Black and Red Angus cattle coat color is controlled by the MC1R (Extension) gene, with the black gene (called the ED allele) being dominant to the red gene (called the e allele). Animals with ED/ED genotype are black, animals with ED/e genotype are black and animals with e/e genotype are red. If you have a red animal, you know its genotype is e/e, whereas a black animal is either ED/ED or ED/e genotype.
Let’s say you have a herd of 250 red cattle and you bring one black bull into the herd to start crossbreeding. If the bull breeds successfully and is homozygous ED/ED genotype his offspring will all be black; if the bull is heterozygous ED/e genotype half of his calves will be black and half will be red. The black gene will increase in the herd over subsequent generations if you don’t cull or select against black animals. That’s pretty simple genetics with one dominant gene determining a trait.
This example is similar to the situation with wolves, particularly Mexican wolves. The Mexican wolf is a subspecies listed under the Endangered Species Act (ESA). Subspecies are animal populations in different areas with some level of genetic differences. Because animals move between areas over time, subspecies are not definite and scientists don’t agree on their validity (see the WLJ articles in the References at the bottom). The Mexican wolf population was started with seven animals in captivity that supplied wolves that were introduced to the wild in Arizona and New Mexico. A breeding program was set up to minimize inbreeding in the captive wolves.
Wolves in the Rocky Mountain states are usually gray or black with color determined by a gene called K. The black K gene is dominant; K/K and K/k genotypes are black color and k/k genotypes are gray color. There is research showing the black K gene is selected in some wild wolves where gray wolves preferentially mate with black wolves and K/k genotypes have greater resistance to canine distemper. The K gene also gives black coat color in dogs. There are no black wolves in the current Mexican population.
Wolves, including gray and black animals, were recently brought into Colorado from Oregon and there is the potential for these wolves to disperse into neighboring New Mexico and Arizona where they could interbreed with Mexican wolves. The wolves in Colorado are northern wolves which is a different subspecies than the Mexican wolf. This wouldn’t be a problem except the Mexican wolf has been protected by the ESA as a genetically unique subspecies. The introduction of the black K gene into the Mexican wolf population, which currently does not have the black K gene, would increase genetic variation, decrease inbreeding, and probably increase overall population fitness. However, this would also change the genetics of the Mexican subspecies. So, there are conflicting management objectives of maintaining the native gene pool of the Mexican wolf subspecies, or increasing population fitness by introducing new genetics, as with crossbreeding livestock.
I calculated possible changes in the black K gene frequency considering migration of wolves from Colorado into the Mexican wolf population which has about 250 animals. Without selection favoring the black K gene, the K gene frequency increases in ten generations from 0% to 2% with one K/k genotype wolf migrant per generation and from 0% to 4% with one KK genotype migrant per generation (see the calculations in the References). In this scenario, the proportion of black wolves in the Mexican population will be 4% to 8% after 10 generations.
With selection favoring black K/k genotype wolves, migration of only one wolf from the Colorado population to the Mexican population increases the black K gene from 0% to 1% in one or two generations. Other analyses show the black K gene will then increase in 10 generations from 1% to a stable level of about 25%, at which time 44% of the population will be black wolves.
This analysis shows that the black K gene could be introduced into Mexican wolves by dispersing northern wolves. It could also be introduced by wolves mating with domestic or feral dogs. This has not been documented in the Mexican wolf population but black wolves or dogs have been reported in the range of Mexican wolves (see the References).
Introduction of the black K gene and other genes from northern wolves would change the genetics of the Mexican wolf subspecies and probably improve its fitness. This is the same genetic process as crossbreeding livestock. Changing the Mexican wolf genetics would be a problem for ESA advocates because the justification of the ESA listing of Mexican wolves is based on its genetic differences from other wolves and changing Mexican wolf genetics could change its subspecies status.
The potential for changing the genetics of the Mexican wolf subspecies raises questions about using subspecies in other ESA listings. Recall that the northern spotted owl and other wildlife have been listed as subspecies under the ESA and caused extensive damage to the natural resource industries and agriculture. Possible migration of the black K gene into Mexican wolves resulting in changing the population’s genetics illustrates the indefinite nature of subspecies and, in my opinion, their inappropriate use in ESA listings. — Dr. Matt Cronin
(Matt Cronin is a biologist with Northwest Biology and Forestry Company LLC in Bozeman, MT, croninm@aol.com. He was a research professor at the University of Alaska. A full list of references can be found below.)
