Host-parasite dynamics involve coevolutionary arms races, which may lead to host specialization and ensuing diversification. Our general understanding of the evolution of host specialization in brood parasites is compromised by a restricted focus on bird and insect lineages. The cuckoo catfish (Synodontis multipunctatus) is an obligate parasite of parental care of mouthbrooding cichlids in Lake Tanganyika. Given the ecological and taxonomic diversity of mouthbrooding cichlids in the lake, we hypothesized the existence of sympatric host-specific lineages in the cuckoo catfish. In a sample of 779 broods from 20 cichlid species, we found four species parasitized by cuckoo catfish (with prevalence of parasitism of 2%-18%). All parasitized cichlids were from the tribe Tropheini, maternal mouthbrooders that spawn over a substrate (rather than in open water). Phylogenetic analysis based on genomic (ddRAD sequencing) and mitochondrial (Dloop) data from cuckoo catfish embryos showed an absence of host-specific lineages. This was corroborated by analyses of genetic structure and co-ancestry matrix. Within host species, parasitism was not associated with any individual characteristic we recorded (parent size, water depth), but was costly as parasitized parents carried smaller clutches of their own offspring. We conclude that the cuckoo catfish is an intermediate generalist and discuss costs, benefits and constraints of host specialization in this species and brood parasites in general.

Department of Biological Sciences University of Zambia Lusaka Zambia

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Ecology and Vertebrate Zoology Faculty of Biology and Environmental Protection University of Lodz Lodz Poland

Institute of Biology University of Graz Graz Austria

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Zobrazit více v PubMed

Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

Antonson, N. D., Rubenstein, D. R., Hauber, M. E., & Botero, C. A. (2020). Ecological uncertainty favours the diversification of host use in avian brood parasites. Nature Communications, 11(1), 4185.

Balakrishnan, C. N., Sefc, K. M., & Sorenson, M. D. (2009). Incomplete reproductive isolation following host shift in brood parasitic indigobirds. Proceedings of the Royal Society B: Biological Sciences, 276(1655), 219-228.

Bayona-Vásquez, N. J., Glenn, T. C., Kieran, T. J., Pierson, T. W., Hoffberg, S. L., Scott, P. A., Bentley, K. E., Finger, J. W., Louha, S., Troendle, N., Diaz-Jaimes, P., Mauricio, R., & Faircloth, B. C. (2019). Adapterama III: Quadruple-indexed, double/triple-enzyme RADseq libraries (2RAD/3RAD). PeerJ, 7, e7724. https://doi.org/10.7717/peerj.7724

Blažek, R., Polačik, M., Smith, C., Honza, M., Meyer, A., & Reichard, M. (2018). Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts. Science Advances, 4(5), eaar4380.

Bogusch, P., Kratochvíl, L., & Straka, J. (2006). Generalist cuckoo bees (Hymenoptera: Apoidea: Sphecodes) are species-specialist at the individual level. Behavioral Ecology and Sociobiology, 60, 422-429.

Brichard, P. (1979). Unusual behaviors in Lake Tanganyika cichlids. Buntbarsche Bulletin, 74, 10-12.

Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Maechler, M., & Bolker, B. M. (2017). {glmmTMB} balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal, 9(2), 378-400.

Bush, S. E., Villa, S. M., Altuna, J. C., Johnson, K. P., Shapiro, M. D., & Clayton, D. H. (2019). Host defense triggers rapid adaptive radiation in experimentally evolving parasites. Evolution Letters, 3(2), 120-128.

Christensen, R. H. B. (2022). Ordinal-regression models for ordinal data. R package version 2022.11-16.

Cohen, M. S., Hawkins, M. B., Knox-Hayes, J., Vinton, A. C., & Cruz, A. (2018). A laboratory study of host use by the cuckoo catfish Synodontis multipunctatus. Environmental Biology of Fishes, 101, 1417-1425.

Cohen, M. S., Hawkins, M. B., Stock, D. W., & Cruz, A. (2019). Early life-history features associated with brood parasitism in the cuckoo catfish, Synodontis multipunctatus (Siluriformes: Mochokidae). Philosophical Transactions of the Royal Society B, 374(1769), 20180205.

Colborne, S. F., Garner, S. R., Longstaffe, F. J., & Neff, B. D. (2016). Assortative mating but no evidence of genetic divergence in a species characterized by a trophic polymorphism. Journal of Evolutionary Biology, 29(3), 633-644.

