Host responses to interspecific brood parasitism: a by-product of adaptations to conspecific parasitism?
Status PubMed-not-MEDLINE Language English Country Great Britain, England Media electronic-ecollection
Document type Journal Article
PubMed
24834103
PubMed Central
PMC4022367
DOI
10.1186/1742-9994-11-34
PII: 1742-9994-11-34
Knihovny.cz E-resources
- Keywords
- Coevolution, Collateral damage, Discrimination, Heterospecific brood parasitism, Intraspecific brood parasitism, Species introductions,
- Publication type
- Journal Article MeSH
BACKGROUND: Why have birds evolved the ability to reject eggs? Typically, foreign egg discrimination is interpreted as evidence that interspecific brood parasitism (IP) has selected for the host's ability to recognize and eliminate foreign eggs. Fewer studies explore the alternative hypothesis that rejection of interspecific eggs is a by-product of host defenses, evolved against conspecific parasitism (CP). We performed a large scale study with replication across taxa (two congeneric Turdus thrushes), space (populations), time (breeding seasons), and treatments (three types of experimental eggs), using a consistent design of egg rejection experiments (n = 1057 nests; including controls), in areas with potential IP either present (Europe; native populations) or absent (New Zealand; introduced populations). These comparisons benefited from the known length of allopatry (one and a half centuries), with no gene flow between native and introduced populations, which is rarely available in host-parasite systems. RESULTS: Hosts rejected CP at unusually high rates for passerines (up to 60%). CP rejection rates were higher in populations with higher conspecific breeding densities and no risks of IP, supporting the CP hypothesis. IP rejection rates did not covary geographically with IP risk, contradicting the IP hypothesis. High egg rejection rates were maintained in the relatively long-term isolation from IP despite non-trivial rejection costs and errors. CONCLUSIONS: These egg rejection patterns, combined with recent findings that these thrushes are currently unsuitable hosts of the obligate parasitic common cuckoo (Cuculus canorus), are in agreement with the hypothesis that the rejection of IP is a by-product of fine-tuned egg discrimination evolved due to CP. Our study highlights the importance of considering both IP and CP simultaneously as potential drivers in the evolution of egg discrimination, and illustrates how populations introduced to novel ecological contexts can provide critical insights into brood parasite-host coevolution.
See more in PubMed
Davies NB. Cuckoos, Cowbirds and other Cheats. London: T & AD Poyser; 2000.
Davies NB, Brooke ML. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts I. Host egg discrimination. J Anim Ecol. 1989;58:207–224. doi: 10.2307/4995. DOI
Stoddard MC, Stevens M. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution. 2011;65:2004–2013. doi: 10.1111/j.1558-5646.2011.01262.x. PubMed DOI
Moksnes A, Røskaft E. Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool. 1995;236:625–648. doi: 10.1111/j.1469-7998.1995.tb02736.x. DOI
Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC. Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour. 1991;116:64–89. doi: 10.1163/156853990X00365. DOI
Grim T, Samas P, Moskát C, Kleven O, Honza M, Moksnes A, Røskaft E, Stokke BG. Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol. 2011;80:508–518. doi: 10.1111/j.1365-2656.2010.01798.x. PubMed DOI
Soler M. Long-term coevolution between avian brood parasites and their hosts. Biol Rev. 2014. doi:10.1111/brv.12075. PubMed
Visser ME, Lessells CM. The costs of egg production and incubation in great tits (Parus major) Proc R Soc Lond B. 2001;268:1271–1277. doi: 10.1098/rspb.2001.1661. PubMed DOI PMC
Jackson WM. In: Parasitic Birds and their Hosts. Rothstein SI, Robinson SK, editor. New York: Oxford University Press; 1998. Egg discrimination and egg-color variability in the northern masked weaver: the importance of conspecific versus interspecific parasitism; pp. 407–416.
