EVOLUTIONARY RELATIONSHIPS AMONG COLONIES OF COLUMBIAN GROUND SQUIRRELS AS SHOWN BY MITOCHONDRIAL DNA

Mitochondrial DNA (mtDNA) from 71 Columbian ground squirrels (Spermophilus columbianus) collected in 12 locations in western Canada were assayed for restriction-site variation with 10 endonucleases. Five of these endonucleases revealed variant patterns, and the composite genotypes were used to develop a linear transformation series among the mtDNA genotypes. Two of the four clones had a wide distribution, while the remaining two clones were geographically restricted. The mtDNA of Columbian ground squirrels was also compared to two other species of Sciuridae: Richardson's ground squirrels (S. richardsonii) and Arctic ground squirrels (S. parryii). Calculation of divergences from fragment length and restriction-site data indicated that Arctic ground squirrels and Richardson's ground squirrels were more closely related to each other than either was to Columbian ground squirrels. The transformation series among clones within the Columbian ground squirrels was rooted using Richardson's and Arctic ground squirrels as out-groups. From these data, we conclude that the colonization by female founders of Columbian ground squirrel populations occurred after deglaciation along the eastern ranges of the Rocky Mountains, while colonies on the western ranges may have been present before extensive deglaciation occurred, having existed in refugia in northwestern Alberta.     

Regulation of population size: evidence from Columbian ground squirrels

The hypothesis that food resources regulate population size was tested in Columbian ground squirrels, Spermophilus columbianus, from 1981 to 1986 in southwestern Alberta, Canada. Two replicate populations received supplemental food resources from 1981 to 1983, and were subsequently monitored until 1986. Two reference (unmanipulated) populations were monitored throughout the 6 years. During the experiment, dramatic increases in population size of about 500% occurred. After supplementation, spring populations declined by about 20% per year, under conditions that produced stressful shortages of food (as evidenced by significant decreases in body mass of ground squirrels). The demographic process that contributed most to increasing and decreasing experimental populations was production of yearlings, through changes in reproductive success and survival of young. Changes in migration contributed secondarily to changes in population size, and changes in adult survival were least important. While similarities of demographic processes were evident between replicates during population increases, a dramatic decrease in survival of young contributed to population decline at one replicate, and normal levels of reproduction and survival were sufficient to produce a decline in the other replicate. Demographic mechanisms may vary, but population regulation of mammalian populations appears strongly dependent on food resources.     

Measures of gene flow in the Columbian ground squirrel

From analyses of published data and a review of the literature, I studied indirect and direct measures of gene flow among populations of Columbian ground squirrels, Spermophilus columbianus. New analyses were used to examine an allozyme data set (seven polymorphic loci) that had been collected by Zammuto and Millar (1985a) from six populations of ground squirrels that were spread over 183 km. G-tests indicated significant variation in allele frequencies among populations, but F-statistics revealed relatively little population differentiation (average F _ST=0.026). F _ST values were used to estimate rates of gene flow indirectly and indicated fairly high rates of gene flow (average N _e m=13.5). Recorded dispersal distances of individual ground squirrels were fairly short (most<4 km, maximum recorded distance was 8.5 km), and the minimum distance between populations used to create the allozyme data set was about 25 km. Thus, direct dispersal among the populations in the allozyme data set was highly unlikely. Small genetically effective populations may have experienced high rates of migration over short distances (about 43% of adults in local populations were immigrants), however, resulting in homogeneous allele frequencies over the geographic range. This explanation provides an alternative to invoking gene flow in the recent past to explain discrepancies between dispersal distances in the field and homogenization of allele frequencies over large ranges, Mammalian species that have virtually complete dispersal of subadult males from the natal area might be expected to exhibit relatively high rates of gene flow, regardless of actual dispersal distances. Genetically effective populations may be much smaller than more extensive ecological populations and experience higher rates of gene flow.     

