Variation in host response to brood parasitism reflects evolutionary differences and not phenotypic plasticity

Although adaptive traits are commonly assumed to decline when the selection pressures favouring them become relaxed, behavioural adaptations against brood parasitism often persist for long periods in isolation from brood parasites. In cases where declines have been observed, it has been unclear whether the lower expression in parasite-free populations represents genetic change or is due to phenotypic plasticity in trait expression. We experimentally tested two host species of brood-parasitic brown-headed cowbirds, Molothrus ater, for egg rejection behaviour in populations (1) that have bred outside the parasiteʹs range for up to 8000 years, (2) that have been in long-term contact with cowbirds or (3) that are within the cowbirdʹs range but are ‘cowbird-naïve’ because cowbirds do not breed locally. American robins, Turdus migratorius, and grey catbirds, Dumetella carolinensis, breeding in allopatry from cowbirds showed lower responsiveness to cowbird eggs than conspecifics breeding in sympatry with cowbirds. Responses of robins and catbirds in cowbird-naïve populations, which have had little or no exposure to cowbirds, were identical to those of conspecifics breeding in the presence of cowbirds, indicating that exposure to cowbirds is not necessary for the full expression of rejection and that this defence shows little or no phenotypic plasticity. Therefore, we conclude that the decline in rejection behaviour of allopatric robins and catbirds reflects genetic change and is not due to phenotypic plasticity.