Behavioral Ecology Advance Access originally published online on October 20, 2004
Behavioral Ecology 2005 16(2):358-363; doi:10.1093/beheco/arh170
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Why long-lived species are more likely to be social: the role of local dominance
Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Address correspondence to J. Ridley. E-mail: j.ridley{at}uea.ac.uk.
Received 8 October 2003; revised 25 August 2004; accepted 10 September 2004.
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ABSTRACT |
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Recent studies have shown that individuals of species that live in groups tend to have high annual survival, but this link has lacked a theoretical explanation. We evaluate two hypotheses that explain how longevity could have led to the evolution of group living. The first is the territory inheritance hypothesis, and it proposes that longevity increases the probability of nonbreeding subordinates surviving long enough to have the opportunity of inheriting their natal territory. Second, we propose a novel hypothesis, the reciprocal altruism hypothesis, which is that longevity increases local dominance by favoring nonaggression pacts among neighboring residents because longevity increases the likelihood of reciprocal altruism. Birds thus accept subordinate residency because the exclusion of nonlocal birds will mean that, if they survive long enough, they will be likely to actually achieve territory inheritance. The reciprocal altruism hypothesis is supported by a wider array of evidence; becomes progressively more powerful as longevity increases, thus producing a positive feedback; explains the evolution of local dominance (whereas the territory inheritance hypothesis assumes its existence); and provides an explanation for why cooperative breeding should be found more often in aseasonal environments.
Key words: cooperative breeding, delayed breeding, localized dominance, reciprocal altruism, short-distance dispersal, social queuing.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONREFERENCES |
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Explaining why some species live in social groups is a long-standing evolutionary challenge, because conspecifics use, and therefore compete for, the same resources. In cooperative breeding groups, some members forgo independent reproduction so as to assist those that do breed, thereby producing a skewed distribution of reproductive success. This is an exceptionally developed form of sociality and has consequently attracted considerable interest (Clutton-Brock, 2002
; Kokko and Ekman, 2002; Kokko and Johnstone, 1999; Stacey and Koenig, 1990). Among vertebrate taxa, sociality is both widespread and patchily distributed. This suggests multiple evolutionary origins and the consequent potential for multiple evolutionary advantages (Dugatkin, 1997), a perspective reinforced by the failure of comparative studies to find any single trait shared across social vertebrates (Bennett and Owen, 2002; Cockburn, 1998; Dugatkin, 1997).
To date, hypotheses to explain the evolution of cooperative breeding in vertebrates have tended to focus on environmental explanations, as reviewed in Hatchwell and Komdeur (2000). However, it has also been pointed out that species' demographic characteristics, such as fecundity or longevity, can predispose them to certain breeding systems (Brown, 1987; Hatchwell and Komdeur, 2000; Kokko and Lundberg, 2001). Most importantly, several studies have shown that cooperative breeding has frequently evolved either in concert with increased longevity or in species that are characterized by long-lived individuals (Arnold and Owens, 1998; Cockburn, 1996; Rowley and Russell, 1990). Although these analyses were all for birds, the hypotheses we present potentially apply to social grouping species in other vertebrate taxa and possibly also some insects (see Cant and Field, 2001).
Why should long-lived individuals be more likely to evolve cooperative breeding? Or to put it another way, why do subordinate individuals in longer-living species choose to become helpers in groups, as opposed to breeding on the best quality unoccupied habitat? The increased benefits of group living reaped by members of longer-living species could be short term, such as increased inclusive fitness, or could be long term, such as an increased expectation of inheriting a breeding position. Kin selection is clearly important in cooperative breeding birds (Cockburn, 1998), and longevity increases overall relatedness in territorial systems (Irwin and Taylor, 2000). However, in general, this is as likely to magnify the inclusive fitness costs of kin competition as it is to magnify the inclusive fitness benefits of kin altruism (Ridley and Sutherland, 2002; Taylor and Irwin, 2000; West et al., 2002). This, together with the fact that it is longevity that is associated with cooperative breeding, suggests that we should direct our search toward long-term benefits.