Behaviour in a population of Columbian ground squirrels, Spermophilus columbianus columbianus

Field observations and films of laboratory encounters were used to describe and quantify behaviour in a population of Columbian ground squirrels. Activity correlated with ambient temperature. Feeding, the most frequent behaviour, decreased during mid-day whereas other behavioural patterns increased. Squirrels nearly always seemed alert, even during other behavioural patterns. Three of seven vocalizations indicated alarm. Possible adult scent-marking nerver exceeded 1 per cent of above-ground activity and decreased seasonally. Juvenile play was frequent; yearling play became more aggressive and was replaced by aggression by mid-season. Adult aggression rarely involved contact; aggression was most frequent during breeding and lactation among males and females, respectively. The behaviour of this population was similar to that observed in other populations of the same and other sciurids. Most differences cannot be explained without ecological investigation of the other populations.     

The demographic basis of population regulation in columbian ground squirrels

Environmental factors influence the dynamics and regulation of biological populations through their influences on demographic variables, but demographic mechanisms of population regulation have received little attention. We investigated the demographic basis of regulation of Columbian ground squirrel (Spermophilus columbianus) populations under natural and experimentally food-supplemented conditions. Food supplementation caused substantial increases in population density, and population densities returned to pretreatment levels when the supplementation ended. Control (untreated) populations remained relatively stable throughout the study period (1981-1986). Because food resources regulated the size of the ground squirrel populations, we used life-table response experiment (LTRE) analyses to examine the demographic basis of changes in population growth rate and thus also demographic influences on population regulation. LTRE analyses of two food-manipulated populations revealed that changes in age at maturity and fertility rate of females generally made the largest contributions to observed changes in population growth rate. Thus, our results suggested that abundance of food resources regulated the size of our study populations through the effects of food resources on age at maturity and fertility rates. Our results also indicated that different demographic mechanisms can underlie population regulation under different environmental conditions, because lower juvenile survival substantially contributed to population decline, but in only one of the populations. Demographic analyses of experimental data, such as those presented here, offer a rigorous and unambiguous means to elucidate the demographic basis of population regulation and to help identify environmental factors that underlie dynamics and regulation of biological populations.     

Evolution of allometries in the worker caste of Dorylus army ants

We investigated the effect of local environment on the demography and population dynamics of arctic ground squirrels ( Spermophilus parryii plesius ) by comparing reproduction, survival, and population trends of squirrels living in low elevation boreal forest and high elevation alpine tundra sites in southwestern Yukon Territory, Canada. Contrary to the trend for most birds and mammals, reproduction was significantly lower at the lower elevation and females living at higher elevation did not delay the age at which they first reproduced. Even though survival in the boreal forest was lower in summer than in the alpine, it was higher over winter so annual adult female survival was similar between sites.
Sensitivity analysis of model parameters revealed that in the forest, population growth rate (λ) was most sensitive to small changes in adult active season survival whereas for the alpine population, λ was most sensitive to changes in juvenile winter survival. In their respective habitats, these parameters also showed high year to year variation and thus contributed greatly to the population trends observed. Even though ground squirrels persisted in the boreal forest, the measured demographic rates indicate the forest was sink habitat (λ<1) and may have relied on nearby grassy meadows for immigrants. In contrast, the alpine habitat maintained a ground squirrel population in the absence of immigration (λ=1).
The variation in demographic rates between ground squirrels living at high and low elevation may arise from phenotypic responses of squirrels to different habitat structure. Arctic ground squirrels rely on sight to detect predators from a safe distance, and the boreal forest, with its lower visibility and higher predator density, appears to be suboptimal habitat.     

