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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C. N. Spottiswoode, R. M. Kilner, N. B. Davies, Blood parasitism, in

Davies N. B., Bourke A. F. G., de L Brooke M., Cuckoos and parasitic ants: Interspecific brood parasitism as an evolutionary arms race. Trends Ecol. Evol. 4, 274–278 (1989). PubMed

S. I. Rothstein, S. K. Robinson,

N. B. Davies,

Brandt M., Foitzik S., Fischer-Blass B., Heinze J., The coevolutionary dynamics of obligate social parasite systems—Between prudence and antagonism. Biol. Rev. 80, 251–267 (2005). PubMed

Kilner R. M., Langmore N. E., Cuckoos PubMed

Medina I., Langmore N. E., The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol. Rev. 91, 569–577 (2016). PubMed

Soler M., Møller A. P., Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343, 748 (1990).

Langmore N. E., Hunt S., Kilner R. M., Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422, 157 (2003). PubMed

Davies N. B., Welbergen J. A., Social transmission of a host defense against cuckoo parasitism. Science 324, 1318–1320 (2009). PubMed

Canestrari D., Bolopo D., Turlings T. C., Röder G., Marcos J. M., Baglione V., From parasitism to mutualism: Unexpected interactions between a cuckoo and its host. Science 343, 1350–1352 (2014). PubMed

Feeney W. E., Medina I., Somveille M., Heinsohn R., Hall M. L., Mulder R. A., Stein J. A., Kilner R. M., Langmore N. E., Brood parasitism and the evolution of cooperative breeding in birds. Science 342, 1506–1508 (2013). PubMed

Lyon B. E., Eadie J. M., Conspecific brood parasitism in birds: A life-history perspective. Annu. Rev. Ecol. Evol. Syst. 39, 343–363 (2008).

Sato T., A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323, 58–59 (1986). PubMed

R. J. Wootton, C. Smith,

Wickler W., ‘Egg-dummies’ as natural releasers in mouth-breeding cichlids. Nature 194, 1092–1093 (1962).

Wagner C. E., Harmon L. J., Seehausen O., Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487, 366 (2012). PubMed

A. Konings,

Wisenden B. D., Alloparental care in fishes. Rev. Fish Biol. Fish. 9, 45–70 (1999).

Payne R. B., Woods J. L., Payne L. L., Parental care in estrildid finches: Experimental tests of a model of

Grim T., Samaš P., Hauber M. E., The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav. Ecol. Sociobiol. 68, 749–759 (2014).

Strausberger B. M., Rothstein S. I., Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav. Ecol. 20, 691–699 (2009).

Hosoi S. A., Rothstein S. I., Nest desertion and cowbird parasitism: Evidence for evolved responses and evolutionary lag. Anim. Behav. 59, 823–840 (2000). PubMed

Reichard M., Polačik M., Tarkan A. S., Spence R., Gaygusuz Ö., Ercan E., Ondračková M., Smith C., The bitterling–mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution 64, 3047–3056 (2010). PubMed

Procházka P., Konvičková-Patzenhauerová H., Požgayová M., Trnka A., Jelínek V., Honza M., Host genotype and age have no effect on rejection of parasitic eggs. Naturwissenschaften 101, 417–426 (2014). PubMed

Hauber M. E., Yeh P. J., Roberts J. O. L., Patterns and coevolutionary consequences of repeated brood parasitism. Proc. R. Soc. Lond. B Biol. Sci. 271 (suppl. 5), S317–S320 (2004). PubMed PMC

Molina-Morales M., Martínez J. G., Martín-Gálvez D., Dawson D. A., Burke T., Avilés J. M., Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime. Evolution 68, 3020–3029 (2014). PubMed

Langmore N. E., Kilner R. M., Why do Horsfield’s bronze-cuckoo

Shizuka D., Lyon B. E., Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463, 223–226 (2010). PubMed

Lotem A., Nakamura H., Zahavi A., Constraints on egg discrimination and cuckoo-host co-evolution. Anim. Behav. 49, 1185–1209 (1995).

Thorogood R., Davies N. B., Cuckoos combat socially transmitted defenses of reed warbler hosts with a plumage polymorphism. Science 337, 578–580 (2012). PubMed

M. H. A. Keenleyside, Parental care, in

R. Coleman, Cichlid egg size summary (1991); http://cichlidresearch.com/eggtabt.html.

M. S. Cohen, “Host-parasite interactions of the African cuckoo catfish

Šulc M., Procházka P., Capek M., Honza M., Common cuckoo females are not choosy when removing an egg during parasitism. Behav. Ecol. 27, 1642–1649 (2016).

Kilner R. M., The evolution of virulence in brood parasites. Ornithol. Sci. 4, 55–64 (2005).

Spottiswoode C. N., Koorevaar J. A., A stab in the dark: Chick killing by brood parasitic honeyguides. Biol. Lett. 8, 241–244 (2012). PubMed PMC

Day J. J., Wilkinson M., On the origin of the PubMed PMC

Salzburger W., Van Bocxlaer B., Cohen A. S., Ecology and evolution of the African Great Lakes and their faunas. Annu. Rev. Ecol. Evol. Syst. 45, 519–545 (2014).

Seehausen O., African cichlid fish: A model system in adaptive radiation research. Proc. R. Soc. Lond. B Biol. Sci. 273, 1987–1998 (2006). PubMed PMC

Koblmüller S., Sturmbauer C., Verheyen E., Meyer A., Salzburger W., Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: PubMed PMC

Koblmüller S., Egger B., Sturmbauer C., Sefc K. M., Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Mol. Phylogenet. Evol. 55, 318–334 (2010). PubMed

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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