Sexes in sync: phenotypic plasticity, sexual selection and phenological synchrony between the sexes in a wild hibernator.

Desynchrony of phenological responses to climate change is a major concern for ecological communities. Potential uncoupling between one of the most fundamental divisions within populations, males and females, has not been well studied. To address this gap, we examined sex-specific plasticity in hibernation phenology in two populations of Columbian ground squirrels (Urocitellus columbianus). We find that both sexes display similar phenological plasticity to spring snowmelt dates in their timing of torpor termination and behavioural emergence from hibernation. As a result of this plasticity, the degree of protandry (i.e. males' emergences from hibernation preceding those of females) did not change significantly over the 27-year study. Earlier male behavioural emergence, relative to females, improved the likelihood of securing a breeding territory and increased annual reproductive success. Sexual selection favouring earlier male emergence from hibernation may maintain protandry in this population, but did not contribute to further advances in male phenology. Together, our results provide evidence that the sexes should remain synchronized, at least in response to the weather variation investigated here, and further support the role of sexual selection in the evolution of protandry in sexually reproducing organisms.

Delayed phenology and reduced fitness associated with climate change in a wild hibernator.

The most commonly reported ecological effects of climate change are shifts in phenologies, in particular of warmer spring temperatures leading to earlier timing of key events. Among animals, however, these reports have been heavily biased towards avian phenologies, whereas we still know comparatively little about other seasonal adaptations, such as mammalian hibernation. Here we show a significant delay (0.47 days per year, over a 20-year period) in the hibernation emergence date of adult females in a wild population of Columbian ground squirrels in Alberta, Canada. This finding was related to the climatic conditions at our study location: owing to within-individual phenotypic plasticity, females emerged later during years of lower spring temperature and delayed snowmelt. Although there has not been a significant annual trend in spring temperature, the date of snowmelt has become progressively later owing to an increasing prevalence of late-season snowstorms. Importantly, years of later emergence were also associated with decreased individual fitness. There has consequently been a decline in mean fitness (that is, population growth rate) across the past two decades. Our results show that plastic responses to climate change may be driven by climatic trends other than increasing temperature, and may be associated with declines in individual fitness and, hence, population viability.

Kin effects on energy allocation in group-living ground squirrels.

The social environment has potent effects on individual phenotype and fitness in group-living species. We asked whether the presence of kin might act on energy allocation, a central aspect of life-history variation. Using a 22-year data set on reproductive and somatic allocations in Columbian ground squirrels (Urocitellus columbianus), we tested the effects of co-breeding and non-breeding kin on the fitness and energy allocation balance between reproduction and personal body condition of individual females. Greater numbers of co-breeding kin had a positive effect on the number of offspring weaned, through the mechanism of altering energy allocation patterns. On average, females with higher numbers of co-breeding kin did not increase energy income but biased energy allocation towards reproduction. Co-breeding female kin ground squirrels maintain close nest burrows, likely providing a social buffer against territorial invasions from non-kin ground squirrels. Lower aggressiveness, lower risks of infanticide from female kin and greater protection of territorial boundaries may allow individual females to derive net fitness benefits via their energy allocation strategies. We demonstrated the importance of kin effects on a fundamental life-history trade-off.

Philopatry and within-colony movements in Columbian ground squirrels.

Philopatry and dispersal result in selection of habitat locations that may differ in resources and social environment and thus should influence fitness components like survival and reproduction. We examined short-distance movements of young and adult females from natal or previous nesting sites within a colony of Columbian ground squirrels (Urocitellus columbianus) in the Rocky Mountains of Alberta, Canada, over a 17-year period. Females of all ages were strongly philopatric, yet a few (10-15%) exhibited movements that took them to new home ranges. We tested three hypotheses to explain the pattern of female natal and breeding movements: (1) that movements of philopatric females promote proximity to close kin; (2) that range shifts favour close kin via bequeathal of territory and (3) that dispersers move to lower density areas where competition for resources is lower. Tests of these three hypotheses revealed that: (1) philopatry and movements of young and older philopatric females led to proximity to mothers and local presence of close kin; (2) breeding dispersal did not result in bequeathal of home range to daughters, but movements of philopatric females suggested that they shared space with close kin and (3) adult females moved to new ranges with lower local densities, though dispersing females also left ranges where local density was significantly lower than for philopatric females. Natal and breeding movements among years produced two opportunities for territorial females: close spatial proximity to close kin via short philopatric movements, and habitats with fewer competitors via longer dispersal movements.

