Tom Wenseleers University of Leuven, Belgium Ph.D. defence May 22nd, 2001 Conflict from Cell to...

Tom Wenseleers University of Leuven, Belgium Ph.D. defence May 22nd, 2001

Conflict from Cell to Colony

Cooperation is Key Feature in

Evolution of Life on Earth

Genes to Genomes

Prokaryotes to Eukaryotes

Unicellular to Multicellular Organisms

Organisms to Societies

Major transitions in evolution

Cooperation seems obvious to explain when viewed in terms of species-level benefits

But erroneous logic: non-cooperative ’free-riders’ outcompete altruists

But potential for conflict

Potential for Conflict in

Most Societies

Conflicts may occur between organisms, but also between cells or genes (’intragenomic conflict’)

In what ratio should males and females

be reared?F

½

M½ ¼

M¾

F

Conflicts in insect societies

Equal Sex-Ratio

Equal Sex-Ratio

3:1 FemaleBiased

Sex-Ratio

Cytoplasmic sex-ratio distorters

Conflict also occurs at the genomic level: maternally transmitted genes favour more female biased sex-ratios than nuclear genes(“intragenomic conflict”)

Cytoplasmic genes such as mitochondria or some bacterial symbionts may manipulate host to produce female biased broods (“cytoplasmic sex-ratio distorters”)

Wolbachia Example of a maternally

transmitted symbiont

Alpha-proteobacterium

Occurs mainly in arthropods (insects+Crustacea) + nematodes

Manipulates host reproduction to favour own spread

FemaleBiased

Sex-Ratios

Male Killing

Feminisation

Parthenogenesis Induction

Cytoplasmic Incompatibility

Effects on host reproduction

NormalOffspring

Production

Reduces fitness of Uninfected Female x Infected Male Crosses

Gives an advantage to infected females

Sterility in diploids, but production

of males only in haplo-diploids

Cytoplasmic incompatibility

Inviable

Phylogeny

Oth

er a

lpha

pro

teobacte

ria

Ehrlichieae

Neorickettsia

Gamm

a

prote

obac

teria

0.1

Wolbachia

CaedibacterMtK

MitochondriaCMS

Orientia MK

Rickettsia MK

Aims of my thesis Part I : empirical

– Does Wolbachia occur in ant societies?

– Alternative explanation for female biased sex-ratios in this group?

Part II : theoretical– What do animal and genomic

conflicts have in common?– Can sociobiological theory be

applied to both?

S e q u e n c e o f E v e n t s

Modelling

Make predictions

DNA Analysis

Measure key parameters

Experiments

Formally test hypotheses

Ideas Hypotheses

Molecular Data

Experimental Data

Integrated approach

Part I. Wolbachia - a cause of intragenomic conflict

in ant colonies

Work plan

Does Wolbachia occur in ant societies and if so in what frequency?

What effects does it have?Three case studies :– Parthenogenetic species– Wood ant Formica truncorum– Leptothorax nylanderi

Host-parasite coevolution?

Polymerase Chain Reaction using Specific Primers

Targets: ftsZ and wsp Wolbachia genes

Positive, negative and nuclear DNA (18S rDNA) controls

Negative samples retested twice

Methodology: PCR Assay

Sensitive& Reliable

High Incidence Worldwide

Indonesia

Chapter 1Wenseleers et al. (1998) Proceedings of the Royal Society of London

# species=50

Florida

Jeyaprakash & Hoy (2000) Insect Molecular Biology

# species=10

Panama

Van Borm et al. (2001) Journal of Evolutionary Biology

# species=7

Europe

# species=50 Chapter 6

3451 samples

Morphological evidence

Present in trophocytes and oocytes

Electron and light microscopical (DAPI) evidence

Work plan

Does Wolbachia occur in ant societies and if so in what frequency? YES, IN HIGH FREQUENCY



Parthenogenesis induction?

Were not infected.Parthenogenesis not induced by

Wolbachia.

PCR Assay

Grasso et al. (2000) Ethology, Ecology & Evolution 12:309-314Wenseleers & Billen (2000) Journal of Evolutionary Biology 13:277-280

6 Parthenogenetic Antsand Cape Honey Bee

N=25036 cols.

