Dynamic egg color mimicry
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27516874
PubMed Central
PMC4972242
DOI
10.1002/ece3.2187
PII: ECE32187
Knihovny.cz E-zdroje
- Klíčová slova
- Avian vision, brood parasitism, coevolution, common cuckoo, mimicry, pigments,
- Publikační typ
- časopisecké články MeSH
Evolutionary hypotheses regarding the function of eggshell phenotypes, from solar protection through mimicry, have implicitly assumed that eggshell appearance remains static throughout the laying and incubation periods. However, recent research demonstrates that egg coloration changes over relatively short, biologically relevant timescales. Here, we provide the first evidence that such changes impact brood parasite-host eggshell color mimicry during the incubation stage. First, we use long-term data to establish how rapidly the Acrocephalus arundinaceus Linnaeus (great reed warbler) responded to natural parasitic eggs laid by the Cuculus canorus Linnaeus (common cuckoo). Most hosts rejected parasitic eggs just prior to clutch completion, but the host response period extended well into incubation (~10 days after clutch completion). Using reflectance spectrometry and visual modeling, we demonstrate that eggshell coloration in the great reed warbler and its brood parasite, the common cuckoo, changes rapidly, and the extent of eggshell color mimicry shifts dynamically over the host response period. Specifically, 4 days after being laid, the host should notice achromatic color changes to both cuckoo and warbler eggs, while chromatic color changes would be noticeable after 8 days. Furthermore, we demonstrate that the perceived match between host and cuckoo eggshell color worsened over the incubation period. These findings have important implications for parasite-host coevolution dynamics, because host egg discrimination may be aided by disparate temporal color changes in host and parasite eggs.
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Antonov, A. , Stokke B. G., Moksnes A., and Røskaft E.. 2008. Getting rid of the cuckoo Cuculus canorus egg: why do hosts delay rejection? Behav. Ecol. 19:100–107.
Avilés, J. M. 2008. Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proc. Biol. Sci. 275:2345–2352. PubMed PMC
Avilés, J. M. , Pérez‐Contreras T., Navarro C., and Soler J. J.. 2008. Dark nests and conspicuousness in color patterns of nestlings of altricial birds. Am. Nat. 171:327–338. PubMed
Cassey, P. , Maurer G., Duval C., Ewan J. G., and Hauber M. E.. 2010. Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens. Behav. Ecol. Sociobiol. 64:1711–1720.
Cassey, P. , Hauber M. E., Maurer G., and Ewen J. G.. 2012. Sources of variation in reflectance spectrophotometric data: a quantitative analysis using avian eggshell colours. Methods Ecol. Evol. 3:450–456.
Cherry, M. I. , and Gosler A. G.. 2010. Avian eggshell coloration: new perspectives on adaptive explanations. Biol. J. Linn. Soc. 100:753–762.
Crowley, P. J. 1999. Excipients as stabilizers. Pharm. Sci. Technol. Today 2:237–243. PubMed
Davies, N. B. , and Brooke M. D.. 1989. An experimental study of co‐evolution between the cuckoo, Cuculus canorus, and its hosts. 1. Host egg discrimination. J. Anim. Ecol. 58:207–224.
Dawkins, R. , and Krebs J. R.. 1979. Arms races between and within species. Proc. Biol. Sci. 205:489–511. PubMed
Dearborn, D. C. , Hanley D., Ballantine K., Cullum J., and Reeder D. M.. 2012. Eggshell colour is more strongly affected by maternal identity than by dietary antioxidants in a captive poultry system. Funct. Ecol. 26:912–920.
Drobniak, S. M. , Dyrcz A., Sudyka J., and Cichoń M.. 2014. Continuous variation rather than specialization in the egg phenotypes of cuckoos (Cuculus canorus) parasitizing two sympatric reed warbler species. PLoS One 9:e106650. PubMed PMC
Dukas, R. 1999. Costs of memory: ideas and predictions. J. Theor. Biol. 197:41–50. PubMed
Eisenhauer, J. G. 2003. Regression through the origin. Teach. Stat. 25:76–80.