Vocal and Escape Responses of Columbian Ground Squirrels to Simulated Terrestrial and Aerial Predator Attacks

Most ground-dwelling sciurids emit nonrepetitive and repetitive calls in response to predators. In this study, I simulated terrestrial (badger Taxidea taxus) and aerial (flying disc) predator attacks to elicit escape and vocal responses in Columbian ground squirrels (Spermophilus columbianus). In response to the badger, ground squirrels often ran, but rarely to a burrow, and were most likely to give nonrepetitive calls before running or without running; rarely did they enter burrows. Ground squirrels in direct line of the flying disc (i.e., “target” squirrels under “attack”), ran to, and into, the nearest escape burrow and rarely gave a nonrepetitive call. Squirrels distant from the flying disc often called, usually while running or after assuming an upright posture at the nearest burrow. These results suggest that ground squirrels incur little cost when calling in response to aerial predators. Nonrepetitive and repetitive calling in response to the badger and flying disc did not differ significantly among age-sex classes; however, parous females were more likely than nonparous females to give both types of calls in response to the badger. Nonparous females either with or without close nondescendant kin rarely called in response to the badger. Thus, there was no indication that females exposed to the badger behaved nepotistically toward close kin other than their juvenile offspring. Nonrepetitive calling in response to the badger apparently functions primarily to warn vulnerable offspring and, hence, is a component of maternal investment. Although the occurrence of antipredator calling in response to the flying disc did not vary significantly among parity-kin classes, there was evidence that adult and yearling females were more likely to emit repetitive, and to a lesser extent, nonrepetitive calls, if close nondescendant kin were in the colony. I conclude that indirect fitness benefits, that is, kin selection, probably contributes to the maintenance of antipredator calling in response to aerial predators.     

Managing anabolic steroids in pre-hibernating Arctic ground squirrels: obtaining their benefits and avoiding their costs

Androgens have benefits, such as promoting muscle growth, but also significant costs, including suppression of immune function. In many species, these trade-offs in androgen action are reflected in regulated androgen production, which is typically highest only in reproductive males. However, all non-reproductive Arctic ground squirrels, irrespective of age and sex, have high levels of androgens prior to hibernating at sub-zero temperatures. Androgens appear to be required to make muscle in summer, which, together with lipid, is then catabolized during overwinter. By contrast, most hibernating mammals catabolize only lipid. We tested the hypothesis that androgen action is selectively enhanced in Arctic ground squirrel muscle because of an upregulation of androgen receptors (ARs). Using Western blot analysis, we found that Arctic ground squirrels have AR in skeletal muscle more than four times that of Columbian ground squirrels, a related southern species that overwinters at approximately 0°C and has low pre-hibernation androgen levels. By contrast, AR in lymph nodes was equivalent in both species. Brain AR was also modestly but significantly increased in Arctic ground squirrel relative to Columbian ground squirrel. These results are consistent with the hypothesis that tissue-specific AR regulation prior to hibernation provides a mechanism whereby Arctic ground squirrels obtain the life-history benefits and mitigate the costs associated with high androgen production.     

Ground squirrel sociality and the quest for the 'holy grail': does kinship influence behavioral discrimination by juvenile Columbian ground squirrels?

Research on social discrimination by ground-dwelling squirrelshas focused on die ability of squirrels to discriminate kinfrom nonkin. The predominant mechanism underlying that abilityis social familiarization. Although familiarity-based mechanismsmay result in kin discrimination where kin are associated reliablyin space and time, past investigations have largely ignoredadditional levels of social discrimination that may result fromongoing familiarization in the natural context Here we presentdata from a cross-fostering experiment that examines the relativecontributions of rearing association and relatedness to subsequentbehavioral discrimination among juvenile Columbian ground squirrels(Spermophilus columbianus). Rearing association significantlyinfluenced recognitive and agonistic behavior among juvenileswhile relatedness proved insignificant in affecting behavioralinteractions. Thus, direct familiarization in the natal burrowis both sufficient and necessary to account for the transitiveappearance of kin-differential behavior among newly emergedjuveniles documented in previous studies. Reanalyses of datafrom field experiments on S. columbianus social discriminationfail to detect any evidence of kin-biased behavior, and evidencefrom studies purporting to document kinship effects is equivocalat best Taken together with more recent findings, the scantdata suggestive of kin discrimination by Columbian ground squirrelsare best viewed as an artifact of selection promoting the discriminationof familiar from unfamiliar individuals at the level of localizedgroups. Fitness payoffs of such discrimination may accrue viareciprocal altruism, or ‘dear-enemy’ recognition,and would promote the evolution and maintenance of socialitywithout recourse to indirect components of inclusive fitnesscommonly invoked to explain ground squirrel sociality. Finally,our data call into doubt the notion that mechanisms allowingthe direct assessment of kinship should be common among themore social sciurids.     