Wolbachia in F. truncorum

With: Lotta Sundström University of Helsinki

Formica truncorum

Extensive variation in sex-ratio produced by different colonies

Linked to facultative sex-ratio biasing :– Workers kill brothers in colonies

headed by singly mated queen– But not in colonies with double

mated queen

Does Wolbachia affect the sex-ratio too?

Effect on the sex-ratio :

– Males should be infected less than queens

– Sex-ratio should be correlated with infection rates

Incompatibility :

– Males and queens should be infected equally

– Uninfected colonies should not be able to survive

Predictions

Formica truncorum

Males (96%) and queens (94%) infected equally

All colonies infected (total # 33) despite production of 6% uninfected queens by each colony

Consistent with an incompatibility effect :

Uninfected queens do not survive past the founding stage due to incompatible matings

Wenseleers, Sundström & Billen (2002) Proceedings of the Royal Society of London series B, in press.

r2 = 0.0097

0

0.25

0.5

0.75

1

0.00 0.20 0.40 0.60 0.80 1.00

Percent infected workers

Inve

stm

ent i

n fe

mal

es

GLM Effects F p

No. of mates 4.88 0.04Infection rate 0.85 0.37Colony size 0.69 0.42

Infection and sex-ratio


r2 = 0.03

0

4

8

12

0.00 0.20 0.40 0.60 0.80 1.00

Proportion infected adult workers

Per

cap

ita

pro

du

ctio

n

Worker production

r2 = 0.28

0

4

8

12

0.00 0.20 0.40 0.60 0.80 1.00

Proportion infected adult workers

Per

cap

ita

pro

du

ctio

n

Sexual production

GLM

Effects F p F p

No. of mates 2.11 0.16 2.5 0.13

Infection rate 2.89 0.11 10.2 0.005

Infection and colony fitness


p<0.015p<0.0001

0

25

50

75

100

Pe

rce

nt

infe

cte

d

Sexuals Adult workers

Worker pupae

Infection rates

N=296 N=158 N=387

Adaptiveclearance to

reduce colony load?


Conclusions

No effects on the sex-ratio

Probably causes incompatible matings

Deleterious effects on colony function, but partly mitigated by clearance of infection in adult workers

Leptothorax nylanderi

Test experimentally whether Wolbachia causes incompatible matings

Setup: antibiotic treatment as an artificial means of creating the uninfected queen x infected male crossing type

Prediction: male production (infertility) following antibiotic treatment

0.4

0.5

0.6

0.7

0.8

0.9

1

Untreated Treated

Pri

ma

ry s

ex

-ra

tio

2 = 10.51, p < 0.001

Antibiotics experiments

4 coloniesN=70

7 coloniesN=152

Work plan




Wolbachia surface protein wsp was sequenced (approx. 550 bp)

Direct cycle sequencing when ants were infected by single strain

Cloning and sequencing when ants were infected by multiple strains (TA-cloning kit, pUC57 vector)

Methodology: Sequencing

28 sequencesAligned with previously sequenced relatives

So

len

op

sis

invi

cta

(im

po

rted

) C

ole

om

egill

a m

acu

lata

len

gi

Dia

ph

ori

na

citr

i P

lute

lla x

ylo

stel

la L

aod

elp

hax

str

iate

llus

Acr

aea

ence

do

n 1

Tri

cho

pri

a T

sp2

Dry

inid

was

p sp

Por

celli

onid

es p

ruin

osus

Sph

aero

ma

rugi

caud

a

Bac

toce

ra c

ucur

bita

e

Trib

oliu

m m

aden

s

Trib

olium

confu

sum

Rhin

ophoridae

unid

Doro

nomyrmex kutte

ri B

Doro

nomyrmex pacis B

2

Trichogramma spp.

