Individual experience as a key to success for the cuckoo catfish brood parasitism
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
J 4584
Austrian Science Fund FWF - Austria
PubMed
35361775
PubMed Central
PMC8971504
DOI
10.1038/s41467-022-29417-y
PII: 10.1038/s41467-022-29417-y
Knihovny.cz E-zdroje
- MeSH
- cichlidy * MeSH
- fyziologická adaptace MeSH
- ptáci MeSH
- sumci * MeSH
- symbióza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Brood parasites are involved in coevolutionary arms races with their hosts, whereby adaptations of one partner elicit the rapid evolution of counter-adaptations in the other partner. Hosts can also mitigate fitness costs of brood parasitism by learning from individual or social experience. In brood parasites, however, the role of learning can be obscured by their stealthy behaviour. Cuckoo catfish (Synodontis multipunctatus) parasitise clutches of mouthbrooding cichlids in Lake Tanganyika and are the only non-avian obligate brood parasites among vertebrates. We experimentally demonstrate that cuckoo catfish greatly enhance their efficiency in parasitising their hosts as they learn to overcome host defences. With increasing experience, cuckoo catfish increased their parasitism success by greater efficiency through improved timing and coordination of intrusions of host spawnings. Hence, within the coevolutionary arms races, brood parasites learn to overcome host defences during their lifetime.
Department of Ecology and Vertebrate Zoology University of Łódź Łódź Poland
Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 Brno Czech Republic
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Kölliker, M., Smiseth, P. T. & Royle, N. J. Evolution of Parental Care. in The Princeton Guide to Evolution (eds. Losos, J. B. et al.) 663–670 (Princeton University Press, 2014).
Davies, N. B. Cuckoos, Cowbirds and Other Cheats. (T & A D Poyser, 2000).
Riedman ML. The evolution of alloparental care and adoption in mammals and birds. Q. Rev. Biol. 1982;57:405–435.
Wisenden BD. Alloparental care in fishes. Rev. Fish. Biol. Fish. 1999;9:45–70.
Alonso‐Alvarez, C. & Velando, A. Benefits and costs of parental care. in The Evolution of Parental Care (eds. Royle, N. J., Smiseth, P. T. & Kölliker, M.) 40–61 (Oxford University Press, 2012).
Spottiswoode, C. N., Kilner, R. M. & Davies, N. B. Brood parasitism. in The Evolution of Parental Care (2012).
Brandt M, Foitzik S, Fischer-Blass B, Heinze J. The coevolutionary dynamics of obligate ant social parasite systems – between prudence and antagonism. Biol. Rev. 2005;80:251–267. PubMed
Medina I, Langmore NE. The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol. Rev. 2016;91:569–577. PubMed
Spottiswoode CN, Stevens M. Host-parasite arms races and rapid changes in bird egg appearance. Am. Nat. 2012;179:632–648. PubMed
Medina I, Kilner RM, Langmore NE. From micro- to macroevolution: brood parasitism as a driver of phenotypic diversity in birds. Curr. Zool. 2020;66:515–526. PubMed PMC
Dawkins R, Krebs JR. Arms races between and within species. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 1979;205:489–511. PubMed
Soler M. Long-term coevolution between avian brood parasites and their hosts. Biol. Rev. 2014;89:688–704. PubMed
Feeney WE, Welbergen JA, Langmore NE. Advances in the study of coevolution between avian brood parasites and their hosts. Annu. Rev. Ecol. Evol. Syst. 2014;45:227–246.
Barron AB, et al. Embracing multiple definitions of learning. Trends Neurosci. 2015;38:405–407. PubMed
Rasa OAE, Heg D. Individual variation and prior experience affect the discrimination of a brood-parasite by its subsocial beetle host. Behav. Ecol. Sociobiol. 2004;57:155–163.
Lotem A, Nakamura H, Zahavi A. Rejection of cuckoo eggs in relation to host age: a possible evolutionary equilibrium. Behav. Ecol. 1992;3:128–132.
