Defence behaviour against brood parasitism is deeply rooted in mainland and island scrub-jays

Abstract

When selection pressures for an adaptation relax, the trait may decline, or it may be maintained if there are no fitness costs. The interactions between avian brood parasites and their hosts are dynamic, with selection pressures changing as host or parasite ranges shift, or as parasites switch to new hosts once old hosts evolve defences. The extent to which hosts retain defences in the absence of parasites has important consequences to parasite–host coevolution. We tested whether island scrub-jays, Aphelocoma insularis , and western scrub-jays, A. californica , have maintained egg ejection behaviour in the absence of brood parasitism and provide an estimate of how long they have maintained ejection. Island scrub-jays and western scrub-jays ejected 100% of foreign eggs placed into their nests, and genetic analyses revealed no evidence of conspecific brood parasitism that could maintain ejection. Extreme variation in intraclutch egg appearance may result in hosts ejecting their own oddly coloured eggs, which would select against the maintenance of ejection. However, island, western and Florida scrub-jays, A. coerulescens , also an ejecter, showed less variation than the common grackle, Quiscalus quiscula , a species that has an extremely high level of intraclutch egg variation and may have lost its rejection defence, because it rejects its own oddly coloured eggs. Based on molecular clock analyses of mitochondrial DNA control region and ND2 sequences, island and western scrub-jays split approximately 140 000–151 000 years ago, western and Florida scrub-jays 1 000 000 years ago, and island and Florida scrub-jays 1 250 000 years ago. Ejection behaviour may have been maintained this long in the absence of parasitism, but it is possible that scrub-jays were parasitized as recently as the end of the Pleistocene 10 000 years ago, when cowbirds were more abundant. Nevertheless, these results indicate that (1) egg ejection is not a costly trait to maintain in scrub-jays, (2) brood parasites may not be able to alternate between well-defended hosts and hosts that have lost ejection defence following past episodes of parasitism and (3) brood parasites may have to deal with host communities that have well-developed defences by evolving specialized adaptations for a single host species or a small set of species.