Adalia bipunctata B

Coleomegilla maculata

Adalia bipunctata A

Acromyrmex octospinosus B3

Acromyrmex insinuator B1

Acromyrmex echinatior B

Solenopsis invicta (native)

Acromyrmex octospinosus B1 Acromyrmex octospinosus B2 Acromyrmex insinuator B2

Myrmica sabuleti Telenomus nawai Encarsia formosa

Diplolepis rosae

Leptopilina australis

Cadra cautella

Tetranychus urticae

Acraea encedon

Culex quinquefasciatus

Culex pipiens (ESPRO)

Drosophila simulans (W

atsonville)

Aedes albopictus (Houston)

Doronom

yrmex pacis B

1

Isopods

Trichopria drosophilae

Asobara tabida

Myrm

ica sulcin

od

is (Sam

so D

)

Myrm

ica sulcin

od

is (Ru

ssia)

Teleu

tom

yrmex sch

neid

eri

Neo

chryso

charis fo

rmo

sa

Fo

rmic

a ru

faD

acu

s d

esti

llato

ria

Do

ron

om

yrm

ex g

oes

swal

di A

2

Do

ron

om

yrm

ex p

acis

A4

Do

ron

om

yrm

ex k

utt

eri A

Fo

rmic

a fu

sca

(Mo

ls D

)

Fo

rmic

a fu

sca

(SJW

B)

Fo

rmic

a fu

sca

(KH

B)

Lep

toth

ora

x ac

ervo

rum

Bac

toce

ra s

p 1

Asc

D

Cat

agly

phis

iber

ica

Glo

ssin

a au

sten

i

Form

ica

poly

cten

a

Form

ica

trunc

orum

Formic

a pra

tensi

s

Asobara t

abida 3

Drosophila

sechellia

Drosophila sim

ulans (Hawaii)

Cadra cautella 2

Doronomyrmex pacis A3

Gnamptogenys menadensis

Phlebotomus papatasi (Israel)

Doronomyrmex goesswaldi A1

Acromyrmex octospinosus A1Solenopsis invicta A (native)Doronomyrmex pacis A2

Solenopsis richteri A

Acromyrmex echinatior A1

Drosophila simulans (Riverside)

Drosophila melanogaster (CantonS)

Drosophila melanogaster (Cairns)

Drosophila simulans (Coffs Harbour)


Nasonia vitripennis A

Drosophila bifasciata

Glossina morsitans centralis

Leptopilina heterotoma 2

Trichogramm

a bourarachae

Trichogramm

a kaykai (LC110)

Muscidifurax uniraptor

Acrom

yrmex insinuator A

Plagiolepis pygmaea

Myrm

ica sulcinodis (Pyrenees)

Formica lem

ani

Myrm

ica rub

ra

Do

ron

om

yrmex p

acis A1

0.050(25 MY)

A B

High strain diversity

So

len

op

sis

invi

cta

(im

po

rted

) C

ole

om

egill

a m

acu

lata

len

gi

Dia

ph

ori

na

citr

i P

lute

lla x

ylo

stel

la L

aod

elp

hax

str

iate

llus

Acr

aea

ence

do

n 1

Tri

cho

pri

a T

sp2

Dry

inid

was

p sp

Por

celli

onid

es p

ruin

osus

Sph

aero

ma

rugi

caud

a

Bac

toce

ra c

ucur

bita

e

Trib

oliu

m m

aden

s

Trib

olium

confu

sum

Rhin

ophoridae

unid

Doro

nomyrmex kutte

ri B

Doro

nomyrmex pacis B

2

Trichogramma spp.

Adalia bipunctata B


Adalia bipunctata A







Diplolepis rosae


Cadra cautella

Tetranychus urticae

Acraea encedon




atsonville)


Doronom

yrmex pacis B

1

Isopods


Asobara tabida

Myrm

ica sulcin

od

is (Sam

so D

)

Myrm

ica sulcin

od

is (Ru

ssia)

Teleu

tom

yrmex sch

neid

eri

Neo

chryso

charis fo

rmo

sa

Fo

rmic

a ru

faD

acu

s d

esti

llato

ria

Do

ron

om

yrm

ex g

oes

swal

di A

2

Do

ron

om

yrm

ex p

acis

A4

Do

ron

om

yrm

ex k

utt

eri A

Fo

rmic

a fu

sca

(Mo

ls D

)

Fo

rmic

a fu

sca

(SJW

B)

Fo

rmic

a fu

sca

(KH

B)

