Abstract
The remarkable phenomenon of nestmate killing behavior among some birds that are obligate brood parasites (OBP) has fascinated scientific researchers for hundreds of years. This “nestmate-cide” behavior has been found in two clades of OBP birds (most OBP cuckoos and all the parasitic honeyguides), though it is absent in parasitic Clamator cuckoos, viduid finches, cowbirds, and the single parasitic duck. Several hypotheses have been developed to explain the existence of nestmate toleraters, including recent acquisition of OBP and insufficient time to evolve nestmate killing behavior, parasitizing a host with a brood reducers strategy, or the occurrence of high costs for killing nestmates. However, none of these hypotheses have provided a complete explanation for the origin of chick killing behavior in OBP birds and its “fixed” distribution pattern within certain clades. There are similarities in the process and consequences of nestmate killing behavior in obligate brood parasites with that of obligate siblicidal behavior. After mapping these two behaviors on recent avian phylogenies, we found that the two clades of brood parasites that exhibit nestmate killing behavior are both within larger clades that contain species with obligate siblicidal behavior. Since no previous studies have considered the potential linkage between obligate siblicidal behavior and parasitic chick killing behavior, we proposed that the evolution of the potential for siblicide may also result in the potential for parasitic chicks to kill nestmates, and that siblicidal behavior may even promote the origin of this “killing-type” OBP.
Zusammenfassung
Das Töten von Mitnestlingen obligat brutparasitischer Vögel: Besteht ein Zusammenhang mit obligatem Geschwistermordverhalten?
Für Jahrhunderte hat Wissenschaftler das bemerkenswerte Phänomen fasziniert, dass manche, obligat brutparasitische (OBP) Vogelarten ihre Mitnestlinge töten. Dieses „Mitnestlingszid“-Verhalten wurde für zwei Zweige OBP Vögel nachgewiesen (die meisten OBP Kuckucke und alle parasitischen Honiganzeiger), findet sich allerdings nicht in parasitischen Kuckucken der Gattung Clamator, Finken aus der Familie Viduidae, Kuhstärlingen und der einzigen parasitischen Entenart. Zur Erklärung der Existenz von Brutparasiten, die ihre Mitnestlinge tolerieren, wurden mehrere Hypothesen aufgestellt, unter anderem die kürzliche Entstehung von OBP und die damit fehlende Zeit Mitnestlingsrmord zu evolvieren, einen Wirt mit Brutreduziererstrategie zu parasitieren, oder hohe Kosten für den Geschwistermord. Dennoch konnte keine dieser Hypothesen eine vollständige Erklärung für die Entstehung des Verhaltens von OBP Vögeln Mit-Nestlinge zu töten und dessen „fixierten“ Verteilungsmusters innerhalb bestimmter Zweige liefern. Es gibt allerdings Ähnlichkeiten im Vorgang und in den Konsequenzen des Tötungsverhaltens von Mitnestlingen obligater Brutparasiten mit dem von obligatem Geschwistermordverhalten. Nach Kartierung beider Verhaltensweisen auf einer modernen phylogenetischen Vogelsystematik fanden wir heraus, dass sich beide brutparasitischen Zweige, die Mit-Nestlingsmordverhalten zeigen, innerhalb größerer Zweige befinden, die Arten mit obligatem Geschwistermordverhalten beinhalten. Da keine frühere Studie diesen potentiellen Zusammenhang zwischen obligatem Geschwistermord- und parasitischem Nestlingsmordverhalten in Betracht gezogen hat, schlagen wir vor, dass die Evolution einer Veranlagung zu Geschwistermord gleichzeitig ein Potential für parasitische Nestlinge darstellt, ihre Mitnestlinge zu töten, und dass Geschwistermordverhalten sogar die Entstehung des „Mord-Typus“ unter OBP begünstigt.
