Kin Selection, Social Polymorphism, and Reproductive Allocation in Ants

Katja Bargum

Kin selection, social polymorphism, and reproductive allocation in ants

Helsinki 2007 Kin selection, social polymorphism, and reproductive allocation in ants

Katja Bargum

Department of Biological and Environmental Sciences University of Helsinki Finland

Academic dissertation

To be presented, with the permission of the Faculty of Biosciences of the University of Helsinki, for public criticism in Auditorium 1041 of Biocenter 2, Viikinkaari 5, on March 30th, 2007, at 12 o´clock noon.

Helsinki 2007 © Katja Bargum (chapters 0, II, IV) © Springer Publishing (chapter I) © Blackwell Publishing (chapters III, V)

Cover illustration © Patrik Karell (2007) Layout © Katja Bargum

Author´s address: Department of Biological and Environmental Sciences P.O. Box 65 (Viikinkaari 1) FI-00014 University of Helsinki Finland e-mail: [email protected]

ISBN 978-952-92-1758-8 (paperback) ISBN 978-952-10-3795-5 (PDF) http://ethesis.helsinki.fi

Helsinki University Printing House Helsinki 2007

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2 Kin selection, social polymorphism, and reproductive allocation in ants

Katja Bargum

This thesis is based on the following articles, which are referred to in the text by their Roman numerals:

I. Bargum, K., Boomsma, J.J. & Sundström, L. 2004. A genetic component to size in queens of the ant Formica truncorum. – Behavioral Ecology and Sociobiology 57:9–16.

II. Bargum, K. & Sundström, L. Colony-level life history trade-offs and reproductive skew in the ant Formica fusca. – Manuscript.

III. Bargum, K. Helanterä, H. & Sundström, L. Genetic population structure, queen supersedure and social polymorphism in a social Hymenoptera. – Journal of Evolutionary Biology, in press.

IV. Bargum, K. & Sundström, L. Multiple breeders, breeder shifts and inclusive fitness returns in an ant. – Submitted manuscript.

V. Lehmann, L., Bargum, K. & Reuter, M. 2006. An evolutionary analysis of the relationship between spite and altruism. – Journal of Evolutionary Biology 19:1507–1516.

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3 Contributions

I II III IV V

Original idea LS, JJB KB, MH, LS KB, HH, LS KB, LS LL, KB, MR

Methods LS, KB, JJB KB KB, HH KB LL

Data collection KB, LS KB, RO KB, LS KB, LS

Data analyses / Model KB KB KB, HH KB LL

Manuscript preparation KB, LS KB, LS KB, HH, LS KB, LS LL, KB, MR

KB: Katja Bargum, LS: Liselotte Sundström, JJB: Jacobus Boomsma, MH: Minttu Hannonen, RO: Riitta Ovaska, HH: Heikki Helanterä, LL: Laurent Lehmann, MR: Max Reuter

Supervised by: Prof. Liselotte Sundström, University of Helsinki, Finland

Reviewed by: Prof. Pekka Pamilo, University of Oulu, Finland Prof. Jes Søe Pedersen, University of Copenhagen, Denmark

Examined by: Dr. Michel Chapuisat, University of Lausanne, Switzerland

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4 Contents

Summary 6 Introduction 6 1. Social polymorphism in ants: causes and life history consequences 9 Benefits of polyandry 11 Benefits of polygyny 11 Population-level patterns 12 Individual fitness consequences of polygyny 12 Skew in sexual versus worker offspring 14 2. Social semantics: Altruism and spite 14 3. Material and methods 15 Study species 15 Field studies 15 Experiments 15 Genetic analyses 16 Modeling 16 4. Main results and discussion 16 Genetic diversity and within-colony variability in F. truncorum and F. fusca 16 Population-level patterns of social polymorphism and life-history traits in F. fusca 17 Reproductive skew in F. fusca 18 Altruism and spite 20 5. Implications and future directions 21 Methodological implications 21 Unresolved issues 21 What determines queen fecundity? 21 What is the role of the workers in determining offspring identity? 22 Concluding remarks 23 6. Acknowledgements to the summary 23 7. Literature cited 23 8. Acknowledgements 30

Chapter I 35

Chapter II 45

Chapter III 65

Chapter IV 83

Chapter V 95 ______

5 Summary ______

Summary

Katja Bargum Department of Bio- and Environmental Sciences P.O. Box 65, 0014 University of Helsinki, Finland

Introduction

Social groups are common across animal species. individuals reproduce (Hamilton 1964). The reasons for grouping are straightforward Hamilton´s rule br > c states that a costly when all individuals gain directly from cooperating. behaviour such as helping can spread when the For example, in many cooperatively breeding benefits b to the recipient weighted by the species, larger group size may result in higher relatedness r outweighs the cost c carried by the survival or foraging success for all members. helper. In the wake of Hamilton´s seminal Accordingly, individuals may help to rear papers, kin selection theory has been widely and offspring other than their own in order to successfully applied to explain cooperation in increase group size (Kokko et al. 2001). However, animal groups, from collaborating microbes the situation becomes more complex when (West et al. 2006b) to the evolution of eusociality helping entails costs to the personal reproduction (Foster et al. 2006; Helanterä & Bargum 2006). of individuals. Moreover, such costs are often However, kin selection theory also not equally shared by all individuals, but instead implicitly predicts conflicts when groups consist lead to some individuals reproducing less than of non-clonal individuals (r<1). Then, individual others. Thus, in cooperatively breeding animals, interests are not perfectly aligned, and each the division of reproduction (reproductive skew) individual is predicted to favour the propagation varies from each individual breeding equally over their own genome over others. Accordingly, to complete monopolisation by one or a few conflicts have been studied at many levels of individuals, as is seen in the eusocial insects. This social complexity, from unicellular organisms to situation poses an evolutionary puzzle, since eusocial insect colonies. Emerging research into altruistic traits that make individuals reproduce microbes shows how conflict can disrupt less than others should disappear over cooperation when genetically non-clonal strains evolutionary time. come together (Rainey & Rainey 2003; Velicer The solution to the puzzle was offered 2003). In social insects, differing interests of by the realisation that individuals may spread colony members lead to conflict over their genes not only through their own reproduction, colony sex ratios, and caste fate reproduction, but also by helping related (Ratnieks et al.¬2006). Indeed, observations on

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6 Summary ______conflicts and conflict resolution in social insects across animal systems, an extensive modeling have provided some of the strongest evidence framework of optimal skew has been developed for kin selection in action (Sundström 1994; (reviewed in Reeve & Keller 2001). Recent studies Sundström et al. 1996, Ratnieks et al. 2006). have also stressed that helpers may stay in Intra-group relatedness varies from expectation of future fitness benefits, through one, when organisms are clonal, through resource inheritance (Kokko & Johnstone 1999; intermediate values where groups consist of Ragsdale 1999; Blumstein & Armitage 1999; extended families, to zero in e.g. male bottlenose Michell 2005; Field et al. 2006). Since cooperation dolphin male alliances (Möller et al. 2001). All is frequently linked to the decision to disperse other factors being equal, this variation is or not, variation in social structure will be predicted to have implications for the extent of reflected in patterns of population structure and cooperation. For example, in many birds, parents gene flow. collaborate to raise young. Multiple mating by Social insects have proven one of the the female lowers relatedness between the most successful fields to study kin selection in a offspring, which some studies show leads to a variety of social settings. Breeding systems in reduction in cooperation, such as decreased Hymenoptera (i.e. wasps, bees and ants) range offspring provision by the male (Burke et al. from solitary breeding and temporary associations 1989; Neff 2003; Westneat & Stewart¬2003). of cobreeders to eusocial colonies displaying However, cooperation may be upheld if complete division of reproduction between the individuals can increase r by preferentially fertile queen and the permanently sterile worker interacting with their closer relatives in the group caste (Sherman et al. 1995). Within eusocial (nepotism) (Widdig et al.¬2002; Griffin & West colonies, additional variation is provided by the 2003; Wahaj et al.¬2004). Alternatively, individuals presence of several reproductive individuals. In may choose to harm non-siblings over siblings many species, the queen mates multiply, which (Pfennig et al. 1994; Evans 1999). Thus, variation causes the colony to consist of half-sib instead in relatedness may have dramatic effects on of full-sib workers. Furthermore, in many species interactions between individuals. colonies contain multiple breeding queens, which On the other hand, cooperation will further dilutes relatedness between colony also be influenced by b and c, i.e. benefits and members, resulting in lower inclusive fitness costs of cooperation, which are in turn determined paybacks from helping. Evolutionary biology is by environmental factors such as ecological thus faced with the challenge to answer why such constraints to leaving the group, and group variation in social structure, or social productivity. For example, individuals may polymorphism, exists, and what the choose to cooperate when the cost for helping consequences are on the individual and is low, as in the long-tailed tit, where individuals population level. help only when their own dispersal is restricted The main part of this thesis (Chapters by ecological constraints (Russell 2001). To I-IV; Fig. 1) takes on this challenge by incorporate all these factors and explain how investigating the dynamics of socially reproductive inequality can be evolutionary stable polymorphic ant colonies. The four chapters

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7 Summary ______investigate the causes and consequences of 1. Social polymorphism in ants: causes different social structures. The thesis ends with and life history consequences a theoretical chapter (V) focusing on different social interactions (altruism and spite), and the All ants are eusocial and most species contain evolution of harming traits (Fig 1). strictly defined queen and worker castes. Social In this summary, I will start by polymorphism is generated by differences in the introducing the reader to the concept of social number of breeders. In many species, colonies polymorphism in ants. Using a kin selection are headed by one singly mated queen. Such a framework, I will point out the potential costs system ensures high fitness payoffs for all and benefits of different social systems, and individuals in the colony. The queen reproduces define predictions that were tested in this thesis. to her full potential, without competition from I will then describe the key results of this thesis other queens. Additionally, all workers are full as they pertain to the topics discussed. I will end sisters and receive high inclusive fitness returns by considering methodological issues raised by from raising their full siblings. this work, as well as future directions towards However, not all ant colonies consist of such answering unresolved questions. simple family units. In many species of ants,

