University of Alberta

Kluane Red Squirrel Project (KRSP)

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Effects of Resource Availability on Individual Reproductive
Success in Red Squirrels

Visit the Kluane Red Squirrel Project webpage:

The long-term objective of the Kluane Red Squirrel Research Project is to determine how short- and long-term changes in resource availability affect life history traits, population dynamics, and microevolution of boreal mammals. We wish to determine how individual behavioural and life history responses to current conditions are shaped by past conditions and future trade-offs. We use a combination of long-term field studies of individuals and experimental manipulation of their environment to address these issues.

This research is conducted near Kluane Lake, Yukon. Since 1987, my students and I have used red squirrels (Tamiasciurus hudsonicus) as a model organism. Squirrels are diurnal small mammals with an average

lifespan of three years. Females produce one litter per year, although they may attempt as many as three. Annual birthdates are flexible with young born as early as March and as late as July. Juveniles emerge from their natal nest by 50 days of age and wean by 70 days of age. Squirrels feed primarily on conifer seed obtained by husking cones. The cones are stored in a traditional central food cache or midden that each individual defends year-round.

All squirrels on the study sites are colour-tagged for visual identification. Each individual's fate and

territory location is determined beginning in March by live-trapping and observation. Females are radio-collared to aid in finding nests so we can enumerate, weigh, and obtain tissue samples from the young shortly after birth. Nests are entered a second time when the juveniles are approximately one month of age to tag and re-weigh the young. Throughout the summer, we conduct regular trapping and visual censuses to record weights, survival of young at emergence and weaning, disappearance of adults, and changes in territory ownership. A subset of juveniles receive radio collars to monitor dispersal. Dispersal distances are typically short (usually less than 100 m), and we have good evidence that a disappearance means death. We also obtain a reliable index of food availability by counting the cones on permanently marked trees in early August. Average cone crops can vary by at least three orders of magnitude among years. We have been successful in measuring energy expenditure, behaviour, and life history traits under natural conditions and have been able to combine this data with experimental manipulations of food resources,
reproductive demands (litter size manipulations), and relatedness within litters (cross-fostering experiments). To date, we have information from over 5000 individuals spanning 6 generations.

Currently, we are pursuing several research directions, and we wish to continue with variations on these themes:

1. Contemporary Adaptation: The application of molecular markers (e.g., microsatellites), quantitative genetics, and genomics to natural populations offers the opportunity to study evolution in action. Andrew McAdam (Assistant Professor, Michigan State University) uses a combination of field manipulations and existing pedigree data for our red squirrel population to examine maternal effects, heritability, and natural selection in this wild mammal population.

Maternal effects are widespread and can have dramatic influences on evolutionary dynamics, but their genetic basis is rarely measured in natural populations. Andrew has used cross-fostering techniques to estimate both direct (heritability) and indirect (maternal) influences on the potential for evolutionary change in nestling growth rates. This juvenile red squirrel trait is heritable but also experiences very large heritable maternal effects. Survival data for 1,352 juveniles born over the last 12 years in this population indicates that selection on juvenile growth rates vary in intensity and direction from one year to the next. Phenotypic changes in juvenile growth rates from one year to the next cannot be explained adequately by simple evolutionary genetic equations (response = selection x heritability). Instead, changes in juvenile growth rates are influenced both directly by contemporary selection as well as indirectly via maternal effects. This combination of short-term experiments and long-term data has revealed the important contributions of maternal effects to the evolutionary dynamics of this juvenile trait.

Over the course of the 1990s, we documented an 18-day advancement in the timing of spring breeding (parturition date) in red squirrels that coincided with patterns of global climate change (i.e., increasing spring temperature and food availability). Females who breed and produce young earlier convey an advantage to their offspring, as these juveniles are larger and more independent than their counterparts by autumn. These early-born juveniles are thus better equipped to survive the winter and subsequently maintain their mothers’ genes in the population. We used quantitative genetics to examine how much of this change towards earlier breeding dates was due to an individual’s flexibility in timing of reproduction from one year to the next (phenotypic plasticity) and how much was due to a change in the frequency of genes in the population from generation to the next. Much advancement in parturition date can be explained by the large degree of phenotypic plasticity for this trait; however, consistent directional selection has also favoured earlier breeding. Analysis of our existing squirrel pedigree revealed significant additive genetic variation in parturition date and indicated that breeding values for parturition date advanced by nearly 3 days over this 10-year period. Therefore, this large phenotypic response in the squirrels to changes in environmental conditions appears to be the result of both phenotypic plasticity and a genetic response to directional selection. David Coltman (Associate Professor, University of Alberta) is further investigating the importance of phenotypic plasticity in parturition date and has developed molecular markers for paternity analysis and pedigree reconstruction to facilitate quantitative genetic analyses. We ultimately hope to examine the squirrel genome to identify the molecular basis of adaptation. Additional collaborators on these projects include Denis Réale at Université du Québec à Montréal, Dominique Berteaux at the Université du Québec à Rimouski, and Jon Slate at University of Sheffield.

