Quantitative Genetics in Red Squirrels:mechanisms of adaptation

• Basics• Red squirrel examples

– Parturition date– Growth rate

• Genomics and the future

Andrew McAdamUniversity of California, Santa Cruz

mcadam@biology.ucsc.edu

Quantitative Genetics

Examines the genetics of continuously varying (quantitative) traits

Understanding the genetic basis to quantitative traits allows us to predict future evolutionary responses to selection

Growth rate (g/day)

# o

bse

rva

tion

s

0

50

100

150

200

250

300

350

400

450

500

550

600

650

700

750

<= 0 (0,.5] (.5,1] (1,1.5] (1.5,2] (2,2.5] (2.5,3] (3,3.5] (3.5,4] > 4

Traditional Quantitative Genetics estimates sources of trait variation by examining the phenotypic resemblance among known relatives.

R = h2 S

J. Merilä

R. Rothman

Schroeder

1. Sources of variation• Heritability• Maternal effects

2. Selection

3. Response to selection

Quantitative Genetics in Red Squirrels

Sp

ruce

Co

nes

1988 1990 1992 1994 1996 1998 20000

50

100

150

200

250

300

350

Parturition Date

1975 1980 1985 1990 1995 2000

Ave

rage

spr

ing

tem

pera

ture

(o C

)

0

2

4

6

8

10

12

Increase in Temperature Increase in Food Abundance

Year of birth

89 90 91 92 93 94 95 96 97 98

Mea

n nu

mbe

r of

spr

uce

cone

s av

aila

ble

durin

g a

fem

ale'

s re

prod

uctiv

e lif

etim

e

20

40

60

80

100

120

140

160

180

Parturition Date - Heritability

h2 = 0.16 ± 0.03 

Matrilineal Pedigree (1989-2001)1059 breeding events

568 females5 generations

Paternity and Maternal Effects??

- Réale et al., 2003, Evolution

S = - 8.96 ± 2.56 Parturition Date (s.d. units)

Lif

etim

e fi

tnes

s re

sid

ual

s

-2 -1 0 1 2 3-2

02

4

Parturition Date - Selection

Fitness: total number of offspring produced in lifetime.

Considered females dead prior to 2000 (n=303)

- Réale et al., 2003, Evolution

Response to Selection (R)

R = h2 S Predicted R = - 1.4 days/gen.Observed R = - 6.0 days/gen.

Generation

1 2 3 4E

stim

ated

bre

edin

g va

lue

(day

s)-3.5

-3.0

-2.5

-2.0

-1.5

-1.0

-0.5

0.0

0.5

133 98 105 38

Plasticity = - 23.1 days/cone index- Réale et al., 2003, Proc. Roy. Soc. L., B

log LYC

0.0 0.5 1.0 1.5 2.0 2.5 3.0

Age

Cor

rect

ed P

artu

ritio

n D

ate

90

100

110

120

130

140

150

160

(1991-2001)n = 11 years

Parturition Date Questions

1. Does food supplementation result in the plastic advancement in breeding?

2. Are there differences in the heritability of parturition date between the experimental and control populations?

3. Does selection on parturition date differ between experimental and control populations?

4. Do these differences in selection result in experimental evolution of earlier breeding?

• Widespread

• Strong in mammals

• Predicted to have important effects on evolutionary dynamics…if heritable

Maternal Effects

Occur when the phenotype of a mother causes phenotypic effects in her offspring

www.sbgmath.com

~25 Days~25 Days

Nestling Growth Rate

(g/day)

Cross-Foster

Percentage of variation in growth in body mass

GeneticMaternalG x EError

10%

8181%%

99%%

h2 = 0.09 ± 0.04

Maternal Growth Rate

Offspring Growth Rate

MaternalEffects

Litter SizeParturition Date

h2 = 0.09

Maternal Growth Rate

Offspring Growth Rate

MaternalEffects

h2 = 0.09

h2t = 0.31

++

- McAdam et al., 2002, Evolution

Food Effects on Growth

log Cones in Previous Year

0.0 0.5 1.0 1.5 2.0 2.5

Ave

rag

e G

row

th R

ate

(g/

da

y)

1.2

1.4

1.6

1.8

2.0

2.2

1999 2000 Food

Gro

wth

ra

te (

g/d

ay)

1.5

1.6

1.7

1.8

1.9

2.0

2.1

Cross-fostered

n =

32

n =

176

n =

72

1989 - 2001

Slope = 0.23 g/day/log conest-1

n = 13 years

Maternal

cov(dir,mat)1999 0.0432000 0.079Food - 0.005

Co

eff

icie

nt

of

Va

ria

tio

n

0.00

0.05

0.10

0.15

0.20

0.25

DirectGenetic

1999 2000 Food

h2t = 0.52*(h2 = 0.10)*

h2t = 0.70

(h2 = 0.12)

h2t = 0.57

(h2 = 0.57)

- McAdam & Boutin, 2003, J. Evol. Biol.

Lin

ear

sele

ctio

n g

rad

ien

ts (

β')

- 0.4

0.0

0.4

0.8

1.2

1.6

1990 1992 1994 1996 1998 2000 All years

*

*

*

*

*

Viability Selection on Growth

- McAdam & Boutin 2003, Evolution

Fitness: survival to potential breeding age

Other variables in model: Litter size, parturition date, sex, year

No spatial variation in selection

Components of Selection

Birth

Emergence

Recruitment

Breeding

Spring temperature (-)

Previous year’s cones (+)

CorrectedGrowth (t)

CorrectedGrowth (t+1)

Selection

Maternal Effectsh2

Response

Maternal Effects and the Response to Selection

1989 1991 1993 1995 1997 1999

Res

po

nse

(g

/day

)

-0.3

-0.2

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

Year

*

* *

1. Observed response greater than predicted by h2

2. Response not independent of selection in the previous generation

- McAdam & Boutin 2003, Proc. Roy. Soc. L., B

Growth Rate Questions

1. Does food supplementation increase nestling growth rates?

2. Does food supplementation eliminate maternal effects?

3. Does selection on growth rates differ between experimental and control populations?

4. Do these differences in selection result in experimental evolution of earlier breeding?

5. Do maternal effects contribute to evolution in the control population but not the food supplemented one?

Genetic Mechanisms of Adaptation

It has recently become possible to use genetic markers to determine regions of the genome (loci?) that contribute to quantitative variation.

Quantitative Trait Loci (QTL’s)

QTL’s can be mapped for natural populations with extensive pedigrees and many molecular markers

Genetics of Speciation in Sticklebacks

- Peichel et al., 2001, Nature

Ecological and Evolutionary Functional Genomics (EEFG)

Genes Genotype Phenotype Phenotype’

Evolution

Genom

ics

Q. Gen

etics

Develo

pmen

t

Selecti

on

Genes Genotype Phenotype Phenotype’

Evolution