Mexican gray wolves were extirpated from the wild in the United States in the mid-1970s. Then 20 years ago they were reintroduced, amidst much controversy, into a small portion of their former range. Controversies continue today regarding both their taxonomic validity and the management strategies used in the captive breeding program and in the extant wild reintroduced population. The purpose of this chapter is to scientifically assess whether Mexican gray wolves are a valid subspecies based on the evidence of morphology, paleontology, genetics, and behavioral ecology.
Gray wolves have great dispersal capabilities, and they travel long distances, averaging 50–100 km and ranging up to several hundred kilometers, before establishing their territories (Jimenez et al., 2017; Mech, 1970; Merrill and Mech, 2000). They are habitat generalists and occupy a wide variety of environments. There is some controversy concerning the way that their historical range was determined, as it was based on a traditional morphological analysis of a relatively small number of historical specimens that postdated the period of time when populations were already in decline (Bogan and Mehlhop, 1983; Nowak, 1995; Young and Goldman, 1944). These facets of wolf biology have been used to argue that the recognition of any subspecies of North American gray wolves, including Mexican gray wolves, cannot be justified biologically.
The designation of the Mexican gray wolf as a subspecies has also been questioned because of disagreements in the application of subspecies concepts (Fredrickson et al., 2015; Haig et al., 2006; Patten and Remsen, 2017). It has been suggested that Mexican gray wolves may not have sufficient morphological and genetic differences from other wolf populations to justify their status as a valid subspecies. Cronin et al. (2015a,b) made this argument because a previous genetic analysis of mitochondrial DNA (mtDNA) sequences had shown that extant and historical samples of Mexican
gray wolves lacked reciprocal monophyly and that they shared haplotypes with wolves in other areas and also with coyotes (Hailer and Leonard, 2008; Leonard et al., 2005). There has also been speculation that the extant Mexican gray wolf population, which was derived from individuals from three captive lineages (Hedrick et al., 1997), may have included ancestry from dogs or coyotes due to a previous admixture (Cronin et al., 2015a).
The Mexican gray wolf was first described as a distinct subspecies of Canis nubilus by Nelson and Goldman (1929) and was classified as the subspecies C. nubilus baileyi. Later, Goldman (1937) reorganized the taxonomy of North American wolves and recognized five wolf subspecies of C. lupus in the southwestern United States and Mexico: C. lupus youngi (southern Rocky Mountain wolf), C. l. monstrabilis (Texas gray wolf), C. l. mogollonensis (Mogollon Mountain wolf), C. l. nubilus (buffalo wolf), and C. l. baileyi (Mexican wolf). Bogan and Mehlhop (1983) examined morphological variation in 253 adult wolf skulls utilizing univariate and multivariate statistical procedures. Their morphometric analysis revealed considerable overlap among many individuals, but determined that C. l. baileyi and C. l. youngi were taxonomically distinct subspecies. Furthermore, they determined that C. l. mogollonensis and C. l. monstrabilis were intermediate between C. l. baileyi and C. l. youngi and referred C. l. monstrabilis and C. l. mogollonensis to C. l. baileyi. Thus, they recognized only three southwestern subspecies: C. l. baileyi, C. l. youngi, and C. l. nubilus. Nowak (1995) condensed 24 previously recognized North American gray wolf subspecies into five subspecies, including C. l. baileyi as one of the remaining five. Bogan and Mehlhop delimited their defined range to include east-central Arizona, southern New Mexico, western Texas, and the highlands of Mexico. But Nowak’s (1995) conclusions suggest a wider historical range of the Mexican gray wolf that would include the Mogollon Plateau. While there is ongoing scientific debate about the precise limits of the range (Heffelfinger et al., 2017; Hendricks et al., 2016), the U.S. Fish and Wildlife Service (FWS) has adopted the range depicted in Figure 4-1.1 The Mexican gray wolf is currently recognized as a subspecies of C. lupus in most well-respected mammalian taxonomic publications, such as Mammalian Species (Mech, 1974), The Mammals of North America (Hall, 1981), and Mammal Species of the World (Wilson and Reeder, 2005).
By the mid-1900s Mexican gray wolves had been nearly extirpated from the wild through intensive predator eradication programs. Total extirpation was narrowly averted when the last surviving wild wolves were captured in Mexico and taken into captivity. No wild populations were known to remain in the United States when the Mexican gray wolf was listed as endangered in 1976, and only a handful of wolves persisted in Mexico. Three wild wolves captured in Mexico in the late 1970s (the McBride lineage) and four additional captive Mexican gray wolves from the Aragon (n = 2) and Ghost Ranch (n = 2) lineages became the founding population (n = 7) for all Mexican gray wolves used for the subsequent reintroduction and captive breeding program.
