Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction

eLetter to the Editor: A comment on Robinson et al. 2019. Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

Robinson et al. (1) present genetic and anatomical data that strongly support the hypothesis that inbreeding depression due to homozygosity of deleterious recessive alleles contributed to a severe decline of the wolf (Canis lupus) population on Isle Royale, Michigan.

In their discussion Robinson et al. cited our 2010 paper (2) and stated:
“The persistence of wolves on Isle Royale was once used to support the claim that a very small population in isolation may persist, and even thrive, without succumbing to genetic deterioration (48, Mech and Cronin 2010). During the past few decades, however, Isle Royale wolves have experienced a precipitous decline following generations of inbreeding and physical degeneration.”

However, Mech and Cronin (2) did not state that a small population in isolation could persist "without succumbing to genetic deterioration," and they even cited the findings of Raikkonen et al. (3) that the Isle Royale population had genetically deteriorated. When the Mech and Cronin (2) paper was written, the Isle Royale population had not yet severely declined. They acknowledged that it was inbred with genetic defects, but pointed out that it had persisted for 60 years. Mech and Cronin’s main point was that genetic deterioration and extinction is not the inevitable fate of small isolated populations. Indeed, small isolated populations are the basis of some modes of speciation (e.g., founder speciation, 4:602).

The primary points made by Mech and Cronin (2) are still relevant and warrant consideration. First, a small population can exist in isolation, and it is not inevitable that it will succumb to inbreeding depression. Second, results from one population, such as the wolves on Isle Royale, should not be generalized and uncritically applied to other populations.

We also note a potential conflict in the general topic of wolf conservation: the importance of genetic variation and heterozygosity to maintain fitness; and the importance of local adaptation which might entail selection for some level of homozygosity and not necessarily a high level of variation. Both of these factors are relevant to subspecies such as the Mexican wolf (C. l. baileyi) which are thought to be locally adapted, but may be susceptible to inbreeding problems (5).

Robinson et al. (1) did a good job of empirically testing the hypothesis that inbreeding would reduce fitness and result in negative population effects in Isle Royale wolves (3). However, we repeat our caution that although this can provide guidance for management of other wolf populations, each population should be assessed independently.

References
1. J. A. Robinson, J. Raikkonen, L. M. Vucetich, J. A. Vucetich, R. O. Peterson, K. E. Lohmueller, R. K. Wayne, Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction. Science Advances 5:eeau0757, pages 1-13, (29 May 2019).
2. D. Mech, M. A. Cronin, Isle Royale study affirms ability of wolves to persist. Biol Conserv. 143, 535-536 (2010).
3. J. Raikkonen, J. A. Vucetich, R. O. Peterson, M. P. Nelson, Congenital bone deformities and the inbred wolves (Canis lupus) of Isle Royale. Biol. Conserv. 142, 1027-1033 (2009).
4. E. Mayr, The Growth of Biological Thought (Belknap, Harvard University Press, Cambridge MA, 1982).
5. National Academies of Sciences, Engineering, and Medicine, Evaluating the taxonomic status of the Mexican gray wolf and the red wolf. (National Academies Press, Washington, DC, 2019).

Matthew A. Cronin, Northwest Biology Company LLC, 1038 Saxon Way, Bozeman, MT 59718, croninm@aol.com
and
L. David Mech, U.S. Geological Survey, Northern Prairie Wildlife Research Center, 8711–37th Street SE, Jamestown, ND 58401, USA, mechx002@umn.edu.