Sociality of Columbian ground squirrels in relation to their seasonal energy intake

Summary Seasonal energy intake was estimated for ten populations of Columbian ground squirrels (Spermophilus columbianus) in northwestern Montana. We calculated daily energy intake for an average ground squirrel in each population using measurements of feeding time, consumption rates of different vegetation types (monocots vs. dicots), and the proportion of monocots and dicots in the diet. These daily energy intakes were multiplied by the length of the plant growing season for each population to estimate seasonal energy intake, i.e. over the ground squirrel active season. Amicable interaction rates measured for each population varied with seasonal energy intake, but not with environmental heterogeneity, sex ratio, or the ratio of adults to juveniles. In particular, amicable interactions among adult-juvenile and juvenile-juvenile pairs increased as seasonal energy intake decreased. The proportion of females breeding as yearlings increased as seasonal energy intake increased. This suggests that harsh environments reduce the energy available for juvenile growth and development, leading to delayed dispersal and age at first reproduction. These responses may promote the formation of kin groups and increased amicable interactions within those groups. The length of the plant growing season may determine environmental harshness across elevational gradients, but at a particular elevation, harshness may depend on factors determining daily food intake.     

Individual variation in the ability of Columbian ground squirrels to select an optimal diet

Summary Columbian ground squirrels (Spermophilus columbianus) were examined for ability to select a diet that maximizes daily energy intake (optimal diet) under free-living field conditions. The optimal diet for each squirrel was determined given constraints (e.g. body size, feeding time) on individual foraging behavior. Most squirrels (63%) consumed a diet not significantly different from one that would maximize their daily energy intake. The remainder (37%) approached an energy maximized diet but appeared to make some incorrect foraging decisions. Both males and females appeared to approach energy maximized diets. An individual's deviation from its optimal diet is relatively constant within a season and not significantly affected by immediate environmental influences such as food abundance, thermal conditions and social environment. The energy cost of deviating from an optimal diet may be large enough to affect fitness. These results suggest that the ability to select an optimal diet can be viewed as a behavioral trait that might be subject to natural selection.     

Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis)

Mammal species characterized by highly fluctuating populations often maintain genetic diversity in response to frequent demographic bottlenecks, suggesting the ameliorating influence of life history and behavioral factors. Immigration in particular is expected to promote genetic recovery and is hypothesized to be the most likely process maintaining genetic diversity in fluctuating mammal populations. Most demographic bottlenecks have been inferred retrospectively, and direct analysis of a natural population before, during, and after a bottleneck is rare. Using a continuous 10-year dataset detailing the complete demographic and genetic history of a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis), we analyzed the genetic consequences of a 4-year demographic bottleneck that reduced the population to seven adult squirrels, and we evaluated the potential “rescue effect” of immigration. Analysis of six microsatellite loci revealed that, while a decline in allelic richness was observed during the bottleneck, there was no observed excess of heterozygosity, a characteristic bottleneck signature, and no evidence for heterozygote deficiency during the recovery phase. In addition, we found no evidence for inbreeding depression during or after the bottleneck. By identifying immigrants and analyzing their demographic and genetic contributions, we found that immigration promoted demographic recovery and countered the genetic effects of the bottleneck, especially the loss of allelic richness. Within 3 years both population size and genetic variation had recovered to pre-bottleneck levels, supporting the role of immigration in maintaining genetic variation during bottleneck events in fluctuating populations. Our analyses revealed considerable variation among analytical techniques in their ability to detect genetic bottlenecks, suggesting that caution is warranted when evaluating bottleneck events based on one technique.     