The U.S. FWS and Mexican authorities established a binational captive breeding program and began reintroduction efforts in the United States in 1998 and in Mexico in 2011. As of November 2017, 114 Mexican gray wolves were living in the wild in Arizona and New Mexico, distributed in 22 packs across the two states. As of July 2017, approximately 31 wild Mexican gray wolves inhabited Chihuahua and Sonora, Mexico, in the northern Sierra Madre Occidental (CONANP, 2017; Garcia Chavez et al., 2017). To maintain genetic diversity and minimize the effects of inbreeding, the wild population is heavily managed and augmented frequently by moving adults (captive and wild) between packs and by cross-fostering captive-born pups into the wild dens. As of July 2017,
1 Text was modified after the release of the prepublication to clarify an issue about the historical range of the Mexican gray wolf.
281 captive wolves lived in 55 facilities. This captive population has retained 83 percent of the heterozygosity of the seven founders (U.S. FWS, 2017b). This is a rapid loss relative to the general accepted guidelines of retaining at least 95 percent of the heterozygosity for 100 years (Allendorf and Ryman, 2002; Soulé et al., 1986). Analyses of 40 whole-genome sequences that represent the extant diversity of North American gray wolves and other wolf-like canid populations have demonstrated that extant Mexican gray wolves show signatures of low population sizes, with low heterozygosity and high inbreeding coefficients (Sinding et al., 2018).
IS THERE EVIDENCE FOR DISTINCTIVENESS OF MEXICAN GRAY WOLF POPULATIONS FROM OTHER NORTH AMERICAN CANIS POPULATIONS?
The Mexican gray wolf was first described as a distinct subspecies in 1929 by Nelson and Goldman, based on 65 specimens that they examined. They characterized this subspecies as having a small body size; a small, narrow, and arched skull with slender and depressed rostrum; and a darker, more reddish pelage coloration than other North American wolves. The type specimen was a male wolf collected by Nelson and Goldman in 1899, which is deposited at the U.S. National
Museum of Natural History (#98312). The type locality is from the area of Colonia García, about 60 miles southwest of Casas Grandes, Chihuahua (U.S. FWS, 2017b).
The Mexican gray wolf is adapted to the warmer and drier climates of the southwest with its smaller body size, slightly taller ears, and slightly darker pelage. The Mexican gray wolf is the smallest extant gray wolf in North America; adults weigh 23–41 kg with a length of 150–180 cm and a height at the shoulder of 63–81 cm (Brown, 1983; Young and Goldman, 1944). As is the case with all gray wolves, females are typically smaller than males. Mexican gray wolves are generally gray, with a darker area (which can be brown to cinnamon and cream in color) over the shoulders and down the spine, and lighter underparts (Brown, 1983). Solid black or white individuals, which are occasionally seen in other North American gray wolves, have never been documented in Mexican gray wolves (U.S. FWS, 2017b). Young and Goldman (1944) described the Mexican gray wolf skull as having a slender rostrum and widely spreading zygomata. Nowak (1995) compared numerous morphometric skull measurements across North America and Europe and found that the Mexican gray wolf “lies almost entirely outside the range of variation of the other groups” (i.e., other species and subspecies of Canis), and they agreed with the findings of Hoffmeister (1986) and Young and Goldman (1944) that the Mexican gray wolf is morphometrically distinct.
Additionally, there has been little evidence to suggest that Mexican gray wolves hybridized with coyotes. Nowak (1979) reported three specimens that statistically appeared to be possible hybrids of C. latrans, based on morphological characters, and suggested that the smallest and most coyote-like of the three was the baileyi subspecies. That specimen was collected in the 1800s at Orizaba, Veracruz, far to the south of any known locality where C. lupus specimens had previously been reported; the other two specimens also date back over a century and could be small individual baileyi wolves. There is also no morphological evidence of coyote introgression from a series of C. l. baileyi specimens taken during intensive control operations in the 20th century (Nowak, 1979, 1995) and no molecular evidence of such in the living population of C. l. baileyi (Wayne and Vilà, 2003). There is no geographical barrier that would serve as an isolating mechanism, suggesting that morphological and behavioral differences were sufficient to maintain historical reproductive isolation between Mexican gray wolves and sympatric coyotes.
Finding: The Mexican gray wolf has, from its discovery, been considered a distinct wolf. Its size, morphology, and coloration pattern distinguish it from other North American wolves.
