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, 11 (1), 671

Genomic Regions Under Selection in the Feralization of the Dingoes

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Genomic Regions Under Selection in the Feralization of the Dingoes

Shao-Jie Zhang et al. Nat Commun.

Abstract

Dingoes are wild canids living in Australia, originating from domestic dogs. They have lived isolated from both the wild and the domestic ancestor, making them a unique model for studying feralization. Here, we sequence the genomes of 10 dingoes and 2 New Guinea Singing Dogs. Phylogenetic and demographic analyses show that dingoes originate from dogs in southern East Asia, which migrated via Island Southeast Asia to reach Australia around 8300 years ago, and subsequently diverged into a genetically distinct population. Selection analysis identifies 50 positively selected genes enriched in digestion and metabolism, indicating a diet change during feralization of dingoes. Thirteen of these genes have shifted allele frequencies compared to dogs but not compared to wolves. Functional assays show that an A-to-G mutation in ARHGEF7 decreases the endogenous expression, suggesting behavioral adaptations related to the transitions in environment. Our results indicate that the feralization of the dingo induced positive selection on genomic regions correlated to neurodevelopment, metabolism and reproduction, in adaptation to a wild environment.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Population structure and genetic diversity of 109 canids.
a Geographic locations of the 109 canids analyzed in this study. The map was drawn by the R Packages (maps: https://CRAN.R-project.org/package = maps). b Principle component analysis of the 109 canids. c Principle component analysis of only the dingo and NGSD, red = dingo from Southeast Australia; blue = dingo from West/central Australia; brown = dingo from Northeast Australia; green = NGSD. d Structure analysis of all the 109 individuals. e A phylogenetic tree for all the 109 individuals. W, wolves (orange in tree); BV, breeds and village dogs outside China/SE Asia (sky blue in tree); NI, indigenous dogs from north China (green brown in tree); TW, Taiwan indigenous dog (gray in tree); SI, indigenous dogs from southern China (purple in tree); D, dingoes (red in tree); NGSD, New Guinea Singing Dogs (green in tree); IN, Indonesian village dogs (deep blue in tree);B, breeds; IB, intermediate breeds; EB, European breeds; PG, Papua New Guinea village dogs; ID, Indian village dogs; AI, African village dogs.
Fig. 2
Fig. 2. Demographic history of dingoes and dogs from southern East Asia.
a Demographic history inferred for indigenous dogs from southern China (SV), Indonesian village dog (IN) and dingo using G-phocs. b Inferred effective population sizes over time for indigenous dogs from southern China (SV), Indonesian village dog (IN), dingo and NGSD using SMC++.
Fig. 3
Fig. 3. Phylogenetic and demographic history analysis of mtDNA.
a Neighbor-joining tree based on mitochondrial genomes from 35 dingoes and 3 NGSDs, and from 169 domestic dogs and 8 wolves from across the Old World, with 4 coyotes as outgroup. The yellow box and inset figure indicate the branch in which all dingoes and NGSDs cluster together with a single domestic dog from South China, and the 3 most closely related dogs outside this branch. b Map depicting geographic sampling of dingoes across Australia. Circles represent the 10 individuals sequenced in this study and triangles 25 additional samples from Cairns et al. The red line indicates the genetic subdivision between the southeastern/eastern part (S/E) and the rest of the continent. c Bayesian analysis of mitochondrial genomes for the sub-dataset identified in Fig. 3. The dingo/NGSD branch including all dingoes and NGSDs and a single South Chinese domestic dog and, as outgroup, the three most closely related dogs outside that branch. The scale axis indicates time estimates using the mutation rate of 7.7 × 10−8 per site per year with SD 5.48 × 10−9 from Thalmann et al.. The colored branches indicate geographical origin of dingo samples, see Fig. 2. The star highlights the single dingo sample from southeast Australia that does not cluster in the S/E-related branch.
Fig. 4
Fig. 4. The result of iHS and PBS2 for three candidate regions.
Blue curves indicate PBS2 value, blue dots indicate iHS value. Thick red horizontal line indicates range of gene, and thin black horizontal line gives the threshold.
Fig. 5
Fig. 5. Functional assay of ARHGEF7.
Dual-luciferase reporter experiments (enhancer assay using pGL3-promoter vectors) using two different human cell lines (HEK293, human embryonic kidney and Daoy, human medullablastoma) and one canine cell line (MDCK, Madin-Darby Canine kidney). All experiments were replicated at least three times. Data are expressed by mean ± SEM with the corresponding data points. Graphpad software was used for statistical analysis. Comparisons were performed using two-tails Student’s t test. **represents p < 0.01.

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