Experiments on Cuckoldry in the Mountain Bluebird

Abstract

Cuckoldry produces both genetic polygyny within otherwise socially monogamous species and cryptic altruism by cuckolds themselves, thus the genetic effects of cuckoldry are extremely severe, and should result in the evolution of both anticuckoldry behaviors and means of evading them in socially monogamous birds. Nonexperimental observations of mountain bluebirds revealed that (1) nesting males usually follow nest-building and foraging females, and escort them in and out of their nest cavities prior to hatching, thereby apprising themselves of their mates' whereabouts and companions at all times and preventing their own cuckoldry; (2) intruder males without adjacent territories proceed directly to nest sites when invading others' territories and sometimes display there before being evicted, thereby stationing themselves at the place where most copulations occur and giving themselves the opportunity to cuckold the males that occupy the nest sites; and (3) resident bluebirds defend their nest sites and territories mostly against members of their own sex, thereby minimizing aggressive encounters with members of the opposite sex and maximizing present and future sexual opportunities, perhaps including the opportunity to make cuckolds of others. That these behaviors probably also serve functions unrelated to cuckoldry does not reduce their role as prophylactic or augmenting behaviors to cuckoldry itself. We conducted two experiments on wild bluebirds in order to provoke them into anticuckoldry behavior. The pilot experiment used live, caged male and female bluebirds as models. The main experiment used stuffed male and female bluebirds as models in addition to live bluebirds. Forty pairs and two lone males were tested in 87 trials, covering all nesting stages. Bluebirds responded much more strongly to live than to stuffed models. They did not show any responses to models that could be interpreted as having evolved solely to thwart cuckoldry. However, they did show a repertory of behaviors from defense of their nest sites to attacks on models that formed a gradient of least aggressive to most aggressive responses and would have driven models away from their nests, mates, and territories (and thus simultaneously ended several threats, including that of cuckoldry) had models been free to flee. That these responses were evolved at least partly to cope with cuckoldry threat was affirmed by their sex-biased occurrence. Probably because bluebirds' responses function to cope with several threats, there were no statistically significant changes in their responses in our experiments from nest stage to nest stage except for mounting attempts and singing which never occurred after hatching. The nonoccurrence of these behaviors after hatching parallels the time course of the much more common behaviors of male following and escorting of females, and all of these behaviors are related to courting and fertilization. Hatching may be the cue used by bluebirds to signal the end of the period of cuckoldry risk because females sometimes begin incubation prior to clutch completion, creating ambiguity as to when laying ends. Males attacked females during some trials but females attacked males as often and as intensely, and mate attacks were fairly uncommon in the experiments and were unrelated to nesting stage. Thus we conclude that mate attacks are only misplaced aggression. Because replacement females are not readily available, it would not be adaptive for a male to drive away his mate, as asserted by Barash (1976-1978), unless he had very little certainty of paternity. On the basis of our results with a superior experimental design and far larger number of trials, birds, and breeding seasons, we categorically reject Barash's (1977) claim that male aggression toward females is the species-typical response of mountain bluebirds to cuckoldry threat. Bluebirds respond to that threat by driving potential or actual cuckolders away in a manner that also reduces or eliminates other threats, and is variable in its intensity and form from pair to pair and encounter to encounter.