Altruism and other forms of social behaviour

All animals have to face challenges during their life and make decisions about how to cope with their varying social and physical environment. Similarly to other phenotypic traits, behaviour (i.e. collection of adopted decisions) is also under the optimizing pressure of natural selection and considered adaptive only if they maximize the performing individual’s fitness through the net benefits associated with their performance. In that sense, only that behaviour will be favoured by natural selection and will be continuously inherited in the genome of individual lineages, which is able to contribute efficiently to the performing individual’ success in terms of survival and/or reproduction (Danchin et al. 2008).

From an evolutionary point of view, a behaviour can be viewed as social if it has fitness consequences for both the actor, i.e. performer of given behaviour and the recipient, toward which the behaviour is directed. Different forms of social behaviour can be categorized according to whether they are beneficial (increase direct fitness) or costly (decrease direct fitness) for these individuals (West et al. 2007); direct fitness is defined as the probability of successful personal reproduction (Foster et al. 2006a). According to Hamilton’s (1964) classification, benefits and costs are calculated on the basis of lifetime consequences of the behaviour and net fitness effect. Following Hamilton’s terminology, behaviours that are beneficial to the actors and costly to the recipients (+/–) are selfish, whereas behaviours that are costly to the actors but beneficial to the recipients (–/+) are altruistic. Those behaviours which entail direct fitness benefits for both actors and recipients (+/+) are called mutually beneficial (West et al. 2006), while behaviours that has negative fitness consequences for both actor and recipient (–/–) are spiteful (Hamilton 1970).

For evolutionary biology, it has been a challenging problem to explain how altruistic behaviours being costly to perform but beneficial to other individuals could evolve and remain evolutionary stable in natural populations. Interestingly, different interpretations of altruism in the relevant literature often generated semantic confusion about this form of social behaviour (e.g. Wilson 2005, Wilson & Hölldobler 2005, Traulsen & Nowak 2006). For example, ‘reciprocal altruism’ (Trivers 1971), the alternate helping through repeated interactions between unrelated individuals cannot be viewed as altruistic in the above sense because it provides delayed direct fitness benefit for the performing individuals. Similarly, the

term ‘weak altruism’ introduced by Wilson (1975, 1977) does not describe solely altruistic acts as it can be applied by definition to behaviours that increase actors’ fitness directly.

Furthermore, terms like ‘cooperation’ or ‘helping’ can also be misleading sometimes as they are used to describe behaviours that are either beneficial (+/ ) or costly (–/ ) to the actors.

However, the precise distinction between mutually beneficial and altruistic behaviours is of great importance for an obvious reason. In contradistinction to mutually beneficial behaviours, altruistic behaviours do not entail direct fitness benefit for the actor (not even in the long term) that could outweigh the cost of performing the behaviour, thus altruism cannot be explained by the usual interpretation of the Darwinian natural selection (that restricts analyses to direct fitness costs and benefits; Sachs et al. 2004).

2. Hamilton’s theory of inclusive fitness

The concept of inclusive fitness introduced by Hamilton (1964) provided a revolutionary explanation for the evolution of altruistic behaviour by taking the indirect fitness benefits of behaviour into account. Hamilton suggested that the inclusive fitness consequence of an altruistic trait should include the trait’s contribution to the bearer’s fitness (direct fitness effect, see above) and also its contribution to the fitness of all individuals that possess the same genes and have been affected by the behaviour of the bearer (indirect fitness effects; Grafen 1984, Frank 1998, Danchin et al. 2008). For example, an individual that helps to raise its sibling’s offspring would suffer costs associated with the helping behaviour (as helping is likely to hinder its own reproduction), but also gains benefits from the reproductive success of its sibling as they are closely related due to common ancestry, and the helping individual also shares a certain amount of genes with the offspring to be raised. Applying the above-mentioned idea, Hamilton (1964, 1970) developed a mathematical theory to expand the Darwinian concept of natural selection from a theory that focused solely on individuals’ direct fitness to different one that takes account of social interactions, suggesting that natural selection leads to organisms acting as if they are maximizing their inclusive fitness (Grafen 2006). Hamilton summarized his idea known as Hamilton’s rule (Frank 1998), which can be expressed by the formula:

rxy×b-c>0 (1)

This equation involves three terms: c, the cost of direct fitness for the actor; b, the direct benefit for the recipient of the altruistic behaviour; and rxy, the degree of relatedness between the actor (x) and the recipient (y). According to this equation, we can expect altruistic behaviour to evolve when the benefit of the recipient multiplied by its relatedness with the actor exceeds the cost of the altruistic individual. Inclusive fitness theory, also known as kin selection after Maynard Smith (1964), was a major breakthrough and deeply influenced our understanding of social behaviour by providing a simple evolutionary explanation of altruistic traits: genes causing a fitness cost to their altruistic bearers can be rewarded if they contribute to enhance the replication of the same genes in related recipients (Dawkins 1976, Danchin et al. 2008).

