Diet adaptation in dog reflects spread of prehistoric agriculture.

M Arendt,K M Cairns,E Axelsson,J W O Ballard,P Savolainen

doi:10.1038/hdy.2016.48

Abstract

Adaptations allowing dogs to thrive on a diet rich in starch, including a significant AMY2B copy number gain, constituted a crucial step in the evolution of the dog from the wolf. It is however not clear whether this change was associated with the initial domestication, or represents a secondary shift related to the subsequent development of agriculture. Previous efforts to study this process were based on geographically limited data sets and low-resolution methods, and it is therefore not known to what extent the diet adaptations are universal among dogs and whether there are regional differences associated with alternative human subsistence strategies. Here we use droplet PCR to investigate worldwide AMY2B copy number diversity among indigenous as well as breed dogs and wolves to elucidate how a change in dog diet was associated with the domestication process and subsequent shifts in human subsistence. We find that AMY2B copy numbers are bimodally distributed with high copy numbers (median 2nAMY2B=11) in a majority of dogs but no, or few, duplications (median 2nAMY2B=3) in a small group of dogs originating mostly in Australia and the Arctic. We show that this pattern correlates geographically to the spread of prehistoric agriculture and conclude that the diet change may not have been associated with initial domestication but rather the subsequent development and spread of agriculture to most, but not all regions of the globe.

Highlights

Despite considerable efforts to understand the timing and location of dog domestication much uncertainty still remains
It was demonstrated that (i) selection had targeted a duplication affecting the gene coding for pancreatic amylase (AMY2B), the enzyme that breaks starch into maltose in the small intestine, resulting in an average sevenfold AMY2B copy number expansion that is estimated to be associated with a 5.4% increase in serum amylase activity for each extra copy (Axelsson et al, 2013; Arendt et al, 2014)
The scarcity of duplications in wolves observed here may indicate that selection for efficient starch digestion acted on a novel mutation in dogs, rather than on standing genetic variation in a common dog and wolf population, in particular considering evidence of admixture between dogs and Middle Eastern wolves (Freedman et al, 2014)

Summary

Introduction

Despite considerable efforts to understand the timing and location of dog domestication much uncertainty still remains. Domestication in Europe is consistent with close mitochondrial DNA relatedness between ancient and extant European wolves and modern dogs (Thalmann et al, 2013), but patterns of genetic variation indicate a southern East Asian, Mongolian or Nepalese origin of dogs (Pang et al, 2009; Shannon et al, 2015; Wang et al, 2015). Analyses of whole-genome sequence data place extant wolves as sister clade to modern dogs, with no leads on the location of dog domestication, but argue for a single event that started between 11 000 and 16 000 YBP (Freedman et al, 2014). Dogs may have been domesticated somewhere in Eurasia 11 000–40 000 YBP

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