Maternal effects and fitness associated

recombination in a host-pathogen

system

Weihao Zhong

Nicholas Priest

07/01/2012

Rutherford & Lindquist (1998) Nature 396, 336-342

McClintock (1984) Science 226, 792-801

Stress

Increased

phenotypic

variation

Increased

genetic

variation

Stress-induced GV:

- Increase the total additive GV available for selection

- Suggest a plausible mechanism for the evolution of sex &

recombination

The problem with recombination

• Recombination load

– “The Reduction Principle” (Feldman et al. 1980)

• Recombination evolves under limited conditions in classic models

– e.g. weak negative epistasis

• But, a constant rate of recombination is assumed

Recombination as a plastic trait

• Numerous examples of stress-induced recombination

– Temperature (Plough 1917; Grell 1971; Zhong & Priest 2011)

– Nutrition (Neel 1941)

– Mating (Priest et al. 2007; Stevison 2011)

– Introduction of deleterious mutations (Tedman-Aucoin & Agrawal 2011)

Meiotic recombination is a plastic trait that is sensitive

to physiological state of the organism.

Fitness-Associated Recombination

• FAR modifiers evolve under

broad range of conditions

(Hadany & Beker 2003):

– Form direct association with

locus under selection

– No epistasis required

• Require maternal effect on

recombination to work in

diploids (Agrawal et al. 2005)

Recombination

Fitness

RecombinationOffspringMother

Stress

Are stress-induced maternal effects

common in nature? Yes!

Tenebrio molitor Tribolium castaneum

Bombus terrestris

Porcellio scaber

Daphnia magna Plodia interpunctella

“Trans-generational immune priming”

1. Does maternal stress affect offspring recombination?

2. Is there a negative relationship between fitness and recombination?

Testing them requires multi-generation experiments

with biologically realistic stress that assess direct

correlation between fitness and recombination.

• Backcross phenotypic markers

• Create heterozygous females, tester male mating

• Score Non-recombinants Recombinants

A B

B

A

X

XWT XWTA B

Multip

le

Genera

tions

General approach

Maternal

Generation

Daughter

Generation

NT+NT

NT+ME

ME+NT

ME+ME

Offspring Scoring

Live pathogen Heat-killed pathogen

Back-crossed marker line

OR

NT ME

OR

Daughters collected

NT ME

Daughters collected

Offspring Scoring

OR

OR

NT+NT

NT+HT

HT+NT

HT+HT

NT HT

NT HT

Metarhizium robertsii

No maternal effect on reproductive output

NT+NT NT+ME ME+NT ME+ME

To

tal sco

red

01

02

03

04

05

06

07

0

a a

b b

77 73 72 64

Maternal: F1,282 = 0.59, p = 0.44

Daughter: F1,282 = 31.2, p < 0.001

Maternal x Daughter: F1,282 = 0.01, p = 0.93

Mother

Daughter

NT+NT NT+HT HT+NT HT+HT

To

tal sco

red

01

02

03

04

05

06

07

0

b

a aa

77 65 73 65

Maternal: F1,276 = 0.82, p = 0.37

Daughter: F1,276 = 3.5, p = 0.05

Maternal x Daughter: F1,276 = 1.45, p = 0.23

Mother

Daughter

“Pathogen exposure enhances host

fitness” - Colin McClure (C15, Friday

@ 11.20)

Maternal effect on recombination

NT+NT NT+ME ME+NT ME+ME

Re

co

mb

ina

tio

n r

ate

(cM

/Mb

)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

65 38 59 37

a a a a

Maternal: χ2 = 0.15, p = 0.70

Daughter: χ2 = 0.33, p = 0.57

Maternal x Daughter: χ2 = 0.01, p = 0.94

NT+NT NT+HT HT+NT HT+HT

Re

co

mb

ina

tio

n r

ate

(cM

/Mb

)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

65 67 53 55

a a a

b

Maternal: χ2 = 3.8, p = 0.05

Daughter: χ2 = 0.62, p = 0.43

Maternal x Daughter: χ2 = 5.2, p < 0.05

Mother

Daughter

Mother

Daughter

No correlation between recombination

& reproductive output

20 40 60 80 100

12

34

56

NT+NT

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

12

34

NT+HT

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

1.0

1.5

2.0

2.5

3.0

3.5

4.0

NT+ME

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80

23

45

ME+ME

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

12

34

HT+NT

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

23

45

ME+NT

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

12

34

5

HT+HT

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

20 40 60 80 100

01

23

HT+ME

Number of Offspring Scored

Rate

of R

ecom

bin

atio

n (

cM

/Mb)

All p > 0.05

Results

1. Does maternal stress affect offspring recombination?

2. Is there a negative relationship between fitness and recombination?

- Live pathogen

- Heat-killed pathogen

- Stress treatment

- Control

Implications

• Fitness Associated Recombination might be

relatively rare in nature (in Diploids)

– Weaker association between modifier and selected

loci

• Maternal ‘priming’ effects can have unexpected

consequences

– Interaction between maternal cues (past stress

exposure) and offspring stress (current exposure)

– Do populations possess stress ‘memory’?

Take-home message

The effects of stress on genetic variation

extend beyond a single generation…

…though exposure to stress does not

always increase the genetic potential for

adaptation.

Acknowledgements

Nicholas Priest

Colin McClure

James Sciberras

Dave Mlynski