Useful References:
McAdam, AG and S Boutin. 2004. Maternal effects and the response to selection in red squirrels. Proceedings of the Royal Society of London, Series B. 271: 75-79.

McAdam, AG and S Boutin. 2003. Effects of food abundance on genetics and maternal variation in the growth rate of juvenile red squirrels. Journal of Evolutionary Biology 16: 1249-1256.

McAdam, AG and S Boutin. 2003. Variation in viability selection among cohorts of juvenile red squirrels ( Tamiasciurus hudsonicus ). Evolution 57: 1689-1697.

McAdam, AG, S Boutin, D Réale and D Berteaux. 2002. Maternal effects and the potential for evolution in a natural population of animals. Evolution 56: 846-851.

Mousseau, T. A. and C. W. Fox. 1998. Maternal Effects as Adaptations. Oxford University Press, New York.

Réale, D, D Berteaux, AG McAdam and S Boutin. 2003. Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution 57: 2416-2432.

Réale, D, AG McAdam, S Boutin and D Berteaux. 2003. Genetic and plastic responses of a northern mammal to climate change. Proceedings of the Royal Society of London B, Series B 270: 591-596.

Wolf, J. B. et al. 1998. Evolutionary consequences of indirect genetic effects. TREE, 13(2): 64-69.

2. Energetics: Murray Humphries (Assistant Professor, McGill University) is using a combination of physiological, behavioural, and ecological techniques to determine the process by which individuals acquire energy from their habitat and allocate this to reproduction. The ability of an organism to acquire energy and convert it into offspring production is a central process linking animal physiology, behaviour, ecology, and evolution. Increases in energy availability have been repeatedly shown to lead to increases in offspring production and population size, but documentation of the behavioural and physiological responses that produce this effect are rare. Comparative physiologists have long attempted to eliminate or minimize the role of environmental factors when measuring physiological traits, and as a result, we understand little about how variation in these traits affects performance under natural circumstances. For example, resting metabolic rate (RMR) has been measured in more than 740 species of birds and mammals, but extremely little is known about its ecological or evolutionary relevance. Initial attempts to evaluate the adaptive consequences of physiological traits have involved either biogeographical or individual trait-survival correlations, but both approaches are seriously affected by confounding variables. A better approach may be to study intra-specific variation in the trait under natural circumstances, using observational and experimental approaches to evaluate alternate hypotheses about the trait's function. This research will evaluate the intra- and inter-individual relationships between energy availability, behaviour, metabolism, and reproductive success of free-ranging red squirrels to evaluate a classic, unresolved hypothesis that postulates an elevated RMR as a requirement for foraging in cold environments. This work is conducted in collaboration with John Speakman at the University of Aberdeen, Scotland.

Useful References:
Humphries, M.M. & S. Boutin 2000. The determinants of optimal litter size in free- ranging red squirrels. Ecology 81, 2867.

Lovegrove, B.G. 2000. The zoogeography of mammalian basal metabolic rate. American Naturalist 6: 201.

Speakman, J.R. 2000. The cost of living: field metabolic rates of small mammals. Advances in Ecological Research 30: 177.

3. Bequeathal and Dispersal: Juvenile survival is often a key determinant of lifetime reproductive success. Parents in resource-limited systems face a trade-off: forcing offspring to disperse could decrease their survival whereas allowing them to stay incurs parental costs. Juveniles also face associated dispersal and philopatry costs and benefits related to resource access, familiarity with local habitat, and genetic or reproductive consequences. The relative costs and benefits to parents and offspring of philopatry should influence dispersal patterns. We have used radio telemetry to obtain detailed movements of juvenile squirrels during the crucial time when they must find a territory. Many juveniles in our system are highly philopatric, and we have strong evidence that those moving off the natal territory incur survival costs. Mothers may also affect settlement patterns of their offspring by sometimes giving up part or all of their territory to their offspring. We called this unusual behaviour bequeathal and have provided experimental evidence to show that this represents a form of parental investment. Our studies suggest that some squirrels own multiple middens in the spring, and Karl Larsen found that females with breeding experience were much more likely to take over middens left vacant by experimental removals in late October than other members of the population. In all cases, the acquired middens were relinquished to offspring in the next breeding season. This raises the intriguing possibility that females may acquire middens as a form of parental investment well in advance of the presence of offspring.