To understand why individual longevity should be associated with cooperative breeding, it is useful to realize that the evolution of cooperative breeding must be preceded by the evolution of group living. Accordingly, any correlation between species' characteristics and cooperative breeding is also a correlation with group living. It is in this light that we examine two mechanisms that link longevity to group living (Figure 1). Although these hypotheses are not mutually exclusive and may have acted synergistically (Figure 1), we show that it is possible to generate predictions with which to discriminate between them. For the first mechanism, the territory inheritance hypothesis, we develop a hypothesis suggested by Kokko and Johnstone (1999), who noted that longevity can increase the probability that a nonbreeder inherits the breeding position. However, we will argue that this produces only a weak relationship between longevity and group living, and further that it predicts the wrong relationship between cooperative breeding and the degree of environmental seasonality.
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For the second mechanism, the reciprocal altruism hypothesis, we propose a new hypothesis: that longevity favors the evolution of local dominance among nonbreeders because longevity strongly increases the probability of achieving reciprocal altruism with neighbors. By local we mean that dominance declines with distance from home, such that, for instance, nonbreeders have a better chance of seizing breeding vacancies on neighboring territories than they do on more distant territories. Local dominance then favors the evolution of group living and in this way explains the taxonomic correlation between longevity and cooperative breeding.
The territory inheritance hypothesis
Where individuals have the option of becoming resident nonbreeders, they must continually choose between delaying breeding and breeding immediately, on the best-quality vacant habitat. Given that delayed breeding must have evolved before helping behavior, delayed breeding would, initially at least, only have made sense if it led to higher individual reproductive success. As such, we need to consider the affect of longevity, on the fitness consequences of a nonbreeding strategy in a good habitat, relative to those of breeding in a poor habitat. The ratio of nonbreeder to breeder fitness is also central to the evolution of group living because it can affect the threshold beneath which poorer territories will not be used at demographic equilibrium (Pen and Weissing, 2000), and group living declines as this threshold decreases. Similarly, the fitness of a breeder divided by that of a nonbreeder is closely associated with the probability of territory inheritance, which is a key factor in the evolution of group living (Kokko and Johnstone, 1999).
To analyze the effect of longevity on the fitness of nonbreeders, relative to the fitness of breeders, we focus on a widespread mode of group formation, whereby groups form through nonbreeders queuing for a breeding vacancy, either on their own, or on a neighboring territory. If annual fecundity and annual survival probability are M and L, respectively, and breeding is discrete from mortality, lifetime reproductive success for breeders is
 | (1) |
s denotes lifetime reproductive success in the spring, that is, immediately before the breeding season when there is no risk of dying before the next chance at reproduction, and similarly, for breeders in the autumn, lifetime reproductive success is
 | (2) |
If fecundity is monopolized by the breeder, lifetime reproductive success for a nonbreeder who is kth in the queue is given by
 | (3) |
Before calculating the nonbreeder to breeder lifetime reproductive success ratio, we introduce two additional parameters: a (the ratio between nonbreeder and breeder survival on the good habitat) and b (the ratio between lifetime reproductive success on the poor and good habitats). Hence, from Equations 1 through 3
 | (4) |
 | (5) |
The equivalent nonbreeder-to-breeder fitness ratio for environments in which breeding and mortality are better approximated as continuous processes may be calculated by noting that the probability a nonbreeder lives longer than a breeder is a/1 + a, meaning that nonbreeder to breeder lifetime reproductive success ratio is
 | (6) |
; Martin et al., 2000). Consistent with this, cooperative breeding is associated with a reduction in clutch size (Arnold and Owens, 1998). If we assume that changes in longevity lead to no net changes in lifetime reproductive success, then for spring dispersal, the ratio of good to poor habitat lifetime reproductive successes depends on fecundity only; namely, b is again a constant. However, for autumn dispersal, if breeders' lifetime reproductive successes are constant as longevity changes, b is proportional to L. However, whether it is breeders' lifetime reproductive successes or breeders' fecundities that are constant, as longevity changes, is relatively unimportant to the effect of changes in longevity on the desirability of queuing (Table 1).
