Wolf History, Conservation, Ecology and Behavior

Wolfology Item #257
v8 n4 (1997)

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Is Incest Common in Gray Wolf Packs?
Deborah Smith, Thomas Meier, Eli Geffen, L. David Mech, John W. Burch, Layne G. Adams, Robert K. Wayne
Wolf packs generally consist of a breeding pair and their maturing offspring that help provision and protect pack young. Because the reproductive tenure of wolves is often short, reproductively mature offspring might replace their parents, resulting in sibling or parent-offspring matings. To determine the extent of incestuous pairings, we measured relatedness based on variability of 20 microsatellite loci of mated pairs, parent-offspring pairs, and siblings in two populations of gray wolves...These results suggest that full siblings or a parent and its offspring rarely mate and that incest avoidance is an important constraint on gray wolf behavioral ecology.
Gray wolves (Canis lupus) live in packs that generally contain a breeding pair and their offspring of one or more litters. Additionally, packs in the wild may include siblings or earlier offspring of one of the breeding pair. Some packs may at least temporarily contain unrelated individuals....However, the common elements of all long-established wolf packs are the breeding pair and their offspring.
The origin and genetic relationships of the breeding pair have been the subject of conjecture. Many pairs are formed from individuals that have dispersed from different packs, met, and pair-bonded. Additional ways in which a breeding pair can develop include (1) an unattached lone wolf replaces one of the breeding pair that had dispersed or died; (2) an offspring replaces one of the parents; (3) parents breed with offspring; and (4) siblings breed with each other. Incestuous matings between parent and offspring or among siblings have been recorded in captive wolves and on Isle Royale, Michigan, where wolves have no other choice than to mate with close relatives because of a lack of immigration from the mainland.
Although there has been some speculation, the frequency of incestuous matings in the wild is unknown.... Peterson et al. (1984), Shields (1983), and Theberge (1983) assumed that inbreeding was common in wolves, although they disagreed on its significance or the degree to which it would be detrimental. Mech (1987) held that the high frequency of wolf dispersal would help ensure a high level of outbreeding in wolf packs....In captive wolves, incestuous mating can lead to an inbreeding depression, but it does not always. In the wild, inbreeding can persist for decades without population extinction, although some researchers believe that it may be the reason small populations do not increase in size.
Nonreproductive, maturing wolves generally help provision and protect young, and as reproductive tenure in wolves is often short, helper wolves have a significant chance to reproduce, possibly within their natal pack. Therefore, because of the uncertainty about the origin of breeding wolf pairs and to better understand the role of inbreeding in wold social behavior, we assessed the genetic relatedness of mated pairs in wolf populations whose mortality is minimally affected by humans....
Because microsatellites are abundant in the mammalian genome, many loci can be surveyed and used to accurately measure relatedness. In this survey we studied 20 microsatellite loci in two wolf populations and calculated relatedness between parents and offspring, among siblings and between mated pairs. We predicted that if avoidance of close inbreeding is an important constraint on wolf behavior, then incestuous matings should be uncommon....
We sampled 130 wolves from 25 packs in Denali [National Park and Preserve, Alaska] from 1986 to 1994 and 33 wolves from 6 packs in the [Superior National Forest, Minnesota] from 1988 to 1993....In 10 Denali packs and all SNF packs, the mated or breeding pair was sampled. We anesthetized wolves by darting them from a helicopter (Denali) or by hypodermic injection when caught in traps (SNF). Wolves were fitted with radiocollars and ear tags, and 5-10 ml of blood was drawn....Wolves were located by aerial telemetry at approximately weekly intervals and observed....
....The Denali and SNF populations had been previously analyzed for variability in 10 microsatellite loci and found to be similar in levels of heterozygosity, allelic diversity, and in the equability of allele frequencies. Consequently, estimates for various categories of relatedness should be similar in both populations....
Captive populations. To determine the correspondence of molecular genetic estimates of kinship with known relatedness, we obtained blood samples...from two captive wolf populations with documented geneologies, the Julian pack and the Forest Lake colony. The Julian pack is located in Julian, California, USA, and was founded with two wild-caught individuals thought to be from different locations in central Alaska. We obtained samples from the single mated pair and their nine offspring of different years. The Forest Lake colony is located near Forest Lake, Minnesota, USA, and includes individuals from a large pedigree of wolves with relationships ranging from inbred siblings to unrelated individuals....