Useful References:
Berteaux, D and S Boutin. 2000. Breeding dispersal in female North American red squirrels. Ecology 81: 1311-1326.

Boutin, S., K.W. Larsen, and D. Berteaux. 2000. Anticipatory parental care: acquiring resources for offspring prior to conception. Proceedings of the Royal Society London B 267: 2081-2085

Larson K.W., C. D. Becker, S. Boutin, and M. Blower. 1997. Effects of hoard manipulations of life history and reproductive success of female red squirrels ( Tamiasciurus hudsonicus ). Journal of Mammalogy 78: 192-203.

Larsen, K.W. and S. Boutin. 1995. Exploring territory quality in the North American red squirrel through removal experiments. Canadian Journal of Zoology 73: 1115-1122.

4. Male Reproductive Success: Given the relative ease with which we can follow maternal lineages in the red squirrel system and relative difficulties to date in determining paternity, our work has focused on factors influencing the lifetime reproductive success of females. However, recent developments in genetic paternity assignment techniques now permit detailed investigations of factors influencing male reproductive success in red squirrels. Although size dimorphism is slight in this species, the sexual selection on male behaviour may be high. Both males and females mate with multiple individuals. Males are unable to restrict reproductive access to females, and the search effort or ability of males may determine their mating success. Annual reproductive success may also be influenced by sperm competition. Current work is examining behavioural, morphological (e.g., body condition and mass), physiological (e.g., plasma testosterone and stress hormone levels), and ecological (e.g., territory size and quality) correlates of male reproductive success.

Useful References:
Foerster, K., K. Delhey, A. Johnsen, J.T. Lifjeld and B. Kempenaers. 2003. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425: 714-717.

Preston, B.P., I.R. Stevenson, J.M. Pemberton, D.W. Coltman and K.Wilson. 2003. Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proceedings of the Royal Society of London B 270: 633-640.

Schwagmeyer, P.L. 1988. Scramble-competition polygyny in an asocial mammal: Male mobility and mating success. American Naturalist 131: 885-892.

5. Stress and Senescence: The stress axis, composed of the hypothalamus, pituitary gland, and adrenal gland, is a crucial system that allows animals to cope with environmental and physical challenges. However, this axis deteriorates as animals senesce. Rudy Boonstra (Professor, University of Toronto) examines how aging proceeds in wild mammals and whether potentially stressful conditions affect brain organization, brain function, and reproductive fitness. Specifically, his work with the red squirrels investigates age-dependant changes in the stress axis by examining both hormonal changes and changes at critical brain sites as a function of age and reproductive history. Additional work on life history strategies in red squirrels is using the long-term data and statistical methodologies to study the influence of the age on fitness components (survival rates, reproductive success).

Useful References:
Boonstra, R. 2004. Coping with changing northern environments: the role of the stress axis in birds and mammals. Integrative and Comparative Biology 44: 95-108.

Boonstra, R., C. J. McColl, and T. J. Karels. 2001. Reproduction at all costs: how breeding compromises the stress response and survival in male Arctic Ground Squirrels. Ecology 82: 1930-1946.

Boonstra, R. and C. J. McColl. 2000. The contrasting stress response of male Arctic Ground Squirrels and Red Squirrels. Journal of Experimental Zoology 286: 390-404.

Charlesworth, B. 1994. Evolution in Age-Structured Populations. 2nd Edition. Cambridge University Press, Cambridge.

Gaillard, J.-M., D. Allaine, D. Pontier, N.G. Yoccoz, and D.E.L. Promislow. 1994. Senescence in natural populations of mammals: a reanalysis. Evolution 48: 509-516.

6. Food Supplementation Experiment: Red squirrels in the southwest Yukon feed almost exclusively on the seeds of white spruce ( Picea glauca ) cones. The abundance of spruce cones varies annually over three orders of magnitude. Recent work in this population (see above) suggests that many aspects of red squirrel behaviour, physiology, life history and genetics are shaped by this large variation in food abundance. We have recently initiated an ambitious large-scale food supplementation experiment whereby an entire population of squirrels will be supplemented with food for the next 5-7 years. My lab will continue collaborations with Murray Humphries, Andrew McAdam, Rudy Boonstra, and David Coltman to investigate the population, behavioural, physiological, and genetic responses of the red squirrels to this experimental manipulation.

Useful References:
Boutin, S. 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Canadian Journal of Zoology 68: 203-220.

For additional information about the Kluane Red Squirrel Project, visit the project website at

Last Modified:2014-11-20