Wolves in the Great Lakes region: a phylogeographic puzzle



    1. Istituto Superiore per la Protezione e la Ricerca Ambientale, Laboratorio di genetica, Via Cà Fornacetta 9, 40064 Ozzano dell’Emilia (BO), Italy
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Ettore Randi, Fax: 0039 051 796628;
E-mail: ettore.randi@infs.it


Empirical studies demonstrate that natural hybridization in animals is more common than thought so far (Mallet 2005), particularly among species that originated recently through cycles of population contraction–expansion arising from climate changes over the last glacial period, the Pleistocene. In addition, the post-glacial global growth of human populations has fostered anthropogenic hybridization events, mediated by habitat changes, the persecution of large predators and the introduction of alien species (Allendorf et al. 2001). The Canis lineage shows cases of both natural and anthropogenic hybridization, exacerbating the controversy about the number of species that should be formally validated in the taxonomic lists, the evolutionary role of genetic introgression and the ways to manage hybrids with invading wild or domesticated populations. The study by Wheeldon et al. (2010), published in this issue of Molecular Ecology, adds a new piece to the intricate puzzle of evolution and taxonomy of Canis in North America. They show that sympatric wolves (C. lupus) and coyotes (C. latrans) are not (extensively) hybridizing in the western North American Great Lakes region (GLR). Widespread hybridization between coyotes and a genetically distinct, but closely related, wolf-like population (the eastern wolf) occurred in the northeastern regions of North America. In Wheeldon et al.’s (2010) opinion, these data should prove definitely that two different species of wolf (the western gray wolf C. lupus and the eastern wolf C. lycaon) and their hybrids are distributed across the GLR.

A number of variable morphological and molecular traits have complicated the taxonomy of Canis in North America (Wilson et al. 2000; Nowak 2003; Koblmuller et al. 2009). The distinction between coyotes (Canis latrans) and wolves is unquestionable. The wolf-like populations, however, are divided into a puzzling mosaic of distinct groups, which are distributed in the northern regions (western gray wolves, eastern wolves and hybrids between eastern wolves and coyotes; Kyle et al. 2006) and in the southeastern United States (red wolves and hybrids with coyotes; Hailer & Leonard 2008). It is not clear how many wolf-like subspecies or species are currently distributed in North America and whether they originated in allopatry or through hybridization and genetic introgression. Their phylogeography remains controversial: some wolf populations could have evolved in the Old World and later migrated to North America (the gray wolf lineage Canis lupus), while other populations may have speciated in North America originating endemic species (the coyote-eastern wolf–red wolf lineage; Wilson et al. 2000). Things are complicated as a result of recent hybridization events of coyotes with wolves and possibly dogs. During the past century, coyotes (Fig. 1) expanded northeastward from the Great Plains following deforestation and the spread of agriculture, concomitantly with the almost complete eradication of wolves from most of the United States (Leonard et al. 2005). Habitat and demographic changes have encouraged the hybridization between coyotes and wolves. During the last two decades, scholars of Canis tried to reconstruct the puzzle, giving almost any plausible solution, such as: (i) the red wolf is a distinct species (C. rufus), endemic of the southeastern United States, or it is a hybrid with coyotes (C. lupus × latrans; see: Hailer & Leonard 2008); (ii) the wolves in the Algonquin area (eastern GLR) are a distinct endemic species, the eastern wolf C. lycaon (Wilson et al. 2000), or they are a subspecies of the gray wolf (C. lupus lycaon; Koblmuller et al. 2009); (iii) the eastern wolf and the red wolf are conspecific, originating in North America in the last 150 000–300 000 years from a common ancestral coyote population (Wilson et al. 2000; Kyle et al. 2006); and (iv) the eastern wolves are hybrids between gray and red wolves (C. lupus × rufus; Nowak 2002), or they are hybrids between gray wolves and coyotes (C. lupus × latrans; Roy et al. 1994).

Figure 1.

 A coyote from Michigan. Coyotes, expanding across deforested areas, hybridized in the past and currently with eastern wolves, originating a widespread hybrid zone in the Great Lakes region of North American (photograph: thanks to Tyler Wheeldon, Trent University).

