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Population genetics of the African wolf (Canis lupaster) across its range: first evidence of hybridization with domestic dogs in Africa

Abstract

Despite the known genetic permeability among wolf-like canids, there is currently no evidence of gene flow between the recently acknowledged African wolf (Canis lupaster) and domestic dogs (C. lupus familiaris). We genotyped African wolves across their range, together with African domestic dogs and ‘reference’ grey wolves (C. l. lupus; not occurring in Africa). Northwestern African wolves showed (1) the greatest genetic diversity as observed from microsatellite loci and mitochondrial + Y-chromosome markers, and (2) possible signs of past admixture with grey wolves. We detected two zones of hybridization between domestic dogs and African wolves, in northwestern Senegal and central Ethiopia. Hybrids were intermediary in the nuclear genetic space separating African wolves from domestic dogs (and grey wolves), and were in majority assigned to domestic dogs in STRUCTURE. Hybrids showed mitochondrial DNA haplotypes of African wolves, suggesting gene flow directionality between male African dogs and female African wolves. The roaming of feral and shepherds’ dogs in degraded habitats occupied by African wolves may have promoted hybridization. Our results provide evidence that, subsequent to the possible hybrid origin of C. lupaster, the genome of the African wolf is still subject to admixture with C. lupus descendants. This could lead to the genetic dilution of endemic African wolf lineages, such as in eastern Africa, but may also imply disease prevalence and competition for resources with domestic dogs. Our study also is the first to show a significant level of differentiation (ΦST and FST) between North African and West African wolves. Wider genetic screening of African wolves across their range should depict more accurately their population dynamics and the potential stakes related to gene flow with domestic dogs.

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Availability of data and material

The new sequences have been deposited in GenBank.

Code availability

Not applicable.

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Acknowledgements

We thank the following persons for participating in the sampling effort: K. Difallah (Setif, Algeria), S. Benyacoub (Station Biologique d’El Mellah, Université d'Annaba, Algeria), A. Abdelhamid (Saint Katherine Protectorate, Nature Conservation Sector, Egyptian Environmental Affairs Agency, Egypt), C.A.M.S. Djagoun (Université d’Abomey-Calavi, Cotonou, Benin), N. Lescureux (Muséum National d’Histoire Naturelle de Paris, France), and G. Dobigny (Centre de Biologie pour la Gestion des Populations, Montpellier, France). Laboratory work at ISEM was conducted on the GenSeq platform of LabEx CeMEB (Centre Méditerranéen Environnement et Biodiversité). We thank the staff of the Service de Systématique Moléculaire, Muséum National d’Histoire Naturelle de Paris, for their assistance during the early phases of the project and related laboratory work. M. Balastre helped with the graphical design of the figures. Two reviewers provided helpful comments on an early draft of the manuscript.

Funding

PG and TT were partly supported by the Action Transversale Muséum ‘Biodiversité actuelle et fossile’, MNHN Paris. KM and PG received support from ‘Soutien aux missions de développement au Sud’, IRD/ISEM Montpellier. KM was funded by the program ‘Stages de perfectionnement en France’, Université de Tizi-Ouzou, Algeria.

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PG, EKR and MA designed the study. KM, SD, EKR, CB, MA and PG collected the genetic samples. KM, FJ, TT and PG did the laboratory work. KM, FJ and PG conducted data treatment and analysis. CB and JB photographed the phenotypes. All the co-authors participated in the writing of the manuscript.

Corresponding authors

Correspondence to Kahina Mallil or Philippe Gaubert.

