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Between Dog and Wolf 3, 2004

IMDb Everywhere. Follow IMDb on. Following induction, NCCs migrate along defined pathways to various sites in the developing embryo. Assignment of identity and the determination of migration routes rely on positional information provided by external signaling cues [ 86 , 87 ]. Together, our results suggest that early selection may have acted on genes essential to the initiation of the neural crest and the definition of migration routes for NCCs. Once in their final destinations, NCC further differentiates as the precursors to many tissues in the developing embryo.

Most of the head, for example, arises from NCCs including craniofacial bones, cartilage, and teeth [ 93 , 94 ]. Ancient dog remains indicate that body size, snout lengths, and cranial proportions of dogs considerably decreased compared to the wolf ancestral state following early domestication [ 95 ].

Further, these remains indicate jaw size reduction also occurred, as evidenced by tooth crowding [ 95 ]. Such alterations are consistent with the domestication syndrome and implicate aberrant NCC migration since decreases in the number of NCCs in facial primordia are directly correlated with reductions in mid-face and jaw sizes [ 18 , 96 ].

Genes associated with both craniofacial and tooth development in vertebrates are found in our candidate loci including SCUBE1 XP , which is essential in craniofacial development of mice, and SATB2 XP , which has roles in patterning of the developing branchial arches, palate fusion, and regulation of HOXa2 in the developing neural crest [ 97 , 98 , 99 ].


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Lastly, when knocked out in mice, Bicoid -related homeodomain factor PITX1 XP not only affected hindlimb growth, but also displayed craniofacial abnormalities such as cleft palate and branchial arch defects [ ], and influences vertebrate tooth development [ ]. Insufficient cartilage, a NCC-derived tissue [ 94 ] that consists of chondrocytes and collagen, in the outer ear of humans results in a drooping ear phenotype linked to numerous NC-associated neurocristopathies e.

Tameness or reduced fear toward humans was likely the earliest trait selected for by humans during domestication [ 3 , , ]. Recapitulating such selection, numerous physiological and morphological characteristics, including domestication syndrome phenotypes i. Genes contributing to neurological function and behavioral responses were observed in our XP-CLR candidate loci, suggesting these genes may influence chemical and morphological differences associated with tameness.

Numerous candidate loci contain genes influencing neurological function and behavioral responses including genes in the dopamine, serotonin, glutamate, and GABA neurotransmission pathways, as well as genes contributing to the connectivity and development of synapses and dendrites.

Between Dog and Wolf

In addition to changes in behavior, alterations in sleep patterns would also likely have occurred early in the domestication process due to the shift from the ancestral nocturnal state of wolves, to that of the diurnal lifestyle also exhibited by humans. Evidenced by this, levels of circadian rhythm determinants e.

We hypothesize that early selection on genes influencing behavior have additional functions in the establishment of circadian rhythms, and that both can be explained by impaired NC function. Humans with Smith-Magenis syndrome display increased aggression and altered circadian rhythms, as well as craniofacial and skeletal deformations, developmental delays, and intellectual disabilities [ ]. Similarly, Williams-Beuren syndrome, another neurodevelopmental disorder, affects sleep patterns as well as contributes to hypersociability in humans [ ]. A recent study in canines linked behavioral changes in breed dogs to structural variants near WBSCR17 , a Williams-Beuren syndrome gene [ ].

Both syndromes display multiple features associated with improper NCC development, resembling phenotypes of neurocristopathies [ , ]. For example, disruption of the transcription factors RAI1 and WSTF in xenopus also disrupted in Williams-Beuren syndrome negatively impacts proper NCC migration, recapitulating the human craniofacial defects associated with the syndromes [ , ].


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Altogether, the top scoring locus, as well as others, indicate overlap of gene functions in influencing behavior and circadian rhythms, and were likely early genetic components of the domestication syndrome. Similar to other domestication scans [ 6 , 9 , 19 ], we did not find SNPs deleteriously altering protein sequence in our predicted sweeps, indicating that gene loss did not have a significant role in dog domestication. Instead, we hypothesize that alterations in gene regulatory pathways or the regulation of transcriptional activity could contribute to broad domestication syndrome phenotypes.