Ericson, M. B. , Grapengiesser S., Gudmundson F., Wennberg A. M., Larkö O., Moan J., et al. 2003. A spectroscopic study of the photobleaching of protoporphyrin IX in solution. Lasers Med. Sci. 18:56–62. PubMed
Fecheyr‐Lippens, D. C. , Igic B., D'Alba L., Hanley D., Verdes A., Holford M., et al. 2015. The cuticle modulates ultraviolet reflectance of avian eggshells. Biol. Open 4:753–759. PubMed PMC
Feldman, D. 2002. Polymer weathering: photo‐oxidation. J. Polym. Environ. 10:163–173.
Fisher, R. A. 1929. Tests of significance in harmonic analysis. Proc. R. Soc. Lond. A 125:54–59.
Fokianos, K. , Fokianos K., Strimmer K., Strimmer K., Wichert S., and Wichert S.. 2004. Identifying periodically expressed transcripts in microarray time series data. Bioinformatics 20:5–20. PubMed
Forstmeier, W. , and Schielzeth H.. 2011. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behav. Ecol. Sociobiol. 65:47–55. PubMed PMC
Geltsch, N. , Bán M., Hauber M. E., and Moskát C.. 2016. When should common cuckoos Cuculus canorus lay their eggs in host nests? Bird Study 63:46–51.
Gervais, C. , Languille M.‐A., Reguer S., Garnier C., and Gillet M.. 2014. Light and anoxia fading of Prussian blue dyed textiles. Heritage Sci. 2:26.
Grim, T. , Samaš P., Moskát C., Kleven O., Honza M., Moksnes A., et al. 2011. Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J. Anim. Ecol. 80:508–518. PubMed
Grim, T. , Samaš P., and Hauber M.. 2014. The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav. Ecol. Sociobiol. 68:749–759.
Hanley, D. , and Doucet S. M.. 2009. Egg coloration in ring‐billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis. Behav. Ecol. Sociobiol. 63:719–729.
Hanley, D. , Cassey P., and Doucet S. M.. 2013a. Parents, predators, parasites, and the evolution of eggshell colour in open nesting birds. Evol. Ecol. 27:593–617.
Hanley, D. , Stoddard M. C., Cassey P., and Brennan P. L. R.. 2013b. Eggshell conspicuousness in ground nesting birds: do conspicuous eggshells signal nest location to conspecifics? Avian Biol. Res. 6:147–156.
Hanley, D. , Grim T., Cassey P., and Hauber M. E.. 2015a. Not so colourful after all: eggshell pigments constrain avian eggshell colour space. Biol. Lett. 11:20150087. PubMed PMC
Hanley, D. , Samaš P., Heryán J., Hauber M. E., and Grim T.. 2015b. Now you see it, now you don't: flushing hosts prior to experimentation can predict their responses to brood parasitism. Sci. Rep. 5:9060. PubMed PMC
Hart, N. S. , and Vorobyev M.. 2005. Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J. Comp. Physiol. A. 191:381–392. PubMed
Hasegawa, M. , Arai E., Watanabe M., and Nakamura M.. 2008. Methods for correcting plumage color fading in the barn swallow. Ornithol. Sci. 7:117–122.
Hauber, M. E. , Tong L., Bán M., Croston R., Grim T., Waterhouse G. I. N., et al. 2015. The value of artificial stimuli in behavioral research: making the case for egg rejection studies in avian brood parasitism. Ethology 121:521–528.
Honza, M. , Procházka P., Morongová K., Čapek M., and Jelínek V.. 2011. Do nest light conditions affect rejection of parasitic eggs? A test of the light environment hypothesis. Ethology 117:539–546.
