1.9 million years old. Besides size, the two specimens display differences in million years ago, therefore the face and braincase shapes, notably the presence of bone buttresses over the orbits or overlapping with Homo habilis both on the occipital. On anatomical, ecological and phylogenetic grounds some have proposed to exclude H. habilis from the genus Homo to call it ‘ habilis’ [16]. temporally and geographically. However, lately some have questioned this African origin and 1251 ml. In 2000, a very large comparable to that observed among have suggested that a more primitive (D2600) found in the site was even recent modern , form of Homo initiated the colonization assigned to a new species, Homo and . Furthermore, of Eurasia. H. erectus could therefore georgicus, distinct from H. erectus [7]. Lordkipanidze et al. [1] suggest that not have migrated ‘out-of’ but ‘in-to’ We know now that this mandible and the morphology seen in Dmanisi Africa [6]. With some human artifacts the skull D4500 both belong to the skulls and crania encompasses not dated at 1.85 million years ago, the same individual — a large male who only that seen in H. erectus, but also Georgian site of Dmanisi has played exhibited a primitive face, a that seen in H. habilis, and a central role in this debate. It is, large-boned masticatory system and a H. rudolfensis. however, best known for its around small brain. The provocative proposal to lump all 1.77 million year-old fossil hominins, these fossils within one polymorphic a truly impressive collection because Lumpers and Splitters species — H. erectus — that would of its preservation and the number Instead of following the trend of have lived for ca. 2 million years in of specimens found on a limited species splitting that is prevalent in Africa and Eurasia has revived a surface. The scientists working at the paleoanthropology, the new study long-lasting debate in hominin site have already unearthed five skulls, swings the pendulum in the opposite — that between ‘lumpers’ four and numerous direction. At Dmanisi, the human and ‘splitters’. Researchers in favor of post-cranial elements of the same remains were accumulated in dens of merging species, the ‘lumpers’, are individuals. carnivores such as giant cheetahs, rejoicing, and several blogs have Since the first discoveries, Eurasian jaguars and saber-toothed already resuscitated the ‘single discussions have surrounded the cats. Whether large cats preyed on species hypothesis’ [8]. This model, nature of this population, which does humans or humans scavenged on the launched at Michigan University in not really match the usual picture of kills of these predators is still unclear. the 1960s, argued that hominins H. erectus. In several aspects it is After some time the dens collapsed and occupied such a peculiar ecological more primitive and ‘habilis-like’. For because of the very rapid accumulation niche, in which culture plays a central example, the endocranial volume of of fossils — geologically speaking — role, that no more than a single hominin D4500 is only 546 ml, at the lower the authors have no doubt they are species could have existed at any range of H. habilis (509–687 ml), dealing with individuals from a single given time in the past. One decade while the endocranial volumes of species. They argue that the shape after it was formulated, the H. erectus range between 691 and variability among the Dmanisi skulls is demonstration of a temporal overlap Current Biology Vol 24 No 2 R84 between late Pleistocene hominins would have who want to classify species still in their and early Homo in and therefore been able to interbreed to making. between Neandertals and modern some extent, but the fact remains that humans in southwestern Asia triggered the amount of gene flow between References the decline of this oversimplified hominin lineages such as Neandertals 1. Lordkipanidze, D., Ponce de Leo´ n, M.S., Margvelashvili, A., Rak, Y., Rightmire, G.P., concept. and modern humans only amounts Vekua, A., and Zollikofer, C.P.E. (2013). A In the camp of the ‘splitters’, to a few percent [12]. This kind of complete skull from Dmanisi, Georgia, and the of early Homo. Science many express skepticism about the hybridization may indeed have 342, 326–331. methodology used by Lordkipanidze occurred only under quite peculiar 2. Kimbel, W.H., Johanson, D.C., and Rak, Y. et al. [1] to assess cranial variability. geographic or demographic (1997). Systematic assessment of a maxilla of Homo from Hadar, Ethiopia. Am. J. Phys. To do this the team used geometric circumstances. Merging most of the Anthropol. 103, 235–262. morphometrics, a powerful multivariate Pleistocene hominins within a single 3. Spoor, F., Leakey, M.G., Gathogo, P.N., Brown, F.H., Anto´ n, S.C., McDougall, I., statistical technique that analyzes the messy ‘species’ as proposed by the Kiarie, C., Manthi, F.K., and Leakey, L.N. (2007). spatial distribution of anatomical most extreme ‘lumpers’ would not Implications of new early Homo fossils from landmarks to quantify shape help much to elucidate human , east of Lake Turkana, Kenya. Nature 448, 688–691. similarities. In this case, the chosen evolutionary history. The challenge 4. Leakey, M.G., Spoor, F., Dean, M.C., measurements primarily capture faced by paleoanthropologists is then Feibel, C.S., Anton, S.C., Kiarie, C., and Leakey, L.N. (2012). New fossils from Koobi the overall skull shape, in particular to follow through time and space Fora in northern Kenya confirm taxonomic the relative size of the face and the phenotypically distinct populations diversity in early Homo. Nature 488, braincase. As a result, a number of even before they eventually become 201–204. 