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References
Alderson GW, Gibbs HL, Sealy SG (1999) Determining the reproductive behaviour of individual brown-headed cowbirds using microsatellite DNA markers. Anim Behav 58:895–905
Anderson DJ (1990) Evolution of obligate siblicide in boobies. 1. A test of the insurance-egg hypothesis. Am Nat 135:334–350
Anderson MG, Harber ME (2007) A recognition-free mechanism for reliable rejection of brood parasites. Trends Ecol Evol 22:283–286
Anderson MG, Moskát C, Bán M, Grim T, Cassey P, Hauber ME (2009) Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS One 4:e7725. doi:https://doi.org/10.1371/journal.pone.0007725
Barker FK, Barrowclough GF, Groth JG (2002) A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implication of an analysis of nuclear DNA sequence data. Proc R Soc Lond B 269:295–308
Broom M, Ruxton GD, Kilner RM (2008) Host life history strategies and the evolution of chick-killing by brood parasitic offspring. Behav Ecol 19:22–34
Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, London
Davies NB, Kilner RM, Noble DG (1998) Nestling cuckoos, Canus canorus, exploit hosts with begging calls that mimic a brood. Proc R Soc Lond B 265:673–678
Dearborn DC (1996) Video documentation of a brownheaded cowbird nestling ejecting an indigo bunting nestling from the nest. Condor 98:645–649
Dearborn DC, MacDade LS, Robinson S, Fink ADD, Fink ML (2009) Offspring development mode and the evolution of brood parasitism. Behav Ecol. doi:https://doi.org/10.1093/beheco/arp026
Edwards TC, Collopy MW (1983) Obligate and facultative brood reduction in eagles: an examination of factors that influence fratricide. Auk 100:630–635
Ericson PGP, Anderson CL, Britton T, Elzanowski A, Johansson US, Källersjö M, Ohlso JI, Parsons TJ, Zuccon D, Mayr G (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2:543–547
Gargett V (1993) The black eagle. A study. Acorn, Randburg
Gerhardt RP, Gerhardt DM, Vas-quez MA (1997) Siblicide in swallow-tailed kites. Wilson Bull 109:112–120
Grim T (2006a) The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol Ecol Res 8:785–802
Grim T (2006b) Cuckoo growth performance in parasitized and unused hosts: not only host size matters. Behav Ecol Sociobiol 60:716–723
Grim T (2006c) Low virulence of brood parasitic chicks: adaptation or constraint? Ornithol Sci 5:237–242
Grim T (2007) Experimental evidence for chick discrimination without recognition in a brood parasite host. Proc R Soc Lond B 274:373–381
Grim T, Kleven O, Mikulica O (2003) Nestling discrimination without recognition: a possible defence mechanism for hosts towards cuckoo parasitism? Proc R Soc Lond B 270:S73–S75
Grim T, Rutila J, Cassey P, Hauber ME (2009a) Experimentally constrained virulence is costly for common cuckoo chicks. Ethology 115:14–22
Grim T, Rutila J, Cassey P, Hauber ME (2009b) The cost of virulence: an experimental study of egg eviction by brood parasitic chicks. Behav Ecol 20:1138–1146
Grim T, Samas P, Moskat C, Kleven O, Honza M, Moksnes A, Røskaft E, Stokke BG (2011) Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518
Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768
Hauber ME (2003) Hatching asynchrony, nestling competition and the costs of interspecific brood parasitism. Behav Ecol 14:227–235
Hauber ME, Moskát C (2008) Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behav Ecol 19:79–86
Honza M, Voslajerová K, Moskát C (2007) Eviction behaviour of the common cuckoo Cuculus canorus chicks. J Avian Biol 38:385–389
Hoover JP (2003) Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea. Anim Behav 65:923–934
Kilner RM (2001) A growth cost of begging in captive canary chicks. Proc Natl Acad Sci USA 98:11394–11398
Kilner RM (2005) The evolution of virulence in brood parasites. Ornithol Sci 4:55–64
Kilner RM (2006) Response to Grim: further costs of virulence for brood parasitic young. Ornithol Sci 5:243–247
Kilner RM, Davies N (1999) How selfish is a cuckoo chick? Anim Behav 58:787–808
Kilner RM, Madden JR, Hauber ME (2004) Brood parasitic cowbird nestlings use host young to produce resources. Science 305:877–879
Langmore NE, Hunt S, Kilner RM (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160
Lawes MJ, Marthews TR (2003) When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model. Behav Ecol 14:757–770
