Genomic signatures of domestication in Old World camels

Abstract

Domestication begins with the selection of animals showing less fear of humans. In most domesticates, selection signals for tameness have been superimposed by intensive breeding for economical or other desirable traits. Old World camels, conversely, have maintained high genetic variation and lack secondary bottlenecks associated with breed development. By re-sequencing multiple genomes from dromedaries, Bactrian camels, and their endangered wild relatives, here we show that positive selection for candidate genes underlying traits collectively referred to as 'domestication syndrome' is consistent with neural crest deficiencies and altered thyroid hormone-based signaling. Comparing our results with other domestic species, we postulate that the core set of domestication genes is considerably smaller than the pan-domestication set - and overlapping genes are likely a result of chance and redundancy. These results, along with the extensive genomic resources provided, are an important contribution to understanding the evolutionary history of camels and the genomic features of their domestication.

Fig. 1. Distribution of genetic variation among Old World camels.

a Summary of the phylogenetic relationships among Old World camels using the alpaca (Vicugna pacos) as an outgroup. b Results from the population clustering analysis. Each horizontal bar corresponds with the proportion of ancestry in either two or three population clusters. c The first two principal components explain 23.3% and 10.1% of the SNP variation, respectively, and easily differentiate the three camel species. d Euler diagram showing the number of segregating SNPs unique to each species and shared between them. Note that the number of C. bactrianus individuals (n = 7) was less than the number of C. ferus and C. dromedarius individuals (n = 9). Approximately 2.1 million SNPs fixed between species are not included.

Fig. 2. Heterozygosity and historical effective population sizes of the three extant camelid species.

a Boxplots of individual heterozygosity inferred from approximately 190,000 nonoverlapping 10-kb windows across the genome and colored by species. The boxplots’ elements include the median (center line), first through third quartiles (colored box), and 1.5× interquartile range (whiskers). b The demographic history of each individual camel colored by species (see legend). All results were scaled using a generation time of five years and a mutation rate of 1.1 × 10⁻⁸ (changes · site⁻¹ · generation⁻¹). The asterisk indicates that C. dromedarius analyses were repeated with mapping to the C. dromedarius reference.

Fig. 3. Genes under selection in Old World camels that overlap candidate domestication genes in other domestic species.

The genes under positive selection in a Camelus dromedarius, b C. bactrianus, and c C. ferus were of functions that could be associated with the neural crest cell (NCC; blue) and thyroid hormone (pink) hypotheses of domestication syndrome, or of other, unknown relationship (green). Genes are shown with an icon of the corresponding domestic species where positive selection has also been reported. Arrows are directed toward a summary icon of known functions for that gene.

Fig. 4. Positive selection in wild camels.

The three 100-kb windows in Camelus ferus (a–c) found to contain evidence of positive selection. The location of variants within each species are shown as vertical lines, and overlapping genes as black bars.