RNPC3 , which affects early development and is linked to dwarfism isolated growth hormone deficiency; [ ] , is also under selection in cats and humans [ 17 , 77 ]. Absence of Sf3b1 disrupts proper NCC specification, survival, and migration [ ]. Phenotypes of this syndrome resemble those of the domestication syndrome including craniofacial, brain, and skeletal abnormalities [ ]. Thus, proper splicing, particularly for transcripts processed by the minor spliceosome, is required for proper NC function and development. Our scan for differentiated copy number states identified few regions that differentiate village dogs and wolves.

A previous study found that dogs and wolves have a similar proportion of CNV loci [ ]. This suggests that copy number expansion or contraction may not have made as significant contributions to the phenotypic changes associated with domestication. The quantification of wolf copy number using a dog genome reference limits the accuracy of the estimates and prevents detection of wolf-specific insertions. Therefore, reassessment of population-specific copy number changes would be improved by the use of a wolf genome reference [ ].

Of note, the top hit from the copy number selection scan corresponded to the AMY2B , a gene linked to increased efficiency of starch digestion in dogs [ 5 , 36 , 37 ]. However, this study utilizes previously implemented copy number estimation techniques [ 34 , 36 ] to identify two independent large-scale duplications 1. Since these large duplications are not fixed in dogs, yet the RNPC3 selected haplotypes are, we speculate that the initial target of selection may have been on RNPC3 which could have global effects on expression and phenotype body size. By comparing village dogs and wolves, we identified candidate domestication regions in the dog genome.

Analysis of gene function in these regions suggests that perturbation of crucial neural crest signaling pathways could result in the broad phenotypes associated with the domestication syndrome. Additionally, these findings suggest links between transcriptional regulation and splicing to alterations in cell differentiation, migration, and neural crest development. Altogether, we conclude that while primary selection during domestication likely targeted tameness, genes that contribute to determination of this behavioral change are also involved in critical, far-reaching pathways that conferred drastic phenotypic changes in dogs relative to their wild counterparts.

The primary selection scans in this paper are based on 43 village dog and 10 gray wolf samples selected from a larger sample set as described below. Additional analysis of candidate genomic regions is based on genotype data from two ancient European samples. For visualization purposes, Fig. From this larger sample set, 37 breed dogs, 45 village dogs, and 12 wolves were selected from the samples described in [ 34 ], and ADMIXTURE [ 39 ] was utilized to estimate the levels of wolf-dog admixture within this subset.

This sample set includes three New Guinea Singing Dogs sequenced as described in [ ]. Fifty-four samples remained following this filtration. We further excluded sites with missing genotype calls in any sample, triallelic sites, and X-nonPAR positions where any male sample was called as heterozygous. The final SNP set contained 7,, sites. Only one sample mxb was removed from the sample set, a sample known to be related to another Mexican wolf in the dataset. Principal component analyses were completed on the remaining 53 samples 43 dogs and 10 wolves using smartpca, a component of Eigensoft package version 3.

Once PCA confirmed clear genetic distinctions between these dogs and wolves, this final sample set was used for subsequent analyses. Finally, village dog and wolf allele frequencies were calculated separately using VCFtools [ ].

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Simulations of dog and wolf demographic history were performed using msprime v. For each autosome, 75 independent simulations were performed using independent random seeds and a pedigree-based genetic map [ ]. The simulation is designed to capture key aspects impacting dog and wolf diversity, rather than a definitive depiction of their demography. With this equation, the X chromosome could be included in F ST calculations.


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  4. Due to differences in effective population size and corresponding expected levels of genetic drift, analyses were performed separately for the chromosome X non-pseudoautosomal region PAR. F ST loci filtration was completed differently for the outlier and non-outlier approach. Significance thresholds for the non-outlier approach were determined as the 99th percentile from F ST score distributions from the simulated genomes.

    Overlapping windows passing these thresholds were merged. Significance threshold for window filtration was set as the 0. Importantly, genotypes in the ancient samples were determined for the sites variable among the modern samples using an approach that accounts for post-mortem ancient DNA damage [ 34 ]. The 5-ky-old German dog CTC was not included in this analysis due to known wolf admixture [ 34 ].