Cruz-Laufer, A. J., Pariselle, A., Jorissen, M. W., Muterezi Bukinga, F., Al Assadi, A., Van Steenberge, M., Koblmüller, S., Sturmbauer, C., Smeets, K., Huyse, T., Artois, T., & Vanhove, M. P. (2022). Somewhere I belong: Phylogeny and morphological evolution in a species-rich lineage of ectoparasitic flatworms infecting cichlid fishes. Cladistics, 38, 465-512.

Davies, N. B., & Welbergen, J. A. (2009). Social transmission of a host defense against cuckoo parasitism. Science, 324(5932), 1318-1320.

Dawkins, R., & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London. Series B. Biological Sciences, 205(1161), 489-511.

Day, J. J., Bills, R., & Friel, J. P. (2009). Lacustrine radiations in African Synodontis catfish. Journal of Evolutionary Biology, 22(4), 805-817.

Day, J. J., Peart, C. R., Brown, K. J., Friel, J. P., Bills, R., & Moritz, T. (2013). Continental diversification of an African catfish radiation (Mochokidae: Synodontis). Systematic Biology, 62(3), 351-365.

Eaton, D. A. R., & Overcast, I. (2020). Ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36, 2592-2594.

Egger, B., Meekan, M., Salzburger, W., Mwape, L., Makasa, L., Shapola, R., & Sturmbauer, C. (2004). Validation of the periodicity of increment formation in the otoliths of a cichlid fish from Lake Tanganyika, East Africa. Journal of Fish Biology, 64(5), 1272-1284.

Feeney, W. E., Welbergen, J. A., & Langmore, N. E. (2014). Advances in the study of coevolution between avian brood parasites and their hosts. Annual Review of Ecology, Evolution, and Systematics, 45, 227-246.

Fussmann, G. F., Loreau, M., & Abrams, P. A. (2007). Eco-evolutionary dynamics of communities and ecosystems. Functional Ecology, 21, 465-477.

Gibbs, H. L., Sorenson, M. D., Marchetti, K., de Brooke, M., Davies, N. B., & Nakamura, H. (2000). Genetic evidence for female host-specific races of the common cuckoo. Nature, 407(6801), 183-186.

Glenn, T. C., Nilsen, R. A., Kieran, T. J., Sanders, J. G., Bayona-Vásquez, N. J., Finger, J. W., & Garcia-De Leon, F. J. (2019). Adapterama I: Universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ, 7, e7755.

Habermannová, J., Bogusch, P., & Straka, J. (2013). Flexible host choice and common host switches in the evolution of generalist and specialist cuckoo bees (Anthophila: Sphecodes). PLoS One, 8(5), e64537.

Hartig, F. (2021). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6.

Honza, M., Procházka, P., Stokke, B. G., Moksnes, A., Røskaft, E., Čapek, M., & Mrlík, V. (2004). Are blackcaps current winners in the evolutionary struggle against the common cuckoo? Journal of Ethology, 22, 175-180.

Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9(5), 1322-1332.

Jezkova, T., & Wiens, J. J. (2017). What explains patterns of diversification and richness among animal phyla? The American Naturalist, 189(3), 201-212.

Jiang, H., Lei, R., Ding, S.-W., & Zhu, S. (2014). Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics, 15(1), 182.

Kawecki, T. J. (1998). Red queen meets Santa Rosalia: Arms races and the evolution of host specialization in organisms with parasitic lifestyles. The American Naturalist, 152(4), 635-651.

Kennerley, J. A., Somveille, M., Hauber, M. E., Richardson, N. M., Manica, A., & Feeney, W. E. (2022). The overlooked complexity of avian brood parasite-host relationships. Ecology Letters, 25(8), 1889-1904.

Koblmüller, S., Sturmbauer, C., Verheyen, E., Meyer, A., & Salzburger, W. (2006). Mitochondrial phylogeny and phylogeography of east African squeaker catfishes (Siluriformes: Synodontis). BMC Evolutionary Biology, 6, 1-16.

Komarova, V. A., Kostin, D. S., Bryja, J., Mikula, O., Bryjová, A., Čížková, D., Šumbera, R., Meheretu, Y., & Lavrenchenko, L. A. (2021). Complex reticulate evolution of speckled brush-furred rats (Lophuromys) in the Ethiopian centre of endemism. Molecular Ecology, 30(10), 2349-2365.

Konings, A. (2019). Tanganyika cichlids in their natural habitat (4th ed.). Cichlid Press.

Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. (2015). Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15(5), 1179-1191.

