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Development of Antisnake Defenses in California Ground Squirrels (Spermophilus Beecheyi): II. Microevolutionary Effects of Relaxed Selection From Rattlesnakes

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Nonvenomous Pacific gopher snakes (Pituophis melanoleucus catenifer) and venomous northern Pacific rattlesnakes (Crotalus viridis oreganus) have coexisted in a predator-prey relationship with California ground squirrels (Spermophilus beecheyi) for many thousands of generations. This long-term relationship has fostered in ground squirrels the evolution of antisnake defenses that consist of physiological resistance to rattlesnake venom and behavioral tactics of probing and harassing that might facilitate snake-species discrimination. Snake harassment by adults might also protect pups by interfering with snake hunting activities. Some ground squirrel populations have colonized habitats where rattlesnakes, but not gopher snakes, are rare or absent. Initial research indicates that squirrels experiencing relaxed selection from rattlesnakes are very aggressive toward their remaining nonvenomous snake predator, the gopher snake. Two experiments investigated the effects of relaxed selection from rattlesnakes by examining: 1) changes in level of venom resistance, 2) the reorganization of antisnake behaviors in lab-born pups and wild-caught adults from different sites, and 3) the role of natural experiences on the development of antisnake behavior in a rattlesnake-adapted population. Level of venom resistance was examined by an in vitro radioimmunoassay of serum-to-venom binding of two populations of Douglas ground squirrels (S. b. douglasii). The ancestors of one population are estimated to have experienced relaxed selection from rattlesnakes for about 9,000 years based on genetic distance and radiocarbon analyses. The antisnake behavior of 60-73 day-old lab-born pups from these two populations was video taped during presentations of a caged rattlesnake or gophcr snake for alternate 5-min trials in a seminatural laboratory setting. Two groups of wild-caught adult Beechey groundsquirrels (S. b. beecheyi) were studied using the same protocol for examining antisnake behavior. One group was obtained from a population that recently colonized a rattlesnake-rare site and exhibits moderate venom resistance. The second group came from a population that exhibits very low venom resistance and inhabits a rattlesnake-free site; relaxed selection from rattlesnakes for this population is estimated to span approximately 60,000 years. Comparisons of Douglas ground squirrels from rattlesnake-abundant and rettlesnakerare sites revealed that venom resistance declined approximately 59% after an estimated 9,000 years of relaxed selection from rattlesnakes. Lab-born Douglas pups from the same rattlesnake-rare site were more aggressive toward the gopher snake than toward the rattlesnake whereas pups from the population experiencing predation from both species of snake treated both snakes as similarly dangerous. Unlike pups, wild-caught adults from the rattesnake-adapted population harassed the rattlesnake more intensely than the gopher snake, a phenomenon that may reflect their experience with snakes in nature and larger body size that reduces their vulnerability to envenomation. Wild-caught Beechey ground squirrels that recently colonized a rattlesnake-rare site did not differentiate the rattlesnake and gopher snake whereas Beechey ground squirrels whose ancestors have experienced prolonged relaxed selection from rattlesnakes were more aggressive toward the gopher snake. Consistent with previous findings, prolonged relaxed selection from rattlesnakes, but not gopher snakes, appears to have reduced the inhibition to harass large gopher snakes. This microevolutionary shift in increased aggressiveness toward the gopher snake could result from the virtual absence of any risk in misidentifying rattlesnakes from gopher snakes.

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Affiliations: 1: Departments of Psychology and Anthropology, University of California, Davis, California 95616 U.S.A


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