Pervasive selection pressure in wild and domestic pigs

Abstract

Animal domestication typically affected numerous polygenic quantitative traits, such as behavior, development and reproduction. However, uncovering the genetic basis of quantitative trait variation is challenging, since they are caused by small allele-frequency changes. To date, only a few causative mutations related to domestication processes have been reported, strengthening the hypothesis that small effect variants have a prominent role. So far, approaches on domestication have been limited to the detection of the global effect of domestication on deleterious mutations and on strong beneficial variants, ignoring the importance of variants with small selective effects. To overcome these difficulties, here we propose to estimate the proportion of beneficial variants based on the asymptotic MacDonald Kreitman (MK) method, according to estimates of variability based on frequency spectrum. We applied this approach to the pig species, analyzing 46 complete genome sequences from 20 European wild boars, 6 Iberian and 20 Large White pigs at different molecular scales: gene, metabolic pathway and whole-genome. Descriptive variability analyses on pig populations indicate that domestic and wild pig populations do not differ in nonsynonymous fixed mutations. Instead, most variants are shared among them, despite that the phenotypes of wild and domestic individuals are clearly divergent. Additionally, asymptotic MK plots based on summary statistics show that small effects variants may affect the final calculation of α, the proportion of beneficial mutations. The distribution of fitness effects inferred with Approximate Bayesian Computation analysis indicates that both wild and domestic pigs display an important quantity of deleterious mutations at low frequency (~83% of total mutations) and a high number of nearly-neutral mutations (~17%) that may have a significant effect on the evolution of domestic and wild populations. Exclusive mutations show that recent demographic changes have severely affected the fitness of populations, especially of the local Iberian breed. Finally, the median proportion of the strong favorable mutations are very scarce in all cases (≤ 0.2%). The median estimated alpha values (weak and strong favorable) are 0.9% for wild and domestic pigs.

Detection of Domestication Signals through the Analysis of the Full Distribution of Fitness Effects using Simulations

“…The literature about the genomic basis of domestication (e.g., Ross-Ibarra et al 2007, Flood and Hancock 2017; Moyers et al 2018; Flori et al 2019; Frantz et al 2020; Leno-Colorado et al 2020) revolves around three main questions: (1) Is domestication driven by few loci of large effect or by many loci of weak effect (polygenic adaptation)? (2) Is domestication dominated by standing variation (variation that was present before the start of domestication) or by new exclusive mutations in the domesticated populations?…”

“…This question is motivated by empirical results. For example, a small number of fixed functional variants have been detected in domestic pig populations in relation to wild populations (Leno-Colorado et al 2020, but see Groenen et al 2012; Rubin et al 2010). Although frequent introgression has been described between pig populations (Frantz et al 2015; Ramírez et al 2015), there are clear phenotypic features that distinguish wild from domestic populations.…”

“…Recently, using the 2D-SFS, a new method to jointly estimate the full DFE between two populations that have recently diverged and share many polymorphisms has been proposed (Huang et al 2021). However, there are few studies comparing the DFE between domesticated and wild populations (Leno-Colorado et al 2020). Here, we use forward simulations, considering the domestication process under different demographic and selective models.…”

“…However, few studies have compared the DFE between domesticated and wild populations (Leno-Colorado et al 2022). First, the analysis of differences between wild and domesticated individuals has been focused on finding large effects that determine the phenotypic differences between these two groups.…”

“…However, few studies have compared the DFE between domesticated and wild populations (Leno-Colorado et al . 2022).…”