Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins

Extensive DNA sequence data have made it possible to reconstruct human evolutionary history in unprecedented detail. We introduce a method to study the past several hundred thousand years. Our results show that (i) the Neanderthal-Denisovan lineage declined to a small size just after separating from the modern lineage, (ii) Neanderthals and Denisovans separated soon thereafter, and (iii) the subsequent Neanderthal population was large and deeply subdivided. They also (iv) support previous estimates of gene flow from Neanderthals into modern Eurasians. These results suggest an archaic human diaspora early in the Middle Pleistocene.human evolution | archaic admixture | introgression | Neanderthals | Denisovans A round 600 kya, Europe was invaded by large-brained hominins using Acheulean stone tools (1, 2). They were probably African immigrants, because similar fossils and tools occur earlier in Africa. They have been called archaic Homo sapiens, Homo heidelbergensis, and early Neanderthals, yet they remain mysterious. They may have been ancestors of Neanderthals and modern humans (3), or ancestors of Neanderthals only (4, 5), or an evolutionary dead end. According to this last hypothesis, they were replaced later in the Middle Pleistocene by a wave of African immigrants that separated Neanderthals from modern humans and introduced the Levallois stone tool tradition to Europe (6, 7). To address this controversy, we introduce a statistical method and use it to study genetic data of Africans, Eurasians, Neanderthals, and Denisovans.Our method extends an idea introduced by Reich et al. (8,9). Their "ABBA-BABA" statistics infer admixture from the frequency with which derived alleles are shared by pairs of samples. As we have shown (10), these estimators have large biases when populations receive gene flow from more than one source. The magnitudes of these biases depend on the sizes and separation times of ancestral populations. Our method avoids bias by estimating these parameters simultaneously.To accomplish this, our method uses an expanded dataset. ABBA-BABA statistics summarize allele sharing by pairs of samples. We extend this approach to include larger subsets, such as trios of samples, and to use all available subsets. This opens a rich and heretofore unused window into population history. Nucleotide Site PatternsAlthough our method can accommodate complex models, we work here with a four-population model of history (Fig. 1A), which has broad empirical support (11,12). In this model, Neanderthals (N ) contribute genes to Eurasians (Y ) but not to Africans (X ). The model allows no gene flow from Denisovans (D), for reasons explained below. Combinations of uppercase letters, such as ND, refer to the population ancestral to N and D. Lowercase letters, such as n and d , refer to individual haploid genomes sampled from these populations.The gene tree describes how genes coalesce within the tree of populations. Fig. 1B illustrates one of many possible gene trees. Although closely linked nucleotide sites tend to share...

Section: Discussionsupporting

confidence: 82%

“…On the other hand, Meyer et al (29) show that 430 ky-old fossils from Sima de los Huesos, Spain are more closely related to Neanderthals than to Denisovans. This implies an early separation of the two archaic lineages.…”

Section: Discussionmentioning

confidence: 99%

Early history of Neanderthals and Denisovans

Rogers

Bohlender

Huff

2017

“…The Atapuerca (SH) sample conforms to this cranial morphology (23), and ancient DNA analysis has shown that the Atapuerca (SH) hominins are members of the Neandertal clade (38). The incomplete braincase from Swanscombe should probably be grouped with the Atapuerca (SH) hominins as well, even though it is more Neandertalderived in its excavated suprainiac area and its bilaterally projecting occipital torus.…”

Section: Discussionmentioning

confidence: 99%

“…This same time period also documents two major technological innovations: the expansion of the Acheulean tradition (42) and the first evidence for widespread, systematic controlled use of fire (43). Both are present at the Aroeira site, whose geographic situation in extreme southwestern Europe suggests that these innovations spread quickly throughout the European continent and were largely independent of hominin morphological diversity [although with the arrival of the Acheulean industry to Western Europe, the possibility of gene flow from outside Europe should also be taken into account (38)]. Well-dated fossils, such as the Aroeira 3 cranium, with a clear technological and ecological context are crucial to building a robust evolutionary scenario during the European Middle Pleistocene.…”

Section: Discussionmentioning

confidence: 99%

New Middle Pleistocene hominin cranium from Gruta da Aroeira (Portugal)

