Genetic Variation in Coat Colour Genes MC1R and ASIP Provides Insights Into Domestication and Management of South American Camelids

Abstract

The domestication of wild vicuña and guanaco by early pre-Inca cultures is an iconic example of wildlife management and domestication in the Americas. Although domestic llamas and alpacas were clearly selected for key, yet distinct, phenotypic traits, the relative patterns and direction of selection and domestication have not been confirmed using genetic approaches. However, the detailed archaeological records from the region suggest that domestication was a process carried out under significant control and planning, which would have facilitated coordinated and thus extremely effective selective pressure to achieve and maintain desired phenotypic traits. Here we link patterns of sequence variation in two well-characterised genes coding for colour variation in vertebrates and interpret the results in the context of domestication in guanacos and vicuñas. We hypothesise that colour variation in wild populations of guanacos and vicunas were strongly selected against. In contrast, variation in coat colour variation in alpaca was strongly selected for and became rapidly fixed in alpacas. In contrast, coat colour variants in llamas were of less economic value, and thus were under less selective pressure. We report for the first time the full sequence of MC1R and 3 exons of ASIP in 171 wild specimens from throughout their distribution and which represented a range of commonly observed colour patterns. We found a significant difference in the number of non-synonymous substitutions, but not synonymous substitutions among wild and domestics species. The genetic variation in MC1R and ASIP did not differentiate alpaca from llama due to the high degree of reciprocal introgression, but the combination of 11 substitutions are sufficient to distinguish domestic from wild animals. Although there is gene flow among domestic and wild species, most of the non-synonymous variation in MC1R and ASIP was not observed in wild species, presumably because these substitutions and the associated colour phenotypes are not effectively transmitted back into wild populations. Therefore, this set of substitutions unequivocally differentiates wild from domestic animals, which will have important practical application in forensic cases involving the poaching of wild vicuñas and guanacos. These markers will also assist in identifying and studying archaeological remains pre- and post-domestication.

Comparative FISH-Mapping of MC1R, ASIP, and TYRP1 in New and Old World Camelids and Association Analysis With Coat Color Phenotypes in the Dromedary (Camelus dromedarius)

“…Another observation about dromedary MC1R , as also noted by Almathen et al (2018), is the low level of sequence variation (just c901C > T) in the coding region, contrasting the 21 sequence variants found in the alpaca MC1R (Feeley and Munyard, 2009). However, a recent study of MC1R sequence variants across all four South American camelids (vicugna, guanaco, llama, and alpaca) suggests that variation in alpacas is the result of human selection for a variety of fiber colors, whereas in wild South American camelids (guanacos and free living vicugnas), there is a selection against non-synonymous substitutions in MC1R (Marin et al, 2018). Likewise, there is low sequence variation of MC1R in wild pigs, but many more variants in domestic pig breeds as a result of human selection (Andersson, 2003).…”

Chromosomal Localization of Candidate Genes for Fiber Growth and Color in Alpaca (Vicugna pacos)

“…Finally, ALX3 is involved in color differentiation in striped rodents (Cuthill et al, 2017), and proposed as a target melanoma gene fusion in humans (Berger et al, 2010). Also, Marín et al (2018) used the genetic variation of MC1R and ASIP genes, that control coat color, to differentiate between wild and domestic South American camelids.…”

Polimorfismos de nucleótido simple (PNSs) del gen MC1R en alpacas negras y marrones

“…Después de la domesticación, la variación fenotípica del color fue una de las primeras características consideradas en la selección artificial (Cieslak et al 2011, Linderholm y Larson 2013, Librado et al 2017. Los genes MC1R (receptor 1 de melanocortina) y ASIP (proteína de señalización agouti) son los principales genes que intervienen en la síntesis y distribución de eumelanina y feomelanina en el vellón de alpacas (Feeley & Munyard 2009, Cieslak et al 2011, Marín et al 2018, pero en otros animales se han descrito más de 150 genes asociados a la expresión del color (Montoliu et al 2011). Estudios moleculares sugieren que la domesticación de la vicuña se inició hace 6000 -7000 años en los andes centrales del Perú, siendo la alpaca descendiente de la vicuña (Kadwell et al 2001, Gentry et al 2004, Fan et al 2020.…”