Animal domestication in the era of ancient genomics

Abstract

The domestication of animals led to a major shift in human subsistence patterns, from a hunter–gatherer to a sedentary agricultural lifestyle, which ultimately resulted in the development of complex societies. Over the past 15,000 years, the phenotype and genotype of multiple animal species, such as dogs, pigs, sheep, goats, cattle and horses, have been substantially altered during their adaptation to the human niche. Recent methodological innovations, such as improved ancient DNA extraction methods and next-generation sequencing, have enabled the sequencing of whole ancient genomes. These genomes have helped reconstruct the process by which animals entered into domestic relationships with humans and were subjected to novel selection pressures. Here, we discuss and update key concepts in animal domestication in light of recent contributions from ancient genomics.

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Fig. 1: Increase in the number of published ancient genomes for domesticated animal species and their wild relatives.
Fig. 2: Influence of ancient genomics on models of animal domestication.
Fig. 3: Major dispersals of domesticated animals uncovered by ancient genomics.
Fig. 4: Spatio-temporal pattern of admixture between cattle and zebu.
Fig. 5: Frequency of alleles underlying modern phenotypes in key domestic animal species.

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Acknowledgements

L.A.F.F. and G.L. were supported by a European Research Council (ERC) grant (ERC-2013–396 StG-337574-UNDEAD) and/or Natural Environmental Research Council grants (NE/K005243/1, NE/K003259/1, NE/S00078X/1, NE/S007067/1 and NE/S007067/1). L.A.F.F. was also supported by a Wellcome Trust grant (210119/Z/18/Z). L.O. was supported by the ERC under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 681605). D.G.B. was supported by ERC Investigator grant 295729-CodeX.

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Glossary

Neolithic

An archaeological period that began ~12,000 years ago in the Near East (later in other parts of the world), following the appearance of farming communities and the domestication of plants and animals. This period marks the latest stage of the ‘Stone Age’ and ends with the development of metallurgy (Bronze Age).

Bronze Age

An archaeological period that began over 5,000 years ago in Southern Europe and part of the Near East. This period is associated with the use of bronze and, in some regions, the advent of more urban societies.

Next-generation sequencing

(NGS). Also known as ultra-high-throughput sequencing. Sequencing technologies that allow researchers to sequence entire genomes (DNA) or transcriptomes (RNA) substantially faster and cheaper than the older technologies.

Endogenous DNA

DNA extracted from the tissue (such as bone or skin) of an organism that is no longer alive, whereas exogenous DNA originates from outside (such as from soil bacteria). The proportion of endogenous DNA molecules can vary considerably depending on the origin and the age of a sample.

Capture techniques

Also known as target enrichment, these techniques help focus sequencing efforts to a subset of the DNA templates present in DNA libraries, through hybridization to target-specific probes.

Neural crest cell

A temporary cell that differentiates into multiple cell types involved in the formation of the nervous component of bones and cartilages. Research suggests that the behaviour of neural crest cells may have been modified by domestication, leading to the development of multiple traits that are common across many domesticated animal species (also known as ‘domestication syndrome’), including depigmentation, smaller brain, floppy ear and shorter muzzle.

Runs of homozygosity

(ROH). Regions of the genome that are depleted of heterozygosity, which can arise when a diploid individual inherits two identical stretches of DNA at a specific position of the genome, due to the mating of two closely related parents (such as cousins). The length and the number of ROH across the genome can provide powerful information to infer levels of inbreeding.

Artificial selection

The process by which humans breed animals to enhance specific characteristics (traits).

Yamnaya culture

An early Bronze Age culture from the northern shore of the Black Sea (Pontic steppe).

Sintashta culture

A Bronze Age culture of the northern Eurasian steppe, which is considered to be an offshoot of the Yamnaya culture.

4.2k event

A severe aridification event beginning ~4,200 years ago, which has been hypothesized to have caused the collapse of multiple civilizations across Eurasia.

Studbooks

Registries that contain the list of animals that belong to the same breed and for which the parents are known.

Breeder’s equation

A mathematical formula that allows breeders to predict the response to selection of a specific heritable trait.

Purifying selection

Also known as negative selection. Removal of deleterious variants in a population by natural selection.

Deleterious variants

Alleles that have a detrimental effect on the phenotype of an individual.

Mutational load

The mutational burden in a population or an individual resulting from deleterious variants.

Relaxed selection

The weakening or removal of a selective pressure, such as when domesticated animals are less subject to selective pressure from predators.

Justinianic plague

A historical pandemic of Yersinia pestis (541–542 ad) that affected Mediterranean port cities, including Constantinople, and that resulted in the death of 25–50 million people.

Black Death

A historical pandemic of Yersinia pestis (1346–1353 ad) that resulted in the death of 75–200 million people across Eurasia and that is thought to have had a profound effect on European history.

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Frantz, L.A.F., Bradley, D.G., Larson, G. et al. Animal domestication in the era of ancient genomics. Nat Rev Genet (2020). https://doi.org/10.1038/s41576-020-0225-0

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