Lep

toth

ora

x ac

ervo

rum

Bac

toce

ra s

p 1

Asc

D

Cat

agly

phis

iber

ica

Glo

ssin

a au

sten

i

Form

ica

poly

cten

a

Form

ica

trunc

orum

Formic

a pra

tensi

s

Asobara t

abida 3

Drosophila

sechellia

Drosophila sim

ulans (Hawaii)

Cadra cautella 2

















Trichogramm

a bourarachae

Trichogramm

a kaykai (LC110)


Acrom

yrmex insinuator A

Plagiolepis pygmaea

Myrm


Formica lem

ani

Myrm

ica rub

ra

Do

ron

om

yrmex p

acis A1

0.050(25 MY)

A B

No match with host phylogeny

Acrom

yrmex insinuator A

Plagiolepis pygmaea

Myrm


Formica lem

ani

Myrm

ica rub

ra

Do

ron

om

yrmex p

acis A1

Hosts diverged 35 MY ago, but share a recently evolved W. strain

(1.7 MY old)

Doro

nomyrmex kutte

ri B

Doro

nomyrmex pacis B

2

Doronom

yrmex pacis B

1

Do

ron

om

yrm

ex g

oes

swal

di A

2

Do

ron

om

yrm

ex p

acis

A4

Do

ron

om

yrm

ex k

utt

eri ADoronomyrm

ex pacis A3Doronomyrmex goesswaldi A1


Do

ron

om

yrmex p

acis A1

So

len

op

sis

invi

cta

(im

po

rted

) C

ole

om

egill

a m

acu

lata

len

gi

Dia

ph

ori

na

citr

i P

lute

lla x

ylo

stel

la L

aod

elp

hax

str

iate

llus

Acr

aea

ence

do

n 1

Tri

cho

pri

a T

sp2

Dry

inid

was

p sp

Por

celli

onid

es p

ruin

osus

Sph

aero

ma

rugi

caud

a

Bac

toce

ra c

ucur

bita

e

Trib

oliu

m m

aden

s

Trib

olium

confu

sum

Rhin

ophoridae

unid

Doro

nomyrmex kutte

ri B

Doro

nomyrmex pacis B

2

Trichogramma spp.

Adalia bipunctata B


Adalia bipunctata A







Diplolepis rosae


Cadra cautella

Tetranychus urticae

Acraea encedon




atsonville)


Doronom

yrmex pacis B

1

Isopods


Asobara tabida

Myrm

ica sulcin

od

is (Sam

so D

)

Myrm

ica sulcin

od

is (Ru

ssia)

Teleu

tom

yrmex sch

neid

eri

Neo

chryso

charis fo

rmo

sa

Fo

rmic

a ru

faD

acu

s d

esti

llato

ria

Do

ron

om

yrm

ex g

oes

swal

di A

2

Do

ron

om

yrm

ex p

acis

A4

Do

ron

om

yrm

ex k

utt

eri A

Fo

rmic

a fu

sca

(Mo

ls D

)

Fo

rmic

a fu

sca

(SJW

B)

Fo

rmic

a fu

sca

(KH

B)

Lep

toth

ora

x ac

ervo

rum

Bac

toce

ra s

p 1

Asc

D

Cat

agly

phis

iber

ica

Glo

ssin

a au

sten

i

Form

ica

poly

cten

a

Form

ica

trunc

orum

Formic

a pra

tensi

s

Asobara t

abida 3

Drosophila

sechellia

Drosophila sim

ulans (Hawaii)

Cadra cautella 2

















Trichogramm

a bourarachae

Trichogramm

a kaykai (LC110)


Acrom

yrmex insinuator A

Plagiolepis pygmaea

Myrm


Formica lem

ani

Myrm

ica rub

ra

Do

ron

om

yrmex p

acis A1

0.050(25 MY)

A B

Multiple infections

Doro

nomyrmex pacis B

2

Doronom

yrmex pacis B

1Do

ron

om

yrm

ex p

acis

A4



Do

ron

om

yrmex p

acis A1

Multi infections may drive speciation

events!

No match with host phylogeny

pratensis

lemani

fusca

rufa

O

100

99

polyctena

truncorum84100

0.02(10 MY)

...and their symbionts

rufa

polyctena

pratensis

truncorum

lemani

fusca

O

Formica hosts...