Wheeldon et al. (2010) specifically aimed at testing whether gray wolves in the western GLR hybridized with western coyotes or with eastern wolves. They genotyped a total of 410 sympatric canids (coyotes, wolves and unknown) sampled from Michigan, Wisconsin, Minnesota and western Ontario (although 44/92 = 48% of the coyotes were collected from a single area west of Minneapolis, MN), using maternal mtDNA control region sequences, four Y-linked microsatellites and 12 autosomal microsatellites. Interestingly, the different markers concordantly indicate a clear genetic distinction between sympatric western Great Lakes gray wolves and coyotes, suggesting that they are reproductively isolated. However, wolf and coyote hybridization in the western GLR is not absent. In fact, a few cases of apparently admixed individuals were detected. Moreover, Wheeldon et al.’s (2010) results confirm Koblmuller et al.’s (2009) findings, showing that the extant GLR wolf population has admixed origin, deriving from hybridization of gray wolves with eastern wolves (in Wheeldon et al.’s opinion) or with coyotes (in Koblmuller et al.’s opinion). These results contribute to better focus the GLR wolf controversy. Coyotes and eastern wolves can hybridize because of their recent shared ancestry (Kyle et al. 2006; Kays et al. 2010). Direct hybridization between gray wolves and coyotes may be difficult, or gene flow between them should be mediated by the eastern wolf, in contrast with the opinions of Lehman et al. (1991) and Koblmuller et al. (2009).

The mosaic of population genetic structuring and hybridization across the GLR has been clarified by Wheeldon et al. (2010) and Koblmuller et al. (2009), which, however, disagrees on how to rank the eastern wolves: are they the survivors of an ancestral and genetically distinct coyote or gray wolf population? The answer should rely on the interpretation of the origin of the unique mtDNA and Y-microsatellite haplogroups that were observed also in the historical hybridizing populations. These divergent haplogroups are linked in basal positions to the coyote and not to the gray wolf modern clades. However, the topologies of the phylogenetic trees cannot be used directly to identify a distinct wolf species (C. lycaon) or simply a distinct ancient coyote population. What is missing in these studies is an explicit operational rule to define species boundaries based on gene tree information. Thus, the rank of the ancestral eastern wolf population remains to be defined. As noted by Schwartz & Vucetich (2009), the solution of the GLR canid controversy is still waiting for additional data and more robust analyses. In perspective, some issues should be more carefully investigated: (i) uncertain subspecies/species delimitation: whole mtDNA and next-generation sequencing may be used to reconstruct robust phylogenies and solve taxonomic uncertainties deriving from limited haplotype information; (ii) uncertain extent of wolf × coyote admixture: gene-flow rates should be better estimated using larger panels of molecular markers (single nucleotide polymorphism, SNP) and population genomic methodologies; and (iii) uncertain time to hybridization: hypothesis testing through population modelling may help understanding whether hybridization occurred in the Pleistocene or after the European colonization.

Although the origin of those populations is still debated, the emerging picture clearly shows a widespread distribution of hybrids across the GLR. Regardless of their origin, these populations live in the wild, filling the ecological niche of large carnivores, and contribute to optimize predator–prey relations and ecosystem functions. In the face of continuing climate and habitat changes, the challenge now is to develop a deeper understanding of population expansion, behavioural interactions and gene introgression dynamics. Disentangling the patterns and consequences of natural vs. anthropogenic hybridization might be difficult, but is of paramount importance for the design of appropriate conservation strategies. A better definition of ‘ecotype’ is strongly needed to the benefit of both theoretical and applied conservation biology of Canis. The ecotype concept will add functional dimensions (morphology, behaviour, mating strategy, disease resistance) to identification rules still based on nonfunctional molecular traits. Next-generation population genomics, and comparative genome scanning in parental species and their hybrids, will predictably contribute to understanding the complexities of hybridization, opening the way to teasing apart neutral vs. adaptive gene introgression (Anderson et al. 2009).