Dynamics of ant-microbial interactions

150 Pages·2011·2.03 MB·English

by  Sandra Breum Andersen

FACULTY OF SCIENCE FFFAAACCCUUULLLTTTYYY OOOFFF SSSCCCIIIEEENNNCCCEEE
UNIVERSITY OF COPENHAGEN UUUNNNIIIVVVEEERRRSSSIIITTTYYY OOOFFF CCCOOOPPPEEENNNHHHAAAGGGEEENNN

Dynamics of ant-microbial interactions
Coevolution along the parasitism-mutualism continuum

A dissertation submitted to the University of Copenhagen in accordance with the
requirements for the degree of the PhD at the Graduate School of Science, Faculty of
Science, University of Copenhagen, Denmark to be defended publicly before a panel
of examiners

Sandra Breum Andersen
December 2011

Academic advisors:
David P. Hughes & Jacobus J. Boomsma
2
Preface
This
PhD
thesis
is
the
result
of
three
years
of
work
at
the
Centre
for
Social

Evolution
at
University
of
Copenhagen,
pleasantly
interrupted
by
shorter
periods

of
fieldwork
in
Panama
and
Brazil
and
a
stay
at
Penn
State
University
USA,
under

supervision
of
David
Hughes
and
Jacobus
(Koos)
Boomsma.
I
was
funded
by
a

grant
from
the
Faculty
of
Science,
University
of
Copenhagen.

My
 project
 proposal
 was
 originally
 aimed
 at
 elucidating
 the
 role
 of

Ophiocordyceps
 fungal
 symbionts
 in
 leaf‐cutting
 ants,
 however
 I
 gradually

became
 less
 and
 less
 convinced
 that
 these
 fungi
 actually
 had
 a
 role
 to
 be

elucidated
and
we
decided
to
make
the
scope
of
the
thesis
broader,
including
a

variety
of
different
microbial
symbionts
of
ants.
I
am
thus
very
grateful
to
be
able

to
 present
 a
 thesis
 including
 work
 on
 three
 exciting
 systems
 of
 microbial

symbioses
with
ants.


The
thesis
is
comprised
of
a
synopsis
of
the
current
understanding
of
symbiotic

interactions,
which
provides
the
theoretical
framework
for
the
following
four

chapters
 of
 original
 empirical
 works,
 prepared
 for
 publication.
 A
 short

concluding
 section
 aims
 at
 putting
 the
 obtained
 results
 into
 a
 broader

perspective.



Sandra
Breum
Andersen



 3
4
Table of Contents

SUMMARIES.....................................................................................................................................7

SYNOPSIS......................................................................................................................................11

INTRODUCTION TO SYMBIOTIC INTERACTIONS.............................................................13

Evolution of interactions –cooperation and conflict.............................................................13

Adaptations to symbiotic life..............................................................................................................15

Complexity of multi-species interactions....................................................................................17

THESIS OBJECTIVES...........................................................................................................................20

The social insect as hosts and symbiotic partners...............................................................20

The model systems................................................................................................................................22

Techniques and fieldwork...................................................................................................................23

Chapter outlines.......................................................................................................................................25

REFERENCES...........................................................................................................................................26

CHAPTER 1....................................................................................................................................31

DECONSTRUCTING A DISEASE-DEFENCE SYMBIOSIS: SPECIFICITY AND
STABILITY OF ACROMYRMEX-PSEUDONOCARDIA ASSOCIATIONS IN
CHANGING ENVIRONMENTS.........................................................................................................31

CHAPTER 2....................................................................................................................................65

DYNAMIC WOLBACHIA PREVALENCE IN ACROMYRMEX LEAF-CUTTER
ANTS: POTENTIAL FOR A NUTRITIONAL SYMBIOSIS....................................................65


 CHAPTER 3..........................................................................................................................97

DISEASE DYNAMICS IN A SPECIALIZED PARASITE OF ANT SOCIETIES..........97

CHAPTER 4..................................................................................................................................127

........................................................................................................................................................................127

HOST SPECIFICITY OF PARASITE MANIPULATION –ZOMBIE ANT DEATH
LOCATION IN THAILAND VS. BRAZIL.......................................................................................127

CONCLUSIONS AND PERSPECTIVES.............................................................................137

PICTURES....................................................................................................................................145

ACKNOWLEDGEMENTS........................................................................................................147

CURRICULUM VITAE...............................................................................................................149



