Relaxed selection diminishes social memory and expression of host defences against cuckoos

Abstract

Behavioral defenses are a key adaptation across animals, but confirming decay under relaxed selection is challenging. If expression involves decision-making, then defenses may only be expressed when the right environmental cues are available (i.e. cryptic plasticity). Even if defenses wane, they could be quickly restored once selection resumes as animals can learn by observing others (i.e. social memory). Here we tested cryptic plasticity and social memory under relaxed selection in a cuckoo host, the Common Reed Warbler, by manipulating perceived parasitism risk with social information in geographically-distinct areas differing in allopatry (100 to 1000 years). Despite predicting social information of a cuckoo vs. a control would elicit otherwise cryptic behavioral defenses, only birds that mobbed model cuckoos prior to manipulation upregulated this defense, and only in the recently allopatric population. Social information also had no effect on low-to-absent rates of foreign egg rejection, a second line of defense common to cuckoo host species. These results contrast with parasitized locations where similar methods provoke mobbing and increase egg rejection ten-fold. Our study therefore suggests that, even when manipulating information to account for reaction norms, behavioral defenses may degrade rapidly under relaxed selection, demonstrating a process facilitating a geographic mosaic of coevolution.