Ecological Mechanisms of Adaptation in Red Squirrels

Andrew McAdamMichigan State University

Ecological and Evolutionary Functional Genomics (EEFG)

Genes Genotype Phenotype Phenotype’

Evolution

Q. Gen

etics

Genom

ics

Develo

pmen

t

Selecti

on

Integrating Evolutionary Approaches

Genes Genotype Phenotype

Q. Gen

etics

/

Genom

ics

Develo

pmen

t

Selecti

onGenotype Phenotype Phenotype’

Evolution

Tradit

ional

Q. Gen

etics

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

- E.O. Wilson

Integrating Evolutionary Approaches

Genes Genotype Phenotype

Q. Gen

etics

/

Genom

ics

Develo

pmen

t

Selecti

onGenotype Phenotype Phenotype’

Evolution

Tradit

ional

Q. Gen

etics

Kluane Red Squirrels

Feeding Observations

Cones

Buds

Needles

Mushrooms

'Animal Matter'

Other

n = 15,309

3m

~450 trees distributed systematically

Monitored since 1988

Spruce Cone Counts

Variation in Spruce Cone Abundance

0

1

2

3

4

5

6

1988 1990 1992 1994 1996 1998 2000 2002 2004

ln (

co

un

t +

1)

Year: F15, 4337 = 312.3, P <0.001dbh: F1, 452 = 90.0, P <0.001

457 trees counted in multiple yearsChecked for changes in tree id and dbh

0

20, 000

40, 000

60, 000

80, 000

100, 000

120, 000

140, 000

160, 000

1988

1990

1992

1994

1996

1998

2000

2002

2004

Con

es p

er s

quirr

el

1 year RMR

ln(cones/tree) = 1.185 x ln (cone count); Jalene15 trees in 5m radius = 1401 trees/ha; midden conditionTerritory size = 0.2ha; Jalene

80 seeds/cone2.2 mg/seed6.62 kcal/g4.2 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

Conest-1

Conest

SelectionPopulationParameters(competition)

Food Abundance

Food abundance affects territory vacancies

Vacancies estimated from changes in population density in core areasOver-winter (OW) vacancies = fall (t-1) - spring (t)New vacancies = fall (t) - fall (t-1)

OW New

r2 = 0.30, n = 16, P = 0.03 r2 = 0.49, n = 16, P = 0.002

2000

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 litters16 years

Factor est. se df t P

Conest 0.13 0.04 13 3.2 0.007

Conest-1 0.03 0.04 13 0.7 0.51

Age 0.24 0.07 1063 3.5 < 0.001

Age2 - 0.03 0.01 1063 - 3.3 < 0.001

Conceptual model

Conest-1

Conest

OW vacancies

- 0.11New

Territories

# Competitors

+*

-*

+**

+*

+*

=> Selection?

~25 Days~25 Days

Nestling Growth Rate

(g/day)

1-2 Days1-2 Days

Food affects offspring growth rates

Factor est. se df t P

Conest-1 0.13 0.023 14 5.7 < 0.001

Food Add 0.76 0.126 1400 6.1 < 0.001

Sex 0.04 0.011 1400 3.8 < 0.001

Conest-1 x Food Add - 0.29 0.039 1400 - 7.4 < 0.001

2167 offspring764 dams within years16 years

Conceptual model - Growth

Conest-1

Conest

OW vacancies

Selection- 0.11

New Territories

# Competitors

+*

-*

+**

+*

+*

-**

-**

Parturition Date

Food affects timing of breeding

n = 16 years

Factor est. se df t P

Conest 1.99 1.14 13 1.7 0.10

Conest-1 -10.57 1.14 13 - 9.3 < 0.001

Age -11.40 1.24 1279 - 9.2 < 0.001

Age2 1.25 0.17 1279 7.3 < 0.001

1297 litters16 years

Selection on Parturition Date

Factor est. se df t P

OW vac. 0.41 0.21 13 2.0 0.07

NEW vac. 0.28 0.15 13 1.9 0.08

…also positive effects of mean parturition date and year

Conceptual model - Parturition date

Conest-1

Conest

OW vacancies

Selection- 0.11

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, 000

40, 000

60, 000

80, 000

100, 000

120, 000

140, 000

160, 000

1988

1990

1992

1994

1996

1998

2000

2002

2004

Con

es p

er s

quirr

el

2006

2008

2010

2012

2014

food addition

Kluane Red Squirrel Experiment

0

20, 000

40, 000

60, 000

80, 000

100, 000

120, 000

140, 000

160, 000

1988

1990

1992

1994

1996

1998

2000

2002

2004

Con

es p

er s

quirr

el

2006

2008

2010

2012

2014

8 kgpeanut 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.

Response Control (± se) ExperimentFood (ln count+1) 2.4 ± 0.4 4.0 ± 0.0

Fall density (sq./ha) 2.6 ± 0.2 3.0??

OW vac. (ha-1) 0.32 ± 0.11 0.15

New vac. (ha-1) - 0.02 ± 0.16 0.0

Litter size 3.0 ± 0.06 3.2?

Parturition date (Julian) 117.6 ± 4.1 101.1

Growth rate (g/day) 1.81 ± 0.05 2.0

Conceptual Model

Conest-1

Conest

SelectionPopulationParameters(competition)

Food Abundance

Quantitative Genetic Predictions - Growth

Scenario Conest Conest-1

Predicted

h2

Response

(g·day-1/gen)

1 0 4 0.62 0.57 0.18

2 4 4 0.22 0.57 0.06

3 - - 0.58 0.57 0.17

1994 0.69 4.18 0.37 0.57 0.10

Predicted response of 0.12 - 0.36 sd/gen

Predicted changes in growth rates

Quantitative Genetic Predictions - Parturition Date

Scenario Conest Conest-1

Predicted

h2

Response

(days/gen)

1 0 4 - 0.34 0.16* - 0.98

2 4 4 - 0.13 0.16* - 0.38

3 - - - 0.29 0.16* - 0.85

1994 0.69 4.18 - 0.73 0.16* - 2.13

Réale et al. 2003

- - - 0.24 0.16* - 0.70

* Effects of food addition are unknown

Predicted response of 0.02 - 0.05 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