References
Western Livestock Journal Articles
April 2024 Resource Science: Black and gray wolves | Resource Science | wlj.net
August 2023 Resource Science: Possible black wolf sighting in Arizona | Resource Science | wlj.net
March 2023 Resource Science: Predicting the numbers of wolves in Colorado | Resource Science | wlj.net
June 2023 Resource Science: Wolf ESA populations are too complicated | Resource Science | wlj.net
March 2023 Resource Science – Wolves in Colorado: The need for management | Resource Science | wlj.net
November 2023 Resource Science: Wolves in CO and Mexican wolves | Resource Science | wlj.net
May 2023 Resource Science: Draft EIS for introducing wolves to CO | Resource Science | wlj.net
March 2022 Resource Science: Wolves—When north meets south | Top Headlines | wlj.net
April 2021 Resource Science: An assessment of wolf numbers, predation in CO | Top Headlines | wlj.net
Genetics references
Anderson, T.M., B.M. vonHoldt, S.I. Candille, M. Musiani, C. Greco, D.R. Stahler, D.W. Smith, B. Padhukasahasran, E. Randi, and J.A. Leonard. 2009. Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339-1343.
Breck, S.W., B.M. Kluever, M. Panasci, J. Oakleaf, T. Johnson, W.B. Ballard, L. Howery, and D.L. Bergman. 2011. Domestic calf mortality and producer detection rates in the Mexican wolf recovery area: Implications for livestock management and carnivore compensation schemes. Biological Conservation 144:930–936.
Carey, J. 2023. Wolf observation report by Catron County Wildlife Investigator. Catron County, New Mexico Information Investigation Report, Case Number IR-052.
Colorado Parks and Wildlife. 2023. Colorado wolf restoration and management plan. Colorado Parks and Wildlife Department, 6060 Broadway, Denver, CO.
Cooke, R.F., L.R. Mehrkam, R.S. Marques, K.D. Lippolis, and D.W. Bohnert. 2017. Effects of a simulated wolf encounter on brain and blood biomarkers of stress-related psychological disorders in beef cows with or without previous exposure to wolves. J. Anim. Sci. 2017.95:1154–1163. doi:10.2527/jas2016.1250
Cronin, M.A., A. Cánovas, A. Islas-Trejo, D.L. Bannasch, A.M. Oberbauer, and J.F. Medrano. 2015. Wolf Subspecies: Reply to Weckworth et al. and Fredrickson et al. J. Hered. 106:417-419.
Cronin, M.A. 2023. Possible black wolf sighting in Arizona. Western Livestock Journal 101(38):2. August 21, 2023. Resource Science: Possible black wolf sighting in Arizona | Resource Science | wlj.net
Cubaynes, S., E.E. Brandell, D.R. Stahler, D.W. Smith, E.S. Almberg, S. Schindler, R.K. Wayne, A.P. Dobson, B.M. vonHoldt, D.R. MacNulty, P.C. Cross, P.J. Hudson, and T. Coulson. 2022. Disease outbreaks select for mate choice and coat color in wolves. Science 378:300-303.
Darwin, C. 1859. On the origin of species by means of natural selection, or preservation of favoured races in the struggle for life. John Murray, London.
Ehrlich, P.R. 2000. Human natures. Island Press, Washington, DC.
Falconer, D.S. 1989. Introduction to quantitative genetics. 3rd ed. Wiley, New York.
Fitak, R.R., S.E. Rinkevich, and M. Culver. 2018. Genome-wide analysis of SNPs is consistent with no domestic dog ancestry in the endangered Mexican wolf (Canis lupus baileyi). J. Hered. 109:372-383.
Fredrickson, R., P.W. Hedrick, R.K. Wayne, B.M. vonHoldt, and M. Phillip. 2015. Mexican wolves are a valid subspecies and an appropriate conservation target. J. Hered. 106:415-416. https://doi.org/10.1093/jhered/esv02.
Fredrickson, R., P. Siminski, M. Woolf, and P.W. Hedrick. 2007. Genetic rescue and inbreeding depression in Mexican wolves. Proc. R. Soc. B. 274:2365–2371. doi:10.1098/rspb.2007.0785
Hay, E.H., and A. Roberts. 2023. Genomic analysis of heterosis in an Angus X Hereford cattle population. Animals. 13:191. https://doi.org/10.3390/ani13020191
Hedrick, P.W., D.W. Smith, and D.R. Stahler. 2016. Negative-assortative mating for color in wolves. Evolution. 70:757-766.
Hedrick, P.W., R.K. Wayne, and R. Fredrickson. 2018. Genetic rescue, not genetic swamping, is important for Mexican wolves. Biol. Conserv. 224:366-367. http://dx.doi.org/10.1016/j.biocon.2018.05.006.
Jimenez, M.D., E.E. Bangs, D.K. Boyd, D.S. Smith, S.A. Becker, D.E Ausband, S.P. Woodruff, E.H. Bradley, J. Holyan, and K. Laudon. 2017. Wolf dispersal in the Rocky Mountains, western United States: 1993-2008. J. Wildl. Manage. 81:581-592.