Isolation and characterization of microsatellite markers in hoary marmots (Marmota caligata)

Microsatellite loci were developed from hoary marmots (Marmota caligata) to aid in the investigation of the social structure and mating system of this species. Seven of the microsatellite loci developed were found to be moderately polymorphic with between two and seven alleles per locus. In addition to the microsatellites developed in hoary marmots we also tested markers developed for other scuirids, namely European alpine marmots (M. marmota), Columbian ground squirrels (Spermophilus columbianus) and European ground squirrels (S. citellus). Of these markers, 13 were polymorphic when amplified in hoary marmots with between two and nine alleles per locus.     

Fitness implications of seasonal climate variation in Columbian ground squirrels

The influence of climate change on the fitness of wild populations is often studied in the context of the spring onset of the reproductive season. This focus is relevant for climate influences on reproductive success, but neglects other fitness‐relevant periods (e.g., autumn preparation for overwintering). We examined variation in climate variables (temperature, rainfall, snowfall, and snowpack) across the full annual cycle of Columbian ground squirrels (Urocitellus columbianus) for 21 years. We investigated seasonal climate variables that were associated with fitness variables, climate variables that exhibited directional changes across the study period, and finally observed declines in fitness (?0.03 units/year; total decline = 37%) that were associated with directional changes in climate variables. Annual fitness of adult female ground squirrels was positively associated with spring temperature (r = 0.69) and early summer rainfall (r = 0.56) and negatively associated with spring snow conditions (r = ?0.44 to ?0.66). Across the 21 years, spring snowmelt has become significantly delayed (r = 0.48) and summer rainfall became significantly reduced (r = ?0.53). Using a standardized partial regression model, we found that directional changes in the timing of spring snowmelt and early summer rainfall (i.e., progressively drier summers) had moderate influences on annual fitness, with the latter statistically significant (ρ = ?0.314 and 0.437, respectively). The summer period corresponds to prehibernation fattening of young and adult ground squirrels. Had we focused on a single point in time (viz. the onset of the breeding season), we would have underestimated the influences of climate change on our population. Rather, we obtained a comprehensive understanding of the influences of climate change on individual fitness by investigating the full lifecycle.     

Replicated population divergence caused by localized coevolution? A test of three hypotheses in the red crossbill‐lodgepole pine system

Several lines of evidence support the hypothesis that local populations of red crossbills (Loxia curvirostra complex) enter into a predator-prey arms race with lodgepole pine (Pinus contorta latifolia) in the absence of competing pine squirrels (Tamiasciurus hudsonicus). Nevertheless, the alternative hypotheses that neutral evolution or factors other than squirrels have caused crossbill population differentiation have not been thoroughly tested. We compared crossbill and pine cone morphology between island populations where squirrels are absent or present, and mainland sites where squirrels are present, in order to distinguish among these hypotheses. All comparisons supported an effect of squirrel absence, not island status, on crossbill and cone morphology. Hence our results provide further evidence that strong localized coevolutionary interactions in a geographic mosaic have driven adaptive population differentiation. In addition, vocal differentiation of crossbills was related to the absence of squirrels, but not to island status. As morphological and vocal differentiation is correlated with reproductive isolation in crossbills, the geographic mosaic of coevolution also seems to promote ecological speciation.     

Genetic diversity and population divergence in fragmented habitats: Conservation of Idaho ground squirrels

