Ancient DNA and human evolution.
[Editorial review]
We are in the midst of a true revolution in ancient DNA research, with an explosion of discoveries that have revealed major new insights into our recent and deeper evolutionary past. This field recently produced publications of high quality nuclear genome sequences for two different archaic hominins – one Neandertal and one ‘Denisovan’ (Meyer et al., 2012, Prüfer et al., 2014). In 2014 alone, there have been papers describing a divergent mitochondrial DNA sequence from a Middle Pleistocene Sima de los Huesos hominin (Meyer et al., 2014); non-neutral patterns of Neandertal nuclear genomic introgression into the modern human gene pool (Sankararaman et al., 2014, Vernot and Akey, 2014); ‘exomes’ – gene coding regions across the genome – from an additional two Neandertal individuals (Castellano et al., 2014); a high quality nuclear genome from an early Eurasian anatomically modern human (Fu et al., 2014); a medium quality nuclear genome from a Clovis culture individual from Montana (Rasmussen et al., 2014); draft nuclear genomes from Late Pleistocene anatomically modern humans who lived ∼36 kya (thousands of years ago) in Russia (Seguin-Orlando et al., 2014) and ∼24 kya in central Siberia (Raghavan et al., 2014b); multiple nuclear genomic datasets from Mesolithic and Neolithic Europeans (Lazaridis et al., 2014, Olalde et al., 2014, Skoglund et al., 2014a), various Paleo-Eskimo cultures (Raghavan et al., 2014a), and historical Amerindians (Malaspinas et al., 2014); and numerous insightful analyses of these now-available data (e.g., Ding et al., 2014, Huerta-Sanchez et al., 2014, Hughes et al., 2014, Khrameeva et al., 2014). Considering recent technological advances and decreasing sequencing costs, the 2015 list of ancient human and archaic hominin genomes is confidently expected to be even longer.
The purpose of this special issue is to capture this moment with a collection of review and primary data articles representing the ancient DNA field as it relates to human and broader primate evolution. The series begins with a review of the history of paleogenomics research and the resulting major recent advances in our understandings of archaic hominin evolutionary biology and population history, anatomically modern human dispersals, ecological interactions and adaptation, and the reconstruction of paleoenvironments, among others (Ermini et al., 2015). Two articles review and describe the technological and ancient DNA methodological advances that have facilitated these recent discoveries (Marciniak et al., 2015), with one focusing specifically on the application of these tools to the vast historical museum collections of non-human primates and other taxa (Burrell et al., 2015). Related to this interest, Kistler and colleagues (2015) present a comparative and population genomic study of the extinct, giant ‘subfossil’ lemurs of Madagascar. Two articles describe paleogenomic approaches for studying the evolutionary history and timing of hominin genetic and phenotypic change (Perry et al., 2015, Sams et al., 2015).
The issue also includes reviews of ancient DNA-related insights into human population history in Europe (Brandt et al., 2015) and Polynesia (Matisoo-Smith, 2015), and Witt and colleagues (2015) present a canine ancient DNA study that informs our understanding of the human population history of the Americas. Indeed, the relevance of ancient DNA studies to human evolution is not at all restricted to direct analyses of hominin genomes, as further illustrated by reviews of ancient DNA studies of dental calculus (Weyrich et al., 2015), fecal and other microbiomes (Warinner et al., 2015), pathogens (Harkins and Stone, 2015), and hominin-plant co-evolutionary processes (Allaby et al., 2015). These papers showcase how ancient DNA studies of our microbes, or other taxa with which we are intimately associated, can indirectly document human evolutionary history.
The articles in this special issue highlight the diversity of paleogenomic applications that can advance our understanding of human and broader primate evolution, and how these might develop over the coming years. With ongoing technical and analytical advances, including improvements in the ability to isolate endogenous DNA from exogenous contamination (Skoglund et al., 2014b) and the ability to obtain DNA sequences from increasingly ancient remains (currently up to the Middle Pleistocene; Orlando et al., 2013, Meyer et al., 2014), we can anticipate a continuing slate of valuable ancient DNA developments and results that will be of interest to Journal of Human Evolution readers.
While we cannot be certain that DNA sequence data can be obtained for Homo floresiensis, we also cannot exclude the possibility, as looking a few years back, it is clear that feats previously considered impossible have now been achieved. Moreover, while recent studies have focused primarily on the analysis of a limited number of genomes, we can anticipate that future studies will increasingly involve the analysis of genome sequencing and genome-wide single nucleotide polymorphism (SNP) datasets at the population scale. For example, there is the strong likelihood that the field will generate a greatly expanded sense of Neandertal spatiotemporal genomic diversity over the next five years. Such developments will advance the power and precision with which we can describe past population histories and demographic events, including subtle and complex patterns of admixture, across a broad range of historical and archeological contexts.
With nonzero levels of admixture between some of our modern human ancestors and Neandertals and Denisovans, it is also possible to reconstruct aspects of archaic hominin soft tissue and cell biology by studying the effects of introgressed or shared ancestral alleles on modern human phenotypic variation. An excellent recent example of this approach is the discovery that an allele that confers a fitness benefit to high-altitude Tibetan modern human populations likely originally introgressed from Denisovans (Huerta-Sanchez et al., 2014). Looking forward, such analyses will likely be more systematic, using genome-wide association study (GWAS) approaches and even taking advantage of the extensive existing database of human GWAS results. Phenotypic interpretations will be further enhanced by paleogenomic advances in the characterization of genome-wide epigenetic variation among archaic hominins and prehistoric and living anatomically modern humans (e.g., DNA methylation maps: Gokhman et al., 2014; nucleosome maps: Pedersen et al., 2014), which in turn can be used to predict patterns of gene expression variation and evolution (Orlando and Willerslev, 2014, Pedersen et al., 2014).
It is thus, undoubtedly, a very exciting time for paleoanthropologists and anyone interested in the study of human and broader primate evolution, which we hope is clearly demonstrated throughout this special issue in a manner that is approachable for geneticists and non-geneticists alike.