Moskát C, Bán M, Hauber ME. Naïve hosts of avian brood parasites accept foreign eggs, whereas older hosts fine-tune foreign egg discrimination during laying. Front. Zool. 2014;11:45. PubMed PMC
Feeney WE, Langmore NE. Social learning of a brood parasite by its host. Biol. Lett. 2013;9:20130443. PubMed PMC
Campobello D, Sealy SG. Use of social over personal information enhances nest defense against avian brood parasitism. Behav. Ecol. 2011;22:422–428.
Davies NB, Welbergen JA. Social transmission of a host defense against cuckoo parasitism. Sci. (80-.). 2009;324:1318–1320. PubMed
White, D. J., Davies, H. B., Agyapong, S. & Seegmiller, N. Nest prospecting brown-headed cowbirds ‘parasitize’ social information when the value of personal information is lacking. Proc. R. Soc. B Biol. Sci. 284, 20171083 (2017). PubMed PMC
White DJ. Avian egg timers: female cowbirds judge past, present, and future when making nest parasitism decisions. Front. Ecol. Evol. 2020;8:203.
Louder, M. I. M., Schelsky, W. M., Albores, A. N. & Hoover, J. P. A generalist brood parasite modifies use of a host in response to reproductive success. Proc. R. Soc. B Biol. Sci. 282, 20171083 (2015). PubMed PMC
Koleček J, Procházka P, Brlík V, Honza M. Cross-continental test of natal philopatry and habitat-imprinting hypotheses to explain host specificity in an obligate brood parasite. Sci. Nat. 2020;107:1–8. PubMed
Ortega, C. P. Cowbirds and Other Brood Parasites. (University of Arizona Press, 1998).
Teuschl Y, Taborsky B, Taborsky M. How do cuckoos find their hosts? The role of habitat imprinting. Anim. Behav. 1998;56:1425–1433. PubMed
Vogl W, Taborsky M, Taborsky B, Teuschl Y, Honza M. Cuckoo females preferentially use specific habitats when searching for host nests. Anim. Behav. 2002;64:843–850.
Šulc M, et al. Caught on camera: circumstantial evidence for fatal mobbing of an avian brood parasite by a host. J. Vertebr. Biol. 2020;69:1.
Davies NB. Cuckoo adaptations: trickery and tuning. J. Zool. 2011;284:1–14.
Sato T. A brood parasitic catfish Synodontis multipunctatus of mouthbrooding cichlid fishes in Lake Tanganyika. Nature. 1986;323:58–59. PubMed
Baerends GP. On causation and function of the pre‐spawning behaviour of cichlid fish. J. Fish. Biol. 1986;29:107–121.
Blažek R, et al. Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts. Sci. Adv. 2018;4:eaar4380. PubMed PMC
Juntti SA, et al. A neural basis for control of cichlid female reproductive behavior by Prostaglandin F2α. Curr. Biol. 2016;26:943–949. PubMed PMC
Sefc KM. Mating and parental care in Lake Tanganyika’s cichlids. Int. J. Evol. Biol. 2011;2011:470875. PubMed PMC
Sawecki J, Miros E, Border SE, Dijkstra PD. Reproduction and maternal care increase oxidative stress in a mouthbrooding cichlid fish. Behav. Ecol. 2019;30:1662–1671.
Kilner RM. The evolution of virulence in brood parasites. Ornithol. Sci. 2005;4:55–64.
Cohen MS, Hawkins MB, Knox-Hayes J, Vinton AC, Cruz A. A laboratory study of host use by the cuckoo catfish Synodontis multipunctatus. Environ. Biol. Fishes. 2018;101:1417–1425.
Reichard M. Cuckoo catfish. Curr. Biol. 2019;29:R722–R723. PubMed
Blažek, R., Polačik, M. & Reichard, M. Group intrusions by a brood parasitic fish are not cooperative. Behav. Ecol. 33, 178–183 (2022).
