Ecological Mechanisms of Adaptation in Red Squirrels

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

2. Ecological and Evolutionary Functional Genomics (EEFG) Q. Genetics Genomics Development Selection Genes Genotype Phenotype Phenotype’ Evolution

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

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

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

6. Kluane Red Squirrels

7. Feeding Observations n = 15,309

8. Spruce Cone Counts 3m • ~450 trees distributed systematically • Monitored since 1988

9. 1988 1990 1992 1994 1996 1998 2000 2002 2004 Variation in Spruce Cone Abundance 6 Year:F15, 4337 = 312.3, P <0.001 dbh:F1, 452 = 90.0, P <0.001 5 ln (count + 1) 4 3 2 1 0 457 trees counted in multiple years Checked for changes in tree id and dbh

10. 1988 1990 1992 1994 1996 1998 2000 2002 2004 160, 000 140, 000 120, 000 100, 000 Cones per squirrel 80, 000 60, 000 1 year 4x RMR 40, 000 1 year RMR 20, 000 0 80 seeds/cone 2.2 mg/seed 6.62 kcal/g 4.2 kJ/kcal =4.89 kJ/cone ln(cones/tree) = 1.185 x ln (cone count); Jalene 15 trees in 5m radius = 1401 trees/ha; midden condition Territory size = 0.2ha; Jalene

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

12. Food abundance influences… Ignore what you read in Larsen et al., 1997

13. Food abundance also influences…

14. 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.

15. Conceptual Model Population Parameters (competition) Conest-1 Food Abundance Selection Conest

16. 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) OW New 2000 r2 = 0.49, n = 16, P = 0.002 r2 = 0.30, n = 16, P = 0.03

17. 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

18. Food affects litter size 1081 litters 16 years

19. Conceptual model OW vacancies -* Conest-1 +* +* New Territories => Selection? - 0.11 +* Conest # Competitors +**

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

21. Food affects offspring growth rates 2167 offspring 764 dams within years 16 years

22. Conceptual model - Growth OW vacancies -* Conest-1 -** +* -** +* Selection New Territories - 0.11 +* Conest # Competitors +**

23. Parturition Date

24. Food affects timing of breeding n = 16 years 1297 litters 16 years

25. Selection on Parturition Date …also positive effects of mean parturition date and year

26. Conceptual model - Parturition date OW vacancies -* Conest-1 +’ +* +’ +* Selection New Territories - 0.11 +* Conest # Competitors +**

27. 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

28. 1988 1994 1998 2002 2004 1990 1992 1996 2000 Kluane Red Squirrel Experiment 160, 000 140, 000 120, 000 100, 000 Cones per squirrel 80, 000 60, 000 40, 000 food addition 20, 000 0 2006 2012 2008 2010 2014

29. 1988 1994 1998 2002 2004 1990 1992 1996 2000 Kluane Red Squirrel Experiment 160, 000 140, 000 120, 000 100, 000 Cones per squirrel 80, 000 60, 000 40, 000 8 kg peanut butter 20, 000 0 2006 2012 2008 2010 2014

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

31. 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

32. Quantitative predictions based on correlations from the past 17 years of data.

33. Conceptual Model Population Parameters (competition) Conest-1 Food Abundance Selection Conest

34. Quantitative Genetic Predictions - Growth Predicted response of 0.12 - 0.36 sd/gen

35. Predicted changes in growth rates

36. Quantitative Genetic Predictions - Parturition Date * Effects of food addition are unknown Predicted response of 0.02 - 0.05 sd/gen

37. Predicted changes in parturition date

38. 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)

39. 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