Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds

Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host's egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts. Obligate brood parasitic birds lay their eggs in the nests of other species. In response to such parasitism, which reduces the fitness of the foster parents, hosts have evolved refined foreign-egg rejection abilities, while parasites have evolved increasing mimicry of the host eggs. But how do hosts recognize and accept their own eggs? Here we hypothesized that hosts learn about their own and foreign eggs through experience with unusual eggs in an early clutch and then they become increasingly better at rejecting the parasite's egg in subsequent nests and breeding attempts. We confirmed such a learning mechanism with a simple field experiment on the American robin, an egg rejecter host of the brown-headed cowbird. In turn, a complex mathematical model revealed that with more learning by the host we see the evolution of an increasingly fine-tuned egg recognition system by the would-be foster parents and a greater mimetic match of the host eggs by the parasites.