Box 1. List of terms used in the introduction

Gynes: female sexual offspring (i.e. future queens)

Monogyny: colonies contain only one queen

Polygyny: colonies contain several queens

Monandry: single mating by the queen

Polyandry: multiple mating by the queen

Queen turnover: the rate of replacement of queens within a colony

the extent to which reproduction is unevenly shared between queens. Reproductive skew: The more unequal the sharing, the higher the skew

offspring who, in contrast to worker offspring, will mate and reproduce Sexual offspring: (i.e. future queens and males)

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8 Summary ______queens are multiply mated (polyandry), or the populations, or even within populations colony encompasses multiple queens (polygyny) (Hölldobler & Wilson 1977, 1990; Keller 1993b; (Hölldobler & Wilson 1977, 1990; Keller 1993b). Sundström et al. 2005). Indeed, in many species, The degree of polyandry varies between species, facultative polygyny appears to be the rule, rather from single mating in fire ants to tens of matings than the exception (Bourke & Heinze 1994; in leafcutter and harvester ants (Strassmann 2001; Keller 1995; Sundström et al. 2005). We may Kronauer et al.¬2004; Denny et al.¬2004; Rheint therefore ask what factors promote and maintain et al.¬2004), and, albeit less dramatically, within social polymorphism in ants. species as well (reviewed in Boomsma & Ratnieks Polyandry and polygyny have been 1996). Similarly, polygyny is often facultative, suggested to entail several costs and benefits for with queen number varying from one to several the parties involved (see Table 1). Both polyandry hundred either within species and between and polygyny pose a cost to workers because the

G eograp

hic and Dispersal

genet

ic morphism structur y

e Social polymorphismpol

Queen turnover Worker interests

Queen-queen interactions Offspring characteristics

Social interactions

Figure 1. Main themes of this thesis

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9 Summary ______increased number of patri- and/or matrilines usually lower than in monogyne colonies where dilutes relatedness among colony members, and the queen reproduces to her full potential thus reduces inclusive fitness returns for workers. without competition from other queens (Elmes For queens, polyandry may be costly when 1973; Herbers 1984; Keller 1988; Sundström multiple mating increases energy consumption 1995b; but see Walin et al. 2001). However, or predation risk of queens (i.e. Bourke & there may be several benefits to polyandry and Franks 1995). Similarly, polygyny poses a cost polygyny which potentially make up for these to resident and joining queens alike, because costs, and maintain social polymorphism in ant the per capita reproductive output per queen is species.

Table 1. Some costs and benefits associated with a) a polyandrous colony structure relative to a monandrous one, and b) a polygyne colony structure relative to a monogyne one, and predictions drawn from these (e.g. Keller 1995; Crozier & Fjerdingstad 2001). Predictions in bold are tested in some form in this thesis.

Costs Benefits Predictions a) Polyandry Queens: Workers: – risky mating – sex allocation manipulation Sex ratio changes with mating frequency Workers: Queens and workers: Genetic diversity contributes to offspring variability (I, II) – indirect fitness loss – genetic diversity Genetic diversity contributes to colony fitness – adequate sperm supply One male´s sperm is not enough

b) Polygyny Queens: Queens: Adoption of related queens (colony daughters) (II,III,IV) – direct fitness loss – avoiding risky dispersal Reproductive skew according to and colony founding worker interests (IV) Rapid queen turnover (III) Workers: Queens and workers: Local mating (III) – indirect fitness loss – colony persistence Genetic clustering of colonies within populations (III) – colony productivity Isolation by distance between populations – genetic diversity Higher colony survival (III) Higher colony productivity Genetic diversity contributes to colony fitness

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10 Summary ______

Benefits of polyandry al. 1993). However, this hypothesis depends on to what extent physiological traits are influenced Some potential benefits of polyandry are laid out by genetic versus environmental factors, which in Table 1. One of the strongest arguments for remains mostly uninvestigated in social insects why colonies may benefit from polyandry is that (but see Fraser et al.¬2000; Hughes et al.¬2003, multiple mating enhances genetic variability Schwander et al.¬2005). Chapters I and II test (Crozier & Fjerdingstad 2001). If genetic this hypothesis. variability is connected to colony fitness, this may offset the reduction in relatedness caused by that Benefits of polygyny same variability. Indeed, the benefit of genetic diversity is one of the main hypotheses to explain Polygyny may, for its part, provide benefits for the evolution of multiple mating in animals in all colony members in the presence of strong general (Jennions & Petrie 2000), as well as the ecological constraints on independent breeding evolution of polyandry and polygyny in social (table 1). If dispersal risks are high and subsequent insects (Sherman et al. 1988; Schmid-Hempel colony founding success low, both workers and 1998; Schmid-Hempel & Crozier 1998; Crozier resident queens favour the adoption of daughter & Fjerdingstad 2001). In accordance with the queens into colonies, since these have low hypothesis, genetically diverse colonies often chances of reproducing otherwise (Rosengren have better performance or higher growth rate & Pamilo 1983; Nonacs 1988; Pamilo 1991a; (Page et al. 1995, Wiernasz et al. 2004). There Keller 1995; Cahan et al. 2002). Similarly, when are several mechanisms that could explain this queen life span is short relative to colony life pattern. Many studies show that genetic diversity span, resident queens and workers can gain benefits the colony through increased parasite inclusive fitness returns if adopted daughter resistance (e.g. bumblebees: Baer & Schmid- queens replace deceased queens (Nonacs 1988). Hempel 2001; honeybees: Tarpy & Seeley 2006; In accordance with these predictions, nestmate leafcutter ants: Hughes & Boomsma 2004). queens are often related in polygyne ant species Genetic diversity may also prevent negative (reviewed in Keller 1995), including our study effects of inbreeding (Crozier & Fjerdingstad species F. fusca (Hannonen & Sundström 2003a, 2001) and reduce within-colony conflict over sex Hannonen et al. 2004, II, III). Despite a short- allocation (Woyciechowski & Lomnicki 1987; term reduction in personal reproduction, adopted Ratnieks & Boomsma 1995). queens stand to gain by avoiding dispersal risks and Lastly, genetic diversity may lead to getting a head start in reproduction, as they can larger variation in individual traits within the forgo the colony growth phase when no colony. A genetically diverse colony may produce reproductive offspring are produced (Oster & more variable new queen offspring, which may Wilson, 1978). be a benefit in a variable environment (Crozier These considerations allow us to predict that & Page 1985), or a more diverse worker force polygyne colonies have longer colony life spans and thus better division of labour (Oldroyd et and shorter queen life spans than monogyne

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11 Summary ______colonies of the same species (Nonacs 1988; increased inbreeding levels in polygyne societies Pamilo 1991a). As a result of shorter queen life if nestmate (and thus mating partner) relatedness spans and recruitment of new queens, the rate is above zero (Pamilo et al. 1997, Ross 2001). at which queens are exchanged (queen turnover) Studies of genetic and behavioural should also be higher in polygyne colonies than differences between social forms have generally in monogyne ones (Nonacs 1988). In agreement focused on cases where monogyne and polygyne with this, queen turnover has been demonstrated colonies are confined to different populations, and in polygyne populations (Seppä 1994; Seppä & the level of polygyny is high. Debate reigns, Walin 1996; Evans 1996; Bourke et al. 1997; however, over whether similar differences can be Pedersen & Boomsma 1999), whereas colonies in expected in populations where the two social forms monogyne populations tend to retain the same coexist, and variation in queen number is less queen across their entire colony life span (Pamilo extreme (i.e. Chapuisat et al. 2004, DeHeer & 1991b, Sundström 1994, Sundström et al. 2003; Herbers 2004; Sundström et al. 2005; Rosset & but see Heinze & Keller 2000; Sanetra & Crozier Chapuisat, 2006). The studies on populations with 2002). We investigate colony survival and the a mixture of two social forms suggest that frequency of queen turnover in chapters III and differences typically seen between social forms IV. in allopatry are absent when the two forms occur in sympatry (Chapuisat et al., 2004, Fournier et Population-level patterns al., 2004; DeHeer & Herbers, 2004). However, a recent study showed that some life history Differences between social forms in dispersal differences may appear also under panmixis and queen philopatry may be mirrored in the (Rosset & Chapuisat, 2006). We investigate the genetic structuring of the population. behaviour and genetic and spatial structuring of Monogyne populations are generally outbred social forms in chapter III. with genetically distinct colonies, but with negligible within- and between-population Individual fitness consequences of structuring (e.g. Pamilo et al. 1997, Sundström polygyny et al. 2005). Conversely, queen philopatry often causes polygyne populations to be In polygyne colonies, the fitness of colony characterized by genetically less distinct members is also determined by the extent of colonies, but extensive genetic structuring reproductive skew. Often, reproduction is not both within populations at a level above shared equally between queens, but instead with individual colonies, and between populations a degree of reproductive skew, so that one or a (e.g. Ross 2001, Sundström et al. 2005). few queens monopolise breeding (Keller 1993b, Furthermore, if philopatry entails mating Bourke & Heinze 1995, Reeve et al. 1998, within or close to the natal nest, it may lead to Hannonen & Sundström 2002, 2003a). The

