Context and Animal Behavior III: The Relationship Between Early Development and Evolutionary Persistence of Ground Squirrel Antisnake Behavior

Abstract

California ground squirrel pups are frequent prey of northern Pacific rattlesnakes and Pacific gopher snakes. Although pups innately recognize that snakes are dangerous, they exhibit adult-like antisnake behaviors that are perilous. For the most part, adults apply antisnake behaviors to directly or indirectly protect pups. Two experiments using video investigated the evolutionary and developmental stability of antisnake behavior with the aim of identifying genetic and epigenetic factors that could account for its precocious, but dangerous expression. In Experiment 1, adult squirrels from Folsom Lake where rattlesnake and gopher snakes are abundant were compared with squirrels from Lake Tahoe and Mount Shasta where these snakes are absent and whose ancestors may have experienced relaxed selection from snakes spanning an estimated 300,000 years. Squirrels interacted with a caged rattlesnake or gopher snake for alternate 5-min trials in a laboratory setting. The results of this experiment revealed that the antisnake behaviors of Lake Tahoe and Mount Shasta squirrels were not substantially different from the Folsom Lake squirrels, a finding that suggests low heritability. In Experiment 2, lab-born pups from Folsom Lake were alternately exposed for 5-min trials to a caged gopher snake and guinea pig. The findings from this experiment indicated that visual recognition of snakes had a sharp onset at 40 to 41 days of age, the first day each pup showed evidence of pattern vision. In other rodents, this developmental period shortly after eye opening coincides with major dendritic growth and leveling off interneural connectivity in visual cortex. In ground squirrels, the early expression of antisnake behaviors that function more effectively in adults than in pups could reflect the requirements shaped by natural selection for the reliable emplacement of neural circuitry subserving snake recognition during the initial, less variable period of neuronal outgrowth.