Alarm Calling Predicted by Inclusive Fitness
KeywordsGround Squirrel Alarm Call Inclusive Fitness Antipredatory Behavior Tufted Capuchin
Alarm calling: vocalizations that alert other animals to immediate danger (Sherman 1977).
Inclusive fitness: a theory to explain cases when an animal behaves in such a way as to promote the advantages of other members of the species not its direct descendants at the expense of its own (Hamilton 1963, p. 354).
Alarm calling is an inherently dangerous behavior, and its adaptive function was poorly understood for decades. Calling individuals suffer direct costs (e.g., predation), and so the ultimate function was initially described as a residual behavior thought to have evolved as a signal from parents to offspring (Maynard-Smith 1965). Subsequent theories described the behavior as individually selective. Trivers (1971) suggested that alarm calls reduce the caller’s vulnerability, while calls may also reveal the predator’s location (Dawkins 1976) or else promote antipredatory behavior in socially living primates. Finally, Hamilton (1971) hypothesized that announcing a predator’s presence may promote aggregation by potential prey and reduce the likelihood that any one individual is killed (reviewed in Cheney and Seyfarth 1981).
Alarm Calling and Kinship
Across taxa, alarm call production is correlated with the probability that kin are within acoustic range (Sherman 1977); alarm callers derive inclusive fitness benefits by warning kin of danger (Bergstrom and Lachmann 2001). In female-philopatric species (where males disperse), adult females produce more calls than adult males, suggesting proximity to relatives drives alarm calling. But that may not be the most parsimonious explanation.
Subsequent investigation into Sherman’s (1977) data on Belding’s ground squirrels (Urocitellus beldingi) found that females with offspring produce more calls than males do, suggesting that rather than inclusive fitness, it was direct fitness benefits that drive the behavior.
Blumstein and colleagues (1997) later supported the idea of direct benefits as well, demonstrating that in yellow-bellied marmots (Marmota flaviventris), a primary predictor of female alarm calling was whether her pups had emerged from underground dens that year. The two hypotheses are not mutually exclusive. That is, as Cheney and Seyfarth (1981) noted, for a female to protect her offspring, she must also stay alive, and so alarm calling may target a broad audience to ensure the survival of multiple individuals. They found support for both hypotheses in vervet monkeys (Chlorocebus pygerythrus), whereby adult females’ alarm called more than adult males, but there was no relationship between calling and number of offspring or the proximity to offspring as might be expected.
A few studies have attempted to test the various hypotheses of alarm calling in primates, with similar findings. Forest guenon alarm call behavior in Tai Forest, Ivory Coast, for example, varies with predator-type (leopard vs. chimpanzee) and is thought to be evolved to deter (especially cryptic) predators that depend on surprise attacks. When the above hypotheses were tested against each other in the same species, new world tufted capuchins (Cebus apella nigritus) showed similar patterns. Like the guenons, the capuchins exhibited predator-specific responses as well. Thus, there is growing evidence that alarm calling to felid predators has evolved as a self-preservation behavior, while calling to predators that can be more readily mobbed (e.g., snakes) may be better explained as a kin-selected behavior.
Shelley and Blumstein (2005) conducted a phylogenetic analysis to investigate whether alarm calling had evolved initially as a selfish or else nepotistic (promoting inclusive fitness) behavior. Their results supported the idea that it initially evolved to communicate to predators, not to nearby kin, and thus while benefits to relatives likely contributed to the persistence of the trait in a population, it was less important than the benefits incurred by the callers themselves. In summary, results from investigations into the function of alarm calling in social animals converge on indirect benefit to group members, often kin, but also on direct benefit to the caller and their offspring.
- Dawkins, R. (1976). The selfish gene. Oxford: Oxford University Press.Google Scholar