John L. Hoogland

Population genetics meets behavioral ecology.

Populations are often composed of more than just randomly mating subpopulations - many organisms from social groups with distinct patterns of mating and dispersal. Such patterns have recieved much attention in behavioral ecology, yet theories of population genetics rarely take social structures into account. Consequently, population geneticists often report high levels of apparent in breeding and concomitantly low efective sizes, even for species that avoid mating between close kin. Recently, a view of gene dynamics has been introduced that takes dispersal and social structure into account. Accounting for social structure in population genetics leads to a different perspective on how genetic variation is partitoned and the rate at which genic diversity is lost in natural populations - a view that is more consistent with observed behaviors for the minimization of inbreeding.

Prairie dogs avoid extreme inbreeding.

Black-tailed prairie dogs (Rodentia: Sciuridae: Cynomys ludovicianus) live in colonies composed of contiguous but separate family groups called coteries. During the 6 years that individuals in a colony were observed, they almost nevermated with close genetic relatives. Inbreeding is avoided in four ways: (i) a young male usually leaves his natal coterie before breeding, but his female relatives remain; (ii) an adult male usually leaves his breeding coterie before his daughters mature; (iii) a young female is less likely to come into estrus if her father is in her coterie; and (iv) an estrous female behaviorally avoids mating with a father, son, or brother in her coterie.

The Evolution of Coloniality in White-tailed and Black-tailed Prairie Dogs (Sciuridae: Cynomys Leucurus and C. Ludovicianus)

In a 6—yr study, I investigated possible selective bases for coloniality in two species of squirrels (Sciuridae): loosely colonial White—tailed Prairie Dogs (Cynomys leucurus) and densely colonial Black—tailed Prairie Dogs (C. ludovicianus). White—tail study sites were in Wyoming and Colorado, USA; Black—tail study sites were in Colorado and South Dakota. I examined three hypotheses that might explain the evolution of coloniality: (a) shortage of suitable habitat, (b) social facilitation of foraging, and (c) reduced predation. The apparent surplus of unused suitable habitat and the absence of isolated individuals both indicated that prairie dogs are not forced to live together because of habitat shortages. An analysis of prairie dog foraging patterns indicated that there is no social facilitation of foraging in terms of either (a) group hunting of either large or elusive prey, (b) the location of large, scattered food supplies, (c) modification of the soil in order to effect the growth of vegetation that is more favorable or more abundant than that which would otherwise result, or (d) group defense of foraging grounds. Three lines of evidence indicate that reduced predation may be the most important benefit of prairie dog coloniality. First, simulated predatory attacks by badgers (Taxidea taxus) indicated that individuals in large wards (subcolonies) detect predators more quickly than do individuals in smaller wards; further, Black—tails detect predators more quickly than do White—tails. Second, individuals in large wards devote proportionately less time to alertness (i.e., scanning for predators) than do individuals in smaller wards, and Black—tails are less vigilant than are White—tails. Third, breeding synchronization and center—edge differences in individual alertness both indicate the possible importance of self herd effects. Interspecific differences in ward size and ward density may ultimately result because White—tail habitats contain significantly more protective cover than do Black—tail habitats.

Infanticide in prairie dogs: lactating females kill offspring of close kin.

Infanticide, although common in a wide range of species including humans and other primates, is poorly understood. A 7-year study under natural conditions reveals that infanticide within colonies of black-tailed prairie dogs (Cynomys ludovicianus) is striking for three reasons. It is the major source of juvenile mortality, accounting for the total or partial demise of 51 percent of all litters born. The most common killers are resident lactating females. The most common victims are the offspring of close kin.

Nepotism and alarm calling in the black-tailed prairie dog (Cynomys ludovicianus)

Abstract At a colony containing 200 individuals of known ages and genetic relationships, I investigated alarm calling by black-tailed prairie dogs (Rodentia: Sciuridae: Cynomys ludovicianus ) during experiments with a stuffed specimen of a natural predator, the badger ( Taxidea taxus ). As in other species of burrowing squirrels, female alarm calls are evidently nepotistic (i.e. function to warn genetic relatives). Male alarm calls are also nepotistic, and individual males vary their rate of alarm calling in response to the presence or absence of close genetic relatives in the home territory. Beneficiaries of alarm calls in other species of squirrels usually include adult or juvenile offspring, but beneficiaries of black-tailed prairie dog alarm calls frequently include only non-descendant kin.

DO BLACK-TAILED PRAIRIE DOGS MINIMIZE INBREEDING ?

Considerable controversy surrounds the importance of inbreeding in natural populations. The rate of natural inbreeding and the influences of behavioral mechanisms that serve to promote or minimize inbreeding (e.g., philopatry vs. dispersal) are poorly understood. We studied inbreeding and social structuring of a population of black‐tailed prairie dogs (Cynomys ludovicianus) to assess the influence of dispersal and mating behavior on patterns of genetic variation. We examined 15 years of data on prairie dogs, including survival and reproduction, social behavior, pedigrees, and allozyme alleles. Pedigrees revealed mean inbreeding coefficients (F) of 1–2%. A breeding‐group model that incorporated details of prairie dog behavior and demography was used to estimate values of fixation indices (F‐statistics). Model predictions were consistent with the minimization of inbreeding within breeding groups (“coteries,” asymptotic FIL = –0.18) and random mating within the subpopulation (“colony,” asymptotic FIS = 0.00). Estimates from pedigrees (mean FIL = –0.23, mean FIS = 0.00) and allozyme data (mean FIL = –0.21, mean FIS = –0.01) were consistent with predictions of the model. The breeding‐group model, pedigrees, and allozyme data showed remarkably congruent results, and indicated strong genetic structuring within the colony (FLS = 0.16, 0.19, and 0.17, respectively). We concluded that although inbreeding occurred in the colony, the rate of inbreeding was strongly minimized at the level of breeding groups, but not at the subpopulation level. The behavioral mechanisms most important to the minimization of inbreeding appeared to be patterns of male‐biased dispersal of both subadults and adults, associated with strong philopatry of females. Incest avoidance also occurred, associated with recognition of close kin via direct social learning within the breeding groups.