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.

Parental investment in the Columbian ground squirrel: empirical tests of sex allocation models.

Parental allocation of resources into male or female offspring and differences in the balance of offspring sexes in natural populations are central research topics in evolutionary ecology. Fisher (Fisher, R. A. 1930. The genetical theory of natural selection, Clarendon Press, Oxford, UK) identified frequency-dependent selection as the mechanism responsible for an equal investment in the sexes of offspring at the end of parental care. Three main theories have been proposed for explaining departures from Fisherian sex ratios in light of variation in environmental (social) and individual (maternal condition) characteristics. The Trivers-Willard model (Trivers, R., and D. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90-92) of male-biased sex allocation by mothers in the best body condition is based on the competitive ability of male offspring for future access to mates and thus superior reproduction. The local resource competition model is based on competitive interactions in matrilines, as occur in many mammal species, where producing sons reduces future intrasexual competition with daughters. A final model invokes advantages of maintaining matrilines for philopatric females, despite any increased competition among females. We used 29 yr of pedigree and demographic data to evaluate these hypotheses in the Colombian ground squirrel (Urocitellus columbianus), a semisocial species characterized by strong female philopatry. Overall, male offspring were heavier than female offspring at birth and at weaning, suggesting a higher production cost. With more local kin present, mothers in the best condition biased their offspring sex ratio in favor of males, and mothers in poor condition biased offspring sex ratio in favor of females. Without co-breeding close kin, the pattern was reversed, with mothers in the best condition producing more daughters, and mothers in poor condition producing more sons. Our results do not provide strong support for any of the single-factor models of allocation to the sexes of offspring, but rather suggest combined influences of relative maternal condition and matriline dominance on offspring sex ratio.

Kin selection in Columbian ground squirrels (Urocitellus columbianus): littermate kin provide individual fitness benefits.

Since W. D. Hamilton's seminal work on the evolution of sociality, a large body of research has accumulated on how kin selection might explain the evolution of cooperation in many group-living species. Our study examined the evolutionary basis of philopatry and cooperation; specifically, whether individuals benefit from the presence of close kin. We applied an individual fitness approach to a 16-year study of Columbian ground squirrels (Urocitellus columbianus) to investigate potential causal paths by which the presence of kin might act on individual fitness. Our results indicate that individual fitness benefits resulted from associations of philopatric female kin, and support the hypothesis that increased tolerance of proximity of kin is a proximate mechanism for these benefits. The major life-history influence of kin on individual fitness was through improved reproductive success, and this benefit may have been owing to philopatric settlement of kin that were recognized through familiarization in the natal burrow. Thus, we demonstrated an evolutionary basis necessary for ongoing kin-selected cooperation in Columbian ground squirrels, though the mechanism of familiarity may determine which kin individuals benefit from cooperative behaviours.

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.

Testing the reproductive and somatic trade-off in female Columbian ground squirrels.

Energetic trade-offs in resource allocation form the basis of life-history theory, which predicts that reproductive allocation in a given season should negatively affect future reproduction or individual survival. We examined how allocation of resources differed between successful and unsuccessful breeding female Columbian ground squirrels to discern any effects of resource allocation on reproductive and somatic efforts. We compared the survival rates, subsequent reprodction, and mass gain of successful breeders (females that successfully weaned young) and unsuccessful breeders (females that failed to give birth or wean young) and investigated "carryover" effects to the next year. Starting capital was an important factor influencing whether successful reproduction was initiated or not, as females with the lowest spring emergence masses did not give birth to a litter in that year. Females that were successful and unsuccessful at breeding in one year, however, were equally likely to be successful breeders in the next year and at very similar litter sizes. Although successful and unsuccessful breeding females showed no difference in over winter survival, females that failed to wean a litter gained additional mass during the season when they failed. The next year, those females had increased energy "capital" in the spring, leading to larger litter sizes. Columbian ground squirrels appear to act as income breeders that also rely on stored capital to increase their propensity for future reproduction. Failed breeders in one year "prepare" for future reproduction by accumulating additional mass, which is "carried over" to the subsequent reproductive season.