vol. 160, no. 4 the american naturalist october 2002 Delayed Dispersal as a Route to Breeding: Territorial Inheritance, Safe Havens, and Ecological Constraints Hanna Kokko1,* and Jan Ekman2 1. Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, United Kingdom; Cooperative breeding has provoked questions about how 2. Evolutionary Biology Center, Population Biology, Uppsala the maintenance of such a behavior can be reconciled with University, Norbyva¨gen 18D, SE-752 36 Uppsala, Sweden natural selection. One key issue is to explain postponing Submitted May 2, 2001; Accepted February 25, 2002 dispersal to breed on one’s own, since staying in a group often entails that subordinates forgo personal reproduction (Wiley and Rabenold 1984; Koenig et al. 1992). This cost on direct fitness has to be overcome by some advantage of staying at home (benefit of philopatry) if delayed dis- abstract: The relative roles of ecological constraints, the benefits of philopatry, and the role of life history continue to be debated in persal is to be explained. Some authors emphasize that the the evolution of natal philopatry and cooperative breeding. We com- cost on direct fitness is small if personal reproduction after pare three routes to breeding: departing to search for territories as dispersing would have been unlikely, which happens if a floater, staying and queuing to inherit the natal territory, or queuing habitats are saturated and gaining a breeding position else- and eventually shifting to a neighboring vacancy. Our model assumed where is, therefore, difficult (the “ecological constraint” a dominance-structured population. It quantifies the benefits of phil- hypothesis; Selander 1964; Brown 1969; Emlen 1982a, opatry for varying-rank subordinates and contrasts it against the benefit of dispersal. We apply the model to data on Siberian jay 1995). Others put more emphasis on the benefits that natal Perisoreus infaustus, a species in which retained offspring do not help philopatry can bring about (Stacey and Ligon 1987, 1991; at the nest. The results indicate that territorial inheritance plays a Zack and Stutchbury 1992) or on life-history traits, such small role in this species (presumably due to inbreeding avoidance), as longevity, that predispose species to become cooperative and territory acquisition is less constrained for dispersing than phil- (Arnold and Owens 1998; Hatchwell and Komdeur 2000). opatric offspring. Nevertheless, small family groups—one or, at the Often, nonreproductive subordinates gain indirect fitness most, two same-sex queuers—are predicted to form because phil- opatric offspring gain nepotistic benefits that improve their survival. through helping (Emlen and Wrege 1989; Mumme et al. This fits with data on group sizes and supports the idea of the natal 1989; Koenig et al. 1992; Mumme 1992; Cockburn 1998), territory as a safe haven for waiting for breeding opportunities. We but in some species, delayed dispersal occurs without off- also discuss our predictions in the light of ecological constraints and spring helping their parents (Gayou 1986; Veltman 1989; clarify recent confusingly different predictions on the role of habitat Ekman et al. 1994; Green and Cockburn 2001). This sug- saturation as an explanation for delayed dispersal and cooperative gests that direct benefits can suffice to explain delayed breeding. We argue that “ecological constraint” is too wide a term to yield useful predictive power and that it is more appropriate to dispersal and serves as a useful reminder that the decision examine the consequences of specific life-history traits on the success to help does not automatically follow from the decision of dispersers. to stay (Emlen 1982a, 1982b; Brown 1987; Kokko et al. 2001). Keywords: dispersal, benefits of philopatry, ecological constraints, co- operative breeding, competition for breeding, queuing. A variety of direct benefits can favor philopatry: sub- ordinates may breed (females) or gain paternity (males) despite the presence of a dominant (Arnold 1990; Brown * Corresponding author. Present address: Department of Biological and En- vironmental Science, University of Jyva¨skyla¨, P.O. Box 35, FIN-40351 Jyva¨s- and Brown 1990; Rabenold et al. 1990; Jennions and Mac- kyla¨, Finland; e-mail: hanna.kokko@jyu.fi. donald 1994; Sherman et al. 1995; Laranzo-Perea et al. Am. Nat. 2002. Vol. 160, pp. 468–484. ᭧ 2002 by The University of Chicago. 