The Idaho ground squirrel, which consists of a northern (Spermophilus brunneus brunneus) and a southern subspecies (S. b. endemicus), has suffered from habitat loss and fragmentation, resulting in a reduction in both numbers and geographic range of the species. The northern Idaho ground squirrel (NIDGS) is listed as a threatened subspecies under the Endangered Species Act, and the southern Idaho ground squirrel (SIDGS) is a candidate. Because Idaho ground squirrel populations are small and often isolated, they are susceptible to inbreeding and loss of genetic diversity through drift. This research evaluates levels of genetic diversity and patterns of population divergence in both subspecies of Idaho ground squirrels. We hypothesized that NIDGS would exhibit lower genetic diversity and greater population divergence due to a longer period of population isolation relative to most SIDGS populations. Genetic diversity and divergence were quantified using 8 microsatellite loci. Contrary to expectations, SIDGS populations exhibited consistently lower levels of microsatellite diversity. Additionally, NIDGS exhibited only modest divergence among populations, while divergence levels among SIDGS populations were highly varied. Preliminary evaluations of mitochondrial DNA diversity and structure revealed lower diversity in NIDGS and some differences in gene flow that warrant further study. Based on our results, we suggest different management strategies for the two subspecies. Habitat restoration appears to be the most desirable conservation strategy for NIDGS populations. In contrast, low genetic diversity observed in SIDGS may warrant supplementation of isolated populations through translocations or captive breeding to mitigate further loss of genetic variability.     

Size increase in high elevation ground squirrels over the last century

There is increasing evidence for morphological change in response to recent environmental change, but how this relates to fluctuations in geographic range remains unclear. We measured museum specimens from two time periods (1902–1950 and 2000–2008) that vary significantly in climate to assess if and how two high elevation contracting species of ground squirrels in the Sierra Nevada of California, Belding's ground squirrel (Urocitellus beldingi) and the golden‐mantled ground squirrel (Callospermophilus lateralis), and one lower elevation, stable species, the California ground squirrel (Otospermophilus beecheyi), have responded morphologically to changes over the last century. We measured skull length (condylobasal length), an ontogenetically more labile trait highly correlated with body size, and maxillary toothrow length, a more developmentally constrained trait predictive of skull shape. C. lateralis and U. beldingi, both obligate hibernators, have increased in body size, but have not changed in shape. In contrast, O. beecheyi, which only hibernates in parts of its range, has shown no significant change in either morphometric trait. The increase in body size in the higher elevation species, hypothesized to be a plastic effect due to a longer growing season and thus prolonged food availability, opposes the expected direction of selection for decreased body size under chronic warming. Our study supports that population contraction is related to physiological rather than nutritional constraints.     

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.     

Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions

We studied daily rhythmicity of body temperature (T _b) before and during hibernation in Anatolian ground squirrels (Spermophilus xanthoprymnus) under natural and laboratory conditions using surgically implanted temperature loggers. Under both conditions, robust daily T _b rhythmicity with parameters comparable to those of other ground squirrel species was observed before but not during hibernation. Euthermic animals had robust daily T _b rhythms with a mean of 37.0°C and a range of excursion of approximately 4°C. No T _b rhythm was detected during torpor bouts, either because T _b rhythmicity was absent or because the daily range of excursion was smaller than 0.2°C. The general patterns of hibernation that we observed in Anatolian ground squirrels were similar to those previously observed by other investigators in other species of ground squirrels.     

Increasing returns in the life history of Columbian ground squirrels

1. We examined positive associations and trade-offs of maternal and reproductive traits in a population of Columbian ground squirrels, Spermophilus columbianus .
2. Structural size, body condition, mother's personal allocation to body mass during reproduction, and timing of littering were estimated for live-trapped reproductive females that were observed during an 8-year period, and were compared to litter mass, litter size, and average pup mass using path analyses.
3. Mothers exhibited age-structured traits that influenced reproductive patterns. Yearling mothers were significantly smaller, bred later, and had smaller litters than older females. Mothers that gained more body mass during reproduction and older mothers in good body condition that were structurally large had larger litters.
4. Early seasonal timing of littering was an important positive influence on successful reproduction by older mothers only in early breeding seasons and in years when conditions for reproduction were good for all females.
5. The number of offspring that survived to 1 year of age was most strongly associated with litter mass and litter size; date of breeding was of secondary influence, with earlier litters exhibiting greater success.
6. In general, mothers that gained the most in body mass during reproduction were concurrently more successful in weaning large litters (perhaps due to better quality of foraging habitat).
7. In addition to expected reproductive trade-offs, reproduction by Columbian ground squirrels exhibited positive associations of life-history traits that may reflect evolutionary increasing returns.