Lyon BE, Eadie JMA. Conspecific brood parasitism in birds: a life-history perspective. Annual Rev Ecol Evol Syst. 2008;39:343–363. doi: 10.1146/annurev.ecolsys.39.110707.173354. DOI
Braa AT, Moksnes A, Røskaft E. Adaptations of bramblings and chaffinches towards parasitism by the common cuckoo. Anim Behav. 1992;43:67–78. doi: 10.1016/S0003-3472(05)80072-7. DOI
Ringsby TH, Moksnes A, Røskaft E, Lerkelund HE. Do conspecific brood parasitism and antiparasite strategies occur in fieldfares Turdus pilaris? Fauna norw Ser C, Cinclus. 1993;16:45–53.
Moskát C, Karcza Z, Csörgö T. Egg rejection in European blackbirds (Turdus merula): the effect of mimicry. Ornis Fenn. 2003;80:86–91.
Avilés JM. Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism. J Avian Biol. 2004;35:295–299. doi: 10.1111/j.0908-8857.2004.03327.x. DOI
Honza M, Procházka P, Stokke BG, Moksnes A, Røskaft E, Čapek M, Mrlík V. Are blackcaps current winners in the evolutionary struggle against the common cuckoo? J Ethol. 2004;22:175–180. doi: 10.1007/s10164-004-0119-1. DOI
Stokke BG, Rudolfsen G, Moksnes A, Røskaft E. Rejection of conspecific eggs in chaffinches: the effect of age and clutch characteristics. Ethology. 2004;110:459–470. doi: 10.1111/j.1439-0310.2004.00978.x. DOI
Hale K, Briskie JV. Response of introduced European birds in New Zealand to experimental brood parasitism. J Avian Biol. 2007;38:198–204. doi: 10.1111/j.0908-8857.2007.03734.x. DOI
Grim T. Equal rights for chick brood parasites. Ann Zool Fenn. 2007;44:1–7.
Procházka P, Honza M. Egg discrimination in the yellowhammer. Condor. 2004;106:405–410. doi: 10.1650/7365. DOI
Lahti DC. Evolution of bird eggs in the absence of cuckoo parasitism. P Natl Acad Sci USA. 2005;102:18057–18062. doi: 10.1073/pnas.0508930102. PubMed DOI PMC
Briskie JV, Sealy SG, Hobson KA. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution. 1992;46:334–340. doi: 10.2307/2409854. PubMed DOI
Grendstad LC, Moksnes A, Røskaft E. Do strategies against conspecific brood parasitism occur in redwings Turdus iliacus? Ardea. 1999;87:101–111.
Cruz A, Wiley JW. The decline of an adaptation in the absence of a presumed selection pressure. Evolution. 1989;43:55–62. doi: 10.2307/2409163. PubMed DOI
Lyon BE, Eadie JMA. An obligate brood parasite trapped in the intraspecific arms race of its hosts. Nature. 2004;432:390–393. doi: 10.1038/nature03036. PubMed DOI
Thompson JN. The Coevolutionary Process. Chicago: University of Chicago Press; 1994.
Futuyma DJ. Evolutionary Biology. 3. Massachusetts: Sinauer Associates; 1998.
Dukas R. Costs of memory: Ideas and predictions. J Theor Biol. 1999;197:41–50. doi: 10.1006/jtbi.1998.0856. PubMed DOI
Marchetti K. Costs to host defence and persistence of parasitic cuckoos. Proc R Soc Lond B. 1992;248:41–45. doi: 10.1098/rspb.1992.0040. PubMed DOI
Thorogood R, Davies NB. Reed warbler hosts fine-tune their defences to track three decades of cuckoo decline. Evolution. 2013;67:3545–3555. doi: 10.1111/evo.12213. PubMed DOI PMC
Kuehn MJ, Peer BD, Rothstein SI. Variation in host response to brood parasitism reflects evolutionary differences and not phenotypic plasticity. Anim Behav. 2014;88:21–28.