Justice-Allen, A., and M.J. Clement. 2019. Effect of canine parvovirus and canine distemper virus on the Mexican wolf (Canis lupus baileyi) population in the USA. J. Wildlife Diseases 55:682–688.
MacNeil, M.D. 2009. Research contributions from 75 years of breeding Line 1 Hereford cattle at Miles City, Montana. J. Anim. Sci. 87:2489–2501. doi:10.2527/jas.2009-1909.
Mech, L.D., S.M. Barber-Meyer, and J. Erb. 2016. Wolf (Canis lupus) generation time and proportion of current breeding females by age. PLoS ONE 11 (6): e0156682. doi:10.1371/journal.pone.0156682.
Odell, E.A., J.R. Heffelfinger, S.S. Rosenstock, C.J. Bishop, S. Liley, A. Gonzalez-Bernal, J.A. Velasco, and E. Martinez-Meyer. 2018. Reply to Hedrick et al.: The role of genetic rescue in Mexican wolf recovery. Biol. Conserv. 224:368-369. https://doi.org/10.1016/j.biocon.2018.05.010.
Schweizer, R.M., A. Durvasula, J. Smith, S.H. Vohr, D.R. Stahler, M. Galaverni, O. Thalmann, D.W. Smith, E. Randi, E.A. Ostrander, R.E. Green, K.E. Lohmueller, J. Novembre, and R.K. Wayne. 2018. Natural selection and origin of a melanistic allele in North American gray wolves. Mol. Biol. Evol. 35:1190–1209. doi:10.1093/molbev/msy031.
U.S. Fish and Wildlife Service. 2023. Final Environmental Impact Statement – Colorado gray wolf 10(j) Rulemaking. September 2023. U.S. Fish and Wildlife Service, Prepared by WSP USA Inc., Greenwood Village, CO 80111. Final Environmental Impact Statement – Colorado gray wolf 10(j) | FWS.gov.
Weckworth, B., N. Dawson, S. Talbot, and J. Cook. 2015. Genetic distinctiveness of Alexander Archipelago wolves (Canis lupus ligoni): reply to Cronin et al. (2015). J. Hered. 106:412-414. doi: 10.1093/jhered/esv02
Calculations for the K gene (M. A. Cronin)
Methods
I estimated K-locus gene frequencies in the Mexican wolf population with migration of northern wolves considering general migration (Falconer 1989):
Equation 2.1: q1 = m(qm – q0) + q0
Equation 2.2: ∆q = m(qm – q0)
Where the migration rate m = 0.004 represents one migrant into the wild Mexican wolf population which is comprised of approximately 250 animals; q0 = the K allele frequency in the population receiving a migrant before migration, qm = the K allele frequency in the migrant population; and q1 = the K allele frequency in the population receiving a migrant after one generation of migration. Separate analyses were done considering one random migrant from a northern wolf population with qm = 0.253 as observed for Yellowstone wolves (Hedrick et al. 2016); qm = 0.5 considering one Kk genotype migrant; and qm = 1.0 considering one KK genotype migrant. ∆q x 10 = q10 is the K allele frequency after ten generations with one migrant/generation. Generation time in wolves is approximately four years (Mech et al., 2016).
Analysis of migration of one migrant in one generation followed by assortative mating and selection involved estimating genotype frequencies and allele frequencies after migration, after assortative mating, and after selection with equations 1a, 1b, and 2, and data for wolves in Yellowstone National Park from Hedrick et al. (2016) considering one migrant with genotype kk, Kk, or KK where:
P = frequency of kk genotypes, H = frequency of Kk heterozygotes, Q = frequency of KK homozygotes,
p = the k allele frequency and q = the K allele frequency,
p = P + H/2; q = H/2 + Q,
P’ H’ Q’ = genotype frequencies after assortative mating,
P’’ H’’ Q’’ = genotype frequencies after selection (after assortative mating),
w = sum of progeny of P, H, and Q,
w’ = sum of progeny after assortative mating.
The expected proportions of genotypes in progeny of the observed genotypes with assortative mating A = 0.43, and selection coefficients kk genotype s1 = 0.221 and KK genotype s2 = 0.987 are calculated with:
Assortative mating, Equation 1a:
w = 1 – A(P2 + ¼ H2 + qH + q2)
Assortative mating, Equation 1b:
P’ = [p2 – A(P2 + ¼ H2)]/w
H’ = (2pq – Aq H)/w
Q’ = [q2(1 – A)]/w
Selection, Equation 2:
w’ = 1 – s1P’ – s2Q’
P’’ = P’ (1 – s1)/w’
H’’ = H’/w’
Q’’ = Q’ (1 – s2)/w’
P’’, H’’, and Q’’ are the expected genotypes of progeny in the first generation (G1) following assortative mating and selection of the observed genotypes in G0. The quantities above were recalculated for a second generation (G2) of assortative mating, and selection, using P’’, H”, and Q’’ as beginning P, H, and Q for the case in which the original migrant was Kk genotype.
