Discrimination behavior in the supercolonial pharaoh ant

140 Pages·2014·5.25 MB·Danish

FACULTY OF SCIENCE
UNIVERSITY OF COPENHAGEN

CENTRE FOR SOCIAL EVOLUTION

DEPARTMENT OF BIOLOGY

PhD thesis

Luigi Pontieri

Discrimination behavior in the

supercolonial pharaoh ant

Academic advisor
Jes Søe Pedersen
June 2014
faculty of science
university of copenhagen
centre for social evolution
department of biology
Danish National Research Foundation
Centre for Social Evolution
Discrimination behavior in the supercolonial
pharaoh ant
This thesis dissertation has been submitted in accordance with the requirements
for the degree of PhD, at the PhD School of The Faculty of Science, University
of Copenhagen, Denmark to be defended publicly before a panel of examiners.
by
Luigi Pontieri
June 2014
Academic advisor
Assoc. Prof. Jes Søe Pedersen
Cover: artwork of queens, workers and brood of Monomorium pharaonis
© Luigi Pontieri
P
reface
This thesis is the result of a three year PhD project carried out at the Centre for Social
Evolution (CSE), Department of Biology, University of Copenhagen in Denmark
under the supervision of Assoc. Prof. Jes Søe Pedersen. During my PhD period I spent
three months in the laboratory of Assoc. Prof. Timothy Linksvayer, Department of
Biology, University of Pennsylvania. I additionally spent a total of three weeks at
the Laboratoire d’Ethologie Expérimentale et Comparée (LEEC), Université Paris
13, Sorbonne Paris Cité, hosted by Prof. Patrizia d’Ettorre. The projects in this thesis
were funded by CSE via a grant from the Danish National Research Foundation (grant
DNRF 57).
The thesis is comprised of a general introduction on the problem of biological invasion
with a special focus on invasive ant species, the traits that makes them successful
invaders and how genetic diversity can affect the recognition system and the intra- and
interspecific interactions that these species present. I then present my model organisms,
a summary of the main findings of my projects and suggested future directions. This is
followed by four chapters of original empirical work, three of which are in preparation
for submission in peer reviewed journals and one is currently submitted.
Luigi Pontieri
Copenhagen, June 2014

c
ontents
SummarieS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
reSumé . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
General introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Introduced SpecIeS and the problem of bIologIcal InvaSIonS . . . . . . . . . . . . . . . . 14
InvaSIve antS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
the “InvaSIve ant Syndrome” . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
the Structure of unIcolonIal populatIonS and the problem of recognItIon . . . . . . . . . 16
ant recognItIon SyStem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
the effect of genetIc dIverSIty on neStmate recognItIon and Supercolony InteractIonS . . 18
the effect of unIcolonIalIty on dISeaSe Spread . . . . . . . . . . . . . . . . . . . . . . 20
model organISmS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
The Pharaoh ant 22
Metarhizium brunneum 26
Short Summary of the theSIS chapterS . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
future perSpectIveS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
referenceS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
chapter 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
genetIc dIverSIty IS more Important than relatedneSS for neStmate dIScrImInatIon In the pharaoh
ant
chapter 2 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
unexpected fuSIon of genetIcally and chemIcally dIvergent colonIeS of the InvaSIve pharaoh ant
chapter 3 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
the StatIStIcal approach to IdentIfy neStmate recognItIon cueS
chapter 4 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115
ant colonIeS prefer Infected over unInfected neSt SIteS
acknowledGementS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 37

e , d
nGliSh anSk
Summaries
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s
ummary
The majority of eusocial insect species live in small, kin structured colonies that are mutually aggressive
and rarely interact. By contrast, a restricted group of ant species show a peculiar social organization
called unicoloniality, where colonies can grow to vast networks of geographically separated but mutually
tolerant nests, also referred to as “supercolonies”. Many unicolonial ants are invasive, as their introduced
supercolonies attain huge size and cause severe economic and ecological damage, affecting in particular
species composition and functioning of ecosystems. There is therefore an increasing need to understand
which factors promote the ecological dominance of these species, and particularly how the discrimination of
both conspecifics and heterospecifics (including parasites) might influence structure and ecological success
of invasive populations. In this PhD thesis I investigated the discrimination behavior of the invasive pharaoh
ant (Monomorium pharaonis) as a model for other invasive and supercolonial ant species. The pharaoh ant
is one of the few ant species that can be reared in the laboratory for many generations. Furthermore, the
possibility to do controlled crosses of colonies provides the unique opportunity to establish colonies of
different genetic composition. These traits make this species a suitable study subject to set up behavioral
experiments that aim to investigate which factors, and to which extent, might influence the inter- and intra-
specific discrimination abilities of invasive ants.
In the first chapter I focused on the nestmate recognition system of pharaoh ants, investigating whether
the cues used for discrimination had a genetic origin and how different level of within-colony genetic
diversity and relatedness influenced the discrimination abilities of the colonies. I show that, despite a general
ability of discriminating nestmates from non-nestmates, the degree of relatedness between colonies did not
influence the overall level of discrimination. Furthermore, I found that genetically low-diverse colonies
displayed better discrimination abilities than high diverse ones and that low genetically diverse colonies
discriminated high diverse non-nestmates better than vice versa.
In the second chapter I investigated whether the high genetic differentiation characterizing natural
colonies of pharaoh ants is sufficient to prevent unrelated colonies to fuse and how different levels of
genetic similarity shape the outcome. By pairing laboratory colonies in a fusion assay, I show that the
majority of unrelated colonies fused despite high initial levels of aggression. Moreover, I also found that the
initial aggression was positively correlated with the chemical and genetic distance between colony pairs,
further confirming the important role of endogenous cues in the nestmate recognition of this species.
The third chapter presents a methodological study on the best procedures for identifying chemical
compounds used for nestmate recognition in social insects. We first compiled datasets of cuticular
hydrocarbons (CHCs) and aggression between colonies of three species of ants (Formica exsecta,
Camponotus aethiops and Monomorium pharaonis) and a simulated dataset. Then, using the available
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information about the exact cues used for nestmate recognition in F. exsecta, we evaluated the power of
different combinations of data transformation and chemical distance calculation in differentiating between
true nestmate recognition (NMR) cues and other compounds. We found that particular combinations of
statistical procedures are more effective in differentiating NMR cues from other compounds. We also
developed a new method for centroid calculation that increased the power of the analysis and can therefore
be used in future studies that aim to identify nestmate recognition cues in other species.
In the fourth chapter I investigated the nest site preference of pharaoh ant colonies and, specifically,
their ability to avoid nests containing infectious pathogens as invasive, supercolonial ants are hypothesized
to be particularly prone to disease. Using binary choice tests between three types of nests, I found that
migrating colonies surprisingly preferred nest sites containing nestmate corpses overgrown with sporulating
mycelium of the generalist fungus Metarhizium brunneum. This unexpected finding can provide new insight
into the important co-evolution of social insects and their pathogens.
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