Samas P, Cassey P, Hauber ME, Grim T. Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology. 2011;117:606–619. doi: 10.1111/j.1439-0310.2011.01917.x. DOI
Samas P, Grim T, Hauber ME, Cassey P, Weidinger K, Evans KL. Ecological predictors of reduced avian reproductive investment in the southern hemisphere. Ecography. 2013;36:809–818. doi: 10.1111/j.1600-0587.2012.07927.x. DOI
Grim T, Honza M. Differences in behaviour of closely related thrushes (Turdus philomelosandT. merula) to experimental parasitism by the common cuckoo Cuculus canorus. Biologia. 2001;56:549–556.
Higgins PJ. Handbook of Australian, New Zealand and Antarctic Birds. Melbourne: Oxford University Press; 2006. p. 7B.
Lahti DC. Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism. Evolution. 2006;60:157–168. doi: 10.1111/j.0014-3820.2006.tb01090.x. PubMed DOI
Reeve HK. The evolution of conspecific acceptance thresholds. Am Nat. 1989;133:407–435. doi: 10.1086/284926. DOI
Sherman PW, Reeve HK, Pfenning DW. In: Behavioural Ecology. Krebs JR, Davies NB, editor. Oxford: Blackwell Scientific; 1997. Recognition systems; pp. 69–96.
Brooke ML, Davies NB. Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature. 1988;335:630–632. doi: 10.1038/335630a0. DOI
Moskát C, Hauber ME. Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts. Anim Cogn. 2007;10:377–386. doi: 10.1007/s10071-007-0071-x. PubMed DOI
Lovászi P, Moskát C. Break-down of arms race between the red-backed shrike (Lanius collurio) and common cuckoo (Cuculus canorus) Behaviour. 2004;141:245–262. doi: 10.1163/156853904322890843. DOI
Lotem A, Nakamura H, Zahavi A. Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav. 1995;49:1185–1209. doi: 10.1006/anbe.1995.0152. DOI
Welbergen JA, Davies NB. Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol. 2009;19:235–240. PubMed
Brown CR. Laying eggs in a neighbor's nest: benefit and cost of colonial nesting in swallows. Science. 1984;224:518–519. doi: 10.1126/science.224.4648.518. PubMed DOI
Weaver HB, Brown CR. Brood parasitism and egg transfer in cave swallows (Petrochelidon fulva) and cliff swallows (P. pyrrhonota) in South Texas. Auk. 2004;121:1122–1129. doi: 10.1642/0004-8038(2004)121[1122:BPAETI]2.0.CO;2. DOI
Hoi H, Darolová A, Krištofík J. Conspecific brood parasitism and anti-parasite strategies in relation to breeding density in female bearded tits. Behaviour. 2010;147:1533–1549. doi: 10.1163/000579510X511060. DOI
Bull PC. Notes on the breeding cycle of the thrush and blackbird in New Zealand. Emu. 1946;46:198–208. doi: 10.1071/MU946198. DOI
Hudec K. Fauna ČSSR. Ptáci – Aves. Vol. 3, Part 1. Praha: Academia; 1983.
Welbergen JA, Davies NB. Direct and indirect assessment of parasitism risk by a cuckoo host. Behav Ecol. 2012;23:783–789. doi: 10.1093/beheco/ars031. DOI
Brooke ML, Davies NB, Noble DG. Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proc R Soc Lond B. 1998;265:1277–1282. doi: 10.1098/rspb.1998.0430. DOI
Soler M, Martín-Vivaldi M, Fernández-Morante J. Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin. Anim Behav. 2012;84:421–426. doi: 10.1016/j.anbehav.2012.05.016. DOI
Soler M, Soler JJ, Martinéz JG, Pérez-Contreras T, Møller AP. Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis. Oecologia. 1998;117:381–390. doi: 10.1007/s004420050671. PubMed DOI
Davies NB, Brooke ML, Kacelnik A. Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc Lond B. 1996;263:925–931. doi: 10.1098/rspb.1996.0137. DOI
Lindholm AK, Thomas RJ. Differences between populations of reed warblers in defences against brood parasitism. Behaviour. 2000;137:25–42. doi: 10.1163/156853900501854. DOI
Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M. Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol. 2008;19:612–620. doi: 10.1093/beheco/arn007. DOI
Rothstein SI. Relic behaviours, coevolution and the retention versus loss of host defences after episodes of avian brood parasitism. Anim Behav. 2001;61:95–107. doi: 10.1006/anbe.2000.1570. PubMed DOI
Honza M, Polačiková L, Procházka P. Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos) Biol J Linn Soc. 2007;92:269–276. doi: 10.1111/j.1095-8312.2007.00848.x. DOI
Polačiková L, Grim T. Blunt egg pole holds cues for alien egg discrimination: experimental evidence. J Avian Biol. 2010;41:111–116. doi: 10.1111/j.1600-048X.2010.04983.x. DOI
Lahti DC, Lahti AR. How precise is egg discrimination in weaverbirds? Anim Behav. 2002;63:1135–1142. doi: 10.1006/anbe.2002.3009. DOI
Spottiswoode CN, Stevens M. Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. P Natl Acad Sci USA. 2010;107:8672–8676. doi: 10.1073/pnas.0910486107. PubMed DOI PMC
Hauber ME, Samas P, Anderson MG, Rutila J, Low J, Cassey P, Grim T. Life-history predicts host behavioural responses to experimental brood parasitism. Ethol Ecol Evol. 2014. doi:10.1080/03949370.2013.851121.