2000), they may eventually inherit the dominant position 0003-0147/2002/16004-0005$15.00. All rights reserved. within the group (territorial inheritance; Woolfenden and Delayed Dispersal as a Route to Breeding 469 Fitzpatrick 1978; Zack and Stutchbury 1992; Russell and be more important than territorial inheritance, especially Rowley 1993; Ragsdale 1999; Queller et al. 2000), or they if incest avoidance frequently prevents territory inheri- may gain a breeding position elsewhere after having spent tance (Koenig et al. 1998). time in the group (Walters et al. 1988; Zack 1990; Zack Here we build a general model of different routes to and Stutchbury 1992; Russell and Rowley 1993; Green and breeding and show under which conditions queuing at Cockburn 2001). These advantages may co-occur with a home (philopatry) is favored. Our aim is threefold. First, “safe haven” mechanism, by which we mean improved we define the fitness benefit of dispersing in a way that survival of offspring in the natal territory (Ekman et al. allows direct comparisons to the benefit of philopatry at 2000). If individuals have to wait for breeding positions, a specific rank position. The model is used to obtain in- survival during the waiting period becomes an important terspecific predictions on characteristics that promote de- predictor of fitness (Faaborg and Bednarz 1990; Ekman et layed dispersal. Second, we apply the model to data on al. 2000; Green and Cockburn 2001). Siberian jays Perisoreus infaustus, a species in which de- Naturally, to explain delayed dispersal, both costs and layed dispersal occurs without helping (Ekman et al. 1994), benefits of delaying have to be considered (Koenig et al. to judge if the model can predict group sizes in a specific 1992). Despite the general agreement that philopatric ad- case. Finally, we use our model to make conceptual ar- vantages must be weighed against the profitability of dis- guments about the ecological constraint hypothesis; here persal, formal comparisons of fitness benefits have been we also compare and clarify predictions from recent mod- lacking for a long time (Wiley and Rabenold [1984] pro- els that make use of constraints. vide an exception). A probable reason is that benefits of In our model, we consider the following routes to be- philopatry are often delayed, and a potentially complicated coming a breeder. An individual may leave the natal ter- dynamic approach is needed to calculate fitness (Lucas et ritory and become a floater who competes for territories al. 1997), although, in a conceptual approach, the benefits elsewhere. We assume that a floater is not able to observe can also be summarized as a single benefit variable (Rags- an arbitrarily large area but is restricted to a specific part dale 1999). Recent models have made progress in this of the population (Zack and Stutchbury 1992). The in- respect: they derive fitness benefits of being nth in a queue dividual may also stay as a philopatric subordinate in its for breeding positions (Field et al. 1999) or compare the natal territory, from where it may eventually inherit the advantages of staying in a queue with either a fixed payoff territory, or it may seize a breeding opportunity in nearby from dispersing (Kokko and Johnstone 1999) or, more territories. We call this latter process “shifting.” While the properly, a payoff that depends on how the population as philopatric individual probably observes a smaller number a whole occupies territories (Kokko and Sutherland 1998; of potential vacancies than a floater, it may survive sub- Pen and Weissing 2000; Kokko and Lundberg 2001). How- stantially better. Higher survival in the natal territory may ever, these models assume either that there is only one be a result of parental nepotism (Ligon 1981; Brown and queuer to inherit the territory or that queuing is strict, Brown 1984; Ekman and Rosander 1992; Ekman et al. and so the only way in which a low-ranking individual 1994), but it can also occur simply because it is advan- can gain fitness is through waiting until all predecessors tageous to live in a familiar environment and have access in the hierarchy have died (see Monnin and Ratnieks 1999 to resources within the territory. The benefits of philopatry for an exception in a slightly different context where the therefore include using the natal territory as a safe haven alternative to queuing is helping). Another simplifying as- from which to vie for local breeding opportunities. sumption of the earlier models is that territory inheritance is guaranteed to be successful: floaters or neighbors never The Model compete with queuers over a vacancy. In reality, in many species a vacancy created by the death When should an individual disperse? A disperser poten- of a dominant breeder can be filled by individuals from tially gains both direct and indirect fitness. Dispersal in- nearby territories (e.g., Mumme and de Queiroz 1985; fluences direct fitness whenever it influences the chances Zack and Rabenold 1989; Zahavi 1990). The individual to obtain a breeding position. Indirect fitness may also who wins the vacancy is not always the one who has been increase, since the absence of the dispersing individual may queuing for the longest (Russell and Rowley 1993; Lar- improve the fitness of relatives who remain in the group, anzo-Perea et al. 2000), although queuing often appears for example, through reduced competition for local re- relatively strict (Wiley and Rabenold 1984; Creel and Waser sources (Hamilton and May 1977).