The most common way of obtaining indirect fitness benefits is when altruistic behaviour is directed toward individuals who are genetically closely related to the actor due to common ancestry, e.g. an actor may help its close relatives’ reproduction since this way it can indirectly contribute to the passing of its own genes to the next generation. There are two mechanisms that can favour the evolution of this type of altruism (Hamilton 1964): kin recognition, when altruistic behaviour is preferentially directed toward relatives, and limited dispersal, which, by creating a neighbourhood of relatives, allows for acting altruistically toward all neighbours (West et al. 2007). Another way to obtain indirect fitness benefits is to behave altruistically only toward individuals who share the same altruistic genes as the actor.

This latter mechanism, coined as ‘green beard effect’ by Dawkins (1976), generates special assortment of altruistic individuals and requires a single gene (or a number of linked genes) that genetically codes both altruistic behaviour and some recognizable phenotypic trait, such as a “green beard” (Hamilton 1964, 1975, Dawkins 1976, Jansen & van Baalen 2006).

3. Interpretation of inclusive fitness theory

Kin selection theory has been the subject of much debate and misunderstanding, originating either from confused redefinition of terms (i.e. what kind of social interactions we consider altruistic), the misuse of related jargon (i.e. various interpretation of kin selection) or from the inappropriate application of Hamilton’s rule (for reviews see Frank 1998, West et al.

2002, 2007, Foster et al. 2006ab). Group selection, introduced by Wynne-Edwards (1962), was an alternative idea for the explanation of the evolution of altruism, emphasizing the importance of selection at group level, but was strongly criticized and refuted by many works

from theoretical point of view (Maynard Smith 1964, 1976, Grafen 1984, Frank 1986b). Ever since, new forms of group selection models have been developed (Wilson 1975, Wilson &

Colwell 1981, Wilson 2005, Wilson & Hölldobler 2005, Traulsen & Nowak 2006), arguing that kin selection theory provides an inappropriate explanation for the evolution of altruism and emphasizing the importance of multiple levels of selection acting on within-population groups (West et al. 2007). These works also state quite often that colony-level selection in insects (Arthropoda, Insecta) is unquestionably necessary to explain the evolution of eusociality (Wilson 2005, Fletcher et al. 2006), a phenomenon that could not be explained prior to Hamilton’s theory. However, the concept of different levels of selection is entirely consistent with the principle of inclusive fitness theory, i.e. organisms are expected to behave as if they were maximizing their inclusive fitness (Grafen 2006, Gardner et al. 2007). These two ideas (i.e. kin selection & colony-level selection) were shown to be mathematically identical and proved to be just different ways of conceptualizing the same evolutionary process (Grafen 1984, Frank 1986a, 1998, Taylor 1990, Queller 1992, Bourke & Franks 1995, Gardner et al. 2007). It was also shown that there is no theoretical or empirical example of group selection that cannot be explained by individual-level selection or kin selection (Lehmann et al. 2007, West et al. 2007). Inclusive fitness and kin selection theory proved to be useful for understanding specific biological cases, making testable predictions and also for constructing a general theoretical overview (Grafen 1984, Frank 1998, Queller 2004, West et al. 2008). In fact, inclusive fitness provided a unifying framework for all possible explanations of cooperation between interacting individuals, and became the central paradigm in social evolution theory (e.g. Frank 1998, Sachs et al. 2004, Foster et al. 2006b, Lehmann &

Keller 2006, West et al. 2007, 2008).

In the last decade, powerful methods for understanding the evolution of altruism have been developed by applying a new approach (Fletcher & Doebeli 2006, 2009, Taylor et al.

2007) that divides the direct fitness effects of altruism on individuals into two parts: one that is due to the self and the other that is due to the ‘interaction environment’. This methodology emphasizes the fundamental importance of the latter to explain altruistic behaviour and provides a more general concept compared to the inclusive fitness approach, enabling, for instance, also the analysis of interspecific mutualism (Fletcher et al. 2006). However, being mathematically equivalent, the results of these direct fitness analyses can also be interpreted in terms of inclusive fitness, which can be considered as a more natural way of understanding fitness consequences originating from the interactions of related individuals (Taylor et al.