Honza, M. , Procházka P., and Požgayová M.. 2012. Within‐ and between‐season repeatability of eggshell colouration in the great reed warbler Acrocephalus arundinaceus . J. Avian Biol. 43:91–96.
Honza, M. , Šulc M., Jelínek V., Pozgayová M., and Procházka P.. 2014. Brood parasites lay eggs matching the appearance of host clutches Brood parasites lay eggs matching the appearance of host clutches. Proc. Biol. Sci. 281:20132665. PubMed PMC
Igic, B. , Cassey P., Grim T., Greenwood D. R., Moskát C., Rutila J., et al. 2012. A shared chemical basis of avian host‐parasite egg colour mimicry. Proc. Biol. Sci. 279:1068–1076. PubMed PMC
Igic, B. , Fecheyr‐lippens D., Xiao M., Chan A., Hanley D., Brennan P. R. L., et al. 2015a. A nanostructural basis for gloss of avian eggshells. J. R. Soc. Interface 12:20141210. PubMed PMC
Igic, B. , Nunez V., Voss H. U., Croston R., Aidala Z., López A. V., et al. 2015b. Using 3D printed eggs to examine the egg‐rejection behaviour of wild birds. PeerJ 3:e965. PubMed PMC
Kennedy, G. Y. , and Vevers H. G.. 1976. A survey of avian eggshell pigments. Comp. Biochem. Physiol. 55:117–123. PubMed
Kilner, R. M. 2006. The evolution of egg colour and patterning in birds. Biol. Rev. 81:383–406. PubMed
Lahti, D. C. , and Ardia D. R.. 2016. Shedding light on bird egg color: pigment as parasol and the dark car effect. Am. Nat. 187:547–563. PubMed
Lightner, D. A. , and Crandall D. C.. 1972. Biliverdin photo‐oxidation in vitro formation of methylvinylmaleimide. FEBS Lett. 20:53–56. PubMed
Maia, R. , Eliason C. M., Bitton P., Doucet S. M., and Shawkey M. D.. 2013. pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol. Evol. 4:906–913.
Mayani‐Parás, F. , Kilner R. M., Stoddard M. C., Rodríguez C., and Drummond H.. 2015. Behaviorally induced camouflage: a new mechanism of avian egg protection. Am. Nat. 186:E91–E97. PubMed
Moksnes, A. , Røskaft E., Hagen L. G., Honza M., Mørk C., and Olsen P. H.. 2000. Common cuckoo Cuculus canorus and host behaviour at reed warbler Acrocephalus scirpaceus nests. Ibis 142:247–258.
Montgomerie, R. 2006. Analyzing colors Pp. 90–148 in Hill G. E. and McGraw K. J., eds. Bird coloration. Harvard Univ. Press, Cambridge, MA.
Moreno, J. , Lobato E., and Morales J.. 2011. Eggshell blue‐green colouration fades immediately after oviposition: a cautionary note about measuring natural egg colours. Ornis Fennica 88:51–56.
Moskát, C. , and Hauber M. E.. 2007. Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts. Anim. Cogn. 10:377–386. PubMed
Moskát, C. , and Honza M.. 2002. European cuckoo Cuculus canorus parasitism and host's rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144:614–622.
Moskát, C. , Székely T., Cuthill I. C., and Kisbenedek T.. 2008. Hosts’ responses to parasitic eggs: which cues elicit hosts’ egg discrimination? Ethology 114:186–194.
Moskát, C. , Bán M., and Hauber M. E.. 2014a. Naïve hosts of avian brood parasites accept foreign eggs, whereas older hosts fine‐tune foreign egg discrimination during laying. Front. Zool. 11:45. PubMed PMC
Moskát, C. , Zölei A., Bán M., Elek Z., Tong L., Geltsch N., et al. 2014b. How to spot a stranger's egg? A mimicry‐specific discordancy effect in the recognition of parasitic eggs. Ethology 120:616–626.