The genetic evidence published to date also overwhelmingly supports the Mexican gray wolf being a subspecies of the gray wolf (Fan et al., 2016; Vilà et al., 1999; vonHoldt et al., 2011, 2016; Wayne et al., 1992). According to a large number of studies using mtDNA sequencing and microsatellite loci as well as studies using next-generation sequencing and genomic technologies, this subspecies has been determined to be the most genetically divergent wolf in North America (Fan et al., 2016; Sinding et al., 2018; Vilà et al., 1999; vonHoldt et al., 2011, 2016; Wayne et al., 1992).
Nonetheless, the designation of the Mexican gray wolf as a separate subspecies has been questioned for several reasons (Cronin et al., 2015a,b). According to Cronin et al. (2015a), “extant and historic samples show that Mexican gray wolves lack mtDNA monophyly, share haplotypes with wolves in other areas and with coyotes (Hailer and Leonard, 2008; Leonard et al., 2005), and extant Mexican gray wolves came from only seven founders that may have included dog ancestry (although genetic data indicate this is improbable and/or of small genetic importance; Garcia-Moreno et al., 1996; Hedrick et al., 1997). These factors indicate that the designation of a Mexican gray wolf subspecies is of questionable validity.” The issue of shared mtDNA haplotypes is important to Cronin et al.’s (2015a) argument because they adopted a subspecies definition that would
require reciprocal monophyly of mtDNA haplotypes as a condition for recognizing subspecies. We address these points below.
Cronin et al.’s (2015a,b) requirement for subspecies definition deviates from the criteria used historically or at present to define and recognize mammalian subspecies, as described in Chapter 2. Thus, the absence of reciprocal monophyly of mtDNA haplotypes would not be a reason to deny the designation of a subspecies under conventional definitions if other morphological, ecological, or genetic differences were present.
Moreover, recent analyses fail to support the proposal that gray wolves trace some of their ancestry to domestic dogs. In particular, Fredrickson et al. (2015) pointed out that a genetic analysis of the three captive lineages using microsatellite and mtDNA analysis (Hedrick et al., 1997) found an absence of dog admixture (Garcia-Moreno et al., 1996; Hedrick et al., 1997). This conclusion was subsequently confirmed with whole-genome analyses (Fan et al., 2016; Fitak et al., 2018).
The issue of mtDNA haplotype sharing is more complex and requires analyses of ancient DNA, and, in conjunction with reconstructions of historical species distributions, it supports another interpretation. This is discussed in the context of the historical population below.
Genetic analyses with mtDNA, microsatellites, and large-scale genomic data sets have shown that the genetic structure of North American gray wolves is strongly influenced by their habitat distribution (Carmichael et al., 2007; Geffen et al., 2004; Hendricks et al., 2018; Muñoz-Fuentes et al., 2009; Musiani et al., 2007; Pilot et al., 2006, 2010; Schweizer et al., 2016a,b; Stronen et al., 2014; vonHoldt et al., 2011). This is also the case of Mexican gray wolves, which are better adapted to the more arid habitat characteristic of their historical distribution range (Nowak, 1995) and have been shown to have strong signatures of genetic structure due to a long history of isolation from other gray wolf populations (Sinding et al., 2018).
Findings: Genetic and genomic analyses confirm that the Mexican gray wolf, is genetically distinct—it is the most genetically distinct subspecies of gray wolf in North America. Arguments against recognizing the Mexican gray wolf as a subspecies are based on a subspecies definition that is not widely accepted in the scientific literature. There is no evidence that Mexican gray wolf genomes include introgression from domestic dogs.
The historical range of the Mexican gray wolf documented by early taxonomists included southern Arizona, southern New Mexico, southwestern Texas, and northern Mexico (Figure 4-1) (Nelson and Goldman, 1929; Young and Goldman, 1944). However, based on a review of ecological, morphological, and genetic data, Parsons (1996) expanded the historical range in 1996 and this expansion was accepted by the Mexican wolf recovery team in its reintroduction plans (U.S. FWS, 1996) (Figure 4-1). Mexican gray wolves are behaviorally and morphologically adapted to survive in these warm, arid environments. The U.S. FWS (2017b) describes the historical habitat use of the Mexican gray wolf as follows: “Historically, Mexican gray wolves were associated with montane woodlands characterized by sparsely to densely forested mountainous terrain and adjacent grasslands in habitats found at elevations of 1,219–1,524 m.” Wolves were known to occupy habitats ranging from foothills characterized by the presence of evergreen oaks (Quercus spp.) or pinyon (Pinus edulis) and juniper (Juniperus spp.) to higher-elevation pine (Pinus spp.) and mixed conifer forests. The factors making these habitats attractive to Mexican gray wolves likely included an abundance of prey, the availability of water, and the presence of hiding cover and suitable den sites. Early investigators reported that Mexican gray wolves probably avoided desert scrub and semidesert grasslands, which provided little cover, food, or water (Brown, 1983). Wolves traveled between suitable habitats using riparian corridors and, later, roads or trails (Brown, 1983).