Grim T, Samas P, Hauber ME. The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav Ecol Sociobiol. 2014;68:749–759. doi: 10.1007/s00265-014-1688-9. DOI
Croston R, Hauber ME. Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius) Behav Ecol Sociobiol. 2014. doi:10.1007/s00265-013-1649-8.
Welbergen J, Komdeur J, Kats R, Berg ML. Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism. Behav Ecol. 2001;12:8–15. doi: 10.1093/oxfordjournals.beheco.a000382. DOI
Moskát C, Szentpeteri J, Barta Z. Adaptations by great reed warblers brood parasitism: a comparison of populations in sympatry and allopatry with the common cuckoo. Behaviour. 2002;139:1313–1329. doi: 10.1163/156853902321104181. DOI
Moreno-Rueda G, Soler M. Reconocimiento de huevos en el gorrión común Passer domesticus, una especie con parasitismo de cría intraespecífico. Ardeola. 2001;48:225–231.
López-de-Hierro MDG, Ryan P. Nest defence and egg rejection in the house sparrow (Passer domesticus) as protection against conspecific brood parasitism. Behaviour. 2008;145:949–964. doi: 10.1163/156853908784089270. DOI
Emlen ST, Wrege PH. Forced copulations and intra-specific parasitism: two costs of social living in the white-fronted bee-eater. Ethology. 1986;71:2–29.
Lyon BE. Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature. 2003;422:495–499. doi: 10.1038/nature01505. PubMed DOI
Riehl C. A simple rule reduces costs of extragroup parasitism in a communally breeding bird. Curr Biol. 2010;20:1830–1833. doi: 10.1016/j.cub.2010.09.005. PubMed DOI
López-de-Hierro MDG, Moreno-Rueda G. Egg-spot pattern rather than egg colour affects conspecific egg rejection in the house sparrow (Passer domesticus) Behav Ecol Sociobiol. 2010;64:317–324. doi: 10.1007/s00265-009-0811-9. DOI
Ležalová-Piálková R, Honza M. Responses of black-headed gulls Larus ridibundus to conspecific brood parasitism. J Ornithol. 2009;149:415–421.
Saino N, Fasola M. Egg and nest recognition by two tern species (Sternidae, Aves) Ethol Ecol Evol. 1993;5:467–476.
Gaston AJ, de Forest LN, Noble DG. Egg recognition and egg-stealing in thick-billed murres Uria lomvia. Anim Behav. 1993;45:301–306. doi: 10.1006/anbe.1993.1034. DOI
Sorenson MD. Evidence of conspecific nest parasitism and egg discrimination in the sora. Condor. 1995;97:819–821. doi: 10.2307/1369192. DOI
Koenig WD, Mumme RL, Stanback MT, Pitelka FA. Patterns and consequences of egg destruction among joint-nesting acorn woodpeckers. Anim Behav. 1995;50:607–621. doi: 10.1016/0003-3472(95)80123-5. DOI
Kendra PE, Roth RR, Tallamy DW. Conspecific brood parasitism in the house sparrow. Wilson Bull. 1988;100:80–90.
