Obligate brood parasites manipulate other species into raising their offspring. Avian and insect brood parasitic systems demonstrate how interacting species engage in reciprocal coevolutionary arms races through behavioral and morphological adaptations and counteradaptations. Mouthbrooding cichlid fishes are renowned for their remarkable evolutionary radiations and complex behaviors. In Lake Tanganyika, mouthbrooding cichlids are exploited by the only obligate nonavian vertebrate brood parasite, the cuckoo catfish Synodontis multipunctatus. We show that coevolutionary history and individual learning both have a major impact on the success of cuckoo catfish parasitism between coevolved sympatric and evolutionarily naïve allopatric cichlid species. The rate of cuckoo catfish parasitism in coevolved Tanganyikan hosts was 3 to 11 times lower than in evolutionarily naïve cichlids. Moreover, using experimental infections, we demonstrate that parasite egg rejection in sympatric hosts was much higher, leading to seven times greater parasite survival in evolutionarily naïve than sympatric hosts. However, a high rejection frequency of parasitic catfish eggs by coevolved sympatric hosts came at a cost of increased rejection of their own eggs. A significant cost of catfish parasitism was universal, except for coevolved sympatric cichlid species with previous experience of catfish parasitism, demonstrating that learning and individual experience both contribute to a successful host response.

Department of Biology University of Konstanz Konstanz Germany

Department of Ecology and Vertebrate Zoology University of Łódź Łódź Poland

Radcliffe Institute for Advanced Study Harvard University 8 Garden Street Byerly Hall Cambridge MA 02138 USA

School of Biology and Bell Pettigrew Museum of Natural History University of St Andrews St Andrews Fife KY16 9TS UK

The Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 603 65 Brno Czech Republic

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Mixed Parentage Broods Indicate Group Spawning in the Brood Parasitic Cuckoo Catfish

Host nest defence does not act as selective agent against plumage polymorphism in brood parasites

Social deprivation in maternal mouthbrooders Tropheus sp. "Caramba" (Teleostei: Cichlidae) decreases the success rate of reproduction and survival rate of fish fry

Low incidence of cannibalism among brood parasitic cuckoo catfish embryos

Individual experience as a key to success for the cuckoo catfish brood parasitism

Parasitic cuckoo catfish exploit parental responses to stray offspring

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