Daura

Sanz

Arsuaga

et al. 2017

The Middle Pleistocene is a crucial time period for studying human evolution in Europe, because it marks the appearance of both fossil hominins ancestral to the later Neandertals and the Acheulean technology. Nevertheless, European sites containing well-dated human remains associated with an Acheulean toolkit remain scarce. The earliest European hominin crania associated with Acheulean handaxes are at the sites of Arago, Atapuerca Sima de los Huesos (SH), and Swanscombe, dating to 400–500 ka (Marine Isotope Stage 11–12). The Atapuerca (SH) fossils and the Swanscombe cranium belong to the Neandertal clade, whereas the Arago hominins have been attributed to an incipient stage of Neandertal evolution, to Homo heidelbergensis, or to a subspecies of Homo erectus. A recently discovered cranium (Aroeira 3) from the Gruta da Aroeira (Almonda karst system, Portugal) dating to 390–436 ka provides important evidence on the earliest European Acheulean-bearing hominins. This cranium is represented by most of the right half of a calvarium (with the exception of the missing occipital bone) and a fragmentary right maxilla preserving part of the nasal floor and two fragmentary molars. The combination of traits in the Aroeira 3 cranium augments the previously documented diversity in the European Middle Pleistocene fossil record

“…(45, 46), which are considered to be close to the root of the Neandertal lineage (47). It has been shown that primate species living in different habitats (e.g., rainforest canopy and open landscapes) differ in auditory capacities, and it is likely that habitat acoustics influence vocalization and audition (8-10).…”

Section: Discussionmentioning

confidence: 99%

Morphology and function of Neandertal and modern human ear ossicles

Stoessel

David

Gunz

et al. 2016

The diminutive middle ear ossicles (malleus, incus, stapes) housed in the tympanic cavity of the temporal bone play an important role in audition. The few known ossicles of Neandertals are distinctly different from those of anatomically modern humans (AMHs), despite the close relationship between both human species. Although not mutually exclusive, these differences may affect hearing capacity or could reflect covariation with the surrounding temporal bone. Until now, detailed comparisons were hampered by the small sample of Neandertal ossicles and the unavailability of methods combining analyses of ossicles with surrounding structures. Here, we present an analysis of the largest sample of Neandertal ossicles to date, including many previously unknown specimens, covering a wide geographic and temporal range. Microcomputed tomography scans and 3D geometric morphometrics were used to quantify shape and functional properties of the ossicles and the tympanic cavity and make comparisons with recent and extinct AMHs as well as African apes. We find striking morphological differences between ossicles of AMHs and Neandertals. Ossicles of both Neandertals and AMHs appear derived compared with the inferred ancestral morphology, albeit in different ways. Brain size increase evolved separately in AMHs and Neandertals, leading to differences in the tympanic cavity and, consequently, the shape and spatial configuration of the ossicles. Despite these different evolutionary trajectories, functional properties of the middle ear of AMHs and Neandertals are largely similar. The relevance of these functionally equivalent solutions is likely to conserve a similar auditory sensitivity level inherited from their last common ancestor.middle ear | homo | 3D shape | covariation T he hominin fossil record can only provide indirect information about auditory capacities of our extinct relatives. Inferences about the evolution of the human sense of hearing require understanding of the interplay between form and function in extant species. When auditory capacities are visualized as audiograms, plotting the sensitivity for different frequencies, anatomically modern humans (AMHs) differ from the W-shaped pattern found in most anthropoid primates. AMHs are characterized by a drastically lowered high-frequency cutoff and maintaining high sensitivity in the low to midfrequencies, resulting in a U-shaped audiogram (1-7). In primates, such hearing variability is assumed to be partly related to forms of vocalization and habitat acoustics (8-10). Diverse hearing capabilities are also related to the morphology of the diminutive middle ear ossicles housed in the tympanic cavity (11, 12). The malleus, incus, and stapes form the ossicular chain that connects the tympanic membrane to the oval window of the inner ear. These bones play an important role in audition by amplifying and regulating the sound waves transmitted to the cochlea (11,(13)(14)(15). In particular, the middle ear acts as a transformer that matches the impedances between the air and the pe...