Mexican gray wolves have life histories typical of other gray wolves, living in packs as an apex predator. They are cooperative obligatory hunters, capturing prey larger than themselves such as elks and Coues’ white-tailed deer (Odocoileus virginianus couesi). Historical estimates of pack size were 2 to 8 wolves (Bednarz, 1988), including adults, pups born that year, and offspring from previous years. The pack size in the Mexican gray wolf recovery area between 1998 and 2016 ranged from 2 to 12 wolves (mean = 4.1; U.S. FWS, 2017b). Mexican gray wolf pups are generally born between early April and early May. The typical lifespan of a wild Mexican gray wolf is 4–5 years, although captive Mexican gray wolves have lived to be 13 years old. The estimated annual survival rate for wild Mexican gray wolves (pups, yearlings, and adults) in the Mexican gray wolf recovery area has ranged from 0.50 to 0.81 (U.S. FWS, 2017b). The average home range size of 138 denning packs in the Mexican gray wolf recovery area in the period 1998–2015 was 510 km2, whereas the home range size for 30 non-denning packs was 888 km2 (U.S. FWS, 2017b).
The Mexican gray wolf recovery area is firmly defined by policy so that when a dispersing wolf travels beyond the designated recovery area, the individual is removed. This negates the possibility of any expansion of the Mexican gray wolf distribution. The geographical centers of Mexican gray wolf recovery in the United States and in northern Sierra Madre Occidental are approximately 418 km apart, which is within the dispersal distance of the Mexican gray wolf. Two Mexican gray wolves have been documented crossing the border from Mexico into the United States since the reintroductions began (U.S. FWS, 2017a). One of these wolves was captured and placed in captivity, and the other was returned to Mexico. It is possible that the two binational populations could merge through dispersal if allowed to do so without human intervention.
Although there is little, if any, evidence of coyote introgression among Mexican gray wolves, increasing coyote numbers due to past wolf extirpation could offer opportunities for the low-density Mexican gray wolf population to hybridize with the high-density coyote population if mate choices become limited. Gray wolves in western North America routinely kill coyotes and do not breed with them in the wild (Smith et al., 2003). However, such interbreeding apparently has occurred in eastern wolves, Great Lakes wolves, and red wolves. The anthropogenic influences on the landscape now also include the presence of free-ranging dogs, owned and feral, which could also mate with Mexican gray wolves. However, to this point behavioral assortative mate selection has apparently prevented hybridization between Mexican gray wolves and coyotes or dogs (Fredrickson et al., 2015).
Findings: Extant wild Mexican gray wolves behave similarly to other North American gray wolves within the confines of the human-constricted Mexican gray wolf recovery area; their wild behavior prior to their 1970 extirpation in the wild is unknown. The Mexican gray wolf represents a smaller form of the gray wolf, which inhabits more arid ecosystems (Nowak, 1995). At present, Mexican gray wolves are behaviorally and ecologically distinct.
IS THERE EVIDENCE FOR CONTINUITY BETWEEN THE HISTORICAL MEXICAN GRAY WOLF LINEAGE AND THE PRESENT MANAGED POPULATIONS?
Paleontology and Morphology
Bogan and Mehlhop (1983) analyzed morphological measurements from 253 adult wolf skulls from the southwestern United States to help define the historical range of the Mexican gray wolf. Bailey (1931), Young and Goldman (1944), Hoffmeister (1986), and Nowak (1995) also examined historical Mexican gray wolves and specimens and described their morphology and phenotype. The extant Mexican gray wolves have a morphology that is similar to the morphology described in the historical studies. Furthermore, the extant Mexican gray wolves are direct descendants from the last
known surviving wild Mexican gray wolves and therefore have inherent continuity with the historical Mexican gray wolves.
Finding: There is morphological continuity between historical and extant Mexican gray wolf lineages.
