Neural and behavioral evolution in an eavesdropper with a rapidly evolving host

The diversification of animal communication systems is driven by the interacting effects of signalers, signal receivers, and the environment. Yet, the critical role of unintended receivers, like eavesdropping enemies, has been underappreciated. Furthermore, contemporary evolution of animal signals is rare, making it difficult to directly observe this process. Ormiine parasitoid flies rely exclusively on acoustic cues to locate singing male orthopteran hosts. In Hawaii, selection imposed by Ormia ochracea has led to recent and rapid diversification of their local host crickets' song. We use complementary lab and field experiments to understand how receiver psychology (sensory and cognitive mechanisms) evolves to accommodate a new host and the evolution of that host's signal. Receiver psychology is critical to our understanding of host-parasite coevolution and animal communication, as the sensory system establishes the limits of behavioral responses that exert selection on signals. We demonstrate that the neural auditory tuning and behavior of O. ochracea have evolved in Hawaii, and these differences likely facilitate the detection of novel host songs. Further, the recently evolved songs are highly variable among males, and flies prefer novel songs with particular spectral characteristics, enabling us to predict how eavesdroppers may shape host song evolution. To our knowledge, this is the first evidence for rapid evolution in the sensory tuning of an eavesdropper. Our work links the evolution of sensory systems, signals, and behavior, heeding the recent call for better integration of sensory and cognitive mechanisms of receivers into our understanding of the evolution of animal communication.