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12 Summary ______magnitude and direction of skew will affect all 2003a; Paxton et al. 2002; Seppä et al. 2002; colony members. Sumner et al. 2002; Langer et al. 2004, 2006), Firstly, for individual queens, a strong but no clear trend has emerged in favour of a reproductive skew means that some queens must particular model (Reeve & Keller 2001). In this forsake most of their reproduction. To explain thesis, the predictions of optimal skew models why such reproductive inequality could be were tested using two factors: relatedness of evolutionary stable across animal systems, a cobreeding queens and colony productivity (II). modelling framework based on inclusive fitness Previous research of our study species F. fusca benefits received by sharing parties has been found that relatedness covaried negatively with developed (Keller & Reeve 1994). Models of reproductive skew, which is in line with restraint optimal skew seek to explain division of or tug-of-war models (Hannonen & Sundström reproduction by considering factors such as 2003a). ecological constraints to leaving the group, Most models of optimal skew look at relatedness of cobreeders and group productivity skew at one point in time only. However, it is (reviewed in Reeve & Keller 2001). The plethora possible that reproductive skew fluctuates over time, of such models that have been developed in so that dominant breeders are replaced. This may recent years (Emlen 1982a,b; Vehrencamp alleviate the situation for subdominants, because 1983a,b; Reeve & Ratnieks1993; Keller & Reeve they may gain a chance to reproduce in the future. 1994; Reeve & Keller 1995; Reeve et al. 1998; In many species of polygyne ants, replacement Johnstone & Cant 1999; Johnstone 2000) can of breeders (queen turnover) is, indeed, frequent be roughly divided into two groups. The (Evans et al. 1996; Pedersen & Boomsma 1999). transactional models assume that either the Accordingly, future fitness benefits are dominant (concession models, Reeve & Ratnieks increasingly being incorporated into models of 1993) or the subdominant breeder (restraint optimal skew (Kokko and Johnstone 1999; models, Johnstone & Cant 1999) controls Ragsdale 1999). reproductive sharing, whereas the tug-of-war For workers, reproductive skew may models (Reeve et al. 1998) view reproductive raise inclusive fitness benefits, since a high skew sharing as an outcome of an ongoing struggle means colony relatedness remains high. between two parties, both with limited control However, this is true only if the dominant queen over sharing. is a close relative of the workers. It has been The predictions of optimal skew suggested that workers may act as a “collective models have been tested on a variety of species dominant” to ensure that their relatives gain (vertebrates: Jamieson 1997; Clutton-Brock et al. reproductive benefits (Reeve & Keller 2001; 2001; Engh et al. 2002; Haydock & Koenig 2002; Reeve & Jeanne 2003). Evidence for such social insects: reviewed in Reeve & Keller 2001; nepotistic actions is rare in social insects, but Fournier & Keller 2001; Hannonen & Sundström intriguingly, Hannonen & Sundström (2003b)

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13 Summary ______found that in F. fusca, workers influence produce less sexuals (Fournier et al. 2004). Thus, reproductive skew by recognising and reproductive skew may actually decrease, instead favouring their relatives during offspring of increase, the inclusive fitness benefits for development. workers. The correlation between sexual and worker skew, and its impact on worker indirect Skew in sexual versus worker offspring fitness, was tested in chapter IV.

A final issue concerns the division of 2. Social semantics: Altruism and spite reproduction into sexual and worker offspring. In social insects, males are produced from Recently, several reviews have argued that the haploid eggs and females (queens and workers) language used to discuss social interactions is from diploid eggs. Caste determination between sometimes confusing, up to the point that it workers and sexual females is considered to be hinders the development of the field due to environmental factors, such as the quantity (Lehmann & Keller 2006; West et al. 2006a). or quality of the food provided to larvae by According to the authors, the semantic workers (but see Cahan & Keller 2003; Fournier confusion partly stems from different fields et al. 2005 for some exceptions). However, from using different words for the same concepts, an evolutionary perspective, sterile workers are and partly from wide-spread terms being ill- a dead end. Therefore, competition between suited to begin with (West et al. 2006a). An queens may be stronger over the production of example of the latter is the term reciprocal sexuals than over that of workers, leading to altruism acts, which do not really represent differences in reproductive skew between offspring altruism since the eventual payback from castes. Such a difference has been found in Pheidole, reciprocity means the act does not bear a cost Myrmica and Solenopsis ants (Fournier et al. 2004; to the actor on the long term (West et al. Ross 1988; Ross 1993; Pamilo & Seppä 1994; but 2006a). In the last chapter of this thesis, we join see Heinze et al. 2001). This may create a situation this effort to clarify concepts by investigating two where the queens that specialize on sexual key concepts of social evolution, namely production effectively parasitize on those that altruism and spite. invest in colony maintenance and produce new According to Hamilton´s original workers. Indeed, socially parasitic species definitions, altruism is defined as an act that helps (inquilines) are thought to have arisen this way the receiver while decreasing the fitness of the (Bourke & Franks 1991; Heinze & Keller 2000). actor. Spite, i.e. behaviours that harm both the A difference in skew between worker and actor and the receiver of the behaviour, has been sexual reproduction may also have adverse effects seen as a phenomenon quite distinct from on the inclusive fitness of workers. In Pheidole altruism (Vickery et al. 2003; West et al.¬2006a). ants, there is a trade-off between a queen’s For a long time, spite was thought unlikely to production of worker and sexual offspring, so occur in animals (Keller et al. 1994), but several that the queens producing more workers recent studies have put forward examples of

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14 Summary ______spiteful interactions (Foster et al. 2000, 2001; 3. Material and methods Gardner & West 2004a; Gardner et al. 2004), as well as modelled the dynamics of these (Vickery Study species (I-IV) et al. 2003; Gardner & West 2004b, Engelstädter Two study species were used in this thesis: the & Charlot 2006). wood ant Formica truncorum (I) and the black However, the distinction between spite ant Formica fusca (II, III, IV). Both these and altruism is not straightforward. This can be species exhibit variation in social form, both illustrated by an example. A well-known form in the extent of multiple mating and multiple of nepotism in brood rearing in social insects queening, and are therefore suited for studies concerns sex allocation. Due to the haplodiploid investigating traits in different social systems. sex determination system of social Hymenoptera, Additionally, due to its small colony size and workers are more related to female than male below ground nesting strategy, F. fusca is easily offspring and would hence benefit from biasing kept under laboratory conditions during the sex ratio produced by the colony towards experimental work (see also Hannonen 2002; females. Such sex ratio biasing has been observed Helanterä 2004). in several species (Sundström 1994; reviewed in Ratnieks et al. 2006) and is based on workers Field studies (I, III-IV) killing male offspring to gain resources to raise To study heritability of size in a natural setting more females (Sundström et al.¬1996). Because of (I), we sampled colonies in two years from a its dual nature favouring more related females and population of F. truncorum in Tvärminne, SW harming less related males, this behaviour has been Finland that has been studied over many years seen as an example of both altruism (Sundström (e.g. Sundström 1994; Sundström 1995a,b, et al. 1996) and spite (Foster et al. 2000, 2001). Sundström et al. 1996, 2003). To study the Additionally, confusion reigns in that causes and consequences of social some models of spite incorporate two polymorphism in F. fusca (III, IV), data on the components when investigating a supposedly same colonies were obtained over several years spiteful behaviour: one harming less related from a population located on an island in individuals and another helping more related Siuntio, SW Finland. individuals (Gardner & West 2004). This issue relates to Foster et al.’s (2000, 2001) definition Experiments (II) of two kinds of spite: Hamiltonian spite, where In chapter II, experiments were conducted to the harming is directed towards negatively related assess the importance of colony productivity individuals, and Wilsonian spite, where harming on offspring traits as well as on reproductive helps the more related individuals by reducing skew, using laboratory two-queen colonies of competition. In chapter V, we attempted to clarify F. fusca. The use of laboratory colonies enabled these issues by modelling the fitness effects of us to manipulate colony productivity as well altruism and spite, as well as helping and harming as reliably assign offspring to either of the behaviours. queens. Field manipulations are not possible

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15 Summary ______in F. fusca since colonies are built underground, 4. Main results and discussion and easily move if disturbed. Moreover, direct parentage assignment is impossible in field Genetic diversity and within-colony colonies, due to the difficulty of sampling variability in F. truncorum and F. fusca (I, colony queens during the reproductive season II) when they dwell deep underground. However, queens can be gathered for experimental use To look at the effect of genetic diversity on before the onset of egglaying in early spring, individual traits, we tested whether multiple mating when the colony aggregates close to the surface affected the size distribution of workers and queens, to warm up. and whether size is heritable in F. truncorum (I). This was done by comparing monoandrous and Genetic analyses (I-IV) polyandrous colonies, as well as half-sibs within Microsatellites developed for Formica ants polygyne colonies. We also looked at how worker (Chapuisat 1996; Gyllenstrand et al. 2002) were size is affected by an extrinsic factor, i.e. the number used for detecting genetic differentiation (III) of workers taking care of larvae in F. fusca (II). and kin structure (II, III, IV) as well as In F. truncorum, we found a significant and determining paternity (I) and maternity (II) of strong heritable component for queen size offspring. Microsatellites are powerful tools for (h2=0.51) in one year, but not in the other. Similarly, analysing such patterns (Queller et al. 1993; genetic variability increased queen size variation in Goldstein & Schlötterer 1999). the year exhibiting size heritability, but not in the other year. The heritability of worker size was low Modeling (V) (h2=0.09) and non-significant, and genetic variability In chapter V, the connection between spite and did not increase worker size variation. altruism was clarified using an indirect fitness In F. fusca, worker size was strongly modeling framework. In this method, the influenced by resource levels, so that large colonies inclusive fitness function of a mutant allele is produced, on average, 5% larger workers. Queen given as a sum of the effects of a focal individual condition or size had no effect on worker bearing the mutant trait on the fitness of all offspring size. This result corresponds to a study individuals in the population, weighted by their in cooperatively breeding meerkats, where relatedness to the focal individual. The method maternal characteristics have little influence on is completely congruent with direct fitness pups after weaning, and offspring size is instead modelling (Taylor & Frank 1996; Rousset & determined by colony traits, such as the number Billiard 2000, Taylor et al. 2007). We analytically of carers available (Russell et al. 2002). These examined the fitness effects of harming and results demonstrate the power of the social helping traits. In an example, we investigated the environment in determining offspring traits, selective pressures for the spread of a harming enabling colonies to adjust the number and size trait in a subdivided population. of workers raised according to resource levels.

