Nucleotide diversity of functionally different groups of immune response genes in Old World camels based on newly annotated and reference-guided assemblies.

BACKGROUND: Immune-response (IR) genes have an important role in the defense against highly variable pathogens, and therefore, diversity in these genomic regions is essential for species' survival and adaptation. Although current genome assemblies from Old World camelids are very useful for investigating genome-wide diversity, demography and population structure, they have inconsistencies and gaps that limit analyses at local genomic scales. Improved and more accurate genome assemblies and annotations are needed to study complex genomic regions like adaptive and innate IR genes. RESULTS: In this work, we improved the genome assemblies of the three Old World camel species - domestic dromedary and Bactrian camel, and the two-humped wild camel - via different computational methods. The newly annotated dromedary genome assembly CamDro3 served as reference to scaffold the NCBI RefSeq genomes of domestic Bactrian and wild camels. These upgraded assemblies were then used to assess nucleotide diversity of IR genes within and between species, and to compare the diversity found in immune genes and the rest of the genes in the genome. We detected differences in the nucleotide diversity among the three Old World camelid species and between IR gene groups, i.e., innate versus adaptive. Among the three species, domestic Bactrian camels showed the highest mean nucleotide diversity. Among the functionally different IR gene groups, the highest mean nucleotide diversity was observed in the major histocompatibility complex. CONCLUSIONS: The new camel genome assemblies were greatly improved in terms of contiguity and increased size with fewer scaffolds, which is of general value for the scientific community. This allowed us to perform in-depth studies on genetic diversity in immunity-related regions of the genome. Our results suggest that differences of diversity across classes of genes appear compatible with a combined role of population history and differential exposures to pathogens, and consequent different selective pressures.

Genomic signatures of domestication in Old World camels.

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.

Author Correction: Longest terrestrial migrations and movements around the world.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A First Y-Chromosomal Haplotype Network to Investigate Male-Driven Population Dynamics in Domestic and Wild Bactrian Camels.

Polymorphic markers on the male-specific part of the Y chromosome (MSY) provide useful information for tracking male genealogies. While maternal lineages are well studied in Old World camelids using mitochondrial DNA, the lack of a Y-chromosomal reference sequence hampers the analysis of male-driven demographics. Recently, a shotgun assembly of the horse MSY was generated based on short read next generation sequencing data. The haplotype network resulting from single copy MSY variants using the assembly as a reference revealed sufficient resolution to trace individual male lines in this species. In a similar approach we generated a 3.8 Mbp sized assembly of the MSY of Camelus bactrianus. The camel MSY assembly was used as a reference for variant calling using short read data from eight Old World camelid individuals. Based on 596 single nucleotide variants we revealed a Y-phylogenetic network with seven haplotypes. Wild and domestic Bactrian camels were clearly separated into two different haplogroups with an estimated divergence time of 26,999 ± 2,268 years. Unexpectedly, one wild camel clustered into the domestic Bactrian camels' haplogroup. The observation of a domestic paternal lineage within the wild camel population is concerning in view of the importance to conserve the genetic integrity of these highly endangered species in their natural habitat.

Longest terrestrial migrations and movements around the world.

Long-distance terrestrial migrations are imperiled globally. We determined both round-trip migration distances (straight-line measurements between migratory end points) and total annual movement (sum of the distances between successive relocations over a year) for a suite of large mammals that had potential for long-distance movements to test which species displayed the longest of both. We found that caribou likely do exhibit the longest terrestrial migrations on the planet, but, over the course of a year, gray wolves move the most. Our results were consistent with the trophic-level based hypothesis that predators would move more than their prey. Herbivores in low productivity environments moved more than herbivores in more productive habitats. We also found that larger members of the same guild moved less than smaller members, supporting the 'gastro-centric' hypothesis. A better understanding of migration and movements of large mammals should aid in their conservation by helping delineate conservation area boundaries and determine priority corridors for protection to preserve connectivity. The magnitude of the migrations and movements we documented should also provide guidance on the scale of conservation efforts required and assist conservation planning across agency and even national boundaries.

Mitogenome Sequencing in the Genus Camelus Reveals Evidence for Purifying Selection and Long-term Divergence between Wild and Domestic Bactrian Camels.

The genus Camelus is an interesting model to study adaptive evolution in the mitochondrial genome, as the three extant Old World camel species inhabit hot and low-altitude as well as cold and high-altitude deserts. We sequenced 24 camel mitogenomes and combined them with three previously published sequences to study the role of natural selection under different environmental pressure, and to advance our understanding of the evolutionary history of the genus Camelus. We confirmed the heterogeneity of divergence across different components of the electron transport system. Lineage-specific analysis of mitochondrial protein evolution revealed a significant effect of purifying selection in the concatenated protein-coding genes in domestic Bactrian camels. The estimated dN/dS < 1 in the concatenated protein-coding genes suggested purifying selection as driving force for shaping mitogenome diversity in camels. Additional analyses of the functional divergence in amino acid changes between species-specific lineages indicated fixed substitutions in various genes, with radical effects on the physicochemical properties of the protein products. The evolutionary time estimates revealed a divergence between domestic and wild Bactrian camels around 1.1 [0.58-1.8] million years ago (mya). This has major implications for the conservation and management of the critically endangered wild species, Camelus ferus.