Studies that have used ancient DNA taken from historical museum specimens in combination with modern DNA samples have also determined that the Mexican gray wolf lineage likely resulted from one of the earliest waves of colonization of C. lupus into the New World (Fan et al., 2016; Leonard et al., 2005; vonHoldt et al., 2011; Wayne and Hedrick, 2011). Phylogenetic analysis of mtDNA (Vilà et al., 1999) suggested that the three most widely recognized subspecies of gray wolf in North America, C. l. baileyi, C. l. nubilus, and C. l. occidentalis, originated from successive waves of wolf colonization from Eurasia during the Pleistocene, with Mexican gray wolves descending from the earliest of these waves. Vilà et al. (1999) attributed the observed phylogenetic relations and patterns to having resulted from “past episodes of isolation followed by admixture” as successive waves of wolves colonized southward. More recently, Sinding et al. (2018) analyzed 40 full genomes of North American wolves and other wolf-like canids, and their results indicated that all extant North American gray wolves descended from the same ancestral genomic makeup and also that the Mexican gray wolves were the most divergent from all other North American wolves. Sinding et al. (2018) proposed that the Mexican gray wolves diverged early from the ancestral wolves via a single colonization event and have since been isolated from the other populations, an alternative to the hypothesis about three historical waves of wolf colonization in North America.
The designation of the Mexican gray wolf as a subspecies has been questioned because samples from the historical population show that Mexican gray wolves lack mtDNA monophyly and that they instead share haplotypes with wolves in other areas and with coyotes (Cronin et al., 2015a,b). According to studies of ancient DNA conducted by Leonard et al. (2005), Mexican gray wolves were historically part of a monophyletic clade, referred to as the “southern clade,” which consisted of the mitochondrial haplotype of extant Mexican gray wolves and closely related haplotypes found in museum specimens that extended further north into the southern Rockies and Great Plains—a finding that is consistent with the Mexican gray wolf having a larger geographic range historically than it does today.
Hendricks et al. (2018) agreed that the southern clade had a wide distribution, which would imply that gene flow was naturally extensive across the recognized limit of the subspecies and that there may have been an admixture of Mexican gray wolves with other wolf populations to the north. It is generally accepted that with highly mobile species such as wolves, subspecies boundaries may include large zones of intergradation (Schweizer et al., 2016b) and that admixture in individuals within such zones might enhance their adaptive potential (Hedrick, 2013). Hendricks et al. (2016) used a multiple-trait data set and geographic distribution models to test the hypothesis that the historical range of Mexican gray wolves extended beyond the boundary currently recognized by the U.S. FWS (Parsons, 1996), and their analysis supported this more extensive range. There was historically a wide distribution of the “southern clade” in the American West (Leonard et al., 2005), indicating that individuals with Mexican gray wolf ancestry coexisted with Northern Rocky Mountain wolves (C. l. irremotus) outside of the presently defined Mexican gray wolf historical range and, therefore, that these areas may represent appropriate habitat for both wolf ecotypes. In addition, Hendricks et al. (2016) used a large panel of canine single nucleotide polymorphism (SNP) markers and mtDNA haplotype information to determine that a southern California wolf historical museum specimen collected (Grinnell et al., 1937) prior to extirpation of wolves in that
area in 1922 had Mexican gray wolf ancestry and that the habitat of the sampling locality was likely historically suitable for Mexican gray wolves.
Hendricks et al. (2018) also pointed out that the more widely distributed historical population of Mexican gray wolves exchanged genes with those wolves in the north that in turn may have exchanged genes with coyotes. The contraction of the range of the Mexican gray wolf and the loss of the populations to the north would, in such a case, leave Mexican gray wolf haplotypes that can be found in coyotes but not vice versa. This hypothesis is supported by the lack of evidence for any recent hybridization between Mexican gray wolves and coyotes and the recent findings by Sinding et al. (2018) that showed that all North American gray wolves carry varying degrees of coyote admixture, including Mexican gray wolves. However, the mode and timing of that ancient admixture remain unexplored.
Findings: While differences in allele frequencies and DNA sequences alone do not demonstrate the distinctiveness of a lineage, the analysis of ancient DNA reinforces the conclusion that the historical population of Mexican gray wolf represents a distinct evolutionary lineage of gray wolf. Furthermore, the extant Mexican gray wolves are direct descendants from the last remaining wild Mexican gray wolves. The known history of the extant Mexican gray wolves suggests that there is continuity between them and the historical lineage.
Mexican gray wolves are distinct from other North American gray wolves morphologically, paleontologically, genetically, genomically, behaviorally, and ecologically.
The Mexican gray wolf is a valid taxonomic subspecies of the gray wolf, Canis lupus, as currently classified as Canis lupus baileyi.
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