5. Schrenk, F., Kullmer, O., and Sandrock, O. anatomical details, such as the dental fully separated species. From (2002). Early Hominid diversity, age and features that distinguish H. habilis and ‘recognition species’ to ‘genetic biogeography of the Malawi-Rift. Hum. Evol. 17, 113–122. H. rudolfensis, are not addressed. species’, the many concepts of species 6. Wood, B. (2011). Did early Homo migrate ‘‘out Notably, closely related species of that have been proposed in biology of’’ or ‘‘in to’’Africa? Proc. Nat. Acad. Sci. USA apes, such as common chimpanzees actually match the succession of 108, 10375–10376. 7. Gabunia L., de Lumley M.-A., Vekua A., and bonobos, are not completely gradual stages these populations Lordkipanidze D., and de Lumley H. (2002). separated by this analysis, while other go through in what has been called a De´ couverte d’un nouvel hominide´ a` Dmanissi (Transcaucasie, Georgie). C. R. Palevol subtler geometric morphometric ‘gray zone’ [13]. Not surprisingly, 1, 243–253. studies are able to discriminate paleontological species tend to 8. Brace, C.L. (1967). The Stages of Human even sub-species of apes [9,10]. combine ancestors and descendants in (Englewood Cliffs, New Jersey: Prentice-Hall). The substantial variation in the the same evolutionary lineage. 9. Gunz, P., Ramsier, M., Kuhrig, M., Hublin, J.-J., Dmanisi sample mostly results from From a taxonomical point a view, and Spoor, F. (2012). The mammalian bony labyrinth reconsidered, introducing a Lordkipanidze et al.’s [1] decision to some have bypassed the difficulty by comprehensive geometric morphometric include one specific skull (D3444) in the favoring the use of vernacular terms, approach. J. Anat. 220, 529–543. analysis. This elderly individual with a such as ‘early modern humans’ or 10. Skinner, M.M., Gunz, P., Wood, B.A., Boesch, C., and Hublin, J.J. (2009). rounded cranial vault is totally ‘’ over that of binomial Discrimination of extant Pan species and edentulous and its facial morphology Linnaean Latin terms. Specifically subspecies using the enamel-dentine junction morphology of lower molars. Am. J. Phys. was strongly remodeled by bone regarding recent humans, this also Anthropol. 140, 234–243. resorption after tooth loss. Finally, resolves some philosophical issues 11. Holliday, T.W. (2003). Species concepts, another problem relates to the large that do not apply when one only deals reticulation, and . Curr. Anthropol. 44, 653–673. proportion in the fossil record of with Pleistocene mice or bears. 12. Green, R.E., Krause, J., Briggs, A.W., non-adult individuals who did not yet However, these vernacular terms are Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W.W., Fritz, M.H.Y., fully develop some aspects of their usually very loosely defined. In many et al. (2010). A draft sequence and preliminary cranio-facial robustness. When all this instances, vague wording such as analysis of the Neandertal genome. Science is taken into account the claim that ‘archaic’ or ‘modern’ to designate 328, 710–722. 13. De Queiroz, K. (2007). Species concepts there is complete overlap between the groups of late Pleistocene humans and species delimitation. Syst. Biol. 56, morphology of H. erectus and other has become almost completely 879–886. 14. Freidline, S.E., Gunz, P., Jankovic, I., African early Homo taxa becomes meaningless. The use of infra-specific Harvati, K., and Hublin, J.J. (2012). A questionable. Linnaean denominations is not comprehensive morphometric analysis of the the answer, either. The choice frontal and zygomatic bone of the Zuttiyeh fossil from Israel. J. Hum. Evol. 62, Fossil Taxonomy between species and sub-species in 225–241. In biology, species are primarily defined paleontology is often purely 15. Benazzi, S., Gruppioni, G., Strait, D.S., and Hublin, J.-J. (2014). Virtual reconstruction of based on whether their members can rhetorical. A caricature example is KNM-ER 1813 Homo habilis cranium. Am. J. have fertile offspring. Unfortunately, provided by Lordkipanidze et al. [1] Phys. Anthropol. 153, 154–160. reproductive incompatibility between themselves, when they finally assign 16. Wood, B., and Collard, M. (1999). The changing face of genus. Homo. Evol. Anthrop. 8, contemporaneous fossil species or the Dmanisi hominins to ‘‘Homo 195–207. between ancestors and descendants erectus ergaster georgicus’’ [1]. The along the same lineage cannot be exceptional discoveries of Dmanisi Department of Human Evolution, Max Planck tested. Most sister species of mammals remind us once more how crucial Institute for Evolutionary Anthropology, that have separated in a similar time- intra-population variability is when Deutscher Platz 6, D-04103 Leipzig, frame, since the beginning of the dealing with the fossil record. It will, Germany. Pleistocene 2.59 million years ago, can however, clearly not put an end to the E-mail: [email protected] still interbreed [11], even if they rarely debate on the limits of H. erectus. do outside of zoos. Most likely, all Nature did not make it easy for those http://dx.doi.org/10.1016/j.cub.2013.12.006