journal article Open Access Sep 21, 2023

Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds

View at Publisher Save 10.1093/evlett/qrad041
Abstract
Abstract
Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host’s egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts.
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References
64
[1]
Abolins-Abols "Endocrine regulation of egg rejection in an avian brood parasite host" (2020)
[2]
Abolins-Abols "Proximate predictors of variation in egg rejection behavior by hosts of avian brood parasites" (2020)
[3]
Akre "Psychophysics and the evolution of behavior" (2014)
[4]
Amundsen "Rejection of common cuckoo Cuculus canorus eggs in relation to female age in the bluethroat Luscinia svecica" Journal of Avian Biology (2003) 10.1034/j.1600-048x.2002.02894.x
[5]
Ausprey "Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system" (2021)
[6]
Embracing multiple definitions of learning

Andrew B. Barron, Eileen A. Hebets, Thomas A. Cleland et al.

Trends in Neurosciences 2015 10.1016/j.tins.2015.04.008
[7]
Canniff "Probing the limits of egg recognition using egg rejection experiments along phenotypic gradients" Journal of Visualized Experiments (2018)
[8]
Croston "Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius)" (2014)
[9]
Davies "Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs" Proceedings of the Royal Society of London B: Biological Sciences (1996) 10.1098/rspb.1996.0137
[10]
Davies (2000)
[11]
Dixit "Why and how to apply Weber’s Law to coevolution and mimicry" (2021)
[12]
Dixit "Combined measures of mimetic fidelity explain imperfect mimicry in a brood parasite-host system" (2023)
[13]
Feeney "Social learning of a brood parasite by its host" (2013)
[14]
Geltsch "When should common cuckoos Cuculus canorus lay their eggs in host nests" (2016)
[15]
Grim "The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences" (2014)
[16]
Hauber "Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism" (2003)
[17]
Hauber "Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs" (2006)
[18]
Hauber "Indirect estimates of breeding and natal philopatry in an obligate avian brood parasite" (2012)
[19]
Hauber "Self-referent phenotype matching is a poor predictor of egg rejection by American robins" (2020)
[20]
Hauber "Clutch size and the rejection of parasitic eggs: a comparative test of the maternal investment hypothesis" (2022)
[21]
Hoover "Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea" (2003)
[22]
Igic "Using 3D printed eggs to examine the egg-rejection behaviour of wild birds" (2015)
[23]
Lotem "Learning to recognize nestlings is maladaptive for cuckoo Cuculus canorus host" (1993)
[24]
Lotem "Rejection of cuckoo eggs in relation to host age: A possible evolutionary equilibrium" (1992)
[25]
Lotem "Constraints on egg discrimination and cuckoo-host coevolution" (1995)
[26]
Luro "Which egg features predict egg rejection responses in American robins? Replicating Rothstein’s (1982) study" Ecology & Evolution (2018) 10.1002/ece3.3759
[27]
Manna "Multiple parasitism reduces egg rejection in the host of a mimetic avian brood parasite" (2019)
[28]
McLaren "Genetic and temporal patterns of multiple parasitism by brown-headed cowbirds (Molothrus ater) on song sparrows (Melospiza melodia)" (2003)
[29]
Medina "The evolution of acceptance and tolerance in hosts of avian brood parasites" (2016)
[30]
Molina-Morales "Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime" (2014)
[31]
Moskat "Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts" (2007)
[32]
Moskat "Naïve hosts of avian brood parasites accept foreign eggs, whereas older hosts fine-tune foreign egg discrimination during laying" (2014)
[33]
Noh "True recognition of nestlings by hosts selects for mimetic cuckoo chicks" (2018)
[34]
Price "The role of phenotypic plasticity in driving genetic evolution" (2003)
[35]
Reeve "The evolution of conspecific acceptance thresholds" (1989)
[36]
Rodriguez-Gironez "How to detect a cuckoo egg: A signal detection theory model for recognition and learning" American Naturalist (1999) 10.1086/303198
[37]
Rothstein "Mechanisms of avian egg recognition: Which egg parameters elicit responses by rejecter species" (1982)
[38]
Ruiz-Raya "Signal detection and optimal acceptance thresholds in avian brood parasite–host systems: Implications for egg rejection" (2020)
[39]
Rutledge "Best of a bad job or masters of illusion: Do nest light conditions make the eggs of brood parasitic brown-headed cowbirds (Molothrus ater) more similar to the eggs of its hosts" Ethology (2021) 10.1111/eth.13109
[40]
Samas "Repeatability of foreign egg rejection: Testing the assumptions of co-evolutionary theory" (2011)
[41]
A Meta-Analysis of Avian Egg Traits Cueing Egg-Rejection Defenses Against Brood Parasitism

Peter Samaš, Mark E. Hauber, Marcel Honza

Frontiers in Ecology and Evolution 2021 10.3389/fevo.2021.703208
[42]
Scharf "The evolution of conspecific acceptance threshold models" (2020)
[43]
Sealy "Removal of Yellow Warbler eggs in association with cowbird parasitism" (1992)
[44]
Servedio "Coevolution of an avian host and its parasitic cuckoo" (2003)
[45]
Servedio "Effects on population divergence of within-generational learning about prospective mates" (2013)
[46]
Shettleworth (2010)
[47]
Soler "Effect of great spotted cuckoo presence on magpie rejection behaviour" (2000)
[48]
Soler "Do first-time breeding females imprint on their own eggs" (2013)
[49]
Soler "Long-term coevolution between avian brood parasites and their hosts" (2014)
[50]
Spottiswoode "Vive la difference! Self/non-self recognition and the evolution of signatures of identity in arms races with parasites" (2019)

Showing 50 of 64 references

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2
Citations
64
References
Details
Published
Sep 21, 2023
Vol/Issue
7(6)
Pages
413-421
License
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Funding
National Science Foundation Award: DEB-1939290
Cite This Article
Kuangyi Xu, Maria R Servedio, Sarah K Winnicki, et al. (2023). Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds. Evolution Letters, 7(6), 413-421. https://doi.org/10.1093/evlett/qrad041
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