Delayed dispersal: Living under the reign of nepotistic parents

Auk, The, Jan 2001 by Ekman, Jan, Bagilone, Vittorio, Eggers, Sonke, Griesser, Michael

THE INCLUSIVE FITNESS concept (Hamilton 1964) formulated consequences of social behavior in gene equivalents. In doing so, it enabled fitness consequences of social behavior to be understood within the framework of genetic inheritance of traits. Delayed dispersal of birds was one system where the inclusive fitness concept was put to test. The key issue was to understand how delayed dispersal could be reconciled with evolution through natural selection, when retained offspring forego personal reproduction while they remain in the natal territory (e.g. Skutch 1961).

Cooperative breeding seems to have a secondary role for the maintenance of delayed dispersal, although 96% of bird species where the offspring remain with their parents into adulthood to form family groups also breed cooperatively (Emlen 1995). Although that association between delayed dispersal and cooperative breeding indicates that delayed dispersal is a permissive factor for the maintenance of cooperative breeding, there is not necessarily a causation going in the opposite direction. Cooperative breeding can be seen as an independent decision, and as such it is a consequence rather than a cause of delayed dispersal (Brown 1987, Stacey and Ligon 1987, Koenig et al. 1992, Emlen 1994, Hatchwell and Komdeur 2000), which is consistent with the observation that dispersal can be delayed without the retained offspring engaging in reproduction. Even if some of the retained offspring in a species participate in cooperatively breeding units, there are usually a substantial fraction of them that do not engage in help-atthe-nest, and only a few species like the White-winged Chough (Corcorax melanorham- phus) can be classified as an obligate cooperative breeder (Brown 1987). Even stronger support for the fact that delayed dispersal does not require any involvement of retained offspring in cooperative breeding comes from a number of species where retained offspring, as a rule, never help (Gayou 1986, Veltman 1989, Birkhead 1991, Ekman et al. 1994, Newton et al. 1994, Walls and Kenward 1996, Green and Cockburn 1999, Robinson 2000). Therefore, it seems that the maintenance of delayed dispersal requires an explanation that does not have to resort to fitness gains of cooperative breeding (see also Hatchwell and Komdeur 2000).

UNRESOLVED ISSUES

The fact that cooperative breeding should not be essential for delayed dispersal is consistent with the view that the behavior of remaining in the natal territory is maintained as a product of ecological constraints on dispersal options. Constraints can come in different forms such as lack of mates (Rowley 1981, Pruett-Jones and Lewis 1990), or high risks involved with dispersal (Emlen 1982). Most attention has been focused on a constraint in limited access to habitat in territorial species (Selander 1964, Brown 1969, Koenig and Pitelka 1981, Emlen 1982, Emlen and Vehrencamp 1983). Populations have restricted ranges, and the question of an ecological constraint in lack of vacant habitat (habitat saturation) therefore is reduced to a matter of the quality of unoccupied habitat (Brown 1969, Koenig and Pitelka 1981, Stacey and Ligon 1991). The offspring should gain from dispersing only as long as unoccupied habitat is of sufficiently high quality to be suitable and offer better conditions than what can be gained in the natal territory (Brown 1969). There is now also a growing insight in the role of variation in habitat quality in shaping dispersal strategies. There is tangible evidence showing that retained offspring postpone dispersal while they wait for territorial vacancies of high habitat quality (Zack and Ligon 1985, Komdeur 1992). Still, that evidence for the role of habitat quality does not mean that delayed dispersal is well understood (Heinsohn et al. 1990). Despite its apparent explanatory power, the concept of an ecological constraint in habitat saturation leaves several questions awaiting to be resolved, including (1) How can one account for the absence of delayed dispersal in species living in saturated habitats? (2) Where to wait for a vacancy, that is, why forego dispersal rather than to disperse and queue for vacancies in a territory of higher quality? (3) How can one explain that delayed dispersal is found predominantly among species with a life-his-- tory characterized by low adult mortality, low fecundity, and deferred maturity?

DISPERSAL IN A SATURATED HABITAT

It is not clear how habitat saturation can account for the lack of delayed dispersal in species, which apparently experience an ecological constraint in accessing habitat that is as severe as in species with cooperative breeding (Brown 1969, Stacey and Ligon 1991, Koenig et al. 1992). That lack of generality in the ecological constraints approach was recognized by Brown (1969). Still, studies of the role of habitat saturation with respect to the timing of dispersal have been confined almost exclusively to studies of cooperative breeders with delayed dispersal (e.g. Brown 1987, Emlen 1997), whereas a critical test by Popperian philosophy should aim for systems that falsify the hypothesis to resolve why the hypothesis fails (Popper 1968). It is now well documented that the habitat saturation model fails to predict the absence of delayed dispersal in several cases including temperate regions parids (genus Parus). Removal experiments not only provided compelling evidence for habitat saturation in several parid species (Ekman et al. 1981, Ekman 1989), but additionally, their social system shares a suite of features with species that delay dispersal and are cooperative breeders. Several of temperate-region tits live in small, coherent, and sedentary groups occupying exclusive territories (Goodbody 1952, Dixon 1956, 1963, 1965; Weise and Meyer 1979, Ekman 1979,1989; Nilsson and Smith 1985, Matthysen 1990) just as the overwhelming majority of cooperative breeders (Emlen 1995). The failure to provide an explanation for the lack of delayed dispersal in the genus Parus is a challenge to the ecological constraints model that has rarely been acknowledged (but see Stacey and Ligon 1991, Koenig et al. 1992), let alone resolved.