H. sapiens and H. neanderthalensis

Evolution in the Genus Homo
Annual Review of Ecology, Evolution, and Systematics
Vol. 42: 47-69 (Volume publication date December 2011)
First published online as a Review in Advance on August 11, 2011
DOI: 10.1146/annurev-ecolsys-102209-144653

There is a long-standing debate about whether H. sapiens arose in Africa and then migrated across the globe, replacing any and all premodern Homo populations, or whether these various migrations of modern humans engaged in significant levels (i.e., detectable genetically or morphologically) of interbreeding with the preexisting premodern Homo populations (e.g., Relethford 2001, Stringer 2002). The multiregional continuity hypothesis argues that once H. sapiens left Africa, significant gene flow took place between them and the hominins they encountered (Wolpoff et al. 2000) and that, moreover, this gene flow influenced the nature of regional variations in morphology seen among extant populations of H. sapiens. The strong version of the recent out-of-Africa model also posits that H. sapiens arose in Africa, but it suggests that no significant gene flow took place between them and the hominins they encountered beyond Africa. In the past two decades most of the genetic evidence has favored the recent out-of-Africa hypothesis. A seminal study from Allan Wilson's lab (Cann et al. 1987) suggested that the common ancestor of all (maternally inherited) modern mitochondrial DNA (mtDNA) lived in Africa approximately 200 ka, and studies investigating the evolutionary history of the paternally inherited Y chromosome suggested that the last common ancestor of modern humans lived well within the past 100 ka (Karafet et al. 2008, Thomson et al. 2000). Investigations of single nucleotide polymorphisms (SNPs) and autosomal microsatellites indicate that genetic diversity is highest in Africa and steadily decreases as the distance from the continent increases (Prugnolle et al. 2005, Ramachandran et al. 2005), and prior to 2010 research on mtDNA had not revealed any evidence of admixture (Briggs et al. 2009, Jakobsson et al. 2008, Krings et al. 1997, Serre et al. 2004, Tishkoff et al. 2009).

This perspective was challenged in 2010 with the publication of the draft sequence of the nuclear genome reconstructed from DNA recovered from three H. neanderthalensis fossils from Vindija Cave in Croatia (Green et al. 2010). This study also found that all of the H. sapiens DNA samples tested (with the notable exception of those from Africa) contained between 1% and 4% of the distinctive DNA sequence recovered from Neanderthal fossils. By identifying and analyzing SNPs between the two groups of genomes, the researchers discovered that Neanderthal DNA is significantly closer to non-African modern human DNA than it is to African DNA, and statistical analysis of the gene flow led the researchers to argue that the gene flow was from Neanderthals to the ancestors of non-African modern humans. This evidence suggests that once early anatomically modern humans left Africa, some interbreeding did occur with the indigenous groups of Neanderthals they encountered, conceivably in the Middle East before modern humans moved into Eurasia and prior to the divergence of the European, East Asian, and Papuan groups. These new data are consistent with the assimilation hypothesis espoused by Fred Smith (Smith 1985; Smith et al. 1989, 2005; Trinkaus & Smith 1985). As new evidence accumulates, the theory of modern human origins will most likely move away from a simple recent out-of-Africa explanation to a more intricate and sophisticated account in which several different groups of ancestors lived in pockets around the globe.

More evidence for taxonomic complexity in later Homo (see above) came from an unexpected source. In 2008 a taxonomically undistinguished hominin distal manual phalanx was recovered from layer 11 (approximately 50–30 ka) at the cave site of Denisova in southern Siberia. Its geographical location plus the subterranean location of the sediments provided near-optimal conditions for DNA preservation, and in April 2010 the complete mitochondrial genome of that unknown hominin was published (Krause et al. 2010). Later in the same year, an enlarged group of researchers published the nuclear genome sequence of the same fossilized phalanx, along with an analysis of the mtDNA and the morphological affinities of a left upper second (M2) or third (M3) molar that had been recovered from layer 11.1 in the south gallery of the Denisova Cave in 2000 (Reich et al. 2010). Comparisons with the nuclear genomes of modern humans and H. neanderthalensis indicate that although the Denisova hominin sequence is more similar to Neanderthal DNA, it is nonetheless distinct enough to be considered a separate population, which the researchers sensibly referred to only informally as Denisovans (Reich et al. 2010, but see Caldararo & Guthrie 2011). Apparently, at least some Melanesian populations of H. sapiens share approximately 4–6% of their DNA with the Denisovans. These landmark papers suggest there is evidence of gene flow from premodern Homo species to modern H. sapiens at two different time periods. The initial episode of admixture occurred soon after anatomically modern humans left Africa, and the second episode involved the ancestors of Melanesian modern human populations living in present day Papua New Guinea.