Poláček M, Griggio M, Bartíková M, Hoi H. Nest sanitation as the evolutionary background for egg ejection behaviour and the role of motivation for object removal. PLoS ONE. 2013;8:e78771. doi: 10.1371/journal.pone.0078771. PubMed DOI PMC
Latif QS, Grenier JL, Heath SH, Ballard G, Hauber ME. First evidence of conspecific brood parasitism and egg ejection in song sparrows, with comments on methods sufficient to document these behaviors. Condor. 2006;108:452–458. doi: 10.1650/0010-5422(2006)108[452:FEOCBP]2.0.CO;2. DOI
Yom-Tov Y. Intraspecific nest parasitism in birds. Biol Rev. 1980;55:93–108.
Thomson GM. The Naturalisation of Plants and Animals in New Zealand. Cambridge: Cambridge University Press; 1922.
Briskie JV. Frequency of egg rejection by potential hosts of the New Zealand cuckoos. Condor. 2003;105:719–727. doi: 10.1650/7106. DOI
Samas P, Heryán J, Grim T. How does urbanization affect dispersal in blackbirds? Sylvia. 2013;49:21–38.
Cepák J. Czech and Slovak Bird Migration Atlas. Aventinum: Prague; 2008.
Polačiková L, Stokke BG, Procházka P, Honza M, Moksnes A, Røskaft E. The role of blunt egg pole characteristics for recognition of eggs in the song thrush (Turdus philomelos) Behaviour. 2010;147:465–478. doi: 10.1163/000579509X12584427339575. DOI
Briskie JV, Mackintosh M. Hatching failure increases with severity of population bottlenecks in birds. P Natl Acad Sci USA. 2004;101:558–561. doi: 10.1073/pnas.0305103101. PubMed DOI PMC
Lindholm AK. Tests of phenotypic plasticity in reed warbler defences against cuckoo parasitism. Behaviour. 2000;137:43–60. doi: 10.1163/156853900501863. DOI
Boulton RB, Cassey P. An inexpensive method for identifying predators of passerine nests using tethered eggs. NZ J Ecol. 2006;30:377–385.
Rothstein SI. An experimental and teleonomic investigation of avian brood parasitism. Condor. 1975;77:250–271. doi: 10.2307/1366221. DOI
Polačiková L, Takasu F, Stokke BG, Moksnes A, Røskaft E, Cassey P, Hauber ME, Grim T. Egg arrangement in avian clutches covaries with the rejection of foreign eggs. Anim Cogn. 2013;16:819–828. doi: 10.1007/s10071-013-0615-1. PubMed DOI
Aidala Z, Huynen L, Brennan PLR, Musser J, Fidler A, Chong N, Machovsky Capuska GE, Anderson MG, Talaba A, Lambert D, Hauber ME. Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines. J Comp Physiol A. 2012;198:495–510. doi: 10.1007/s00359-012-0724-3. PubMed DOI
Grim T. Host recognition of brood parasites: implications for methodology in studies of enemy recognition. Auk. 2005;122:530–543. doi: 10.1642/0004-8038(2005)122[0530:HROBPI]2.0.CO;2. DOI
Grafen A, Hails R. Modern Statistics for the Life Sciences. Oxford: Oxford University Press; 2002.
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009;24:127–135. doi: 10.1016/j.tree.2008.10.008. PubMed DOI
SAS Institute Inc. SAS/STAT 9.2 User´s Guide. Cary, NC: SAS Institute Inc; 2008.
Rearing a virulent common cuckoo is not extra costly for its only cavity-nesting host
Probing the Limits of Egg Recognition Using Egg Rejection Experiments Along Phenotypic Gradients
Does contrast between eggshell ground and spot coloration affect egg rejection?
Egg discrimination along a gradient of natural variation in eggshell coloration