Krüger, O., Sorenson, M. D., & Davies, N. B. (2009). Does coevolution promote species richness in parasitic cuckoos? Proceedings of the Royal Society B: Biological Sciences, 276(1674), 3871-3879.

Kuwamura, T. (1986). Parental care and mating systems of cichlid fishes in Lake Tanganyika: A preliminary field survey. Journal of Ethology, 4(2), 129-146.

Lawson, D. J., Hellenthal, G., Myers, S., & Falush, D. (2012). Inference of population structure using dense haplotype data. PLoS Genetics, 81, e1002453.

Malinsky, M., Trucchi, E., Lawson, D. J., & Falush, D. (2018). RADpainter and fineRADstructure: Population inference from RADseq data. Molecular Biology and Evolution, 35(5), 1284-1290.

Marchetti, K., Nakamura, H., & Gibbs, H. L. (1998). Host-race formation in the common cuckoo. Science, 282(5388), 471-472.

Martínez, J. G., Molina-Morales, M., Precioso, M., & Avilés, J. M. (2020). Age-related brood parasitism and egg rejection in magpie hosts. The American Naturalist, 195(5), 876-885.

Medina, I., & Langmore, N. E. (2016). The evolution of host specialisation in avian brood parasites. Ecology Letters, 19(9), 1110-1118.

Morita, M., Ugwu, S. I., & Kohda, M. (2018). Variations in the breeding behavior of cichlids and the evolution of the multi-functional seminal plasma protein, seminal plasma glycoprotein 120. BMC Evolutionary Biology, 18(1), 197.

Moskát, C., Bán, M., & Hauber, M. E. (2014). Naïve hosts of avian brood parasites accept foreign eggs, whereas older hosts fine-tune foreign egg discrimination during laying. Frontiers in Zoology, 11(1), 45.

Ochi, H. (1993). Maintenance of separate territories for mating and feeding by males of a maternal mouthbrooding cichlid, Gnathochromis pfefferi, in Lake Tanganyika. Japanese Journal of Ichthyology, 40(2), 173-182.

Park, A. W., Farrell, M. J., Schmidt, J. P., Huang, S., Dallas, T. A., Pappalardo, P., Drake, J. M., Stephens, P. R., Poulin, R., Nunn, C. L., & Davies, T. J. (2018). Characterizing the phylogenetic specialism-generalism spectrum of mammal parasites. Proceedings of the Royal Society B: Biological Sciences, 285(1874), 20172613.

Payne, R. B., Hustler, K., Stjernstedt, R., Sefc, K. M., & Sorenson, M. D. (2002). Behavioural and genetic evidence of a recent population switch to a novel host species in brood-parasitic indigobirds Vidua chalybeata. Ibis, 144(3), 373-383.

Peart, C. R., Dasmahapatra, K. K., & Day, J. J. (2018). Contrasting geographic structure in evolutionarily divergent Lake Tanganyika catfishes. Ecology and Evolution, 8(5), 2688-2697.

Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7(5), e37135.

Poisot, T., Bever, J. D., Nemri, A., Thrall, P. H., & Hochberg, M. E. (2011). A conceptual framework for the evolution of ecological specialisation. Ecology Letters, 14, 841-851.

Pollock, H. S., Hoover, J. P., Uy, F. M., & Hauber, M. E. (2021). Brood parasites are a heterogeneous and functionally distinct class of natural enemies. Trends in Parasitology, 37(7), 588-596.

Poulin, R., Krasnov, B. R., & Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology, 27(8), 355-361.

Prusińska, M., Mamcarz, A., & Kupren, K. (2009). Early ontogeny of Tropheus moorii Boulenger 1898 (Pisces, Cichlidae, Lake Tanganyika) in laboratory conditions. Polish Journal of Natural Science, 23, 888-903.

R Core Team. (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

Reichard, M. (2019). Cuckoo catfish. Current Biology, 29(15), R722-R723.

Ronco, F., Büscher, H. H., Indermaur, A., & Salzburger, W. (2020). The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. Journal of Great Lakes Research, 46(5), 1067-1078.

Ronco, F., Matschiner, M., Böhne, A., Boila, A., Büscher, H. H., el Taher, A., Indermaur, A., Malinsky, M., Ricci, V., Kahmen, A., Jentoft, S., & Salzburger, W. (2021). Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature, 589(7840), 76-81.

Rothstein, S. I., Patten, M. A., & Fleischer, R. C. (2002). Phylogeny, specialization, and brood parasite-host coevolution: Some possible pitfalls of parsimony. Behavioral Ecology, 13(1), 1-10.

