Persistence versus decline of host defenses against brood parasitism: A model system for studies of relaxed selection and phenotypic plasticity

The expression of adaptive traits often declines when the selection pressures favoring them become relaxed, although it is difficult to determine whether these declines represent genetic changes or variation due to phenotypic plasticity. Host defenses against brood parasitic birds, which lay their eggs in the nests of other birds (the hosts) and reduce host fitness, provide an excellent system for studies of relaxed selection and phenotypic plasticity. Hosts may become free from brood parasitism because parasites avoid using well-defended hosts or because of range changes by parasite or host. Whether defenses persist in the absence of parasitism has implications for trait evolution under relaxed selection and for long-term coevolutionary trajectories of parasites and hosts. I assessed whether host defenses against brood parasitic Brown-headed Cowbirds, Molothrus ater, in North America persist under relaxed selection by comparing the responses of hosts breeding in the presence of cowbirds (Sympatric), in long-term isolation from cowbirds (Allopatric) and within the cowbird's range, but where cowbirds were locally uncommon (Naive populations). American Robins, Turdus migratorius, and Gray Catbirds, Dumetella carolinensis, ejected foreign eggs from their nests less frequently in Allopatric populations compared to Sympatric populations. The lower responsiveness in Allopatric populations reflects evolutionary differences rather than phenotypic plasticity, because Naive robins and catbirds, which have had little exposure to cowbirds, rejected experimental parasitism as frequently as their Sympatric counterparts. Genetic drift may explain declines in rejection behavior because neither species is likely to make costly recognition errors in the absence of cowbirds. Yellow Warblers, Dendroica petechia , deserted experimentally parasitized nests and gave two cowbird-specific nest defense behaviors (seet calls and nest protection behavior) less frequently in the Naive population than in the nearby Sympatric population, suggesting that the expression of these defenses is plastic and increases with exposure to cowbirds. Allopatric warblers rejected experimental parasitism and gave seet calls and nest protection behavior to cowbird models as frequently as Naive warblers, indicating the innate components of these defenses have persisted for approximately 6,300 years of isolation from cowbirds. Collectively, these results suggest that behavioral defenses against cowbird parasitism impose little or no cost under relaxed selection.