Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes

Abstract

Traditionally, the process of domestication is assumed to be initiated by humans, involve few individuals and rely on reproductive isolation between wild and domestic forms. We analyzed pig domestication using over 100 genome sequences and tested whether pig domestication followed a traditional linear model or a more complex, reticulate model. We found that the assumptions of traditional models, such as reproductive isolation and strong domestication bottlenecks, are incompatible with the genetic data. In addition, our results show that, despite gene flow, the genomes of domestic pigs have strong signatures of selection at loci that affect behavior and morphology. We argue that recurrent selection for domestic traits likely counteracted the homogenizing effect of gene flow from wild boars and created 'islands of domestication' in the genome. Our results have major ramifications for the understanding of animal domestication and suggest that future studies should employ models that do not assume reproductive isolation.

The ‘heritability’ of domestication and its functional partitioning in the pig

“…In agreement with other studies, for example, Frantz et al (2015), the first principal component neatly represents either the Chinese or European origin, proving that continent is the single most influential factor in explaining genetic structure of S. scrofa. Note that the international breeds, Duroc and Large White, are shifted towards Asia: a result of the well-known admixing process with Chinese pigs.…”

“…More recently, Frantz et al (2015) reported an analysis of 100 Asian and European complete pig genomes. They looked for potential selective signals that were shared between Asian and European populations.…”

“…The most significant one was on SSC4, 82.37-82.39 Mb. This region does not contain any known gene but is close to gene PLAG1 (SSC4: 82, 606, 862-82, 608, 850 bp), which is under strong selection in European domestics (Rubin et al, 2012;Frantz et al, 2015). To contrast these results, we carried a 100 kb genomewide analysis with our approach and we found that the window containing PLAG1, made up of 891 SNPs, has a h 2 G = 0.69; this is the 493 largest heritability out of the 23 395 windows analyzed (2% upper distribution of h 2 G ).…”

Maintaining genetic integrity of coexisting wild and domestic populations: Genetic differentiation between wild and domestic Rangifer with long traditions of intentional interbreeding

“…This behavioral factor in selection addresses the recent hypothesis of the existence of “islands of domestication” within the genome wherein selection for desirable behavioral traits allows breeders to maintain domestic behavior within an interbred population (Frantz, 2015). Our results suggest that behavioral selection may indeed be important at the level of individual selection, but there is no evidence in this study suggesting that it can lead to hybridizing an entire population.…”

“…However, new models of domestication suggest that while spatial separation of wild and domestic types is often sought, various domestic species ranging from pigs to horses have also been cross‐bred for specific characteristics by allowing controlled introgression from wild herds. (Ottoni, 2013; Jónsson, 2014; Frantz, 2015). For most domestic breeds, this idea remains a hypothesis as the original free‐ranging wild forms have become largely extinct or restricted to a few isolated areas (Clutton‐Brock, 1987).…”