Nepotism and marmot alarm calling

Alarm calling may be risky if the sounds direct a predator’s attention to the caller. How can a potentially dangerous behaviour be maintained by natural selection? Hamilton’s (1964) inclusive fitness (kin selection) hypothesis has often been invoked to explain alarm calling (Maynard Smith 1965; West Eberhard 1975), particularly in ground-dwelling sciurids such as chipmunks (Smith 1978), prairie dogs (Hoogland 1983, 1995, 1996), and ground squirrels (e.g. Sherman 1977; Dunford 1977; Schwagmeyer 1980; Davis 1984; MacWhirter 1992). Information about which individuals call, who is warned, and how calling affects the survival and reproductive success of callers and listeners is crucial for evaluating the relevance of kin selection to specific antipredator vocalizations. For example, alarm trills of Belding’s ground squirrels, Spermophilus beldingi, to terrestrial predators reduce the callers’ survival but alert relatives. Thus they are nepotistic (Sherman 1977, 1980). In contrast, alarm whistles to swooping hawks increase the callers’ own chances of escaping, suggesting that their function is self-preservation (Sherman 1985). Blumstein et al. (1997) examined the costs and benefits of alarm calling by yellow-bellied marmots, Marmota flaviventris. They reported that females whose young had recently emerged from their natal burrow called more frequently to actual and simulated predators than adult males, nonparous adult females, or yearlings of either sex. Blumstein et al. (page 173) concluded that ‘alarm calling in group-living yellow-bellied marmots is a form of direct parental care and inclusive fitness, broadly defined, is of little importance in the maintenance of alarm calling,’ and that, in agreement with Armitage (1987), ‘yellowbellied marmots appear to care primarily about the welfare of their descendant kin’ (page 183). In reaching these conclusions, Blumstein et al. made three assertions with which we disagree, as did Sherman (1980) in response to some similar claims by Shields (1980). We also question the empirical support for their ‘parental care only’ interpretation. (1) Blumstein et al. (page 173) assert that, compared to kin selection, ‘a more parsimonious explanation (Williams 1966) is that callers primarily produce alarm calls to warn their descendant kin, particularly vulnerable offspring who have much to gain from being warned (Maynard Smith 1965; Shields 1980). ’ In our opinion, there are two reasons why parsimony is not an appropriate justification for preferring parental care over kin selection. First, methodological parsimony is the general principle that, in explaining a given phenomenon, one should postulate the smallest number of novel theoretical processes possible. For example, to explain how an airborne flying fish gets back into the sea, it is not parsimonious to propose a special adaptive mechanism because gravity is sufficient (Williams 1966, page 11). In explaining any adaptation, ‘one should assume the adequacy of the simplest form of natural selection, that of alternative alleles in Mendelian populations, unless the evidence clearly shows that this theory does not suffice’ (Williams 1966, page 5). Inclusive fitness theory does just this. It is no more complex and no less parsimonious than parental care because of the inherent probabilistic sharing of alleles between all relatives, descendant or collateral. Second, Blumstein et al.’s argument (also Armitage 1987) confuses parsimony with tradition. As Dawkins (1979, page 185) put it ‘good old-fashioned individual selection has always included parental care as an obvious consequence of selection for individual fitness. What the theory of kin selection has added is that parental care is only a special case of caring for close relatives. If we look in detail at the genetical basis of natural selection, we see that ‘‘individual selection’’ is anything but parsimonious, while kin selection is a simple and inevitable consequence of the differential gene survival that, fundamentally, is natural selection. ’ Among Dawkins’s (1979) 12 misunderstandings of kin selection, the first (page 185) was that ‘kin selection is a special, complex kind of natural selection, to be invoked only when ‘‘individual selection’’ proves inadequate. ’ (2) Blumstein et al. assert (page 173) that: ‘by invoking kin selection, sensu lato, without distinguishing the direct and indirect components, researchers imply that indirect fitness benefits are an important driving force behind apparently altruistic behaviours such as alarm calling. ’ However, inclusive fitness theory does not address the relative importance of direct (personal and descendant kin) and indirect (nondescendant kin) fitness components. Indeed, inclusive fitness unifies rather than Correspondence: M. E. Hauber, Section of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca, NY 14853-2702, U.S.A. (meh20@cornell.edu).