Studying Phenotypic Evolution in Domestic Animals: A Walk in the Footsteps of Charles Darwin

Abstract

Charles Darwin used domesticated plants and animals as proof of principle for his theory on phenotypic evolution by means of natural selection. Inspired by Darwin's work, we developed an intercross between the wild boar and domestic pigs to study the genetic basis for phenotypic changes during domestication. The difference in coat color is controlled by two major loci. Dominant white color is due to two consecutive mutations in the KIT gene: a 450-kb duplication and a splice mutation. Black spotting is caused by the combined effect of two mutations in MC1R: a missense mutation for dominant black color and a 2-bp insertion leading to a frameshift. A major discovery made using this pedigree is the identification of a single-nucleotide substitution in intron 3 of the gene for insulin-like growth factor 2 (IGF2) that is underlying a quantitative trait locus affecting muscle growth, size of the heart, and fat deposition. The mutation disrupts the interaction with a repressor and leads to threefold increased IGF2 expression in postnatal muscle. In a recent study, we have identified the IGF2 repressor, and this previously unknown protein, named ZBED6, is specific for placental mammals and derived from a domesticated DNA transposon.

Mining the pig genome to investigate the domestication process

“…Indeed, the extraordinary phenotypic diversity of livestock combined with the availability of resource populations and high-throughput molecular tools offers a unique opportunity to understand domestication from a molecular perspective (Andersson, 2009). Although behavioural traits were the most important component of the adaptation of pigs to a human-controlled environment (MignonGrasteau et al, 2005) and some of these traits exhibit moderate heritabilities (Johnson and McGlone, 2011), no genetic variant influencing swine temperament or docility has been found to date (Table 1, but see other associated domestication traits on Figure 2 in Trut, 1999).…”

“…Another pigmentation gene targeted by artificial selection is KIT. Variation in the number of KIT copies and one polymorphism associated with the skipping of exon 17 are the major determinants of the white coat that has been fixed in several cosmopolitan breeds, such as Large White and Landrace (Giuffra et al, 2002, Andersson, 2009. It is not known why certain pigmentation patterns were selected by ancient farmers, but it is possible that coat colours were used as markers to identify improved variants (Andersson, 2003).…”

Pigeonetics takes flight: Evolution, development, and genetics of intraspecific variation

“…Domesticated species are important models for rapid evolutionary change over short time scales (Akey et al, 2010; Andersson, 2009; Boyko et al, 2010; Driscoll et al, 2009; Gaut, 2015; Price, 2002; Ross-Ibarra et al, 2007). Some of the same evolutionary processes that operate during selective sweeps and sexual selection in natural populations also shape domestic populations (Andersson, 2009; Careau et al, 2010; Gregory, 2009; Price, 2008; Price, 2002).…”

“…Some of the same evolutionary processes that operate during selective sweeps and sexual selection in natural populations also shape domestic populations (Andersson, 2009; Careau et al, 2010; Gregory, 2009; Price, 2008; Price, 2002). Like their wild ancestors, domesticated species have undergone genetic adaptation to various climates and living conditions, including human preferences, making them excellent models for variation under natural selection and divergence by prezygotic isolation (Andersson, 2009; Driscoll et al, 2009; Hartl and Clark, 2007). …”

“…One of the most-intensively studied pigmentation genes in vertebrates is melanocortin-1-receptor ( Mc1r) , which has been implicated in color variation in many organisms, including humans (Andersson, 2009; Gross et al, 2009; Hoekstra, 2006; Manceau et al, 2010; Mundy, 2005; Rosenblum et al, 2014; Sulem et al, 2007). Analysis of Mc1r sequences in feral pigeons with different color phenotypes did not identify an association between Mc1r genotype and pigment variation (Derelle et al, 2013).…”