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, 28 (21), 3441-3449.e5

Interspecific Gene Flow Shaped the Evolution of the Genus Canis

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Interspecific Gene Flow Shaped the Evolution of the Genus Canis

Shyam Gopalakrishnan et al. Curr Biol.

Erratum in

Abstract

The evolutionary history of the wolf-like canids of the genus Canis has been heavily debated, especially regarding the number of distinct species and their relationships at the population and species level [1-6]. We assembled a dataset of 48 resequenced genomes spanning all members of the genus Canis except the black-backed and side-striped jackals, encompassing the global diversity of seven extant canid lineages. This includes eight new genomes, including the first resequenced Ethiopian wolf (Canis simensis), one dhole (Cuon alpinus), two East African hunting dogs (Lycaon pictus), two Eurasian golden jackals (Canis aureus), and two Middle Eastern gray wolves (Canis lupus). The relationships between the Ethiopian wolf, African golden wolf, and golden jackal were resolved. We highlight the role of interspecific hybridization in the evolution of this charismatic group. Specifically, we find gene flow between the ancestors of the dhole and African hunting dog and admixture between the gray wolf, coyote (Canis latrans), golden jackal, and African golden wolf. Additionally, we report gene flow from gray and Ethiopian wolves to the African golden wolf, suggesting that the African golden wolf originated through hybridization between these species. Finally, we hypothesize that coyotes and gray wolves carry genetic material derived from a "ghost" basal canid lineage.

Keywords: African golden wolf; African hunting dog; Ethiopian wolf; canid hybridization; canid phylogeography; gray wolf; phylogenomics.

Figures

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Figure 1
Figure 1
Map Showing the IUCN Ranges, Range Overlaps, and Sampling Locations of the Canids Included in This Study The overlaps in ranges are shown in blended colors (orange, dark purple, dark olive green, light teal, etc.). Since IUCN does not have range information for African golden wolf, the IUCN range of golden jackal has been split in two; the Eurasian part is shown as the range of golden jackal, and the African part is shown as the range of African golden wolf. Further details on the samples, including their sampling location and source, can be found in Data S1, and their estimated heterozygosities—which are inversely proportional to their population sizes—are shown in Figure S1.
Figure 2
Figure 2
Nuclear and Mitochondrial Phylogeny of Basal Canids (A) The maximum-likelihood estimate of the mitochondrial phylogeny for a subset of the samples, using de novo mitochondrial assemblies obtained with MtArchitect. The node labels show the bootstrap support for the node. (B) The phylogeny estimated from nuclear DNA by ASTRAL-II, where monophyletic clusters have been collapsed into a single leaf node. The tip labeled “African golden wolf-hybrid” represents a single known hybrid from the Sinai Peninsula—labeled “African golden wolf Egypt” in the mtDNA phylogeny—as described in the main text. The mean local posterior probabilities are shown for branches where this value is less than 1. The full nuclear phylogeny containing the sample relationships, branch supports, branch lengths proportional to divergence times, and estimated split times can be found in Figures S2A and S2B and Table S2. (C) For a subset of the internal branches in the nuclear phylogeny, the quartet frequencies of the three possible configurations around each branch in the underlying unrooted tree are shown. The red bar represents the configuration shown in the phylogeny, and the two blue bars represent the two alternative configurations. For every quartet, the frequency of the true bipartition has previously been shown to be at least one-third [8], indicated here by a dotted line. Each alternative configuration is labeled by the bipartition it creates, with labels corresponding to those in (A). For example, the second bar of the panel labeled 12 swaps the positions of golden jackal (6) and Ethiopian wolf (5), whereas the third bar puts them as sister to each other. This plot summarizes the gene tree incongruence around examined branches.
Figure 3
Figure 3
Gene Flow among the Crown Canid Species (A) This figure summarizes the relationships among the species (phylogeny) and the various gene flow events inferred from the samples included in this study. Gene flow events are indicated with red arrows, and dotted red arrows show possible gene flow events that have been inferred in this study but have not been previously reported. (B–D) These figures show the gene flow among the different crown canid species using D statistics. These D statistics show significant gene flow between the gray wolf, African golden wolf, golden jackal, and Ethiopian wolf. One principal new finding is structure within the African golden wolves, splitting into Northwestern and Eastern clades, which show genetic affinity to gray wolves and Ethiopian wolves, respectively. A second principal finding is inferred gene flow from an unknown canid lineage, related to the dhole, into the ancestor of the coyote and the gray wolves. We hypothesize this may explain the unexpected basal placement of the coyote in the mitochondrial tree. Further evidence of gene flow in the crown canids is shown in Figure S3.
Figure 4
Figure 4
Modeling the Ancestry of African Golden Wolves (A) TreeMix tree with all samples, estimated using the pairwise correlation of allele frequencies between all groups of samples. This tree is fit with three migration edges. The first three migration edges all indicate extensive gene flow from the gray and Ethiopian wolves into the African golden wolves, suggesting a hybrid origin for this species. (B and C) The QP graph is an admixture graph estimated using all pairwise D statistics between samples. Estimated genetic drift is shown along the solid lines in units of f2 distance (parts per thousand), and estimated mixture proportions are given along the dotted lines. Names of specific modern populations are shown in full, whereas hypothetical ancestral individuals are represented by letters. (B) This tree shows all the possible placements—highlighted in red—for the Northwestern African golden wolf, chosen due to their low levels of gene flow with the Ethiopian wolf. These were modeled as possible internal and external nodes and as an admixed group from all possible node pairs. (C) The best fitting graph with a Z value closest to 0, modeling the Ethiopian wolf-like and gray wolf-like ancestry of Northwestern and Eastern African golden wolves, as well as gene flow into modern Ethiopian wolves from the Eastern African golden wolves. This admixture graph suggests that the African golden wolves are probably a species of hybrid origin, derived from the gray wolf and Ethiopian wolf as the parental species. Further, Figure S4 shows admixture graphs showing potential gene flow from a “ghost” basal canid lineage into the ancestor of wolves and dogs.

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