Unlocking the origins and biology of domestic animals using ancient DNA and paleogenomics

Abstract

Animal domestication has fascinated biologists since Charles Darwin first drew the parallel between evolution via natural selection and human-mediated breeding of livestock and companion animals. In this review we show how studies of ancient DNA from domestic animals and their wild progenitors and congeners have shed new light on the genetic origins of domesticates, and on the process of domestication itself. High-resolution paleogenomic data sets now provide unprecedented opportunities to explore the development of animal agriculture across the world. In addition, functional population genomics studies of domestic and wild animals can deliver comparative information useful for understanding recent human evolution.

Fig. 1

Timelines of domestication for 11 animal species with relevant stratigraphy and climate chronologies. For each species, the time periods of significant pre-domestication human–animal interactions are also shown. Domestication timeline data [4, 5]. Stratigraphy information was obtained from the International Commission on Stratigraphy website [264, 265]. The Quaternary temperature plot was generated from the GISP2 ice core temperature and accumulation data [–268]

Fig. 2

Evolution and phenotypic diversity of domestic animals. The wild progenitor species are shown on the left and the domesticated animals are shown on the right. Except for the aurochs, all wild progenitor species are extant. The aurochs image is an artistic reconstruction of Bos primigenius. Image permissions: wolf (Creative Commons CC BY-SA 4.0); dog (CC BY-SA 2.5); bezoar (ID 79845213©Wrangel | Dreamstime.com); goat (CC BY-NC 2.0 - Fir0002/Flagstaffotos); aurochs and taurine bull (CC BY-SA 3.0); wild boar (CC BY-SA 3.0); pig (public domain), red jungle fowl (CC BY-SA 3.0); and chicken (CC BY-NC 2.0 - Fir0002/Flagstaffotos)

Fig. 3

Geography of archaeological DNA survival prior to the discovery of high endogenous DNA content in the mammalian petrous bone. a Expected DNA survival after 10,000 years for 25-bp fragments and 150-bp fragments close to the ground surface (modified with permission from [90]). b Illustration of a sheep (Ovis aries) petrous bone retrieved from a Middle Neolithic site at Le Peuilh, France (modified with permission from [269])

Fig. 4

Stacked bar chart and line graph showing the number of ancient samples with whole-genome sequence data (paleogenomes) from domesticated species and their wild relatives. Each genus is represented by a different color and the line indicates the total number of paleogenomes generated. The graph was produced in R using ggplot2 (data from [, , , , , , , –146, 169, 191])

Fig. 5

Taurine–zebu admixture and genomic introgression in hybrid African cattle. a Interpolated synthetic map illustrating spatial distribution of admixture, which is generated from the first principal component (PC1) of a principal component analysis (PCA) of genetic variation across African cattle populations (modified with permission from [205]). b Genetic structure plot generated from high-density SNP data (Illumina BovineHD BeadChip with 777,962 SNPs) showing individual animal proportions assuming two source populations (N’Dama, n = 24; East African Zebu, n = 92; Nellore, n = 34) (the authors, unpublished results). The structure plot was generated using fastSTRUCTURE [270] and visualised using DISTRUCT [271]. c Chromosomal local ancestry plot for bovine chromosome 7 (BTA7) showing Bos taurus and Bos indicus ancestry in East African Zebu cattle (the authors, unpublished results). Nuclear oxidative phosphorylation (OXPHOS) genes are highlighted, illustrating the potential of admixed cattle for evaluating mitonuclear disequilibria. The plot was generated using the efficient local ancestry inference (ELAI) method [272]

Fig. 6

Reticulate evolution in European wild aurochs and domestic cattle. a Geographic contour map of localized ancient British aurochs (Bos primigenius) genomic admixture with modern European cattle breeds (modified from [69] under the terms of the Creative Commons Attribution 4.0 International License, http://creativecommons.org/licenses/by/4.0). b Spatio-temporal model of historical admixture and gene flow in European cattle populations