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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 vicuña (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 vicuña. 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 1α. Conclusions The unprecedented introgression signatures within both domestic camelid genomes may reflect post-conquest changes in agriculture and the breakdown of traditional management practices.

Additional file 1: Figure S1. K-mer distribution. Figure S2. Detailed sampling map of all sequenced individual. Figure S3. Treemix phylogeny and variance plot. Figure S4. Introgression segments into llama (fd). Figure S5. PSMC plot for all four SAC species. Figure S6. MSMC plots for (a) guanaco; (b) llama; (c) vicuña; (d) alpaca. Figure S7. Manhattan plot of selection signatures detected in the comparison between vicuña and alpaca (XP-EHH upper, FST bottom). Figure S8. Manhattan plot of selection signatures detected in the comparison between guanaco and llama (XP-EHH upper, FST bottom). Figure S9. Comparison between region-wide FST and SNP distribution among wild ancestors and domestic relatives for the OR5 and OR2 olfactory receptor family. Figure S10. Comparison between region-wide FST and SNP distribution among wild ancestors and domestic relatives for the HoxD gene clusters and OLA1 gene related to morphology development. Figure S11. SNP distribution among wild ancestors and domestic relatives with evidence of introgression from llama to alpaca on Chr10. Figure S12. SNP distribution among wild ancestors and domestic relatives with evidence of introgression from alpaca to llama: CORIN, FGF21, GNAS, TAGLN. Figure S13. cDNA sequence, expression histogram, Western Blot and protein expression histogram for the alpaca skin FGF5 expression analysis. Figure S14. The phylogeny of South American camelids with segments of high guanaco ancestry removed from alpaca genomes. Table S1. Statistics of the clean data for the de novo genomes. Table S2a-c. Assembly statistics for each species. Table S3. Genome coverage assessed by transcriptome unigenes. Table S4. The BUSCO results of the three new assembled SAC genomes. Table S5. K-mer analysis. Table S6. Aligned sequence data for de novo genomes. Table S6a. Aligned sequence between the de novo genomes and related species: pairwise whole-genome alignment was performed using LASTZ. Table S6b. Synteny analysis for aligned de novo genomes. Table S7a-c. the number of predicted genes for each species. Table S8. Sampling details. Table S9. Resequencing data summary. Table S10. ABBA-BABA statistics. Table S11. Introgressed segments from llama into alpaca using fd and LAI. Table S12. Introgressed segments from alpaca into llama using fd and LAI. Table S13. Introgressed segment and genes showing low and high LAI introgression on the inferred X-chromosome of alpaca. Table S14. Selection signatures detected in comparisons between vicuña and alpaca (XP-EHH). Table S15. Selection signatures detected in comparisons between vicuña and alpaca (FST). Table S16. Selection signatures detected in comparisons between vicuña and alpaca (overlap between methods). Table S17. Selection signatures detected in comparisons between guanaco and llama (XP-EHH). Table S18. Selection signatures detected in comparisons between guanaco and llama (FST). Table S19. Selection signatures detected in comparisons between guanaco and llama (overlap between methods). Table S20. Olfactory receptor gene numbers in South American camelids, compared to the cow. Table S21. PCR and qPCR primers. Table S22. Blood and skin tissue expression counts for de novo sequenced SACs and Chinese alpaca, respectively. Supplementary Note S1 - De novo Genome Sequencing a. Genome size estimation. b. De novo sequencing, assembly and annotation. Supplementary Note S2 - Introgression analysis. Supplementary Note S3- Sample collection, DNA extraction and permits.

Additional file 2. Review history.

Nature Communications 5:5188; doi: 10.1038/ncomms6188 (2014); Published 21 Oct 2014; Updated 28 Jan 2015 In this Article Junyi Wang is incorrectly listed as one of several equally contributing authors. The correct list of equally contributing authors is: Huiguang Wu, Xuanmin Guang, Mohamed B. Al-Fageeh, Junwei Cao, Shengkai Pan and Huanmin Zhou.

Bactrian camel (Camelus bactrianus), dromedary (Camelus dromedarius) and alpaca (Vicugna pacos) are economically important livestock. Although the Bactrian camel and dromedary are large, typically arid-desert-adapted mammals, alpacas are adapted to plateaus. Here we present high-quality genome sequences of these three species. Our analysis reveals the demographic history of these species since the Tortonian Stage of the Miocene and uncovers a striking correlation between large fluctuations in population size and geological time boundaries. Comparative genomic analysis reveals complex features related to desert adaptations, including fat and water metabolism, stress responses to heat, aridity, intense ultraviolet radiation and choking dust. Transcriptomic analysis of Bactrian camels further reveals unique osmoregulation, osmoprotection and compensatory mechanisms for water reservation underpinned by high blood glucose levels. We hypothesize that these physiological mechanisms represent kidney evolutionary adaptations to the desert environment. This study advances our understanding of camelid evolution and the adaptation of camels to arid-desert environments.