Dynamics of evolutionary succession and coordination between opposite adaptations in cuckoo hosts under antagonistic coevolution

Abstract

Adaptations are driven by specific natural selection pressures throughout biological evolution. However, these cannot inherently align with future shifts in selection dynamics, thus manifesting in opposing directions. We performed field experiments on cuckoo hosts to investigate the coexistence and conflict between two evolutionarily successive but opposing behavioral adaptations-egg retrieval and rejection. Our findings provide key insights. (1) Egg rejection against brood parasites in hosts reshapes egg retrieval to flexible reactions-retrieval, ignoring, or outright rejection of foreign eggs outside the nest cup, departing from instinctual retrieval. (2) Parasitism pressure and egg mimicry by parasites remarkably alter the proportions of the three host reactions. Host species with higher parasitism pressure exhibit frequent and rapid rejection of non-mimetic foreign eggs and reduced ignoring or retrieval responses. Conversely, heightened egg mimicry enhances retrieval behaviors while diminishing ignoring responses. (3) Cuckoos employ consistent mechanisms for rejecting foreign eggs inside or outside the nest cup. Direct rejection of eggs outside the nest cup shows that rejection precedes retrieval, indicating prioritization of specific adaptation over instinct. (4) Cuckoo hosts navigate the conflict between the intentions and motivations associated with egg rejection and retrieval by ignoring foreign eggs, a specific outcome of the rejection-retrieval tradeoff.