Evolutionary Dissipation of an Antisnake System: Differential Behavior By California and Arctic Ground Squirrels in Above- and Below-Ground Contexts

Abstract

Abstract Arctic ground squirrels (Spermophilus parryii ablusus) have been free from snake predation for about 3 million years. To evaluate the effects of this prolonged relaxation of natural selection, lab-born Arctic ground squirrels were compared to snake-inexperienced California ground squirrels (Spermophilus beecheyi fisheri) from a habitat where rattlesnake and gopher snake predation is intense. Their behavior was video taped during 10-min encounters with a Pacific gopher snake (Pituophis melanoleucus catenifer) in a seminatural above-ground setting and in an artificial burrow. In separate trials, a domesticated Norway rat was used as a control for the effects of encountering a novel animate object; this rat was enclosed in a slowly moving opaque nylon bag above ground but was allowed to move freely below ground. No evidence was found that, after prolonged relaxed selection from snakes, Arctic ground squirrels retained the specialized behavioral antisnake defenses evident in California ground squirrels. Although we originally hypothesized that the more constrained burrow context might limit the evolutionary dissipation of behavioral antisnake defenses, we found no evidence of a more intact system in Arctic squirrels below than above ground. Arctic squirrels used many of the same general kinds of motor patterns as California squirrels, but in ways that failed to differentiate the gopher snake from the rat in either above- or below-ground contexts. In contrast, the California squirrels tail flagged only in the presence of the snake above ground and differentially applied substrate-throwing at the snake and rat burrow intruders, harassing the snake more than twice as much as the rat. Above ground, California ground squirrels were more conservative toward both adversaries than Arctic ground squirrels were, keeping their distance and therefore experiencing fewer noxious consequences, such as snake strikes. However, this result was context dependent. Below ground, California ground squirrels were more willing than Arctic ground squirrels to approach and harass both burrow intruders. Although repeated striking evoked occasional snake-directed substrate throwing above ground, Arctic ground squirrels never threw substrate at the snake in the burrow. In comparison with California ground squirrels, Arctic ground squirrels appear to enter their first gopher snake encounter with both a much lower assessment of the risk involved and less clearly defined knowledge about how to deal with these risks. We conclude that 3 million years of genetic drift has altered the cognitive system structuring the meaning of snakes to Arctic ground squirrels in various settings.