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The effects of changes in longevity on the desirability of queuing relative to breeding are illustrated in Figure 2 and are summarized in more detail for seasonal environments in Table 1. Together these show that under most scenarios, increased longevity does not favor queuing relative to breeding. When dispersal is restricted to the autumn (i.e., postbreeding), longevity will select against group living, because the fitness of queuers relative to breeders decreases with longevity. This would presumably produce a negative relationship between longevity and cooperative breeding. Only those species for which dispersal occurs in the spring season (i.e., prebreeding) have inheritance probabilities that increase with survivorship (see also Kokko and Johnstone, 1999
) (Figure 2), and then only if breeders and nonbreeders have similar survival rates. This would provide a potential link between longevity and group-living species in seasonal environments with spring dispersal. So, are group-living species more likely to disperse in the spring, before breeding? As it turns out, there is no clear seasonality in the timing of dispersal in group-living species (Ekman et al., 2001; Komdeur and Edelaar, 2001; Rabenold, 1990; Stacey and Ligon, 1991; Walters et al., 1992; Woolfenden and Fitzpatrick, 1984).
More generally, because the risk of mortality is never either completely continuous (aseasonal environments) or completely discrete (seasonal environments), we can view the aseasonal and spring dispersal lines in Figure 2 as the bounds to the range of relationships possible for spring dispersal in any possible environment. This leads us to predict a weaker relationship for species living in more aseasonal environments, which contrasts with comparative evidence showing cooperative breeding to be more common in the tropics (Arnold and Owens, 1998; Cockburn, 1996).
Moreover, with only one or two exceptions, all the transitions to cooperative breeding in Arnold and Owens' (1998) study were associated with increases in longevity 
L of less than 5%, with the pretransition survival probabilities L all exceeding 50%. These figures give an upper bound to the payoff associated with an increase in longevity (Figure 3). Specifically, for the case of a spring-dispersing highest queuer, in a strongly seasonal environment in which breeders and nonbreeders have identical survival, the increase is 6.5% (Equations 1 and 2). However, in any other case the longevity associated payoff will be less than 6.5%, because most queuers necessarily rank lower than beta, nonbreeders often have lower survival rates than breeders, pretransition survivorships are typically higher than 0.5, environments are often aseasonal, and increases in survival are mostly less than 0.05. In summary, although there are possibly scenarios in which increased survival makes waiting for breeding position advantageous, the capacity for nonbreeders to survive longer tends to be cancelled out by a lower turnover of breeders.
Finally, the territory inheritance hypothesis requires the important assumption that nonbreeders already have local dominance (Figure 1). That is, for longevity to be able to increase the benefit of queuing relative to breeding, resident nonbreeders must already be better at capturing breeding vacancies than are floaters (nonresident nonbreeders). However, why any local dominance should exist is left unexplained.
The reciprocal altruism hypothesis
We now outline our hypothesis that increased longevity favors the evolution of local dominance, by making reciprocal altruism among neighbors more advantageous because of the increased probability of repeated interactions between the same players (Axelrod and Hamilton, 1981). This is especially true in territorial systems (Taylor and Irwin, 2000). Reciprocal altruism then facilitates local dominance through favoring the formation of reciprocally beneficial nonaggression pacts, with the result that territorial individuals are initially more aggressive to strange individuals (Getty, 1987; Temeles, 1994). Consequently, a local individual has a prerogative to local breeding vacancies because it needs only to maintain already established social relationships, whereas foreign individuals must pay the cost of simultaneously establishing relationships with all its neighbors (Ens et al., 1995; Krebs, 1982). Although not necessary for our case, territory holders can even cooperatively defend their territories, which has been dubbed the "dear enemy" effect (Getty, 1987). Examples of socially mediated territorial dominance have been reported in a wide range of taxa, including mammals (Rosell and Bjorkoyli, 2002), birds (Beletsky and Orians, 1989; Eason and Hannon, 1994; Godard, 1993), fish (Hojesjo et al., 1998; Leiser and Itzkowitz, 2003), lizards (Trigosso-Venario et al., 2002), crabs (Backwell and Jennions), and amphibians (Owen and Perrill, 1998). Although these ideas were originally introduced to explain the local dominance of territory holders over floaters, we suggest that they explain equally well the local dominance of resident nonbreeders that participate in territorial defense.
Axelrod and Hamilton (1981) identified longevity and sedentariness as the two key facilitators of reciprocal altruism. Although longevity has been our focus here, we also know that for lower taxonomic classifications, sedentariness (holding the same territories for long periods and/or not migrating) correlates positively with cooperative breeding (Arnold and Owens, 1998). Spatial structuring, such as the territoriality that is widespread in group-living species (Zack and Stutchbury, 1992), further restricts movement and thus makes iterated social interactions even more likely (Taylor and Irwin, 2000).
