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1,000 ancient genomes: gene-economy innovation in cattle, sheep and goat

Periodic Reporting for period 3 - AncestralWeave (1,000 ancient genomes: gene-economy innovation in cattle, sheep and goat)

Période du rapport: 2023-12-01 au 2025-05-31

The frame for exploration of the interwoven history of humans and their livestock is often characterised as in three broad episodes where domesticate ruminant genetics and human agency have interacted to revolutionize lifeways:
● Initial domestications circa 11 kya in Southwest Asia where the keeping of animals as walking meat stores led to control of their breeding and development of beneficial new traits. This emergence of small scale livestock management was followed a millennium later by a major economic shift toward extensive herding throughout the region.
● The secondary products revolution, i.e. the intensification circa 6 kya of use of those animal products which are harvested without killing such as milk, wool and traction (e.g. woolly sheep emerged in the Near East, enabling intensive wool production which then dominated textile economy and trade for millennia).
● The development of exceptionally productive landraces, later formalized into breeds, in Europe in recent millennia which today form the genetic source of the majority of the worlds production herds (e.g. German/Dutch black and white dairy cattle).

This project is using genome sequencing of ancient genomes sampled through time and space to untangle the complex temporal weave of key gene ancestries in these partner animals in order to detect human agency in breeding and, in collaboration with archaeologist partners, to test the concepts of, and sharpen timeframes and origins of innovation within these episodes. It will also seek to use ancient epigenetics to explore archaeological variation in gene activation patterns, and will correlate genomic signals of mobility with information from cognate disciplines.
The projecthas continuted to successfully generate ancient genome data from cattle, sheep and goat and to analyse it to assess prehistoric mobility, understand the domestication process and the emergence of secondary products. In this period we have continued our sampling and generated substantial genome data from sheep, goat, and cattle, including (particularly in cattle) from wild relatives. The leveraging of genome data via imputation to yield more accurate, complete coverage has been evaluated as useful for the first time in ancient livestock (Erven et al 2022, Frontiers in Genetics) and a pipeline is established for cattle which is being written for publication (Erven et al, in prep) and also goat. We anticipate to replicate this approach in sheep using the pending release of an extensive ovine genotype resource by the genomics community for that species. If this resource does not emerge early in 2024 we will generate our own calls of published sheep genomes as an alternative input.

The project has reported goat genomes from the dawn of their domestication ~10,000 years ago in the Zagros Mountains (Daly et al 2021 PNAS USA) attracting international news coverage) giving the earliest yet evidence of human management and noting that domesticates and wild were already genetically distinct. Interestingly, selection by humans for particular traits - eg pigmentation - that we know had occurred by 8,000 year ago, did not seem to have occurred at this early stage. We have also used ancient genomes to describe previously unknown wild relative variation in early Anatolia (Daly et al 2022 eLife).

Two papers addressed the nature of the population bottlenecks involved in the domestications of sheep (Sandeval-Casetellanos et al. 2024 Science Advances) and cattle (Rossi et al. 2024, Nature). Rossi et al. also unveiled how the evolution of the extinct ancestor of cattle, the aurochs, was shaped by palaeolithic climate fluctuations in a way that mirrored human population prehistory.

These data have been analysed to assess prehistoric mobility e.g. we identified a major secondary influx of sheep into Bronze Age Europe from the steppe, mirroring massive human migrations (Daly et al. 2025, Science). This work also showed evidence for selection in the Neolithic by humans and the nature of development of wool traits and other secondary products. A large extension of the European ancient cattle data set has been analysed and shows the dynamic history of aurochs introgression but also those genes which have been under selection in recent millennia. This work will be finalised and submitted in the next period. Also, goat and sheep ancient genome data have been extended considerably, e.g. highlighting the contrasting modes of Neolithic expansion along the Mediterranean and Danubian routes, and adding more samples from the earliest domesticated sites in the Near East.

A large extension of the European ancient cattle data set has been analysed and shows the dynamic history of aurochs introgression but also those genes which have been under selection in recent millennia. This work will be finalised and submitted in the next period. Also, goat and sheep ancient genome data have been extended considerably, e.g. highlighting the contrasting modes of Neolithic expansion along the Mediterranean and Danubian routes, and adding more samples from the earliest domesticated sites in the Near East. Methodological advances included the testing and verification of imputation to leverage partial ancient animal data to achieve genome-wide diploid calls enabling deeper and more informative analyses (Erven et al. 2024 MBE) and development of a capture assay with bisulfite sequencing to diagnose the castrated state in ancients. The project has continued to engage with other laboratories via research visits and other exchanges to standardise and more deeply develop ancient livestock genomics.
These data and analyses will be a step-change in domesticate research. They include new methods - for example, imputation of these ancient livestock genomes using modern reference panels is novel and a highly efficient way to leverage the expensive and difficult-to-retrieve ancient data. It will give millions of marker calls across whole genomes from low coverage starting data - making cost effective screening of wider numbers of samples feasible. A framework of animal genomes sampled through time and space will inform on the key genetic changes linked to biological, cultural and economic evolution. It will also be a key resource for future studies.
Aurochs Skull St Petersburg credit Dan Bradley
Sheep-in-arid-landscape,-southeastern-Morocco.-Photo-by-J.-Peters,-LMU
Hoofprints in mud-brick at Ganj Dareh (see Daly et al 2021)
Scottish-Blackface-Applecross,Scotland J.-Peters,
Pleistocene-Aurochs-Upper-Rhine-Valley,-credit-Staatliche-Schlosser-and-Garten-Hessen
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