Ecological Mechanisms of Adaptation in Red Squirrels Andrew McAdam Michigan State University

Ecological and Evolutionary Functional Genomics (EEFG) GenesGenotypePhenotypePhenotype’ Evolution Q. Genetics Genomics Development Selection

Integrating Evolutionary Approaches GenesGenotypePhenotype Q. Genetics / Genomics Development Selection Genotype Phenotype Phenotype’ Evolution Traditional Q. Genetics

"What we understand best about evolution is mostly genetic, and what we understand least is mostly ecological." - E.O. Wilson

Integrating Evolutionary Approaches GenesGenotypePhenotype Q. Genetics / Genomics Development Selection Genotype Phenotype Phenotype’ Evolution Traditional Q. Genetics

Kluane Red Squirrels

Feeding Observations n = 15,309

3m  ~450 trees distributed systematically  Monitored since 1988 Spruce Cone Counts

Variation in Spruce Cone Abundance ln (count + 1) Year: F 15, 4337 = 312.3, P <0.001 dbh: F 1, 452 = 90.0, P < trees counted in multiple years Checked for changes in tree id and dbh

0 20, , , , , , , , Cones per squirrel 1 year RMR ln(cones/tree) = x ln (cone count); Jalene 15 trees in 5m radius = 1401 trees/ha; midden condition Territory size = 0.2ha; Jalene 80 seeds/cone 2.2 mg/seed 6.62 kcal/g 4.2 kJ/kcal =4.89 kJ/cone 1 year 4x RMR

Winter Summer Reproduction Cone Production All squirrels conceive prior to the arrival of current year cones

Food abundance influences… Population density Sullivan 1990 Reproductive rate Sullivan 1990? Juvenile growth rate Boutin & Larsen & 1993 McAdam & Boutin 2003a,b Parturition date Réale et al., 2003 Bequeathal behaviour Berteaux & Boutin 2000 Juvenile survival Klenner & Krebs 1991 Humphries & Boutin 2000 McAdam & Boutin 2003a Costs of reproduction Humphries & Boutin 2000 Ignore what you read in Larsen et al., 1997

Food abundance also influences… Variation in growth McAdam & Boutin 2003b Selection on growth McAdam & Boutin 2003a Selection on parturition date?? Réale et al., 2003

Hypothesis: The abundance of spruce cones is an ecological mechanism of adaptation in red squirrels. Selection on red squirrel life history traits (e.g. parturition date, growth rates) is controlled by the abundance of food. Annual variation in the abundance of spruce cones results in fluctuations in natural selection that minimize sustained evolutionary responses to selection.

Conceptual Model Cones t-1 Cones t Selection Population Parameters (competition) Food Abundance

Food abundance affects territory vacancies Vacancies estimated from changes in population density in core areas Over-winter (OW) vacancies = fall (t-1) - spring (t) New vacancies = fall (t) - fall (t-1) OWNew r 2 = 0.30, n = 16, P = 0.03 r 2 = 0.49, n = 16, P =

Food affects offspring production Age at first reproduction - Boutin et al., unpub. Reproductive rate - Boutin et al., unpub. Litter size All influenced by future and not previous year’s cones

Food affects litter size 1081 litters 16 years Factorest.sedftP Cones t Cones t Age < Age < 0.001

Conceptual model Cones t-1 Cones t OW vacancies New Territories # Competitors +* -* +** +* => Selection?

~25 Days Nestling Growth Rate (g/day) 1-2 Days

Food affects offspring growth rates Factorest.sedftP Cones t < Food Add < Sex < Cones t-1 x Food Add < offspring 764 dams within years 16 years

Conceptual model - Growth Cones t-1 Cones t OW vacancies Selection New Territories # Competitors +* -* +** +* -**

Parturition Date

Food affects timing of breeding n = 16 years Factorest.sedftP Cones t Cones t < Age < Age < litters 16 years

Selection on Parturition Date Factorest.sedftP OW vac NEW vac …also positive effects of mean parturition date and year

Conceptual model - Parturition date Cones t-1 Cones t OW vacancies Selection New Territories # Competitors +* -* +** +* +’

Goal: To perform a replicated food supplementation experiment across multiple generations to test the hypothesis that food abundance controls life history adaptation in red squirrels Mimic ‘mast’ conditions for all individuals in each of 3 populations for the next 5 years

Kluane Red Squirrel Experiment 0 20, , , , , , , , Cones per squirrel food addition

Kluane Red Squirrel Experiment 0 20, , , , , , , , Cones per squirrel kg peanut butter

One experimental population 49 females 100 middens supplemented 1kg peanut butter added to each feeder in October 2004

NSF Plan Add 2 (or 3) new grids –(SU, KL, AG, Food1, Food2, Control?) Supplement all individuals (~100) on each food grid Follow standard monitoring protocol –Add 2 (or 3) spring technicians –Add 2 or 3 grad students –Add 2 or 3 summer assistants

Quantitative predictions based on correlations from the past 17 years of data. ResponseControl (± se)Experiment Food (ln count+1) 2.4 ± ± 0.0 Fall density (sq./ha) 2.6 ± ?? OW vac. (ha -1 ) 0.32 ± New vac. (ha -1 ) ± Litter size3.0 ± ? Parturition date (Julian) ± Growth rate (g/day) 1.81 ±

Conceptual Model Cones t-1 Cones t Selection Population Parameters (competition) Food Abundance

Quantitative Genetic Predictions - Growth ScenarioCones t Cones t-1 Predicted  h2h2 Response (g·day -1 /gen) Predicted response of sd/gen

Predicted changes in growth rates

Quantitative Genetic Predictions - Parturition Date ScenarioCones t Cones t-1 Predicted  h2h2 Response (days/gen) * * * * Réale et al * * Effects of food addition are unknown Predicted response of sd/gen

Predicted changes in parturition date

Test Predictions Selection –Adults: lifetime selection –Juveniles: survival to breeding age –Adults: offspring surviving to spring Evolution –Phenotypic changes (corrected / common garden) –Changes in breeding values (animal model)

Sub-projects Experimental and observational approaches to Genotype x Environment Local adaptation, gene flow and introgression Inbreeding and outbreeding depression Adaptation of energy acquisition and expenditure