Levels of Inbreeding Among Prairie Dogs

Because inbreeding and outbreeding both involve distinct benefits, some optimal level of inbreeding-outbreeding should result under natural conditions. Testing this hypothesis has been difficult, mainly because the detailed pedigrees necessary for defining levels of inbreeding have been unavailable for animals other than humans. A 14-yr study of black-tailed prairie dogs (Cynomys ludovicianus) has shown that individuals avoid extreme inbreeding with close kin such as parents, offspring, and full and half siblings, but they regularly inbreed with more distant kin such as full and half first cousins, full and half first cousins once removed, full and half second cousins, and so on. Previous research with other wild animals has not documented such a high frequency of moderate inbreeding. An examination of five measures of reproductive success failed to reveal inbreeding depression.

Breeding Groups and Gene Dynamics in a Socially Structured Population of Prairie Dogs

Genetic substructuring of a colony of black-tailed prairie dogs ( Cynomys ludovicianus ) was examined using three different sources of information: allozyme alleles, pedigrees, and demography (a “breeding-group” model based on mating and dispersal patterns). Prairie dogs and their social breeding groups (called “coteries”) were studied under natural conditions during a 15-year period. Prairie-dog coteries exhibited substantial genetic differentiation, with 15–20% of the genetic variation occurring among coteries. Mating patterns within the colony approximated random mating, and, thus, mates tended to originate from different coteries. Social groups of black-tailed prairie dogs resulted in genetic substructuring of the colony, a conclusion that was supported by estimates from allozyme alleles and colony pedigrees. Predictions of the breeding-group model also were consistent with and supported by estimates from allozyme and pedigree data. Some methodological problems were revealed during analyses. Although individuals of all ages usually are pooled for biochemical estimates of among-group genetic differentiation, our estimates of among-coterie variation from allozyme data were somewhat higher for young than for older prairie dogs, perhaps due to sampling effects caused by mating patterns and infanticide of offspring. Pedigree estimates of among-coterie genetic differentiation were significantly positive for young prairie dogs, adult females, and adult males. Those estimates were always more accurate for the offspring generation, however, because pedigree data were always more complete for young and genetic differences among coteries were diluted by virtually complete dispersal of males away from their natal coteries.

Variance in male and female reproductive success in a harem-polygynous mammal, the black-tailed prairie dog (Sciuridae: Cynomys ludovicianus)

SummaryBlack-tailed prairie dogs are colonial rodents that live in contiguous social groups called coteries. A typical coterie contains one adult (≧2 years old) male, three or four adult females, and several yearlings and juveniles of both sexes. A large coterie sometimes contains two or more adult males. Using detailed behavioral observations on 164 females (of which 160 copulated) and data from four polymorphic loci from parents and offspring of 121 litters, we examined the black-tail mating system.Most females (101/164=62%) copulated with a single adult male, and only 3 of the 102 litters with ≧2 offspring (3%) showed unequivocal evidence of multiple paternity. Adult males usually copulated with several different adult females.In one-male coteries, females usually copulated exclusively with the resident adult male (RAM) (82/112=73%); this trend was confirmed by electrophoresis of blood smaples. In multimale coteries, each female frequently copulated with at least two different RAMs (28/52=54%); in 4 of 5 multimale coteries (80%) which produced two or more litters whose paternities could be unequivocally resolved by electrophoresis, two different RAMs each sired at least one litter.Of the 164 females, 30 (18%) copulated with both the RAM (or one of the RAMs, in multimale coteries) and an extracoterie adult male, but only 3 (2%) copulated exclusively with an extracoterie adult male. Electrophoresis showed that 9 of 121 litters (7%) were sired by an extracoterie adult male.Intersexual comparisons of annual reproductive success and lifetime reproductive success both indicate that black-tails are polygynous (i.e., that variance in reproductive success is greater for males than for females).

Prairie Dogs: An Ecological Review and Current Biopolitics

Abstract In recent years, people have interpreted scientific information about the black-tailed prairie dog (Cynomys ludovicianus) in various, and sometimes conflicting, ways. Political complexity around the relationship among black-tailed prairie dogs, agricultural interests, and wildlife has increased in recent years, particularly when prairie dogs occur on publicly owned lands leased to private entities for livestock grazing. Some have proposed that estimates of prairie dog (Cynomys spp.) numbers from 1900 are inflated, that prairie dog grazing is not unique (other grazers have similar affects on vegetation), and that prairie dogs significantly reduce carrying capacity for livestock and wildlife. We address all these issues but concentrate on the degree of competition between prairie dogs and ungulates because this motivates most prairie dog control actions. We conclude that the available information does not justify holding distribution and numbers of prairie dogs at a level that is too low to perform their keystone ecological function. We further conclude that it is especially important that prairie dogs be sufficiently abundant on public lands to perform this function.