Next we estimate how strongly longevity increases the benefits of reciprocal altruism, so as to make comparisons with the three relationships, we derived earlier for the influence of longevity on nonbreeder to breeder fitness ratios (Figure 2). Specifically, we consider the length of time two neighbors will expect to share a border, or equivalently the length of time neighbors have to trade favors. This parameter determines the evolutionary stability of reciprocal altruism (Axelrod and Hamilton, 1981). Again, as in Figure 2, mortality can be either a constant year-round threat or it can be seasonal. Further, where mortality is seasonal, individuals can disperse to territories either after the mortality season but before breeding season (which, for convenience, we call the spring), or after the breeding season but before the mortality season (which we call the autumn). Assuming individuals settle on their breeding territories for life, they will be neighbors with any given partner until one dies. The probability that two neighbors both survive any give year is L2, and accordingly, the length of time they can expect to be neighbors is 1/(1 – L2) in the spring (from Equation 1) and L2/( 1 – L2) in the autumn (from Equation 2). Consequently, in the spring, an increase in survivorship from 0.5 to 0.55 lengthens partnership times by
 | (7) |
L2idi), thus a 0.5 to 0.55 increase in survivorship lengthens partnership times by
 | (8) |
Some caution is required when comparing payoffs between our two hypotheses (Figure 3) because they measure only the relative increases in nonbreeder fitness and local dominance, not absolute fitness values. However, that said, the cooperation-related indices (Equations 7 and 8) are higher than the analogous estimates for the territory inheritance hypothesis (Figure 3), especially in aseasonal environments (details in Figure 3 legend), which is consistent with the evidence that cooperative breeding is more common in tropical environments (Arnold and Owens, 1998; Cockburn, 1996). Furthermore, the cooperation-related payoffs estimates are lower limits (payoffs increase with longevity), in contrast to the territory inheritance payoffs, which are upper limits (payoffs decrease with longevity) (Figure 3). Finally, there is an additional mechanism by which longevity increases localized dominance, which is not included in these calculations. Not only does longevity increase the reliability of one's dear enemies, via reciprocal altruism, but because longevity decreases the turnover of breeders, it also increases the number of familiar neighbors from whom one could expect support.
Testing the hypotheses
We have focused exclusively on the potential for longevity to favor delayed dispersal. However, although it is true that delayed dispersal necessarily leads to group living, not all such groups breed cooperatively (see Ekman et al., 2001) and not all cooperatively breeding groups form this way (Hatchwell and Komdeur, 2000). Accordingly, at best longevity, reciprocal altruism, and local dominance could only explain some cases of cooperative breeding. Furthermore, although the evidence we have presented is clearly consistent with a role for reciprocal altruism in the evolution of local dominance, argument alone can not rule out other explanations. In Table 2 we list five such explanations and suggest some appropriate predictions to test our hypothesis that reciprocal altruism underpins the link between sociality and longevity. Although these hypotheses are alternative in the sense that one can derive predictions with which to discriminate among them, they are not mutually exclusive and may in reality have acted in either concert or succession. Indeed, it may be more useful to view our first hypothesis as the simplest possible, namely, null, model; the more detailed second hypothesis would then only stand if it were to constitute a significant addition to the former. Furthermore, current and past adaptive value need not be the same thing. For instance, an increase in longevity may originally have favored group living by inflating the fitness benefits of queuing relative to breeding, but group living may now persist through reciprocal altruism.
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How longevity predisposed species to evolve cooperative breeding is thus now an empirical question. Either longevity increases the fitness of queuers relative to breeders, or longevity increases the likelihood that neighbors cooperate. If cooperation among neighbors is rendered evolutionarily stable because any bird that cheats by trying to jump a queue suffers retaliation by multiple players (i.e., all neighboring birds, with whom it will be less familiar than the higher queuers), this would demonstrate how models assuming a series of dyadic interactions underestimate the importance of reciprocal altruism in social evolution.
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ACKNOWLEDGEMENTS |
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We thank Jos Barlow, Matt Gage, Hanna Kokko, Phil Stephens, and three anonymous referees for insightful suggestions. J.R.'s PhD was funded by the School of Biological Sciences at the UEA.
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