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16 Summary ______

Overall, our results suggest that in the species genetic or spatial differentiation. Queen turnover we studied, worker size is highly plastic, with was measured over four generations of workers environmental factors overshadowing possible in both monogyne and polygyne colonies. heritable effects (see also Hughes et al. 2003; Our study revealed no strong pattern Schwander et al. 2005). This implies genetic of spatial or genetic patterning in the population, diversity is not needed to maintain efficient or between social forms. However, the young division of labour. Obviously, our results do not age of our study population prompts us to rule out other benefits of genetic diversity, such consider the possibility that the observed pattern as parasite resistance or inbreeding avoidance. may not represent a stable state. One form may Although the genetic component for come to dominate due to selective pressures, or queen size is potentially strong and enables differences in behaviour may cause partial or total polyandrous colonies to produce more variable genetic isolation between the two forms (Bourke offspring queens, the extent of fluctuation in the & Heinze 1994; Ross & Keller 1995; Gyllenstrand estimated heritability between sampling times et al. 2005; Sundström et al. 2005). On the other indicates that often, environmental factors may hand, the transient and dynamic character of override genetic ones. Thus, it is unlikely that genetic populations of pioneer species such as F. fusca, variation in offspring queen size confers large fitness which expand rapidly but persist only for a short benefits to polyandrous colonies. In addition, the time (Savolainen & Vepsäläinen 1988), may inconsistency of the estimates highlights the prevent the build-up of genetic differentiation problems of studying heritability in the field, where between social forms, or prevent the eventual environmental conditions are not static (Hoffmann domination of one form altogether. In & Merilä 1999, Wilson et al. 2006). accordance with this, the populations of F. fusca studied to date all encompass a mixture of Population-level patterns of social monogyne and polygyne colonies (Hannonen et polymorphism and life history traits in al., 2004; Helanterä 2004). F. fusca (III) Despite the lack of genetic or spatial differentiation, colony-level behaviours partly To study the patterns of social polymorphism, conformed to our expectations. Although we did we used long-term field data from a field not find a difference in colony survival between population of F. fusca (III, IV). Workers, worker social forms, which could be due to the limited pupae and sexual pupae were sampled from the sample size, queen turnover differed dramatically same nests during two years (1997 and 1999). between social forms. In the monogyne colonies, From genotypes of workers from the first queen turnover was absent and the same queen sampling occasion, nests were assigned as was retained over the whole study period. In the monogyne or polygyne. Population genetic polygyne colonies, we found that queen methods were used to investigate whether the replacement was frequent between years. In social form of colonies corresponded with addition, no colonies switched social structure

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17 Summary ______in the four years examined. Our results, in investigated the effect of colony productivity and conjunction with previous studies (Chapuisat et al., queen relatedness on reproductive skew by 2004; Fournier et al., 2004; DeHeer & Herbers, carefully manipulating and measuring 2004, Rosset & Chapuisat, 2006), imply that productivity. As found in previous studies, differences between social forms may appear reproductive skew varied from equal sharing to independently from one another, even when the complete domination by one queen. Despite forms occur in sympatry. large differences in productivity between A proximate reason for the differences experimental treatments, we did not find a between social forms in the amount of queen connection between the extent of offspring turnover may be that queens in polygyne colonies sharing between queens and productivity. are in worse condition than queens in monogyne Reproductive skew was on the same level in both colonies (Ross & Shoemaker 1997; Rüppell et treatments, and did not correlate with colony al. 2001a,b). In accordance with this, in F. fusca, productivity within treatments. This goes against queen condition decreases with increasing queen predictions of transactional models of number (II). It may be that this is due to polygyne reproductive skew. colonies investing fewer resources into new Most surprisingly, queen relatedness, queens, since many daughter queens can avoid which was previously found by Hannonen & the energetically costly dispersal and colony Sundström (2003a) to correlate negatively with founding stage and instead remain in the natal reproductive skew, did not have an effect on skew colony (Keller 1995; Heinze & Keller 2000). in our study. The main difference between the Another possibility is that the lower condition two studies was that laboratory colonies were reflects a trade-off for the queens between collected from slightly different places. This may reproduction and somatic maintenance. In imply that patterns of reproductive skew vary polygyne colonies, competition between queens between populations, making it more difficult to over reproduction may force queens to invest draw general conclusions. more into reproduction than they would if The failure to find support for the breeding alone. If this is the case, queen turnover models of reproductive skew, as well as the may be the result of fluctuations in fecundity over conflicting results compared to earlier studies, time, rather than queen mortality. These lead us to question the applicability of optimal possibilities are discussed further in the section skew theory to our study system. Observed on reproductive skew. differences in skew patterns between studies of the same species have caused some authors to Reproductive skew in F. fusca (II, IV) suggest that optimal skew may function on a larger scale than individual colonies. For instance, Reproductive skew was the focus of two chapters in a certain population, most colonies will (II, IV). In chapter II, we tested assumptions experience the same ecological conditions, and of reproductive skew theory in two-queen it may make more sense to correlate the extent colonies of the black ant, Formica fusca. We of skew with traits of populations or species

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18 Summary ______rather than individual colonies (Hannonen et Finally, the question of skew in different al.¬2004; Liebert & Starks 2006). offspring castes was investigated in chapter (IV). Alternatively, it may be that models of Reproductive skew was found to be higher in reproductive skew are not well suited to describe sexual offspring than in worker offspring (IV). reproductive sharing in highly derived social This implies that there may indeed be large fitness systems such as polygyne ants. Many of the differences between queens, with some queens assumptions of the optimal skew models (i.e. dominating the production of sexuals. However, that individuals possess an option to leave the shifts in breeders across seasons, as observed in group, as well as accurate information on the chapter III, may alleviate the potential fitness reproduction of others, and of surrounding differences between individual queens. ecological conditions) may not be fulfilled in Nevertheless, fewer queens produced sexual multiple-queen colonies (Kokko 2003; Liebert & offspring than worker offspring, which suggests Starks 2006; Nonacs et al. 2006). Thus, we may that only a subset of all queens ever come to have to abandon the hope that models of optimal produce gynes. skew will serve as a “unifying framework” (Reeve Proximately, differences in reproductive & Ratnieks 1993; Keller & Reeve 1994) for apportionment to the two castes could be due understanding cooperation across animal to the timing of egglaying. In F. fusca, sexuals are systems (Kokko 2003; Leibert & Starks 2006; produced from the first eggs laid (pers. obs.). If Nonacs et al.¬2006). a subset of queens start egglaying early, these On a proximate level, previous studies will produce most of the gynes, leaving worker suggest that initial queen fertility is the key factor production to the later egglayers. Accordingly, influencing who gains reproductive majority laboratory studies show that reproduction is (Hannonen et al.¬2002; Hannonen & Sundström often highly skewed at the onset of egglaying 2002). Fecundity may fluctuate over time, for (R.Ovaska and K. Bargum, in prep.) instance if it is associated with age (Brian, 1988, Interestingly, the difference in Bourke, 1991; Hannonen et al., 2002). Such reproductive skew favoured worker interests. Adult fluctuations would give rise to a pattern of high workers were significantly more related to the queen turnover in colonies, like the one observed reproductive brood than to the worker brood. As in chapter III. This would imply that at any point a result, tending workers gained enhanced inclusive in time, a colony will consist of queens at their fitness returns. The non-random pattern of queen reproductive peak and queens who are either past contribution to workers and sexuals raises the their reproductive peak or are yet to reach it. The critical relatedness between workers and sexuals, implication of this is that any measure of skew thereby promoting colony cohesion. taken at one point in time may not reflect the Two mechanisms could be creating lifetime reproductive success of individuals. This higher relatedness between adult workers and highlights the importance of incorporating sexuals. Switches could be connected to the age future fitness benefits into reproductive skew of the queen, so that queens who have already (Kokko & Johnstone 1999; Ragsdale 1999). reproduced once (and therefore are mothers of

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19 Summary ______the current workers) are in a head start position However, this is not to say that both helping at commencement of egglaying, leading to the and harming cannot occur at the same time. observed pattern of higher worker relatedness In fact, either is likely to evolve more easily to gynes. On the other hand, the result is with the help of the other. To return to our consistent with workers intervening to ensure original example of sex ratio biasing, harming that the sexuals raised are their close relatives. the male larvae may be favoured already by Such nepotism could be accomplished either by alleviating resource competition for the female helping queens which are their closest relatives larvae. That workers then help the females by gain a head start, or by raising closely related feeding them the males may further strengthen larvae into gynes rather than into workers. the selection for sex ratio biasing. In conclusion, regardless of whether or Since altruism and spite are two sides not direct nepotism occurs, the system serves the of the same coin, chapter V suggests it would inclusive fitness benefit of workers, in turn be clearer to classify behaviours according to alleviating the dilution of relatedness caused by their effect on the direct recipient¬(i.e. harming polygyny. An analogous example of this pattern or helping). The study further investigated when can be found in cooperatively breeding groups of harming can be selected for. The results suggest white-winged choughs, where individuals with a that in large populations, helping relatives is consort of relatives more often obtain dominance favoured over harming non-relatives. This is status than single individuals (Heinsohn et al. 2000). because helping specifically increases the Thus, by serving kin interests, breeding systems productivity of kin, while the benefit of reduced including multiple breeders may nevertheless competition due to harming is diluted in a large enhance social cohesion. population (Gardner & West 2004b). In contrast, harming is favoured over helping in small Altruism and spite (V) populations. In this situation, the reduction of competition caused by harming creates two benefits In the final chapter, we investigated the dynamics for the actor (i.e. the individual performing the of altruism and spite. From our analysis, it is clear harming action). Firstly, the actor’s own offspring that any trait that reduces the fitness of less related are more likely to survive (resulting in a direct individuals necessarily increases that of related ones. benefit) and second, relatives of the actor have Therefore, from a fitness perspective any behaviour a higher chance of survival (providing a kin- qualifying as spiteful also classifies as altruistic. selected benefit). The combination of both Additionally, the difference between Hamiltonian benefits makes harming a more efficient strategy and Wilsonian spite disappears: the reduction of than helping in small populations. Accordingly, the fitness for negatively related individuals examples of harming traits found in nature are automatically leads to an increase of fitness for often connected with small effective population positively related ones. Thus, there is no need for a sizes (i.e. few gene lineages), such as sex ratio biasing separate helping component for the behaviour to in ants (Sundström 1994; Sundström et al. 1996), qualify as Wilsonian, as is sometimes assumed or bacteriocine production by bacteria (Gardner et (Gardner & West 2004). al. 2004).