 5
6
SUMMARIES
ENGLISH
DANSK


 7
8
Summary 



The
life
history
of
social
insects,
with
division
of
labour,
cooperative
brood
care

and
overlapping
generations,
affects
the
strategies
of
the
associated
symbionts.
A

high
 density
 of
 related
 individuals
 could
 be
 an
 open
 invitation
 to
 recurrent

disease
 epidemics,
 but
 the
 complementary
 layers
 of
 social
 and
 individual

immunity
efficiently
protect
the
society.
In
this
thesis
the
interaction
between

ants
 and
 three
 different
 microbial
 symbionts
 are
 dealt
 with,
 covering
 the

spectrum
from
parasitism
to
mutualism
and
something
in
between.





Two
chapters
focus
on
the
leaf‐cutting
ants
native
to
South
and
Central
America

that
are
(in)famous
for
their
ability
to
defoliate
vegetation
surrounding
their

colonies,
making
them
the
dominant
herbivores
of
the
region.
The
leaf‐cutter

ants
are
the
most
advanced
of
the
fungus‐growing
ants
and
this
is
what
makes

them
capable
of
living
on
leaves:
in
underground
chambers
the
ants
farm
fungus

that
degrade
the
substrate
the
ants
bring
it,
in
return
letting
the
ants
feed
on
the

fungus.
The
association
between
the
ants
and
the
fungus
are
the
corner
stones
in

an
intriguing
multi‐trophic
interaction
involving
also
other
fungi
and
bacteria.


One
of
these
bacterial
partners
called
Pseudonocardia
grow
on
the
cuticle

of
some
leaf‐cutter
ants,
visible
to
the
naked
eye
as
a
white
patch
on
the
ants’

chest,
and
used
by
the
ants
as
antibiotic
factories
employed
against
a
parasite
of

the
fungus
garden.
The
diversity
of
the
bacteria
on
the
ants
has
been
the
subject

of
some
controversy.
We
found
a
low
diversity
with
only
one
strain
of
bacteria

dominating
on
the
ants.
By
comparing
ants
collected
in
the
field
and
in
the
lab

from
the
same
colonies
we
show
that
this
association
is
highly
stable,
even
after

10
years
in
the
lab
and
exposure
to
many
other
bacteria.




Another
bacterial
partner
is
of
the
genus
Wolbachia
and
these
are
live

inside
the
ants’
tissues.
Wolbachia
are
found
associated
with
a
wide
range
of

insects
and
typically
as
a
reproductive
parasite,
yet
what
they
may
do
in
the
leaf‐
cutter
ants
is
not
well
understood.
Our
work
show
that
the
ants
are
found
in

great
numbers
in
sterile
workers
and
surprisingly
also
extracellularly
in
the
gut,

suggesting
a
new
potential
role
in
the
ant’s
nutritional
system.

In
 contrast
 to
 these
 likely
 helpful
 bacteria
 carpenter
 ants
 in
 tropical

regions
of
the
world
are
attacked
by
parasitic
fungi
of
the
genus
Ophiocordyceps.

When
infected,
the
ants
are
manipulated
into
leaving
their
colony
and
die
in

‘graveyards’,
biting
under
leaves.
The
last
two
chapters
of
the
thesis
deals
with

the
disease
pressure
of
this
parasite
experienced
by
the
ant
colonies,
which
is

found
to
be
surprisingly
low,
and
how
the
social
structure
of
the
host
apparently

has
 shaped
 the
 life‐strategy
 of
 the
 parasite
 into
 iteroparity.
 In
 addition,

differences
in
the
manipulation
was
found
between
species
in
Thailand
and

Brazil,
 likely
 reflecting
 variation
 in
 host
 behaviour
 and
 environmental

parameters.


Together,
the
four
chapters
highlights
different
ways
in
which
the
symbionts
of

ants
have
adapted
to
the
social
structure
of
the
host.



 9
Resumé
De
sociale
insekters
livshistorie,
med
opdeling
af
arbejdsopgaver,
fælles
pleje
af

afkom
og
overlappende
generationer,
påvirker
strategierne
hos
de
forskellige

symbionter
 der
 associerer
 med
 kolonien.
 En
 høj
 tæthed
 af
 nært
 beslægtede

individer
 kan
 synes
 at
 være
 en
 åben
 invitation
 til
 gentagne
 epidemiske

sygdomsudbrud,
 men
 de
 kompletterende
 lag
 af
 hhv.
 individuel
 og
 social

immunitet
beskytter
effektivt
kolonien.
Denne
afhandling
ser
på
hvordan
tre

forskellige
 symbionter
 interagerer
 med
 myrer,
 dækkende
 hele
 spektret
 fra

mutualisme
til
parasitisme
og
noget
ind
i
mellem.