Nakagawa, S. , and Schielzeth H.. 2013. A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods Ecol. Evol. 4:133–142.
Navarro, J. Y. , and Lahti D. C.. 2014. Light dulls and darkens bird eggs. PLoS One 9:e116112. PubMed PMC
Procházka, P. , Konvičková‐Patzenhauerová H., Požgayová M., Trnka A., Jelínek V., and Honza M.. 2014. Host genotype and age have no effect on rejection of parasitic eggs. Naturwissenschaften 101:417–426. PubMed
R Development Core Team . 2014. R: a language and environment for statistical computing. R Development Core Team, Vienna, Austria.
Reynolds, S. J. , Martin G. R., and Cassey P.. 2009. Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim. Behav. 78:209–215.
Riehl, C. 2010. A simple rule reduces costs of extragroup parasitism in a communally breeding bird. Curr. Biol. 20:1830–1833. PubMed
Samas, P. , Hauber M. E., Cassey P., and Grim T. T.. 2014. Host responses to interspecific brood parasitism: a by‐product of adaptations to conspecific parasitism? Front. Zool. 11:34. PubMed PMC
Schielzeth, H. 2010. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1:103–113.
Schielzeth, H. , and Forstmeier W.. 2009. Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20:416–420. PubMed PMC
Siddiqi, A. , Cronin T. W., Loew E. R., Vorobyev M., and Summers K.. 2004. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio . J. Exp. Biol. 207:2471–2485. PubMed
Spottiswoode, C. N. 2013. A brood parasite selects for its own egg traits. Biol. Lett. 9:20130573. PubMed PMC
Stoddard, M. C. , and Prum R. O.. 2008. Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of New World buntings. Am. Nat. 171:755–776. PubMed
Stoddard, M. C. , and Stevens M.. 2010. Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye. Proc. Biol. Sci. 277:1387–1393. PubMed PMC
Stoddard, M. C. , and Stevens M.. 2011. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:2004–2013. PubMed
Stoddard, M. C. , Marshall K. L., and Kilner R. M.. 2011. Imperfectly camouflaged avian eggs: artefact or adaptation? Avian Biol. Res. 4:196–213.
Stokke, B. G. , Honza M., Moksnes A., Røskaft E., and Rudolfsen G.. 2002. Costs associated with recognition and rejection of parasitic eggs in two European passerines. Behaviour 139:629–644.
Šulc, M. , Procházka P., Čapek M., and Honza M.. 2016. Birds use eggshell UV reflectance when recognizing non‐mimetic parasitic eggs. Behav. Ecol. 27:677–684.
Trnka, A. , and Grim T.. 2014. Testing for correlations between behaviours in a cuckoo host: why do host defences not covary? Anim. Behav. 92:185–193.
Vorobyev, M. , and Osorio D.. 1998. Receptor noise as a determinant of colour thresholds. Proc. Biol. Sci. 265:351–358. PubMed PMC
Vorobyev, M. , Osorio D., Bennett A. T. D., Marshall N. J., and Cuthill I. C.. 1998. Tetrachromacy, oil droplets and bird plumage colours. J. Comp. Physiol. A. 183:621–633. PubMed
Wojaczyński, J. 2014. Degradation pathways for porphyrinoids. Top. Heterocycl. Chem. 33:143–202.
Wyllie, I. 1981. The cuckoo. B.T. Batsford Ltd, London.
Yousif, E. , and Haddad R.. 2013. Photodegradation and photostabilization of polymers, especially polystyrene: review. Springerplus 2:398. PubMed PMC
Yu, Y. , Li Z., and Pan J.. 2016. Changes in pigment, spectral transmission and element content of pink chicken eggshells with different pigment intensity during incubation. PeerJ 4:e1825. PubMed PMC
Zuur, A. F. , Ieno E. N., and Elphick C. S.. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1:3–14.
Probing the Limits of Egg Recognition Using Egg Rejection Experiments Along Phenotypic Gradients