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20 Summary ______

5. Implications and future directions larger effect on the population than sampling workers. Collecting sterile workers in the field is Methodological implications akin to non-lethal sampling, whereas collecting sexual offspring deprives the population of The results of this thesis have some implications potential future reproductives. for the methodology used in social insect research. The rapid replacements of breeders shown in Unresolved issues polygyne colonies of F. fusca (III, IV) indicates that measuring the individual fitness of queens may not As is the case with all scientific endeavours, the be a straightforward enterprise. Since all queens may work presented in this thesis raises as many not reproduce at one single point in time, questions as it answers. Below, I discuss a few of quantifying lifetime reproductive success would these questions, and ponder ways to resolve them require many, rather than one, sampling occasion. through future work. Therefore, it may prove interesting to follow a queen throughout her reproductive lifespan. The feasibility What determines queen fecundity? of this is further discussed in the section on queen fecundity below. This thesis together with previous work on F. fusca An additional methodological issue is suggests that queens vary in their fecundity, and raised by the finding that the genetic composition that fecundity is a proximate reason for reproductive of worker offspring differs from that of sexual domination (Hannonen 2002, II). Natural colonies offspring (IV). This indicates that measures of show frequent queen replacement, and this may effective queen numbers, effective population size also be due to temporal shifts in fecundity (III). and reproductive skew gained by using worker This raises the so far unresolved issue of what offspring does not reflect the pattern of gene flow determines queen fecundity. through the generations, which happens mainly Fecundity may be a heritable trait, and through sexuals. Hence, regardless if we are subsequently could be studied through a interested in evolutionary questions of who quantitative genetic framework. Although we found reproduces, or conservation aspects of how genetic a heritable component to queen size in the species variation is maintained and spread, we should F. truncorum (I), there was no evidence that queen sample sexual offspring instead of workers. size or queen condition influenced fecundity in However, this raises both practical and ethical issues. F. fusca (Hannonen & Sundström 2002, II). There Firstly, sexual offspring may not be easily available. may, however, be other individual, heritable In most species of ants, sexual offspring are only characteristics that influence fecundity. Overall, present for a short time in the colony. Sometimes, introducing a quantitative genetic framework may the developmental time of sexual brood stretches prove fruitful in social insects, due to comparatively over several seasons, and some ant species, like easy sampling, large sample sizes and clear Formica fusca, do not regularly produce sexual brood generations (Tsuji 1995; Wiernazs & Cole 2003, I). in the laboratory. Secondly, from a research ethical Another factor affecting queen fecundity perspective, sampling sexual offspring may have a may be queen age. Several studies of cobreeding

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21 Summary ______vertebrates have shown that age may correlate level, such as decreased colony productivity. Hence, with fecundity, but tracking the age of insects nepotism bearing a large cost (reducing productivity presents challenges. To study the effect of queen or overt aggression) will be evolutionarily unstable, age in F. fusca would ideally involve following whereas low-cost changes are more probable (Keller colonies with queens of known ages over time. 1997). Thus, studies in other species could benefit However, pilot experiments have revealed the from concentrating on looking for small shifts, difficulty in introducing new queens into colonies rather than major effects. with a species with strong nestmate recognition. A Furthermore, it is important to consider more promising road may lie in utilizing indirect species-specific differences when predicting in cues to queen age, such as physiological changes in which study system we may find nepotism. queens, and correlating these to fecundity. Nepotism requires recognising differences in relatedness between individuals. However, different What is the role of the workers in social systems may affect the feasibility of such determining offspring identity? recognition, leading to informational constraints. For instance, chemical analyses show that in F. Kin selection theory predicts that individuals favour truncorum, half-sibs with different fathers are their kin over unrelated individuals. In multiple probably not different enough to enable workers queen colonies we may therefore expect that to distinguish between patrilines (Boomsma et al. workers would favour queens and offspring 2004). Recognition may therefore require that according to their degree of relatedness to these. individuals differ in both their paternal and maternal Currently, evidence for such nepotism is sparse, genome as well as through maternal effects, as is but studies on F. fusca have indicated that the case with offspring of different queens in nepotism may, in fact, play a role in offspring multiple-queen colonies (Dani et al. 2004). production (Hannonen & Sundström 2003b; IV). Consequently, nepotism may be more likely in However, further studies are needed to elucidate polygyne, rather than polyandric species, such as whether this is indeed the case, and what the the honeybee (Tarpy et al. 2004). On the other hand, mechanisms of such a choice are. This also raises extreme polygyny may lead to an overload of the question of why the phenomenon has not been recognition cues, again making it impossible to demonstrated in other species (reviewed in Keller distinguish between individuals. Accordingly, in 1997; Tarpy et al. 2004; Ratnieks et al. 2006). many strongly polygyne species even nestmate Firstly, it is worthwhile to note the low recognition is lost, and colonies will raise eggs laid impact of nepotism on offspring production in F. by non-nestmate queens. In these circumstances, fusca. Changes are small and relative, i.e. shifts in lack of nepotism comes as no surprise (DeHeer & the identity of eggs versus pupae, or, potentially, Ross 1997; Holzer et al. 2006). Hence, it would between workers and sexual offspring, and seem that to resolve the question of the importance therefore possible to distinguish only by of nepotism in multiple-queen colonies, further comparison. This is in accordance with kin selection studies should concentrate on detecting small theory, which predicts that the benefit of nepotistic nepotistic acts in species with weak polygyny and acts will be balanced against costs on the colony good recognition systems.

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22 Summary ______

Concluding remarks 6. Acknowledgements

In conclusion, this thesis shows that social Many thanks to Henna Piha, Emma Vitikainen and polymorphism has the potential to affect Sedeer El-Showk for providing helpful comments individual behaviour and traits. However, the on this summary. thesis also demonstrates that spatial and temporal variation between both populations and 7. Literature cited environments may affect individual and colony traits, to the degree that results obtained in one Baer, B. & Schmid-Hempel, P. 2001. Unexpected place or at one time may not be applicable in consequences of polyandry for parasitism and other situations. It may thus prove fruitful to fitness in the bumblebee, Bombus terrestris. Evo- lution 55:1639–1643. investigate the factors which can explain these Blumstein, D.T. & Armitage, K.B. 1999. Coopera- differences. The accumulating amount of both tive breeding in marmots. Oikos 84: 369-382. data and theory opens up opportunities for large- Boomsma, J. J. & Ratnieks, F. L. W. 1996. Paternity scale spatial and temporal comparisons, as well in eusocial Hymenoptera. Phil. Trans. R. Soc. as meta-analyses and review work (i.e. on Lond. B 351:947–975. Boomsma, J.J., Nielsen, J., Sundström, L., Oldham, reproductive skew: Reeve & Keller 2001; Nonacs N.J., Tentschert, J., Petersen, H.C. & Morgan, et al. 2006). Additionally, we may benefit from D. 2003. Informational constraints on optimal focusing on life-history traits and trade-offs to sex allocation in ants. Proc. Natl. Acad. Sci. USA explain variation between individuals. Here, the 100:8799–8804. social insect research could learn from the study Bourke, A.F.G. 1991. Queen behaviour, reproduc- of social vertebrates, where such traits have long tion and egg cannibalism in multiple-queen colonies of the ant Leptothorax acervorum. Anim. been studied. Behav. 42:295–310. This also raises the issue of pluralism Bourke, A.F.G. & Franks, N.R. 1991. Alternative versus synthesis. To what extent can we expect social adaptations, sympatric speciation and the evo- systems to conform to the same rules? In the effort lution of parasitic, inquiline ants. Biol. J. Lin. to bring together many fields, it is important to Soc. 43:157–178. Bourke, A.F.G. & Franks, N.R. 1995. Social evolu- keep in mind differences in the systems analysed. tion in ants. Princeton University Press, Sometimes, as in the case of reproductive skew, we Princeton. may analyse the same phenomenon using many Bourke, A.F.G. & Heinze, J. 1994. The ecology of different models, without one model necessarily communal breeding - the case of multiple-queen being superior to others. On the other hand, the leptothoracine ants. Philos. Trans. R. Soc. Lond. B 345:359–372. case of altruism and spite demonstrates how Bourke, A.F.G., Green, H.A.A. & Bruford, M.W. different terms may be applied to what is 1997. Parentage, reproductive skew and queen essentially the same thing. Hence, the study of turnover in a multiple-queen ant analysed with social interactions stands before the challenge microsatellites. Proc. R. Soc. Lond. B 264:277– of simultaneously striving for pluralism and 283. Burke, T., Davies, N.B., Bruford, M.W. & Hatchwell, maintaining a unitary framework (Cahan et al. B.J. 1989. Parental care and mating behaviour 2002; Lehmann & Keller 2006, West et al. 2006a).