White DJ, Ho L, de los Santos G, Godoy I. An experimental test of preferences for nest contents in an obligate brood parasite, Molothrus ater. Behav. Ecol. 2007;18:922–928.
Brooke M, de L, Davies NB. A failure to demonstrate host imprinting in the Cuckoo (Cuculus canorus) and alternative hypotheses for the maintenance of egg mimicry. Ethology. 1991;89:154–166.
Polačik M, Reichard M, Smith C, Blažek R. Parasitic cuckoo catfish exploit parental responses to stray offspring. Philos. Trans. R. Soc. B Biol. Sci. 2019;374:20180412. PubMed PMC
Baldwin JM. A new factor in evolution. Am. Nat. 1896;30:441–451.
Paenke, I., Sendhoff, B. & Kawecki, T. J. Influence of plasticity and learning on evolution under directional selection. Am. Nat. 170, E47–58 (2007). PubMed
Mery F, Kawecki TJ. The effect of learning on experimental evolution of resource preference in Drosophila melanogaster. Evolution (N. Y). 2004;58:757–767. PubMed
Robinson BW, Dukas R. The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos. 1999;85:582–589.
Cole EF, Morand-Ferron J, Hinks AE, Quinn JL. Cognitive ability influences reproductive life history variation in the wild. Curr. Biol. 2012;22:1808–1812. PubMed
Cauchard L, Boogert NJ, Lefebvre L, Dubois F, Doligez B. Problem-solving performance is correlated with reproductive success in a wild bird population. Anim. Behav. 2013;85:19–26.
Guigueno MF, Macdougall-Shackleton SA, Sherry DF. Sex differences in spatial memory in brown-headed cowbirds: males outperform females on a touchscreen task. PLoS One. 2015;10:e0128302. PubMed PMC
Smith C, Philips A, Reichard M. Cognitive ability is heritable and predicts the success of an alternative mating tactic. Proc. R. Soc. B Biol. Sci. 2015;282:20151046. PubMed PMC
Honza M, Požgayová M, Procházka P, Tkadlec E. Consistency in egg rejection behaviour: responses to repeated brood parasitism in the blackcap (Sylvia atricapilla) Ethology. 2007;113:344–351.
Hosoi SA, Rothstein SI. Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim. Behav. 2000;59:823–840. PubMed
Davies, N. Cuckoo: Cheating by Nature. (Bloomsbury Publishing, 2015).
Gloag R, Fiorini VD, Reboreda JC, Kacelnik A. Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests. Behav. Ecol. Sociobiol. 2014;68:681–689.
Soler M, Soler JJ, Martinez JG, Moller AP. Magpie host manipulation by great spotted cuckoos: Evidence for an avian mafia? Evolution (N. Y). 1995;49:770–775. PubMed
Abolins-Abols, M. & Hauber, M. E. Proximate predictors of variation in egg rejection behavior by hosts of avian brood parasites. J. Comp. Psychol. 10.1037/com0000225 (2020). PubMed
Wright JJ, Page LM. Taxonomic revision of Lake Tanganyikan Synodontis (Siluriformes: Mochokidae) Bull. Fla. Mus. Nat. Hist. 2006;46:99–154.
Day JJ, Bills R, Friel JP. Lacustrine radiations in African Synodontis catfish. J. Evol. Biol. 2009;22:805–817. PubMed
Takahashi T, Koblmüller S. Brood parasitism of an open‐water spawning cichlid by the cuckoo catfish. J. Fish. Biol. 2020;96:1538–1542. PubMed
Brooks ME, et al. {glmmTMB} Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling. R. J. 2017;9:378–400.
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. (2021).
Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models using lme4. J. Stat. Softw. 2015;67:1–48.
Mixed Parentage Broods Indicate Group Spawning in the Brood Parasitic Cuckoo Catfish
Low incidence of cannibalism among brood parasitic cuckoo catfish embryos
figshare
10.6084/m9.figshare.14822838.v4