To
kapitler
fokuserer
på
bladskærermyrerne
fra
Syd
og
Central
Amerika,
som
er

berømte
og
berygtede
for
deres
evner
udi
defoliering
af
vegetationen
omkring

deres
kolonier,
med
en
sådan
effektivitet
at
de
er
de
dominerende
herbivorer
i

regionen.
 Bladskærermyrerne
 er
 de
 højst
 udviklede
 af
 de
 svampedyrkende

myrer,
 og
 heri
 ligger
 forklaringen
 på
 hvordan
 de
 kan
 leve
 af
 blade:
 I

underjordiske
kamre
dyrker
myrerne
en
svamp
og
denne
nedbryder
bladene
for

myrerne
 der
 til
 gengæld
 for
 lov
 at
 spise
 af
 svampen.
 Mutualismen
 mellem

myrerne
og
svampen
er
grundlaget
for
en
avanceret
fler‐laget
symbiose
der

involverer
flere
forskellige
svampe
og
bakterier.


 Én
af
disse
bakterielle
partnere
kaldet
Pseudonocardia
gror
på
myrernes

exoskelet
og
kan
ses
med
det
blotte
øje
som
en
hvid
plet
på
myrernes
bryst.

Bakterierne
 bruges
 af
 myrerne
 som
 mobile
 antibiotikafabrikker
 som
 kan

aktiveres
hvis
en
parasitisk
svamp
invaderer
deres
svampehave.
Diversiteten
af

disse
bakterier
har
længe
været
noget
kontroversiel.
Vores
studium
fandt
en
lav

diversitet
hvor
kun
én
slags
bakterie
dominerer.
Ved
at
sammenligne
myrer
der

var
 indsamlet
 i
 felten
 og
 i
 laboratoriet
 fra
 de
 samme
 kolonier
 viser
 vi
 at

associationen
er
meget
stabil,
selv
efter
op
til
10
år
i
laboratoriet
omgivet
af

kolonier
med
andre
bakterier
har
myrerne
de
samme
som
i
felten.


 En
anden
slags
bakterier
af
slægten
Wolbachia
lever
inde
i
myrernes
væv.

Wolbachia
 findes
 i
 et
 bredt
 udvalg
 af
 insekter,
 oftest
 som
 reproduktive

parasitter,
men
hvordan
de
påvirker
bladskærer
myrerne
er
ikke
klart.
Vores

studium
viser
at
bakterierne
findes
i
vævet
i
højt
antal
i
de
ellers
sterile
arbejder

myrer
og
overraskende
nok
også
ekstra
cellulært
i
dele
af
tarmen.
Dette
kunne

tyde
på
at
bakterierne
spiller
en
rolle
i
myrernes
fordøjelses
system.


I
 modsætning
 til
 de
 tilsyneladende
 hjælpsomme
 bakterier
 angribes

’tømrer’
 myrer
 i
 verdens
 tropiske
 egne
 af
 parasitiske
 svampe
 af
 slægten

Ophiocordyceps.
Inficerede
myrer
manipuleres
til
at
forlade
deres
koloni
og
dø
i

’kirkegårde’
fastbidt
i
blade.
De
sidste
to
kapitler
i
afhandlingen
fokuserer
på

hvilken
effekt
svampen
har
på
myrekoloniens
tilstand,
hvilken
konkluderes
at

være
overraskede
lav,
og
hvordan
myreværtens
sociale
struktur
har
påvirket

svampen
livsstrategi
i
retning
af
iteroparitet.
Dertil
kommer
en
sammenligning

af
selve
myremanipulationen
mellem
arter
fra
Brasilien
og
Thailand,
hvor
en

forskel
 blev
 fundet,
 formentlig
 afhængig
 af
 forskelle
 i
 myrernes
 adfærd
 og

miljømæssige
variabler.


Tilsammen
 afdækker
 de
 fire
 kapitler
 forskellige
 aspekter
 af
 symbionters

tilpasning
til
en
social
myre
vært.


 10