A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids

Abstract

High-throughput genotyping technologies developed for model species can potentially increase the resolution of demographic history and ancestry in wild relatives. We use a SNP genotyping microarray developed for the domestic dog to assay variation in over 48K loci in wolf-like species worldwide. Despite the high mobility of these large carnivores, we find distinct hierarchical population units within gray wolves and coyotes that correspond with geographic and ecologic differences among populations. Further, we test controversial theories about the ancestry of the Great Lakes wolf and red wolf using an analysis of haplotype blocks across all 38 canid autosomes. We find that these enigmatic canids are highly admixed varieties derived from gray wolves and coyotes, respectively. This divergent genomic history suggests that they do not have a shared recent ancestry as proposed by previous researchers. Interspecific hybridization, as well as the process of evolutionary divergence, may be responsible for the observed phenotypic distinction of both forms. Such admixture complicates decisions regarding endangered species restoration and protection.

Figure 1.

Genetic variation of wolf-like canids in the 48K SNP data set. Sample size (N), average observed and expected heterozygosity (H_O, H_E), percent of loci that are polymorphic (P), and could not be scored (missingness, M) are shown. Except for dog (SE = 0.01), all standard errors for (H_O, H_E) are <0.001. A modified relationship tree (Lindblad-Toh et al. 2005) and divergence dates are presented (Perini et al. 2009). (Inset) Tree depicts admixture hypotheses with dashed lines among North American canid populations (Supplemental Table S1). Map depicts historic species distributions and admixture zone (data from Nowak 2009; Rutledge et al. 2010b).

Figure 2.

Distribution map of gray wolf and coyote sample locations and regions. Sample sizes are indicated in parentheses.

Figure 3.

Principal component analysis of all wolf-like canids for the 48K SNP data set (IRNP, Isle Royale National Park).

Figure 4.

structure clustering analysis of domestic and wild canids for the 44K SNP pruned data set (see Supplemental Table S2). Separate analyses of North American (n = 68) and Eurasian (n = 74) wolves further resolves biologically informative clusters (K = 7; the top layer in plot). The three captive Mexican wolf colonies (Studbook, S; Ghost Ranch, G; and Aragon, A) are shown. See discussion in the Supplemental Material for an explanation of how K values were chosen for presentation. Coyote abbreviations: Midwest/Southern, MID; Northeastern, NE; and Western, WEST. North American abbreviations: Algonquin, Alg; Isle Royale NP, IRNP; Minnesota, MN; Ontario, Ont; Wisconsin, WI; Alaska/Canada, AK/Ca; British Columbia, BC; Mexico, Mex; Northern Canada, NCa; Northern Quebec, NQue; and Yellowstone, YNP. Eurasian abbreviations: Belarus, Be; Bulgaria, Bu; Croatia, Cr; Greece, Gr; India, In; Iran, Ir; Israel, Is; Italy, It; Lithuania, Li; Middle East, ME; Oman, Om; Poland, Po; Russia, Ru; Saudi Arabia, SA; Slovakia, Sl; Southwest Asia, SWA; Spain, Sp; Sweden, Sw; Turkey, Tu; and Ukraine, Uk.

Figure 5.

(Left) Extent of LD (genotypic association, r²) as a function of inter-SNP distance (Kb) for all North American canid populations. (Right) Autozygosity frequency distribution of runs of homozygosity (ROH) for all North American canid populations.

Figure 6.

Ancestry analysis of 38 canine autosomes. Plots show ancestry blocks and their assignments for representative individuals of canid populations with average size of blocks, percent ancestry, and number of generations since most recent admixture (τ) indicated. Two-ancestor (coyote, A; gray wolf, B) analyses are presented for a Great Lakes wolf from Minnesota (C), a captive red wolf (D), and an Algonquin wolf (E). Three-ancestor analyses (coyote, A; gray wolf, B; dog, F) are presented for a Northeastern coyote from Vermont (G), a Southern coyote from Louisiana (H), and a Midwestern coyote from Ohio (I). Individual results are given in Supplemental Tables S5 and S6.