Gyllenstrand, unpublished

Work plan



Host-parasite coevolution? NO, OCCASIONAL HORIZONTAL TRANSMISSION

Part II. Theoretical aspects ofconflict and cooperation

With: Francis Ratnieks and Kevin Foster

University of Sheffield

Animal vs. intragenomic conflict

What do animal and intragenomic conflict have in common?

Is there a “general theory of conflict” that provides insight into the evolution of conflict at both levels?

Theories of conflict

Two Approaches in the Study of Conflict

Kin SelectionHamilton

Game Theoryvon Neumann &

Morgenstern

Single method

r.B > CCost Dependson Social Context

Generalised Hamilton’s rule

Wenseleers & Ratnieks submitted

j jgB.r - C+E . > 0β

Hamilton’s rule(costs & benefits

independent of social context)

Terms thattake into

account socialcontext

Consequence ofboth cooperating

Regression of genotype on joint behaviour


0 -B

B -C

DOVE HAWK

DO

VE

HA

WKANIMAL CONFLICT

COOPERATEDRIVE

CO

OP

ER

ATE

DR

IVE

GDC.(1-k)1/2

GDC.k GDD/2

GENOMIC CONFLICT(MEIOTIC DRIVE)


Shows that game theoretic logic of conflict at both levels is the same

But can genes also be related?

Yes, kinship measures genetic correlation and for 2 genes at a locus this is the inbreeding coefficient FIT

When genes are related they are selected to be altruistic !

Application of generalised Hamilton’s rule allows detailed analysis

Spite: Hamilton’s unproven theory

Medea killed her children to take away the smile from her husband’s face.

Example of a paradoxical behaviour that harms another at no benefit to self (“spite”)

We showed that some forms of intragenomic conflict qualify as spiteful behaviour (Maternal effect lethals, queen killing in the fire ant)

Foster, Ratnieks & Wenseleers (2000) Trends in Ecology & Evolution 15:469-470Foster, Wenseleers & Ratnieks (2001) Annales Zoologici Fennici, in press

Why become a worker? Why do social insect females work

for the benefit of others?

Usual explanation: indirect genetic benefit when altruism is directed towards relatives (’kin selection’)

But is relatedness in insect societies high enough?

E.g. honey bee: queen mates with several males so that workers mostly rear half-sisters (r=0.3)

New calculations Female should become a queen with a

probability of (1-Rf)/(1+Rm) (self determination)

– = 20% for stingless bees (singly mated)

– = 56% for honey bees (polyandrous)

Too high for the colony as a whole, since queens are only needed for swarming (“tragedy of the commons”)

Adult workers and mother queen selected to prevent production of excess queens (“policing”)

Comparative predictions hold

Self determination20% queen production

stingless bees

Policing of caste fate0.02% queen production

honey bees

Individual Freedom Causes a Cost to Society

But females prefer to become

queen with probability

of 56% !

Efficient Society but

No Individual Freedom

THE SAME TENSION OCCURS IN HUMAN SOCIETY !

General conclusions Part I : empirical

– Does Wolbachia occur in ant societies? YES, IN HIGH FREQUENCY

– Alternative explanation for female biased sex-ratios in this group? PROBABLY NOT

– Other effects? INCOMPATIBILITY (SPECIATION?)

Part II : theoretical– What do animal and genomic conflicts have in

common? SAME LOGIC– Can sociobiological theory be applied to both?

YES (GENERALISED HAMILTOM’S RULE)– What do we learn from this more generally?

DEEPER INSIGHT INTO THE FUNCTIONING OF HUMAN SOCIETIES (TOC)

The End

AcknowledgementsProf. Dr. J. Billen Prof. Dr. R. Huybrechts Prof. Dr. J.J. Boomsma Dr. F. ItoDr. K.R. Foster Dr. F.L.W. RatnieksProf. S.A. Frank Dr. L. Sundström Dr. D.A. Grasso Drs. S. Van Borm Prof. Dr. F. Volckaert Academy of Finland, British Council,

FWO-Vlaanderen, Vlaamse Leergangen, EU Network “Social Evolution”

Tom Wenseleers University of Leuven, Belgium Ph.D. defence May 22nd, 2001 Conflict from Cell to...

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