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Harnessing ancient genomes to study the history of human adaptation

Key Points

  • Ancient DNA provides transformative insight into the history of human adaptation via the ability to directly track genetic variant frequency changes across space and time.

  • Analyses of human, archaic hominin, and domesticated plant and animal ancient genomic data sets can each inform our understanding of past human evolution and behaviour.

  • The number of published ancient genomic data sets is growing substantially each year, contributing expanded precision and power to evolutionary analyses based on these data.

  • Human ancient genome data have already helped characterize the histories of biological adaptations to northern latitudes and cold climates, agriculture-associated dietary shifts, and a changing infectious disease landscape.

  • After migrating out of Africa, ancient human populations acquired genetic variants conferring fitness advantages in Eurasian environments through adaptive introgression with archaic hominin populations who had already been inhabiting this region for hundreds of thousands of years.

  • Ancient genome data reveal some substantial time lags between documented environmental or cultural changes and the appearance and spread of genetic variants associated with human biological adaptations, with possible implications for intervening human health and/or potential compensatory cultural behaviours.

Abstract

The past several years have witnessed an explosion of successful ancient human genome-sequencing projects, with genomic-scale ancient DNA data sets now available for more than 1,100 ancient human and archaic hominin (for example, Neandertal) individuals. Recent 'evolution in action' analyses have started using these data sets to identify and track the spatiotemporal trajectories of genetic variants associated with human adaptations to novel and changing environments, agricultural lifestyles, and introduced or co-evolving pathogens. Together with evidence of adaptive introgression of genetic variants from archaic hominins to humans and emerging ancient genome data sets for domesticated animals and plants, these studies provide novel insights into human evolution and the evolutionary consequences of human behaviour that go well beyond those that can be obtained from modern genomic data or the fossil and archaeological records alone.

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Figure 1: The recent (and ongoing) ancient genomic explosion.
Figure 2: Ancient genomic signatures of positive natural selection.
Figure 3: Biocultural adaptation to dairying and milk consumption.
Figure 4: Adaptive archaic introgression.
Figure 5: Insights into the timing of different trait evolution processes for domesticated species based on ancient DNA.

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Acknowledgements

The authors thank C. Bergey and R. George for discussion about the manuscript. This work was supported by grants from the National Science Foundation (BCS-1554834 and BCS-1317163; to G.H.P.).

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Correspondence to George H. Perry.

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Supplementary information S1 (table)

Spatiotemporal frequencies of the European lactase persistence allele. (PDF 186 kb)

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Glossary

Adaptation

A process of phenotypic and corresponding genetic change over time for traits that confer increased reproductive fitness in a given environmental context.

Positive natural selection

A mechanism of evolution in which a genetically mediated trait that confers a relative fitness advantage increases in frequency over time because of that advantage. In this Review, we refer to positive selection as an adaptive process that can act on new or previously existing genetic variants.

Phenotype

Physical traits of an organism; often refers to externally visible traits but may include internal and microscopic or biochemical traits.

Ancient DNA

DNA from palaeontological, archaeological, or historical but pre-modern biological specimens that is often damaged and degraded and recovered in small quantities.

Exome

All or nearly all protein-coding gene regions of the nuclear genome; in humans, representing approximately 1% of the genome.

Single-nucleotide polymorphism

(SNP). A single position in the reference genome at which the specific nucleotide present (thymine, guanine, cytosine, or adenine) varies among individuals in a population or species.

Archaic hominins

Now-extinct populations or species that are distinct from anatomically modern humans but that share a more recent common ancestor with modern humans than with chimpanzees — for example, Neandertals and Denisovans.

Anatomically modern humans

Hominins recognizable phenotypically as early members of our own species, Homo sapiens, first appearing >200,000 years BP in Africa.

Adaptive introgression

The process of a genetic variant that was originally introduced into a population via admixture increasing in frequency by positive natural selection because it confers a fitness advantage.

Genetic drift

Changes in genetic variation over time that are due to random (chance) processes, apart from natural selection.

Gene flow

Movement of genetic variation between populations, for example, through migration or admixture.

Neolithic

A cultural period in human prehistory characterized by early technological and demographic shifts associated with the transition to farming and pastoralism, occurring at different times across regions.

Domestication

A process of plant and animal evolution mediated by human selection for particular phenotypes (artificial selection), sometimes combined with commensal adaptation to human-constructed niches.

Biocultural adaptation

The process of interaction between human cultural and adaptive biological change (for example, dairying and the ability of adults to digest milk sugars).

Zoonotic

The ability of a pathogen to be directly or indirectly transmitted to humans from animals sharing the same habitat.

Admixture

Interbreeding between previously isolated populations.

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Marciniak, S., Perry, G. Harnessing ancient genomes to study the history of human adaptation. Nat Rev Genet 18, 659–674 (2017). https://doi.org/10.1038/nrg.2017.65

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