4. Revised versions of the Hamilton’s rule

Inclusive fitness theory and Hamilton’s rule can be applied in any situation involving conflict or cooperation (Hamilton 1964, Treisman 1977). However, it is often neglected that limited dispersal, the same mechanism that favours the evolution of altruistic behaviour toward relatives, may also lead to increased competition between related individuals, reducing or even completely removing the net advantage of altruism (West et al. 2002, Griffin & West 2002, Griffin et al. 2004). The importance and extent of how this kind of competition influences selective processes in nature have been demonstrated by a recent work on fig wasps (West et al. 2001). The level of fighting between fig wasp males has always been a classic example of how kin selection operates as less fighting was predicted to occur in species where competing males were highly related (Hamilton 1979, Trivers 1985). However, West et al. (2001) found that fighting level did not correlate with relatedness across the fig wasp species; in fact, competition between relatives was so intense that it possibly removed any advantage of being altruistic. Instead, fighting levels could be well explained by the direct benefit of winning: males fought more aggressively when there were fewer females to compete for within a fruit.

The effect of competition between relatives can be incorporated into the Hamilton’s rule in several ways (Grafen 1984, Queller 1994, Frank 1998, West et al. 2002). For instance, as West et al. (2002) pointed out, the influence of competition between relatives on kin selection can be investigated by extending Hamilton’s rule to include all individuals whose fitness is affected by an altruistic behaviour. This idea can be summed up in the following equation:

rxy×b-c-rxe×d>0, (2)

where rxy is the genetic relatedness between the altruist and the beneficiary of its altruism (i.e.

the standard r, see above), r_xe is the altruist’s relatedness to the competitors of the beneficiary, and d is the general decrease in fitness of these competitors associated with the altruistic act.

If the altruist is unrelated to the competitors of the beneficiary (rxe=0) or the altruistic act leads to no increase in the general level of competition (d=0), then the classic equation for Hamilton’s rule holds (West et al. 2002). As the altruist becomes more related to the

competitors of the beneficiary (increasing rxe, for example, when competition becomes more local) and/or the altruistic act increases the general level of competition (increasing d), the advantage of being altruistic is reduced. In the extreme, if an individual equally related to both the beneficiary and its competitors, then altruism cannot be favoured, irrespective of the values of b and c (West et al. 2002). Following another concept, Queller’s (1994) model incorporates competition between relatives into the r term of Hamilton’s rule. He showed that standard estimations of relatedness usually overestimate the importance of kin selection and relatedness should be measured at the correct scale, i.e. relatedness to the beneficiary of the altruism has to be measured with respect to the individuals with which the beneficiary will compete (defined here as r_c), rather than with respect to the global population (r_xy). If competition between relatives does occur (rxe>0), then the effective relatedness will be lower (rc<rxy).

All in all, recent refinements of Hamilton’s original rule provided sufficient conceptual solutions to allow for the fact that limited dispersal may induce both high relatedness and increased competition between interacting individuals, and showed that kin selection theory and Hamilton’s rule are correct, but care must be taken when applying them to a specific social system (Griffin & West 2002, West et al. 2002, Griffin et al. 2004).

II. T

HESIS OBJECTIVES

I used the above general framework of inclusive fitness theory to address several questions about how relatedness (more precisely, genetic relatedness due to common ancestry) among individuals may affect different aspects of social behaviour in a relatively simple social system. I aimed to investigate whether individuals of a gregarious bird species discriminate their kin during social interactions in the non-reproductive period, and if they do, such behaviours can be linked to indirect fitness benefits or not. In this thesis, therefore, I looked into five main issues to explore the possible relationship between genetic relatedness and social behaviour in wintering flocks of house sparrows (Passer domesticus). All of the studies presented here were carried out by the Ornithological Group at the University of Pannonia. For all studies I participated in most stages of the work, from bird ringing, behavioural observations through data analyses until the preparations of related manuscripts.

Study 1. What is the kin composition of wintering house sparrow flocks like?

To explore the relationship between genetic relatedness and social behaviour in the species, it is essential to gain adequate information about the kin composition of wintering sparrow flocks, i.e. whether house sparrows have the possibility to interact with related group-mates in natural circumstances. For this purpose, we used intense ringing and observation of wild birds, in combination with molecular genetic data on relatedness and investigated whether feeding aggregations of house sparrows include also aggregations of related individuals (Chapter IV).

Study 2. Do house sparrows discriminate their kin during social foraging?

An important, well studied type of social interactions of sparrows occurs during social foraging, when individuals use alternative behavioural tactics (“producer” and “scrounger”

strategies) to maximize their food intake while adjusting their behaviour to various ecological conditions. Hamilton’s rule predicts kin-discriminative behaviour during social foraging if either the cost of being scrounged or the benefit of the scrounger is high; in the former case reduced scrounging from kin, whereas in the latter case increased scrounging from kin can be expected. To test whether relatedness affects foraging tactic use in house sparrows, we

differently related individuals. Specifically, we tested whether sparrows use the aggressive and non-aggressive form of scrounging tactic at a different rate and with different success against closely related and unrelated flock-mates (Chapter V).

