Inferring Allele Frequency Trajectories from Ancient DNA Indicates That Selection on a Chicken Gene Coincided with Changes in Medieval Husbandry Practices

Ancient DNA provides an opportunity to infer the drivers of natural selection by linking allele frequency changes to temporal shifts in environment or cultural practices. However, analyses have often been hampered by uneven sampling and uncertainties in sample dating, as well as being confounded by demographic processes. Here, we present a Bayesian statistical framework for quantifying the timing and strength of selection using ancient DNA that explicitly addresses these challenges. We applied this method to time series data for two loci: TSHR and BCDO2, both hypothesised to have undergone strong and recent selection in domestic chickens. The derived variant in TSHR, associated with reduced aggression to conspecifics and faster onset of egg laying, shows strong selection beginning around 1,100 years ago, coincident with archaeological evidence for intensified chicken production and documented changes in egg and chicken consumption. To our knowledge, this is the first example of preindustrial domesticate trait selection in response to a historically attested cultural shift in food preference. For BCDO2, we find support for selection, but demonstrate that the recent rise in allele frequency could also have been driven by gene flow from imported Asian chickens during more recent breed formations. Our findings highlight that traits found ubiquitously in modern domestic species may not necessarily have originated during the early stages of domestication. In addition, our results demonstrate the importance of precise estimation of allele frequency trajectories through time for understanding the drivers of selection.

The authors are grateful to Brian Follett for his comments on the biological functions of the TSHR gene. L.L., R.A., K.D., and G.L. were supported by Natural Environment Research Council, UK (grant numbers NE/K005243/1, NE/K003259/1). M.G.T. was supported by Wellcome Trust Senior Investigator Award (grant number 100719/Z/12/Z) and Leverhulme Trust (grant number RP2011-R-045). A.M. and A.E. were supported by the European Research Council Consolidator grant (grant number 647787-LocalAdaptation). R.A., N.S., and G.L. were supported by Arts and Humanities Research Council (grant number AH/L006979/1). R.A. and G.L. were supported by European Research Council (grant number ERC-2013-StG 337574-UNDEAD).