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. 2018 Nov 5;28(21):3441-3449.e5.
doi: 10.1016/j.cub.2018.08.041. Epub 2018 Oct 18.

Interspecific Gene Flow Shaped the Evolution of the Genus Canis

Shyam Gopalakrishnan  1 , Mikkel-Holger S Sinding  2 , Jazmín Ramos-Madrigal  3 , Jonas Niemann  3 , Jose A Samaniego Castruita  3 , Filipe G Vieira  3 , Christian Carøe  3 , Marc de Manuel Montero  4 , Lukas Kuderna  4 , Aitor Serres  4 , Víctor Manuel González-Basallote  4 , Yan-Hu Liu  5 , Guo-Dong Wang  6 , Tomas Marques-Bonet  7 , Siavash Mirarab  8 , Carlos Fernandes  9 , Philippe Gaubert  10 , Klaus-Peter Koepfli  11 , Jane Budd  12 , Eli Knispel Rueness  13 , Claudio Sillero  14 , Mads Peter Heide-Jørgensen  15 , Bent Petersen  16 , Thomas Sicheritz-Ponten  16 , Lutz Bachmann  17 , Øystein Wiig  17 , Anders J Hansen  18 , M Thomas P Gilbert  19
Affiliations

Affiliations

  • 1 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark. Electronic address: shyam@snm.ku.dk.
  • 2 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; Natural History Museum, University of Oslo, Oslo, Norway; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; University of Greenland, Manuutoq 1, Nuuk, Greenland.
  • 3 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
  • 4 Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain.
  • 5 State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, Yunnan, China.
  • 6 State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  • 7 Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain; Catalan Institution of Research and Advanced Studies (ICREA), Passeig de Lluís Companys, 23, 08010, Barcelona, Spain; CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain; Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, 08193 Cerdanyola del Vallès, Barcelona, Spain.
  • 8 Department of Electrical and Computer Engineering, University of California, San Diego, San Diego, CA, USA.
  • 9 Centre for Ecology, Evolution and Environmental Changes (CE3C), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal.
  • 10 Institut des Sciences de l'Evolution de Montpellier (ISEM), UM-CNRS-IRD-EPHE, Université de Montpellier, Montpellier, France.
  • 11 Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Avenue NW, Washington, DC 20008, USA; Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, 41A Sredniy Prospekt, St. Petersburg 199034, Russia.
  • 12 Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates.
  • 13 Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway.
  • 14 Wildlife Conservation Research Unit, Zoology, University of Oxford, Tubney House, Tubney OX13 5QL, UK; IUCN SSC Canid Specialist Group, Oxford, UK.
  • 15 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland.
  • 16 DTU Bioinformatics, Department of Bio and Health Informatics, Technical University of Denmark, Lyngby, Denmark; Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia.
  • 17 Natural History Museum, University of Oslo, Oslo, Norway.
  • 18 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; University of Greenland, Manuutoq 1, Nuuk, Greenland.
  • 19 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; Norwegian University of Science and Technology, University Museum, Trondheim, Norway.

Interspecific Gene Flow Shaped the Evolution of the Genus Canis

Shyam Gopalakrishnan et al. Curr Biol. .
. 2018 Nov 5;28(21):3441-3449.e5.
doi: 10.1016/j.cub.2018.08.041. Epub 2018 Oct 18.

Authors

Shyam Gopalakrishnan  1 , Mikkel-Holger S Sinding  2 , Jazmín Ramos-Madrigal  3 , Jonas Niemann  3 , Jose A Samaniego Castruita  3 , Filipe G Vieira  3 , Christian Carøe  3 , Marc de Manuel Montero  4 , Lukas Kuderna  4 , Aitor Serres  4 , Víctor Manuel González-Basallote  4 , Yan-Hu Liu  5 , Guo-Dong Wang  6 , Tomas Marques-Bonet  7 , Siavash Mirarab  8 , Carlos Fernandes  9 , Philippe Gaubert  10 , Klaus-Peter Koepfli  11 , Jane Budd  12 , Eli Knispel Rueness  13 , Claudio Sillero  14 , Mads Peter Heide-Jørgensen  15 , Bent Petersen  16 , Thomas Sicheritz-Ponten  16 , Lutz Bachmann  17 , Øystein Wiig  17 , Anders J Hansen  18 , M Thomas P Gilbert  19

Affiliations

  • 1 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark. Electronic address: shyam@snm.ku.dk.
  • 2 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; Natural History Museum, University of Oslo, Oslo, Norway; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; University of Greenland, Manuutoq 1, Nuuk, Greenland.
  • 3 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
  • 4 Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain.
  • 5 State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, Yunnan, China.
  • 6 State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
  • 7 Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain; Catalan Institution of Research and Advanced Studies (ICREA), Passeig de Lluís Companys, 23, 08010, Barcelona, Spain; CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain; Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, 08193 Cerdanyola del Vallès, Barcelona, Spain.
  • 8 Department of Electrical and Computer Engineering, University of California, San Diego, San Diego, CA, USA.
  • 9 Centre for Ecology, Evolution and Environmental Changes (CE3C), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal.
  • 10 Institut des Sciences de l'Evolution de Montpellier (ISEM), UM-CNRS-IRD-EPHE, Université de Montpellier, Montpellier, France.
  • 11 Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Avenue NW, Washington, DC 20008, USA; Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, 41A Sredniy Prospekt, St. Petersburg 199034, Russia.
  • 12 Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates.
  • 13 Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway.
  • 14 Wildlife Conservation Research Unit, Zoology, University of Oxford, Tubney House, Tubney OX13 5QL, UK; IUCN SSC Canid Specialist Group, Oxford, UK.
  • 15 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland.
  • 16 DTU Bioinformatics, Department of Bio and Health Informatics, Technical University of Denmark, Lyngby, Denmark; Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia.
  • 17 Natural History Museum, University of Oslo, Oslo, Norway.
  • 18 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; University of Greenland, Manuutoq 1, Nuuk, Greenland.
  • 19 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; Norwegian University of Science and Technology, University Museum, Trondheim, Norway.

Erratum in

  • Interspecific Gene Flow Shaped the Evolution of the Genus Canis.
    Gopalakrishnan S, Sinding MS, Ramos-Madrigal J, Niemann J, Samaniego Castruita JA, Vieira FG, Carøe C, de Manuel Montero M, Kuderna L, Serres A, González-Basallote VM, Liu YH, Wang GD, Marques-Bonet T, Mirarab S, Fernandes C, Gaubert P, Koepfli KP, Budd J, Rueness EK, Sillero C, Heide-Jørgensen MP, Petersen B, Sicheritz-Ponten T, Bachmann L, Wiig Ø, Hansen AJ, Gilbert MTP. Gopalakrishnan S, et al. Curr Biol. 2019 Dec 2;29(23):4152. doi: 10.1016/j.cub.2019.11.009. Curr Biol. 2019. PMID: 31794747 Free PMC article. No abstract available.

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.

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Figures

None

Graphical abstract

Graphical abstract

Graphical abstract
Figure 1

Figure 1

Map Showing the IUCN Ranges,…

Figure 1

Map Showing the IUCN Ranges, Range Overlaps, and Sampling Locations of the Canids…

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…

Figure 2

Nuclear and Mitochondrial Phylogeny of Basal Canids (A) The maximum-likelihood estimate of the…

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…

Figure 3

Gene Flow among the Crown Canid Species (A) This figure summarizes the relationships…

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…

Figure 4

Modeling the Ancestry of African Golden Wolves (A) TreeMix tree with all samples,…

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.
See this image and copyright information in PMC

References

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