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of polyandrous dunnocks Prunella modularis re- DeHeer, C.J. & Ross, K.R. 1997. Lack of detect- lated to paternity by DNA fingerprinting. Na- able nepotism in multiple-queen colonies of the ture 338:249–251. fire ant Solenopsis invicta (Hymenoptera: Brian, M.W. 1988. The behavior and fecundity of Formicidae). Behav. Ecol. Sociobiol. 40:27–33. queens of different ages in synthetic groups of Denny, A.J., Franks, N.R., Powell, S. & Edwards, Myrmica rubra L with different worker popula- K.J. 2004. Exceptionally high levels of multiple tions. Insectes Soc. 35:153–166. mating in an army ant. Naturwissenschaften Cahan, S.H., Blumstein, D.T, Sundström, L., Liebig, 91:396–399. J. & Griffin, A. 2002. Social trajectories and the Elmes, G. 1973. Observations on the density of evolution of social behavior. Oikos 96:206–216. queens in natural colonies of Myrmica rubra (Hy- Cahan, S.H. & Keller, L. 2003. Complex hybrid ori- menoptera: Formicidae). J. Anim. Ecol. 42:761– gin of genetic caste determination in harvester 771. ants. Nature 424:306–309. Emlen, S.T. 1982a. The evolution of helping. I. An Chapuisat, M. 1996. Characterization of ecological constraints model. Am. Nat. 119:29– microsatellite loci in Formica lugubris B and their 39. variability in other ant species. Mol. Ecol. 5:599– Emlen, S.T.1982b. The evolution of helping. II. The 601. role of behavioral conflict. Am. Nat. 119:40– Chapuisat, M., Bocherens, S. & Rosset, H. 2004. 53. Variable queen number in ant colonies: No im- Engelstadter, J. & Charlot, S. 2006. Outbreeding pact on queen turnover, inbreeding, and popu- selects for spiteful cytoplasmic elements. Proc lation genetic differentiation in the ant Formica Roy Soc Lond B 273:923–929. selysi. Evolution 58(5):1064–1072. Engh, A.L., Funk, S.M., Van Horn, R.C., Scribner, Clutton-Brock, T.H., Brotherton, P.N.M., Russell, K.T., Bruford, M.W., Libants, S., Szykman, M., A.F., O’Riain, M.J., Gaynor, D., Kansky, R., Grif- Smale, L. & Holekamp, K.E. 2002. Reproduc- fin, A., Manser, M., Sharpe, L., McIlrath, G.M., tive skew among males in a female-dominated Small, T., Moss, A. & Monfort, S. 2001. Coop- mammalian society. Behav. Ecol. 13:193–200. eration, control, and concession in meerkat Evans, J.D. 1996. Queen longevity, queen adoption, groups. Science 291:478–481. and posthumous indirect fitness in the faculta- Crozier, R.H. & Page, R. 1985. On being the right tively polygyne ant Myrmica tahoensis. Behav. Ecol. size: male contributions and multiple mating in Sociobiol. 39:275–284. social Hymenoptera. Behav. Ecol. Sociobiol. Evans, T.A. 1999. Kin recognition in a social spi- 18:105–115. der. Proc. R. Soc. Lond. B. 266:287–292. Crozier, R.H & Fjerdingstad, E.J. 2001. Polyandry Field, J., Cronin, A. & Bridge, C. 2006. Future fit- in social Hymenoptera – disunity in diversity? ness and helping in social queues. Nature 441: Ann. Zool. Fenn. 38:267–285. 214–217 Dani, F.R., Foster, K.R., Zacchi, F., Seppä, P., Foster, K.R., Wenseleers, T. & Ratnieks, F.L.W. Massolo, A., Carelli, A., Arevalo, E., Queller, 2000. Spite in social insects. Trends Evol. Ecol. D.C., Strassmann, J.E. & Turilazzi, S. 2004. Can 15: 469–470. cuticular lipids provide sufficient information Foster, K.R., Wenseleers, T. & Ratnieks, F.L.W. for within-colony nepotism in wasps? Proc. R. 2001. Spite: Hamilton’s unproven theory. Ann. Soc. Lond. B 271:745–753. Zool. Fenn. 38: 229–238. DeHeer, C.J. & Herbers, J.M. 2004. Population ge- Foster, K.R., Wenseleers, T. & Ratnieks, F.L.W. netics of the socially polymorphic ant Formica 2006. Kin selection is the key to altruism. Trends podzolica. Insectes Soc. 51:309–316. Ecol. Evol. 21:57–60.

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Fournier, D & Keller, L. 2001. Partitioning of re- Hannonen, M. and Sundström, L. 2003a. Repro- production among queens in the Argentine ant, ductive sharing among queens in the ant Formica Linepithema humile. Anim. Behav. 62:1039–1045. fusca. Behav. Ecol. 14:870–875. Fournier, D., Aron, S. & Keller, L. 2004. Signifi- Hannonen, M. & Sundström, L. 2003b. Worker cant reproductive skew in the facultatively nepotism among polygynous ants. Nature polygyne ant Pheidole pallidula. Mol. Ecol. 13:203– 421:910. 210. Hannonen, M., Sledge, M.F., Turillazzi, S. & Fournier, D., Estoup, A., Orivel, R.M., Foucaud, J., Sundström, L. 2002. Queen reproduction, Jourdan, H., Le Breton, J. & Keller, L. 2005. chemical signalling and worker behaviour in Clonal reproduction by males and females in polygyne colonies of the ant Formica fusca. Anim. the little fire ant. Nature 435:1230–1234. Behav. 64:477–485. Fraser, V.S., Kaufmann, B., Oldroyd, B.P. & Cro- Hannonen, M., Helanterä, H. & Sundström, L. zier, R.H. 2000. Genetic influence on caste in 2004. Habitat age, breeding system and kinship the ant Camponotus consobrinus. Behav. Ecol. in the ant Formica fusca. Mol. Ecol.13:1579–1588. Sociobiol. 47:188–194. Haydock, J. & Koenig, W.D. 2000. Reproductive Gardner, A. & West, S.A. 2004a. Spite among sib- skew in the polygynandrous acorn woodpecker. lings. Science 305: 1413–1414. Proc. Natl. Ac. Sci. USA 99:7178–7183. Gardner, A. & West, S.A. 2004b. Spite and the scale Heinze, J. & Keller, L. 2000. Alternative reproduc- of competition. J. Evol. Biol. 17: 1195–1203. tive strategies: a queen perspective in ants. Gardner, A., West, S.A. & Buckling, A. 2004. Bac- Trends Ecol. Evol. 15(12):508–512. teriocins, spite and virulence. Proc. R. Soc. Lond. Heinze, J., Trunzer, B., Hölldobler, B. & Delabie, B 271:1529–1535. J.H.C. 2001. Reproductive skew and queen re- Goldstein, D.B. & Schlötterer, C. (eds). 1999. latedness in an ant with primary polygyny. Ins. Microsatellites – Evolution and Application. Ox- Soc. 48:149-153. ford University Press, Oxford. Heinsohn R., Dunn P., Legge S. & Double, M. 2000. Griffin, A.S. & West, S.A. 2003. Kin discrimina- Coalitions of relatives and reproductive skew tion and the benefit of helping in cooperatively in cooperatively breeding white-winged breeding vertebrates. Science 302:634–636. choughs. Proc. R. Soc. Lond. B 267: 243–249. Gyllenstrand, N., Gertsch, P.J. & Pamilo, P. 2002. Helanterä, H. 2004. Kinship and conflicts over male Polymorphic microsatellite DNA markers in the production in Formica ants. PhD thesis, Univer- ant Formica exsecta. Mol. Ecol. Notes 2:67-–69. sity of Helsinki. Gyllenstrand, N., Seppä, P. & Pamilo, P. 2005. Re- Helanterä, H. & Bargum, K. 2006. Pedigree relat- stricted gene flow between two social forms in edness, not greenbeard genes, explain eusociality. the ant Formica truncorum. J. Evol. Biol. 18:978– Oikos, in press. doi: 10.1111/j.2006.0030- 984. 1299.15411.x. Hamilton, W.D. 1964. The genetical evolution of Herbers, J.M. 1984. Queen-worker conflict and social behaviour. I and II. J. Theor. Biol. 7:1–52 eusocial evolution in a polygyne ant species. Hannonen, M. 2002. Proximate and ultimate de- Evolution 38:631–643. terminants of reproductive skew in the ant Hoffmann, A.A. & Merilä, J. 1999. Heritable varia- Formica fusca. PhD thesis, University of Helsinki. tion and evolution under favourable and Hannonen, M. and Sundström, L. 2002. Proximate unfavourable conditions. Trends Ecol. Evol. determinants of reproductive skew in polygyne 14:96–101. colonies of the ant Formica fusca. Ethology Holzer, B., Kümmerli, R., Keller, L. & Chapuisat, 108:961–973. M., 2006. Sham nepotism as a result of intrin-

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sic differences in brood viability in ants. Proc. Keller, L., Milinski, M., Frischknecht, M., Perrin, Roy. Soc. Lond. B 273, 2049-2052. N., Richner, H. & Tripet, F. 1994. Spiteful ani- Hughes, W.O.D. & Boomsma, J.J. 2004. Genetic di- mals still to be discovered. Trends. Evol. Ecol. versity and disease resistance in leaf-cutter ant 9: 103. societies. Evolution 58:1251–1260 Kokko, H. 2003. Are reproductive skew models Hughes, W.O.H., Sumner, S., Van Borm, S. & evolutionary stable? Proc. R. Soc. Lond. B. Boomsma, J.J. 2003. Worker caste polymorphism 270:265–270. has a genetic basis in Acromyrmex leaf-cutting Kokko, H. & Johnstone, R.A. 1999. Social queuing ants. Proc. Natl. Acad. Sci. 100:9394–9397. in animal societies: a dynamic model of repro- Hölldobler, B. & Wilson, E.O. 1977. The number ductive skew. Proc. R. Soc. Lond. B 266:571– of queens: an important trait in ant evolution. 578. Naturwissenschaften 64(8):8–15. Kokko, H., Johnstone, R.A. & Clutton-Brock, T.H. Hölldobler, B. & Wilson, E.O. 1990. The ants. 2001. The evolution of cooperative breeding Belknap Press, Cambridge, MA. through group augmentation. Proc. R. Soc. Jamieson, I.G. 1997. Testing reproductive skew Lond. B 268:187–196. models in a communally breeding bird, the Kronauer, D.J.C., Schoning, C., Pedersen, J.S., pukeko, Porphyrio porphyrio. Proc. R. Soc. Lond. Boomsma, J.J. & Gadau, J. 2004. Extreme queen- B 264:335–340. mating frequency and colony fission in African Jennions, M.D. & Petrie, M. 2000. Why do females army ants. Mol. Ecol. 13:2381–2388. mate multiply? A review of the genetic benefits. Langer, P., Hogendoorn, K. & Keller, L. 2004. Tug- Biol. Rev. 75:21-64. of-war over reproduction in a social bee. Na- Johnstone, R.A. 2000. Models of reproductive ture 428:844–847. skew: a review and synthesis. Ethology 106:5– Langer, P., Hogendoorn, K., Schwarz, M.P. & 26. Keller, L. 2006. Reproductive skew in the Aus- Johnstone, R.A. & Cant, M.A. 1999. Reproductive tralian allodapine bee Exoneura robusta. Anim. skew and the threat of eviction: a new perspec- Behav. 71:193–201. tive. Proc. R. Soc. Lond. B 266:275–279. Lehmann, L. & Keller, L. 2006. The evolution of Keller, L. 1988. Evolutionary implications of po- cooperation and altruism: a general framework lygyny in the Argentine ant, Iridomyrmex and a classification of models. J. Evol. Biol. humilis (Mayr) (Hymenoptera: Formicidae): an 19:1365–1376. experimental study. Anim. Behav. 36:159–165. Leibert, A.E. & Starks, P.T. 2006. Taming of the Keller, L. 1993a. The assessment of reproductive skew: transactional models fail to predict repro- success of queens in ants and other social in- ductive partitioning in the paper wasp Polistes sects. Oikos 67:177–180. dominulus. Anim. Behav. 71:913–923. Keller, L. (ed.). 1993b. Queen number and social- Mitchell, J. 2005. Queue selection and switching ity in insects. Oxford University Press, Oxford. by false clown anemonefish, Amphriprion ocellaris. Keller, L. 1995. Social life: the paradox of mul- Anim. Behav. 69:643–652. tiple-queen colonies. Trends Ecol. Evol. Möller, L.M., Beheregaray, L.B., Harcourt, R.G. & 22 10(9):355–360. Krutzen, M. 2001. Alliance membership and Keller, L. 1997. Indiscriminate altruism: unduly nice kinship in wild male bottlenose dolphins parents and siblings. Trends Ecol. Evol. 12:99- (Tursiops aduncus) of southeastern Australia. 103. Proc. R. Soc. Lond. B 268:1941–1947. Keller, L., & Reeve, H.K. 1994. Partitioning of re- Neff, B.D. 2003. Decisions about paternal care in production in animal societies. Trends Ecol. response to perceived paternity. Nature Evol. 9:98–102. 422:716–719.