Layne JN (1982) Status of sibling aggression in Florida sandhill cranes. J Field Ornithol 53:272–274
Ligon JD (1993) The role of phylogenetic history in the evolution of contemporary avian mating and parental care systems. In: Power DM (ed) Current ornithology. Plenum, New York, pp 1–46
Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host coevolution. Anim Behav 49:1185–1209
Maddison DR, Maddison WP (2005) Macclade 4.08. Sinauer, Sunderland
Martín-Gálvez D, Soler M, Soler JJ, Martín-Vivaldi M, Palomino JJ (2005) Food acquisition by common cuckoo chicks in rufous bush robin nests and the advantage of eviction behavior. Anim Behav 70:1313–1321
Moskát C, Hauber ME (2010) Chick loss from mixed broods reflects severe nestmate competition between an evictor brood parasite and its hosts. Behav Process 83:311–314
Moskát C, Székely T, Kisbenedek T, Karcza Z, Bártol I (2003) The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arundinaceus. J Avian Biol 34:16–19
Moskát C, Avilés JM, Bán M, Hargitai R, Zölei A (2008) Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts. Behav Ecol Sociobiol 62:1885–1890
Ottoson U, Backman J, Smith HG (1997) Begging affects parental effort in the pied flycatcher, Ficedula hypoleuca. Behav Ecol Sociobiol 41:381–384
Payne RB (1997) Family Cuculidae (Cuckoos). In: Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world. Lynx, Barcelona, pp 508–607
Robert M, Sorci G (2001) The evolution of obligate interspecific brood parasitism in birds. Behav Ecol 12:128–133
Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecof Syst 21:481–508
Simmons R (1988) Offspring quality and the evolution of cainism. Ibis 130:339–357
Slagsvold T (1998) On the origin and rarity of interspecific nest parasitism in birds. Am Nat 152:264–272
Soler M (2001) Begging behaviour of nestlings and food delivery by parents: the importance of the breeding strategy. Acta Ethol 4:59–63
Soler M (2002) Breeding Strategy and begging intensity: influences on food delivery by parents and host selection by parasitic cuckoos. In: Wright J, Leonard ML (eds) The evolution of begging. Kluwer, Dordrecht, pp 413–427
Soler JJ, Martinez JG, Soler M, Møller AP (2001) Coevolutionary interactions in a host-parasite system. Ecol Lett 4:470–476
Sorenson MD, Payne RB (2002) Molecular genetic perspectives on avian brood parasitism. Integr Comp Biol 42:388–400
Sorenson MD, Payne RB (2005) A molecular genetic analysis of cuckoo phylogeny. In: Payne RB (ed) The cuckoos. Oxford University Press, Oxford, pp 68–94
Sorenson MD, Sefc KM, Payne RB (2003) Speciation by host switch in brood parasitic indigobirds. Nature 424:928–931
Stokke BG, Moksnes A, Røskaft E (2002) Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds. Evolution 56:199–205
Tanaka KD, Ueda K (2005) Horsfield’s hawk cuckoo nestlings simulate multiple gapes for begging. Science 308:653
Tarlow EM, Wikelski M, Anderson DJ (2001) Hormonal correlates of siblicide in Galapagos Nazca boobies. Horm Behav 40:14–20
Turtumoygard T, Slagsvold T (2010) Evolution of brood parasitism in birds: constraint related to prey type. Behaviour 147:299–317
Winfree R (1999) Cuckoos, cowbirds and the persistence of brood parasitism. Trends Ecol Evol 14:338–343
Yamauchi A (1995) Theory of evolution of nest parasitism in birds. Am Nat 145:434–456
Zieliński P (2002) Brood reduction and parental infanticide—are the white stork Ciconia ciconia and the black stork C. nigra exceptional? Acta Ornithol 37:113–119
Acknowledgments
This paper benefited from helpful suggestions by the editor, anonymous reviewers, and the members from Kimball/Braun laboratory. We really appreciate the thorough review and great comments given by Edward Braun and Colette St Mary. We are also grateful to Zhengwang Zhang for a consistent support during the process of this paper. N.W. was supported on a fellowship from the China Scholarship Council and a Singer Seed Grant to R.T.K. and E.L.B.
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Wang, N., Kimball, R.T. Nestmate killing by obligate brood parasitic chicks: is this linked to obligate siblicidal behavior?. J Ornithol 153, 825–831 (2012). https://doi.org/10.1007/s10336-011-0800-4
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DOI: https://doi.org/10.1007/s10336-011-0800-4