Because wolves live in packs that are primarily family units, there is considerable opportunity for incestuous matings and for reproductive succession by helpers. Most adolescent wolves disperse from their natal packs when three years old or less, but some remain longer or disperse only a short distance to nearby packs. Consequently, incestuous matings are possible, especially with the death of one of the mated pair. Instead of dispersing, a young wolf could attempt to challenge a parent for breeding rights. In fact, in other carnivores, subdominants that are excluded by the dominant male from copulation or whose reproduction is hormonally suppressed may produce occasional offspring through sequestered matings or following the death of a dominant individual or a change in the dominance hierarchy. A viable reproductive strategy in wolves might involve subdominant helpers forgoing dispersal for the possibility of direct reproduction within their natal pack ("biders"). However, observed incestuous matings in wolves occur primarily when wolves are prevented from outbreeding, such as in captivity or on Isle Royale. These observations suggest that wolves might breed incestuously only when dispersal opportunities are limited spatially.
We find no evidence in two natural wolf populations that mated pairs are related as parents and offspring or as siblings....In fact, wolf 75 from SNF had three different mates during the period of the study; each time he paired with an unrelated individual rather than related packmates. However, a larger sampling of mated pairs might reveal that some are highly related. The binomial probability that a sample of 16 mated pairs would yield no highly related pairs if their frequency in the population was 20% is only 0.03, but it is 0.19 if their frequency was only 10% in the population. Therefore, the formation of highly related pairs must be relatively rare, but we cannot exclude its possibility or the possibility of incestuous matings of more distantly related individuals.
These results imply an aversion to incestuous matings because wolves have far more opportunities to breed with a sibling or a parent than with an unrelated individual. Such opportunities include replacement of one of the breeding pair or the establishment of new packs by siblings. Breeding tenure is short; a preliminary estimate of mean tenure of breeding wolves in the Denali population is 4 years. Our results suggest that adult offspring rarely replace a parent when the opposite-sex parent is present....
We cannot exclude other possible means by which inbred offspring may be produced in wolf packs. For example, inbreeding could result from multiple paternity due to the union of the breeding female and her mate and a son, from sequestered matings between parents and their offspring, or from matings between siblings. Such incestuous matings would be difficult to detect if they involved the female parent and her son. However, the insemination by one male of both his mate and daughters or matings between siblings would result in multiple litters. In the SNF, multiple litters were observed only rarely, and pack size is small, suggesting this is an uncommon source of inbred offspring. In Denali, packs are larger, and we have observed multiple litters in some packs that were of uncertain paternity, leaving open the possibility of father-daughter or sibling matings in large wolf packs. However, in a preliminary study, none of the 10 adult mated dyads from large packs appears to be related as siblings or as parent-offspring.
In sum, our results show that within wolf packs, mated wolves are rarely related as siblings or as parent-offspring. This observation suggests that in general, wolf packs are established by unrelated or more distantly related wolves. Offspring do not often, if ever, replace either parent unless the opposite-sex parent is first replaced by an unrelated wolf, nor do full siblings often become the breeding pair. Despite frequent opportunities, incestuous reproductive succession is not a common means to attain reproductive success.
Interbreeding avoidance may be one of the primary motivations for individuals to disperse, although ecological and kinship factors critically influence the probability of dispersal. In Minnesota gray wolves, interpack aggression is the largest source of mortality aside from that caused by humans. Consequently, the risks of dispersing and defending a new territority near hostile wolves might be sufficient cause for maturing wolves to remain in their natal pack....
Figure 1: The decrease in the mean difference between consecutive relatedness estimates as a function of the number of microsatellite loci analyzed.
Figure 2: Mean relatedness (R) and SDs for different relationship categories in captive wolves.
Figure 3: Frequency distribution of R values for unrelated and highly related captive wolves.
Figure 4: Mean relatedness (R) and SDs for different relationship categories in wild wolves.
Table 1: Histories and relatedness of bonded wolf pairs in the Superior National Forest, Minnesota.
Table 2: Histories and relatedness of bonded wolf pairs in Denali National Park, Alaska.
References: 53