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42991_2020_59_MOESM1_ESM.eps

Supplementary file1 Figure S1. Midpoint rooted maximum likelihood phylogenetic tree of African wolves, grey wolves and African domestic dogs based on 402 bp cytochrome b sequences (cytb1; A) and 297 bp control region sequences (CR1; B). Values at nodes correspond to bootstrap support > 75 %. Bars indicate 0.5 / 2.0% divergence in A and B, respectively. Sample numbers refer to Table S1. Yellow box = cluster “grey wolves / African domestic dogs”; green box = cluster “African wolves”; orange box = African wolf x African domestic dog hybrid; asterisk = African domestic dog clustering with African wolves. (EPS 831 kb)

42991_2020_59_MOESM2_ESM.psd

Supplementary file2 Figure S2. Midpoint rooted maximum likelihood phylogenetic trees of African wolves, grey wolves and African domestic dogs based on 158 bp cytochrome b sequences (cytb2; A) and 126 bp control region sequences (CR2; B). Values at nodes correspond to bootstrap support > 75 %. Bars indicate 0.5 / 1.0% divergence in A and B, respectively. Sample numbers refer to Table S1. Yellow box = cluster “grey wolves / African domestic dogs”; green box = cluster “African wolves”; orange box = African wolf x African domestic dog hybrid; asterisk = African domestic dog clustering with African wolves. (PSD 785 kb)

42991_2020_59_MOESM3_ESM.eps

Supplementary file3 Figure S3. Distribution of Y-chromosome haplotypes among African wolves (Algeria, Senegal), grey wolves and African domestic dogs. (EPS 1480 kb)

42991_2020_59_MOESM4_ESM.psd

Supplementary file4 Figure S4. Plots of the probabilistic assignments inferred in STRUCTURE among individuals of African wolves, African domestic dogs, grey wolves and their hybrids, using autosomal loci. Each individual is represented by a vertical bar. K varies from 2 to 8. (PSD 17356 kb)

42991_2020_59_MOESM5_ESM.eps

Supplementary file5 Figure S5. Optimal K values derived from the analysis with STRUCTURE of the combined dataset (autosomal + Y-chromosome loci; A) and the autosomal loci alone (B), figured as ΔK (left) and Ln Pr(X|K) (right) plots. (EPS 2806 kb)

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Supplementary file6Table S1. Detailed list of the 62 samples used in this study. Columns for cytochrome b (cytb) and control region (CR) indicate (i) haplotype number (see Fig. 2) and ii) Genbank accession numbers for new haplotypes (after hyphen) and already published haplotypes (between brackets). Cytochrome b and control region haplotypes with haplotype numbers in parenthesis are short fragments that 100% matched with one or several longer fragments. Control region haplotypes without haplotype number correspond to unique, short fragments not figured in Fig. 2 (but figured in Figs S1B and S2B). Taxonomic assignments from mitochondrial DNA (cytb and CR ML trees) and microsatellites (STRUCTURE; K=4) are given in colors: yellow = grey wolf + African domestic dog; green = African wolf; orange = African dog x African wolf hybrid; red = potential grey wolf x African wolf hybrids (see Discussion). (XLSX 20 kb)

Supplementary file 7 Table S2. List of the 10 microsatellite loci used in this study. (DOCX 14 kb)

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Supplementary file 8 Table S3. Mitochondrial diversity among African wolves (Algeria, Senegal and Ethiopia), grey wolves and African domestic dogs. (h) haplotype number, (Hd) haplotype diversity, (π) nucleotide diversity, (k) average number of nucleotide differences. Cytb1-CR1 and cytb2-CR2 correspond to the long and short cytochrome b and control region fragments, respectively. (DOCX 14 kb)

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Supplementary file 9 Table S4. Pairwise differentiation (ΦST) among African wolves (Algeria, Senegal, Ethiopia), grey wolves and African domestic dogs. Cytb1 and CR1 correspond to the long cytochrome b and control region fragments, respectively. (DOCX 14 kb)

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Supplementary file 10 Table S5. Genetic differentiation (FST) among African wolves (Algeria, Senegal, Ethiopia), grey wolves and African domestic dogs, based on autosomal loci. (EPS 13 kb)

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Mallil, K., Justy, F., Rueness, E.K. et al. Population genetics of the African wolf (Canis lupaster) across its range: first evidence of hybridization with domestic dogs in Africa. Mamm Biol 100, 645–658 (2020). https://doi.org/10.1007/s42991-020-00059-1

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Keywords

  • Africa
  • African wolf
  • Canis lupaster
  • Domestic dog
  • Hybridization
  • Population genetics