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26 Summary ______

Nonacs, P. 1988. Queen number in colonies of Queller, D.C., Strassmann, J.E. & Hughes, C.R. social Hymenoptera as a kin-selected adaptation. 1993a. Microsatellites and kinship. Trends Ecol. Evolution 42(3):566–580. Evol. 8:285–288. Nonacs, P. Leibert, A.E. & Starks, P.T. 2006. Trans- Ragsdale, J.E. 1999. Reproductive skew theory ex- actional skew and assured fitness return mod- tended: The effect of resource inheritance on els fail to predict patterns of cooperation in social organization. Evol. Ecol. Res. 1:859-–874. wasps. Am. Nat. 167:467–480. Rainey, P.B. & Rainey, K. 2003. Evolution of co- Oldroyd, B., Rinderer, T., Buco, S.M. & Beaman, operation and conflict in experimental bacte- L.D. 1993. Genetic variance in honey bees for rial populations. Nature 425:72–74. preferred foraging distance. Anim Behav Ratnieks, F.L.W. & Boomsma, J.J. 1995. Facultative 45:323–332. sex allocation by workers and the evolution of Oster, G. & Wilson, E. 1978. Caste and ecology in polyandry by queens in social Hymenoptera. the social insects. Princeton University Press, Am. Nat. 145:969-–993. Princeton. Ratnieks, F.L.W., Foster, K.R. & Wenseleers, T. Page, R.E., Robinson, G.E., Fondrk, M.K. & Nasr, 2006. Conflict resolution in insect societies. Ann. M.E. 1995. Effects of worker genotypic diver- Rev. Ent. 51:581–608. sity on honey bee colony development and be- Reeve, H.K. & Jeanne, R.L. 2003. From individual havior (Apis mellifera L.). Behav. Ecol. Sociobiol. control to majority rule: extending transactional 36:387–396. models of reproductive skew in animal societ- Pamilo, P. 1991a). Evolution of colony character- ies. Proc. R. Soc. Lond. B 270:1041–1045. istics in social insects. II. Number of reproduc- Reeve, H.K. & Keller, L. 1995. Partitioning of re- tive individuals. Am. Nat. 138:412–433. production in mother-daughter versus sibling as- Pamilo, P. 1991b). Life-span of queens of the ant sociations: A test of optimal skew theory. Am. Formica exsecta. Insectes Soc. 38:111–119. Nat. 145:119–132. Pamilo, P. & Seppä, P. 1994. Reproductive compe- Reeve, H.K. & Keller, L. 2001. Tests of reproduc- tition and conflicts in colonies of the ant Formica tive skew models in social insects. Ann. Rev. Ent. sanguinea. Anim. Behav. 48:1201–1206. 46:347–385. Pamilo, P., Gertsch, P. Thorén, P. & Seppä, P. 1997. Reeve, H.K. & Ratnieks, F.L.W. 1993. Queen-queen Molecular population genetics of social insects. conflict in polygynous societies: mutual toler- Annu. Rev. Ecol. Syst. 28:1–25. ance and reproductive skew. Pages 45-85 in L. Paxton, R.J., Ayasse, M., Field, J. & Soro, A. 2002. Keller, ed. Queen number and sociality in in- Complex sociogenetic organization and repro- sects (L. Keller, ed). Oxford University Press, ductive skew in a primitively eusocial sweat bee, Qxford. Lasioglossum malachurum, as revealed by Reeve, H.K., Emlen, S.T. & Keller, L. 1998. Re- microsatellites. Mol. Ecol. 11:2405–2416. productive sharing in animal societies: repro- Pedersen, J.S. & Boomsma, J.J. 1999. Effect of habi- ductive incentives or incomplete control by tat saturation on the number and turnover of dominant breeders? Behav. Ecol. 9:267–278. queens in the polygyne ant, Myrmica sulcinodis. J. Rheindt, F.E., Gadau, J., Strehl C.P. & Hölldobler, Evol. Biol. 12:903–917. B. 2004. Extremely high mating frequency in Peeters, C. & Ito, F. 2001. Colony dispersal and the the Florida harvester ant (Pogonomyrmex evolution of queen morphology in social Hy- badius). Behav. Ecol. Sociobiol. 56:472–481. menoptera. Annu. Rev. Entomol. 46:601–630. Rosengren, R. & Pamilo, P. 1983. The evolution of Pfennig, D.W., Sherman, P.W. & Collins, J. P. 1994. 1 polygyny and polydomy in mound-building Kin recognition and cannibalism in polyphenic Formica ants. Acta Entomologica Fennica 42:65– salamanders. Behav. Ecol. 5:225–232. 77.

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27 Summary ______

Ross, K.G. 1988. Differential reproduction in mul- tactics in females: the case of size polymorphism tiple-queen colonies of the fire ant Solenopsis in winged ant queens. Insectes Soc 46:6–17. invicta (Hymenoptera: Formicidae). Behav. Ecol. Sanetra, M. & Crozier, R. 2002. Daughters inherit Sociobiol. 23:341–355. colonies from mothers in the ‘living-fossil’ ant Ross, K.G. 1993. The breeding system of the fire Nothomyrmecia macrops. Naturwissenschaften ant Solenopsis invicta: effects on colony genetic 89:71–74. structure. Am. Nat. 141:554-576 Savolainen, R. & Vepsäläinen, K. 1988. A compe- Ross, K.G. 2001. Molecular ecology of social tition hierarchy among boreal ants: impact on behaviour: analyses of breeding systems and ge- resource partitioning and community structure. netic structure. Mol. Ecol. 10:265–284. Oikos 51:135–155. Ross, K.G. & Keller, L. 1995. Ecology and evolu- Schmid-Hempel, P. 1998. Parasites in social insects. tion of social organization: Insights from fire Princeton University Press, Princeton. ants and other highly eusocial insects. Annu. Rev. Schmid-Hempel, P. & Crozier, R.H. 1998. Polyan- Ecol. Syst. 26:631–656. dry versus polygyny versus parasites. Phil. Trans. Ross, K.G. & Shoemaker, D.D. 1997. Nuclear and Roy. Soc. Lond. B. 354:507–515. mitochondrial genetic structure in two social Schwander, T., Rosset, H. & Chapuisat, M. 2005. forms of the fire ant Solenopsis invicta: insights Division of labour and worker size polymor- into transitions to an alternate social organiza- phism in ant colonies: the impact of social and tion. Heredity 78: 690–702. genetic factors. Behav. Ecol. Sociobiol. 59:215– Rosset, H. & Chapuisat, M. 2006. Alternative life- 221. histories in a socially polymorphic ant. Evolu- Seppä, P. 1994. Sociogenetic organization of the tionary Ecology, in press. DOI 10.1007/s10682- ants Myrmica ruginodis and Myrmica lobicornis - 006-9139-3. number, relatedness and longevity of reproduc- Rousset, F. & Billiard, S. 2000. A theoretical basis ing individuals. J. Evol. Biol. 7:71–23 95. for measures of kin selection in subdivided Seppä, P. & Walin, L. 1996. Sociogenetic organiza- populations: finite populations and localized tion of the red ant Myrmica rubra. Behav. Ecol. dispersal. J. Evol. Biol. 13:814–825. Sociobiol. 38:207-217. Russell, A. F. 2001. Dispersal costs set the scene Seppä, P. Queller, D.C. & Strassmann, J.E. 2002. for helping in an atypical cooperative breeder. Reproduction in foundress associations of the Proc. R. Soc. Lond. B 268:95–99. social wasp, Polistes carolina: conventions, com- Russell, A.F., Clutton-Brock, T.H., Brotherton, P. petition, and skew. Behav. Ecol. 13:531–542. N. M., Sharpe, L.L., McIlrath, G.M., Dalerum, Sherman, P.W., Lacey, E.A., Reeve, H.K. & Keller, F.D., Cameron, E.Z. & Barnard, J.A. 2002. Fac- L. 1995. The eusociality continuum. Behav. Ecol. tors affecting pup growth and survival in co- 6:102–108. operatively breeding meerkats Suricata suricatta. Sherman, P.W., Seeley, T.D. & Reeve, H.K. 1988. J. Anim. Ecol. 71:700:709. Parasites, pathogens and polyandry in social hy- Rüppell, O., Heinze, J., & Hölldobler, B. 2001a. menoptera. Am. Nat.131:602–610. Alternative reproductive tactics in the queen- Snyder, L. 1993. Nonrandom behavioral interac- size-dimorphic ant Leptothorax rugatulus (Em- tions among genetic subgroups in a polygynous ery) and their consequences for genetic popu- ant. Anim. Behav. 46: 431–439. lation structure. Behav. Ecol. Sociobiol. 50:189– Strassmann, J.E. 2001. The rarity of multiple mat- 97. ing in social Hymenoptera. Ins. Soc. 48:1–13. Rüppell, O., Heinze, J., & Hölldobler, B. 2001b. Sumner, S., Casiraghi, M., Foster,W. & Field, J. 2002. Complex determination of queen body size in High reproductive skew in tropical hover wasps. the queen size dimorphic ant Leptothorax rugatulus Proc. R. Soc. Lond. B 269:179–186. (Formicidae: Hymenoptera). Heredity 87:33–40. Sundström, L. 1994. Sex-ratio bias, relatedness Rüppell, O. & Heinze, J. 1999. Alternative dispersal asymmetry and queen mating frequency in ants.

