Abstract
Polymorphism is a general phenomenon in the natural world evolving as a result of frequency-dependent selection. Such polymorphism has recently received increasing attention in parasitic cuckoo-host systems, in which egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to investigate the effect of host egg polymorphism on the rate of successful parasitism (SPR) by cuckoos to help better understand the role of egg polymorphism in cuckoo-host systems. Five key conclusions can be drawn from these calculations: (1) The contrast of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the SPR of cuckoos; (2) hosts can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportion of the two morphs if cuckoos also evolve egg dimorphism as a counter-adaptation; (3) the escalation of egg polymorphism in hosts further reduces the SPR in cuckoos, although the efficiency of such an effect decreases with the number of host egg morphs; (4) cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs; and (5) an increase in the number of cuckoo egg morph does not increase the total SPR of cuckoos for parasitizing hosts with polymorphic eggs. Egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to show that the disruptive evolution of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the rate of successful parasitism by cuckoos (SPR). Hosts with obvious egg polymorphism suffer low parasitism rates and they can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportions of the two morphs if cuckoos also evolve egg dimorphism as a counteradaptation, whilst cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs.
Significance statement
Egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to show that the disruptive evolution of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the rate of successful parasitism (SPR) by cuckoos. Hosts with obvious egg polymorphism suffer low parasitism rates and they can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportions of the two morphs if cuckoos also evolve egg dimorphism as a counteradaptation, whilst cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs.
Similar content being viewed by others
References
Allen JA, Clarke BC (1984) Frequency dependent selection: homage to E. B. Poulton. Biol J Linn Soc 23:15–18
Clarke BC (1962) Balanced polymorphism and the diversity of sympatric species. In: Nichols D (ed) Taxonomy and geography. Systematics Association, Oxford, pp. 47–70
Cook LM (1998) A two-stage model for Cepaea polymorphism. Philos T Roy Soc B 353:1577–1593
Cook LM, Dennis RLH, Mani GS (1999) Melanic morph frequency in the peppered moth in the Manchester area. Proc R Soc Lond B 266:293–297
Fossøy F, Sorenson MD, Liang W et al (2016) Ancient origin and maternal inheritance of blue cuckoo eggs. Nat Commun 7:10272
Galeotti P, Rubolini D, Dunn PO, Fasola D (2003) Colour polymorhism in birds: causes and functions. J Evol Biol 16:635–646
Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406
Lahti DC (2005) Evolution of bird eggs in the absence of cuckoo parasitism. P Natl Acad Sci USA 102:18057–18062
Leimar O (2005) The evolution of phenotypic polymorphism: randomized strategies versus evolutionary branching. Am Nat 165:669–681
Liang W, Yang C, Stokke BG et al (2012) Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts. J Evol Biol 25:916–929
Liang G, Yang C, Wang L, Liang W (2014) Variation in parasitism rates by common cuckoos among three populations of the Oriental reed warblers. Sichuan J Zool 33:674–677
Maan ME, Eshuis B, Haesler MP, Schneider MV, van Alphen JJM, Seehausen O (2008) Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia 2008:621–629
Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, Oxford
Sandoval CP (1994) Differential visual predation on morphs of Timema cristinae (Phasmatodeae: Timemidae) and its consequences for host range. Biol J Linn Soc 52:341–356
Skelhorn J, Rowe C (2005) Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey. Biol Lett 1:500–503
Spottiswoode CN, Stevens M (2012) Host-parasite arms races and rapid changes in bird egg appearance. Am Nat 179:633–648
Théry M, Casas J (2002) Predator and prey views of spider camouflage. Nature 415:133
Thorogood R, Davies NB (2012) Cuckoos combat socially transmitted defenses of reed warbler hosts with a plumage polymorphism. Science 337:578–580
Thorogood R, Davies NB (2013) Hawk mimicry and the evolution of polymorphic cuckoos. Chin Birds 4:39–50
Wente WH, Phillips JB (2003) Fixed green and brown color morphs and a novel color–changing morph of the Pacific tree frog Hyla regilla. Am Nat 162:461–473
Yang C, Liang W, Cai Y et al (2010) Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host. PLoS One 5:e10816
Yang C, Wang L, Cheng SJ, Hsu YC, Liang W, Møller AP (2014a) Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften 101:727–734
Yang C, Liu Y, Zeng L, Liang W (2014b) Egg color variation, but not egg rejection behavior, changes in a cuckoo host breeding in the absence of brood parasitism. Ecol Evol 4:2239–2246
Yang C, Li D, Wang L, Liang G, Zhang Z, Liang W (2014c) Geographic variation in parasitism rates of two sympatric cuckoo hosts in China. Zool Res 35:67–71
Yang C, Wang L, Cheng SJ, Hsu YC, Stokke BG, Røskaft E, Moksnes A, Liang W, Møller AP (2015a) Deficiency in egg rejection in a host species as a response to the absence of brood parasitism. Behav Ecol 26:406–415
Yang C, Su T, Liang W, Møller AP (2015b) Coevolution between the large hawk-cuckoo (Cuculus sparverioides) and its two sympatric Leiothrichidae hosts: evidence for recent expansion and switch in host use? Biol J Linn Soc 115:919–926
Yang C, Huang Q, Wang L, Jiang A, Stokke BG, Fossøy F, Tunheim OH, Røskaft E, Liang W, Møller AP (2016) Plaintive cuckoos do not select tailorbird hosts that match the phenotypes of their own eggs. Behav Ecol 27:835–841
Acknowledgements
We would like to thank M. Soler and the two anonymous reviewers for their constructive criticism and helpful comments on our manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The paper was entirely theoretical and hence did not require ethical approval.
Funding
This work was supported by the National Natural Science Foundation of China (Nos. 31260514 and 31672303 to CY, 31272328 and 31472013 to WL) and the Program for New Century Excellent Talents in University (NCET-13-0761).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by M. Soler
Electronic supplementary material
ESM 1
(DOCX 30 kb)
Rights and permissions
About this article
Cite this article
Yang, C., Liang, W. & Møller, A.P. Why do hosts with obvious egg polymorphism suffer low parasitism rates under avian brood parasitism? A theoretical consideration. Behav Ecol Sociobiol 71, 30 (2017). https://doi.org/10.1007/s00265-016-2256-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-016-2256-2