Study 3. How does relatedness influence aggressive interactions in the sparrow flocks?

Inclusive fitness theory can be applied in any situation involving also conflict and competition, in which case it predicts restricted level of aggression between related individuals (at least by its original form, i.e. without local kin competition). To test whether genetic relatedness affects agonistic interactions between house sparrows, we observed captive flocks in which birds could interact with differently related individuals. Specifically, we tested whether sparrows show reduced aggression against kin compared to unrelated flock-mates, and also whether the presence of relatives influences their success, as measured by the achieved rank of birds in dominance hierarchy (Chapter VI).

Study 4. Are kin group-mates more associated with each other in the flocks than unrelated birds?

Socio-positive interactions (such as joining others in non-aggressive activities) are often entailed by important fitness consequences to the participants and genetic relatedness among group-members has been found to affect such affiliative behaviour in various vertebrate species. To test whether kinship affects social preference in house sparrows, we observed captive flocks in which birds could join differently related individuals in different social activities. Particularly, we investigated whether preference between sparrow flock-mates increases with genetic relatedness or familiarity from early developmental period influencing affiliation between flock-mates (Chapter VII).

Study 5. Does the presence of kin affect network position of individuals in the flocks?

In groups of interacting individuals there are often differences between group-members in the number of their social interactions and how central or peripheral they are within the social network (in terms of connectivity to others). To investigate the effect of relatedness on the network positions of house sparrows in their flocks, we used within-group

significantly different from equivalent random networks, and (ii) if they are, how kinship among group-mates affects individuals’ centrality in the network (Chapter VIII).

III. G

ENERAL

M

ETHODS

1. Model species

The house sparrow (Passer domesticus) is the member of the Old World sparrow family Passeridae, and despite the recent population declines in Western Europe, is one of the most widely distributed bird species all over the world. Sparrows live in rural and urban habitats close to humans and are well known for their gregariousness and adaptive capabilities (Anderson 2006). For several reasons, this species seemed to be an ideal subject for the study of kin-biased social behaviours in a non-reproductive context.

Firstly, house sparrows are characterized by sedentary behaviour: after settling at a breeding site, adult birds may live within a small area throughout the year (Summers-Smith 1963, Perrins 1998, Anderson 2006). Natal dispersal is also limited in the species, although significant variation is found among populations and the reported frequency of dispersal may depend on the spatial scale on which it is studied. For example in a meta-population living in an archipelago, only 9.6% of female and 5.7% of male offspring dispersed from their natal island before their first breeding (Altwegg et al. 2000). On the other hand, Fleischer et al.

(1984) reported much higher frequencies of dispersal (52% of females, 27% of males) among neighbouring (usually within 1 km) colonies breeding in a farmland area. However, ringing data suggest that the majority of young sparrows settle close (usually < 2 km) to their natal area (Anderson 2006) and a significant proportion may remain in their natal colony. Such limited movements could result in most sparrows staying with their relatives (e.g. siblings or parents) in the non-breeding flocks at feeding and roosting sites around the breeding colonies.

Secondly, sparrows are highly social, found in flocks at and around their feeding and roosting sites throughout the non-breeding season. These flocks usually consist of ten to 30 or more individuals and flock-members perform various activities together such as foraging, roosting, and dust bathing (Anderson 2006). Flock-members also form social hierarchy and gain social status through aggressive interactions, competing frequently for resources with each other, particularly for food and roosting sites (e.g. Møller 1987, Liker & Barta 2001).

Because sparrows perform such wide variety of interactions, their wintering flocks are frequently used as model systems in studies of social behaviour, especially aggression and status signalling (Møller 1987, Liker & Barta 2001, Bókony et al. 2006; see Nakagawa et al.

2007 for a review) and problem solving in groups (Liker & Bókony 2009). The species is also

one of the best known producer–scrounger systems (Liker & Barta 2002, Lendvai et al. 2004, 2006), as sparrows usually feed in flocks and use both producer (actively searching for food) and scrounger (exploiting other’s food findings) tactics during foraging (Barnard & Sibly 1981, Johnson et al. 2001, Liker & Barta 2002). However, despite the intense research on the social behaviour of the species, we essentially lack adequate information about the kinship structure of sparrow flocks and how relatedness impacts their social behaviour.

one of the best known producer–scrounger systems (Liker & Barta 2002, Lendvai et al. 2004, 2006), as sparrows usually feed in flocks and use both producer (actively searching for food) and scrounger (exploiting other’s food findings) tactics during foraging (Barnard & Sibly 1981, Johnson et al. 2001, Liker & Barta 2002). However, despite the intense research on the social behaviour of the species, we essentially lack adequate information about the kinship structure of sparrow flocks and how relatedness impacts their social behaviour.

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