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28 Summary ______

Nature 367:266–267. Vickery, W.L., Brown, W.S. & FitzGerald, G.J. Sundström, L. 1995a. Dispersal polymorphism and 2003. Spite: altruism’s evil twin. Oikos 102: physiological condition of males and females 413–416. in the ant, Formica truncorum. Behav. Ecol. 6:132– Wahaj, S.A., Van Horn, R.C., Van Horn, T.L., hy- 139. ena (Crocuta crocuta): nepotism among siblings. Sundström, L. 1995b. Sex allocation and colony Behav. Ecol. Sociobiol. 56:237–247. maintenance in monogyne and polygyne colo- Walin, L., Seppä, P. & Sundström, L. 2001. Repro- nies of Formica truncorum (Hymenoptera; ductive allocation within a polygyne, Formicidae): the impact of kinship and mating polydomous colony of the ant Myrmica rubra. structure. Am. Nat. 146:182–201. Ecol. Ent.26:537–546. Sundström, L., Chapuisat, M. & Keller, L. 1996. Wenseleers, T. & Ratnieks, F.L.W. 2004 Tragedy of Conditional manipulation of sex ratios by ant the commons in Melipona bees. Proc. R. Soc. workers – a test of kin selection theory. Science Lond.¬B 271:S310–S312. 274: 993–995. West, S.A., Griffin, A.S. & Gardner, A. 2006a. So- Sundström, L., Keller, L. & Chapuisat, M. 2003. cial semantics: altruism, cooperation, mutualism, Inbreeding and sex-biased gene flow in the ant strong reciprocity and group selection. J. Evol. Formica exsecta. Evolution 57:1552–1561. Biol., in press. doi:10.1111/j.1420- Sundström, L., Seppä, P. & Pamilo, P. 2005. Ge- 9101.2006.01258.x. netic population structure and dispersal patterns West, S.A., Griffin, A.S., Gardner, A. & Diggle, S.P. in Formica ants – a review. Ann. Zool. 2006b. Social evolution theory for microorgan- Fenn.42:163–177. isms. Nature Rev. Microbiol. 4:597–607. Tarpy, D.R., Gilley, D.C. & Seeley, T.D. 2004. Lev- Westneat, D. F. & Stewart, I. R. K. 2003. Extra- els of selection in a social insect: a review of pair paternity in birds: causes, correlates, and conflict and cooperation during honey bee (Apis conflict. Ann. Rev. Ecol. Evol. Syst. 34:365— mellifera) queen replacement. Behav. Ecol. 396. Sociobiol. 55:513–523. Widdig, A., Nürnberg, P., Krawczak, M., Streich, Tarpy, D.R. & Seeley, T.D. 2006. Lower disease in- W.J. & Bercovitch, F. 2002. Affiliation and ag- fections in honeybee (Apis mellifera) colonies gression among adult female rhesus macaques: headed by polyandrous vs monandrous queens. a genetic analysis of paternal cohorts. Behaviour Naturwissenschaften 93:195–199. 139:371–391. Taylor, P.D. & Frank, S.A. 1996. How to make a Wiernasz, D.C., & Cole, B.J. 2003. Queen size me- kin selection´model. J. Theor. Biol. 180:27–37. diates queen survival and colony fitness in har- Taylor, P.D., Wild, G. & Gardner, A. 2007. Direct vester ants. Evolution 57:2179–2183. fitness or inclusive fitness: how shall we model Wiernasz, D.C., Perroni, C.L. & Cole, B.J. 2004. kin selection? J. Evol. Biol, in press. doi:10.1111/ Polyandry and fitness in the western harvester j.1420-9101.2006.01196.x. ant, Pogonomyrmex occidentalis. Mol. Ecol. 13:1601– Tsuji, K. 1995. Reproductive conflicts and levels 1606. of selection in the ant Pristomyrmex pungens: con- Wilson, A.J., Pemberton, J.M., Pilkington, J.G., textual analysis and partitioning of covariance. Coltman, D.W., Mifsud, D.V., Clutton-Brock, Am. Nat. 146:586–607. T.H. & Kruuk, L.E.B. 2006. Environmental cou- Vehrencamp, S.L. 1983a. A model for the evolu- pling of heritability and selection limits evolution of despotic versus egalitarian societies. tion. PLOS Biol. 4(7), doi:10.1371/ Anim. Behav. 31:667–682. journal.pbio.0040216 Vehrencamp, S.L. 1983b. Optimal degree of skew Woyciechowski, M. & Lomnicki, A. 1987. Multiple in cooperative societies. Am. Zool. 23:327–335. mating of queens and the sterility of workers Velicer, G.J. 2003. Social strife in the microbial among eusocial Hymenoptera. J. Theor. Biol. world. Trends Microbiol. 11: 330–337. 128:317–327.

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8. Acknowledgements

Firstly, I want to thank Lotta – the best supervisor anybody could have. You kept your door open, inspired my work and had incredible faith in my abilities. I respect you for your scientific knowledge as well as for your vision of what science is all about. You showed your broad- mindedness by encouraging me when I dabbled in many things that did not directly contribute towards the thesis, such as science writing, teaching and administrative tasks. Thank you! I also want to acknowledge my collaborators Laurent Lehmann, Max Reuter and Koos Boomsma. Special thanks to Laurent for an excellent express modeling course. Thanks also to Jes Pedersen and Pekka Pamilo for pre-examining this thesis. To Team:Antzz (past and present): I’m lucky to have worked in such an inspiring and fun group. It´s ironic that such collaborative and dynamic people should study conflicts! Cathy, Cedric, Christine, Elina, Emma, Hanni, Heikki, Kalle, Kriko, Luppa, Marianne, Mikko, Minttu, Perttu, Riitta, Sedeer, Tuomo, Vienna: thanks for the many happy hours drinking coffee and counting ants. Thanks also to Soile for her excellent work in the lab, and to our many field assistants in Tvärminne – Anniina, Hannele, Mikko P., Terhi, and many others. Special thanks goes to Heikki, with whom I’ve shared three offices, seven summers at Tvärminne and nine conference trips. Through your loyal friendship I know a little more about football, science, music, and life in general. Perttu and Emma, thank you for your generous scientific advice and for making sure the coffee pot was always on. Riitta, thank you for your contribution to this thesis. Finally, I want to thank Minttu, the original Formica fusca queen, in whose footsteps I have followed in so many ways. Thanks for being a great friend, all the way from Japan to Turku. Thanks also to our sister group, LEED. The journal clubs have been almost as fun as the “test-a-hypothesis” lunches. Hanna – thanks for the collaborations, I look forward to continuing them! Thanks to the Tvärminne possee, especially Christoph, Kimi, Kongo, Marja, Maria, Markus and Topi for the many fantastic summers. Raija, Lallu and Eva also deserve thanks for their valuable help in providing facilities and practical help. During my PhD work, I´ve been lucky enough to travel and meet some great people. Thanks to the international alliance of social insects, especially Adam, Chris DH, Chris Y, Niclas, and Tom. I’ll miss you all! Special thanks to Kevin, whose company is never boring, whether we’re discussing Alanis Morrissette or spite. Thanks for the good times! Thanks to the people at the department who have made my many years there so enjoyable through social football, more or less serious scientific discussions, or just plain drinking.

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Special thanks to Andrés, Chris, Inari, Jukka, Mike and Paula for many good moments. Jonna: thanks for helping me out with the practical things before the defense. Jostein my friend: thanks for dragging me to bars and distracting me from the thesis stress. Many thanks to my friends from my student days, especially the class of ’97, who made biology so much fun that almost half of us ended up doing a PhD. Patte: thanks for sharing the PhD experience with me, and for designing the cover to this book. Hope I can help you on the last leg of your PhD as well! Thanks also to “the other” Katja. Since our first day at Uni, we´ve gone everywhere together: to lectures, fieldtrips, and many many late night afterparties. My warmest thanks for your loyalty and your friendship. This thesis was funded by the Finnish School in Conservation and Wildlife Biology (LUOVA), as well as grants from the Waldemar von Frenckell and Otto A. Malm foundations, and the University of Helsinki. Thank you! Outside of biology, I want to thank my choir, Grex Musicus, for many musical and geographical diversions over the years. Through the choir, I´ve met many amazing people who have become great friends. Special thanks to Heidi, the energy injection, Lare the lad, and Eppu, my favourite boy next door. Thanks to Matti, my mentor. You generously devoted your time and energy to opening many doors for me, both in my mind and in the world surrounding me. Thank you! I have a 16 hour bus trip through Finland to thank for making a fantastic friend. Agent Henna Bauer: you are truly my hero. Henna, Markus & Aarne: thanks for making me part of your family. Daniel has been there for me through most of my PhD. Thank you for supporting me when I didn’t have a clue about what to do next. You made me try my wings, and thanks to you, I feel that that nothing is impossible. My high school friends Cami, Kiiski, Maija and Sonja form my eclectic second family. I admire you all so much and am incredibly lucky to be your friend. Thanks for being there for me, every day, for almost 15 years. Lastly, I want to thank my family. Anja, Niklas, Nadja and Joel: thank you for your love, and for reminding me about what is important in life. Mamma och pappa: you’ve loved and supported me unconditionally since I was small. Your faith in me gave me faith in myself, and I can never thank you enough. This thesis is dedicated to my grandfather, the most influential natural scientist in my life. Stargazing with faffa taught me where to look for the next galaxy. My eyes are still on it.

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31 Helsinki University Printing House ISBN 978-952-92-1758-8 Helsinki 2007