Genomic analysis of the domestication and post-Spanish conquest evolution of the llama and alpaca

Background Despite their regional economic importance and being increasingly reared globally, the origins and evolution of the llama and alpaca remain poorly understood. Here we report reference genomes for the llama, and for the guanaco and vicuna (their putative wild progenitors), compare these with the published alpaca genome, and resequence seven individuals of all four species to better understand domestication and introgression between the llama and alpaca. Results Phylogenomic analysis confirms that the llama was domesticated from the guanaco and the alpaca from the vicuna. Introgression was much higher in the alpaca genome (36%) than the llama (5%) and could be dated close to the time of the Spanish conquest, approximately 500 years ago. Introgression patterns are at their most variable on the X-chromosome of the alpaca, featuring 53 genes known to have deleterious X-linked phenotypes in humans. Strong genome-wide introgression signatures include olfactory receptor complexes into both species, hypertension resistance into alpaca, and fleece/fiber traits into llama. Genomic signatures of domestication in the llama include male reproductive traits, while in alpaca feature fleece characteristics, olfaction-related and hypoxia adaptation traits. Expression analysis of the introgressed region that is syntenic to human HSA4q21, a gene cluster previously associated with hypertension in humans under hypoxic conditions, shows a previously undocumented role for PRDM8 downregulation as a potential transcriptional regulation mechanism, analogous to that previously reported at high altitude for hypoxia-inducible factor 1 alpha. Conclusions The unprecedented introgression signatures within both domestic camelid genomes may reflect post-conquest changes in agriculture and the breakdown of traditional management practices.

Agro-Scientific Research in the Public Interest of China 201303119 Strategic Priority Program of the Chinese Academy of Sciences XDB31000000 National Natural Science Foundation of China (NSFC) 31821001 Cardiff University Chinese Academy of Sciences President's International Fellowship Initiative Young Sanjin Scholars Distinguished Professor program in Shanxi Agricultural University CXTD201201 Aid Program for Innovation Research Team in Shanxi Agricultural University CXTD201201 FONDECYT grant CONICYT of Chile 1140785 Science and Technology Department of Qinghai Province Major Project "Sanjiangyaun National Park Animal Genome Program" Second Tibetan Plateau Scientific Expedition and Research Program (STEP) 2019QZKK0501