Salvador, S., & Chan, P. (2004). Determining the number of clusters/segments in hierarchical clustering/segmentation algorithms. Proceedings of the Sixteenth IEEE International Conference on Tools with Artificial Intelligence, ICTAI, 12(15), 576-584.

Sato, T. (1986). A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature, 323(6083), 58-59.

Seehausen, O., & Wagner, C. E. (2014). Speciation in freshwater fishes. Annual Review of Ecology, Evolution, and Systematics, 45, 621-651.

Šimková, A., Morand, S., Jobet, E., Gelnar, M., & Verneau, O. (2004). Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): A case of intrahost speciation. Evolution, 58(5), 1001-1018.

Sless, T. J. L., Danforth, B. N., & Searle, J. B. (2023). Evolutionary origins and patterns of diversification in animal brood parasitism. American Naturalist, 202, 107-121. https://doi.org/10.1086/724839

Sorenson, M. D., Sefc, K. M., & Payne, R. B. (2003). Speciation by host switch in brood parasitic indigobirds. Nature, 424(6951), 928-931.

Spottiswoode, C. N., Kilner, R. M., & Davies, N. B. (2012). Brood parasitism. In N. J. Royle, P. T. Smiseth, & M. Kolliker (Eds.), The evolution of parental care (pp. 226-356). Oxford University Press.

Spottiswoode, C. N., & Stevens, M. (2012). Host-parasite arms races and rapid changes in bird egg appearance. American Naturalist, 179(5), 633-648.

Spottiswoode, C. N., Tong, W., Jamie, G. A., Stryjewski, K. F., DaCosta, J. M., Kuras, E. R., Green, A., Hamama, S., Taylor, I. G., Moya, C., & Sorenson, M. D. (2022). Genetic architecture facilitates then constrains adaptation in a host-parasite coevolutionary arms race. Proceedings of the National Academy of Sciences of the United States of America, 119(17), e2121752119.

Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313.

Starling, M., Heinsohn, R., Cockburn, A., & Langmore, N. E. (2006). Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry. Proceedings of the Royal Society B: Biological Sciences, 273(1596), 1929-1934.

Strausberger, B. M., & Rothstein, S. I. (2009). Parasitic cowbirds may defeat host defence by causing rejecters to misimprint on cowbird eggs. Behavioral Ecology, 20, 691-699.

Takahashi, T., & Koblmüller, S. (2020). Brood parasitism of an open-water spawning cichlid by the cuckoo catfish. Journal of Fish Biology, 96(6), 1538-1542.

Tartally, A., Thomas, J. A., Anton, C., Balletto, E., Barbero, F., Bonelli, S., Bräu, M., Casacci, L. P., Csősz, S., Czekes, Z., Dolek, M., Dziekańska, I., Elmes, G., Fürst, M. A., Glinka, U., Hochberg, M. E., Höttinger, H., Hula, V., Maes, D., … Nash, D. R. (2019). Patterns of host use by brood parasitic Maculinea butterflies across Europe. Philosophical Transactions of the Royal Society B, 374(1769), 20180202.

Thorogood, R., Spottiswoode, C. N., Portugal, S. J., & Gloag, R. (2019). The coevolutionary biology of brood parasitism: A call for integration. Philosophical Transactions of the Royal Society B, 374(1769), 20180190.

Wisenden, B. D. (1999). Alloparental care in fishes. Reviews in Fish Biology and Fisheries, 9, 45-70.

Wright, J. J., & Page, L. M. (2006). Taxonomic revision of Lake Tanganyikan Synodontis (Siluriformes: Mochokidae). Bulletin of the Florida Museum of Natural History, 46(4), 99-154.

Yamane, H., Watanabe, K., & Nagata, Y. (2013). Diversity in interspecific interactions between a nest-associating species, Pungtungia herzi, and multiple host species. Environmental Biology of Fishes, 96, 573-584.

Yoder, J. B., & Nuismer, S. L. (2010). When does coevolution promote diversification? American Naturalist, 176, 802-817.

Zimmerman, H., Tolman, D., & Reichard, M. (2023). Low incidence of cannibalism among brood parasitic cuckoo catfish embryos. Behavioral Ecology, 34(4), 521-527.

Zimmermann, H., Blažek, R., Polačik, M., & Reichard, M. (2022). Individual experience as a key to success for the cuckoo catfish brood parasitism. Nature Communications, 13(1), 1723.

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