Results
For general migration without assortative mating or selection the K allele frequency increases from q0 = 0.000 to q1 = 0.001 and q10 = 0.010 with one random northern wolf migrant/generation (qm = 0.253 observed for Yellowstone wolves); from q0 = 0.000 to q1 = 0.002 and q10 = 0.020 with one Kk genotype migrant/generation (qm = 0.5); and from q0 = 0.000 to q1 = 0.004 and q10 = 0.040 with one KK genotype migrant/generation (qm = 1.0, Table 1). In this scenario without selection or assortative mating and assuming Hardy-Weinberg conditions, the proportion of black wolves (i.e., Kk heterozygotes + KK homozygotes = 2p10q10 + q102), after ten generations is 0.020 with random migrants, 0.040 with Kk genotype migrants, and 0.078 with KK genotype migrants.
Migration of one wolf from the northern population to the Mexican population followed by assortative mating (proportion of negative assortative mating A = 0.43) and selection against kk (selection coefficient s1 = 0.221) and KK (s2 = 0.987) homozygotes (Hedrick et al. 2016) results in no change in q if the migrant is kk genotype (q” = 0.000), q increasing from 0.000 to q” = 0.005 if the migrant is Kk genotype, and q increasing from 0.000 to q” = 0.009 if the migrant is KK genotype (Table 2). A second generation of assortative mating and selection considering only an original migrant with Kk genotype (i.e., without new migrants) increases q to q” = 0.010 (Table 2). In this scenario with assortative mating and selection, the proportions of Kk heterozygotes + KK homozygotes (i.e., black wolves, genotypes H’’ + Q’’, Table 2) after one generation is 0.000 with a kk genotype migrant, 0.009 with a Kk genotype migrant, and 0.018 with a KK genotype migrant.
These results indicate that with negative assortative mating and selection, the K allele frequency q is approximately 0.01 after one generation with one KK migrant and after two generations with one Kk migrant. Hedrick et al. (2016) show that with an initial q = 0.01, q will increase to an equilibrium value of 0.242 in ten generations, and there is a high probability of successful introgression when the K allele is introduced into a population. This would be the case if the conditions of migration, assortative mating and selection analyzed here occur in the Mexican wolf population.
Discussion
Both scenarios, general migration of one migrant/generation without assortative mating and selection, and one migrant with assortative mating and selection, result in introgression of the K allele into the Mexican wolf population. The actual frequency of an introduced K allele in the Mexican wolf population could be affected by factors other than those considered here. For example, migration rates will vary under different conditions and canine distemper has occurred in Mexican wolves (Justice-Allen and Clement, 2019) which affects the fitness of K-locus genotypes (Cubaynes et al., 2022).
The K allele could also be introduced into Mexican wolves via hybridization with domestic or feral dogs as with the original introgression of the K allele into North American wolves. This apparently has not occurred in the extant Mexican wolf population (Fitak et al., 2018) although black canids have been reported in the range of Mexican wolves (J. Carey personal communication, Carey, 2023, Cronin, 2023).
Introgression of the K allele, and alleles at other loci, from the northern wolf subspecies would change the gene pool of the Mexican wolf subspecies and probably enhance its fitness. Whether this would be a positive impact by increasing fitness or a negative impact by changing the gene pool of the Mexican wolf has been discussed (Hedrick et al. 2018; Odell et al. 2018, U.S. Fish and Wildlife Service, 2023:4-38 to 4-40). Alteration of a subspecies gene pool could change its degree of genetic differentiation from other subspecies which is potentially important because of the ESA focus on genetic differentiation of subspecies, despite their indefinite nature (see Cronin et al., 2015, Fredrickson et al., 2015, Weckworth et al., 2015). Indeed, the plains wolf subspecies (C. l. nubilus) was native to the northern Rocky Mountain states but the northern wolf subspecies (C. l. occidentalis) was transplanted into, and now occupies, this region. These considerations illustrate the complexities of using subspecies designations in endangered species management.
Acknowledgements
L. D. Mech, J. Rabe, S. Cubaynes, J. Carey, and J. Heffelfinger for providing data and information on Yellowstone and Mexican wolves. G. Chorak and reviewers provided comments on the manuscript. Luke Cronin assisted with data analysis.
