BackgroundTrait polymorphism can evolve as a consequence of frequency-dependent selection. Coevolutionary interactions between hosts and parasites may lead to selection on both to evolve extreme phenotypes deviating from the norm, through disruptive selection.Methodology/Principal findingHere, we show through detailed field studies and experimental procedures that the ashy-throated parrotbill (Paradoxornis alphonsianus) and its avian brood parasite, the common cuckoo (Cuculus canorus), have both evolved egg polymorphism manifested in discrete immaculate white, pale blue, and blue egg phenotypes within a single population. In this host-parasite system the most common egg colours were white and blue, with no significant difference in parasitism rates between hosts laying eggs of either colour. Furthermore, selection on parasites for countering the evolution of host egg types appears to be strong, since ashy-throated parrotbills have evolved rejection abilities for even partially mimetic eggs.Conclusions/SignificanceThe parrotbill-cuckoo system constitutes a clear outcome of disruptive selection on both host and parasite egg phenotypes driven by coevolution, due to the cost of parasitism in the host and by host defences in the parasite. The present study is to our knowledge the first to report the influence of disruptive selection on evolution of discrete phenotypes in both parasite and host traits in an avian brood parasitism system.

Cuckoo parasitism in Nagano Prefecture in Japan has shown dramatic changes in the parasitism rate, host usage by the cuckoo, and defensive behavior of hosts during the past 60 yr. To gain insights into these phenomena, we model the population dynamics of a cuckoo-host association together with the population genetics of a rejecter gene in the host population. Analysis shows that both the dynamical change in the host-parasite association and the establishment of the host's counteradaptation crucially depend on the product of two factors, the carrying capacity of the host and cuckoo's searching efficiency. When the product is less than a critical value, the host population cannot evolve a counteradaptation even if parasitized by the cuckoo. Hence, the lack of counteradaptation does not necessarily imply that the host population only recently has become parasitized. As the product becomes larger, the rejection behavior will be eventually established at higher levels in the host population In this case, the spreading of rejection behavior is very fast, which suggests that the cuckoo-host association reaches an equilibrium state within a relatively short period. These results make possible new interpretations of several circumstances reported about cuckoo-host associations.

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An epidemic of pine wilt disease has been spreading in wide areas of Japan for nearly a century. The disease is caused by the pinewood nematode, Bursaphelenchus xylophilus, with the pine sawyer, Monochamus alternatus, as vector. The spread of disease is facilitated by an obligatory mutualism between the nematode and the pine sawyer: the pine sawyer helps the nematode transmit to a new host tree, while the nematode supplies the pine sawyer with newly killed trees on which to lay eggs. We present a mathematical model to describe the host-vector interaction between pines and pine sawyers carrying nematodes, on the basis of detailed data on the population dynamics of pine sawyers and the incidence of pine wilt disease at a study site located on the northwest coast of Japan. We used the model to simulate the dynamics of the disease and predict how the epidemic could be controlled by eradication of the pine sawyer. The main results are as follows: (1) There is a minimum pine density below which the disease always fails in invasion. However, even if the pine density exceeds this minimum, the disease fails in invasion due to the Allee effect when the density of pine sawyers is very low. (2) The minimum pine density increases disproportionately with increase in the eradication rate. (3) The probability that a healthy tree will escape from infection until the epidemic dies out decreases sharply with increase in the initial pine density or the initial density of pine sawyers.