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      Model eggs fail to detect egg recognition in host populations after brood parasitism is relaxed

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          Abstract

          Background

          Obligate brood parasites exert strong selective pressure on target hosts. In response, hosts typically evolve anti-parasitism strategies, of which egg recognition is one of the most efficient. Generally, host egg-recognition capacity is determined using model eggs. Previous studies have shown that some host species, which are capable of detecting parasite eggs, do not reject model eggs. However, it is unknown that whether the reaction to model eggs varies among distinct populations of the same host in relation to the degree of parasitism pressure.

          Results

          Here, we compared the rejection frequencies of model eggs and real eggs between mainland and island populations of the plain prinia ( Prinia inornata), which are respectively sympatric and allopatric with their brood parasite, the common cuckoo ( Cuculus canorus). Our results indicated that the mainland and island populations rejected real eggs at similar rates, but rejected model eggs, which were similar in size to real eggs but heavier, at significantly different rates: the island population rejected fewer model eggs, possibly because the rejection motivation of this population was lower due to absence of parasitism.

          Conclusions

          Our results indicated that some factors affecting the decision to reject, such as rejection motivation, varied according to the degree of parasitism pressure, and thus influenced the frequency of egg rejection. Furthermore, our results suggested that model eggs should be used with caution in comparative studies of egg recognition abilities among species or populations subjected to different intensities of brood parasitism. That is, model eggs may fail to accurately detect egg recognition in host populations with little to no risk of parasitism.

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          Most cited references14

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          Coevolution in Action: Disruptive Selection on Egg Colour in an Avian Brood Parasite and Its Host

          Background Trait polymorphism can evolve as a consequence of frequency-dependent selection. Coevolutionary interactions between hosts and parasites may lead to selection on both to evolve extreme phenotypes deviating from the norm, through disruptive selection. Methodology/Principal finding Here, we show through detailed field studies and experimental procedures that the ashy-throated parrotbill (Paradoxornis alphonsianus) and its avian brood parasite, the common cuckoo (Cuculus canorus), have both evolved egg polymorphism manifested in discrete immaculate white, pale blue, and blue egg phenotypes within a single population. In this host-parasite system the most common egg colours were white and blue, with no significant difference in parasitism rates between hosts laying eggs of either colour. Furthermore, selection on parasites for countering the evolution of host egg types appears to be strong, since ashy-throated parrotbills have evolved rejection abilities for even partially mimetic eggs. Conclusions/Significance The parrotbill-cuckoo system constitutes a clear outcome of disruptive selection on both host and parasite egg phenotypes driven by coevolution, due to the cost of parasitism in the host and by host defences in the parasite. The present study is to our knowledge the first to report the influence of disruptive selection on evolution of discrete phenotypes in both parasite and host traits in an avian brood parasitism system.
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            Relic behaviours, coevolution and the retention versus loss of host defences after episodes of avian brood parasitism.

            Most previous studies of brood parasitism have stressed that host defences, such as egg recognition, are lost in the absence of parasitism. Such losses could result in coevolutionary cycles in which parasites shift away from well-defended hosts only to switch back to them later at a time when these hosts have lost much or all of their defences and the parasite's current hosts have built up effective defences. However, the alternative 'single trajectory' model predicts that parasites rarely switch back to old hosts because ex-hosts retain egg recognition for long periods in the absence of parasitism. If true, egg recognition by the host may be a 'relic behaviour', because in the absence of parasitism its adaptive value is close to neutral. Using artificial nonmimetic eggs, I tested for egg recognition in two populations that are currently unparasitized but that are descended from lineages likely to have been parasitized in the past: the grey catbird, Dumetella carolinensis, on Bermuda and the loggerhead shrike, Lanius ludovicianus, in California. Both of these populations showed long-term retention, ejecting nonmimetic eggs at rates of nearly 100%. Because potential present-day selection pressures, such as conspecific parasitism, do not explain this egg recognition, Bermuda catbirds apparently retain recognition from North American conspecifics that were cowbird hosts before colonizing Bermuda and shrikes retain recognition from Old World congeners that were hosts of cuckoos. Retention is also indicated by passerines in California and the Caribbean that had high rejection rates of nonmimetic eggs before coming into contact with cowbirds. These new data suggest that both the coevolutionary cycles and single trajectory models have importance and that rejection behaviour can have insignificant costs, which is consistent with evolutionary lag explanations for the acceptance of parasitic eggs shown by some cuckoo and many cowbird hosts. Copyright 2001 The Association for the Study of Animal Behaviour.
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              Diversity of parasitic cuckoos and their hosts in China

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                Author and article information

                Contributors
                ccyang@hainnu.edu.cn
                liangwei@hainnu.edu.cn
                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                12 May 2020
                12 May 2020
                2020
                : 17
                : 14
                Affiliations
                [1 ]GRID grid.440732.6, ISNI 0000 0000 8551 5345, Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, , Hainan Normal University, ; Haikou, 571158 China
                [2 ]GRID grid.443395.c, ISNI 0000 0000 9546 5345, State Forestry Administration of China Key Laboratory for Biodiversity Conservation in Mountainous Areas of Southwest Karst, School of Life Sciences, , Guizhou Normal University, ; Guiyang, 550001 China
                [3 ]GRID grid.260567.0, ISNI 0000 0000 8964 3950, Department of Natural Resources and Environmental Studies, , National Dong Hwa University, ; 97401 Hualien, Taiwan
                [4 ]GRID grid.460789.4, ISNI 0000 0004 4910 6535, Ecologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech, , Université Paris-Saclay, ; F-91405 Orsay Cedex, France
                Author information
                http://orcid.org/0000-0001-9405-2749
                Article
                362
                10.1186/s12983-020-00362-0
                7216403
                32426018
                06ed2d29-58ee-4433-8a49-3809e42eeba3
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 7 November 2019
                : 4 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31772453
                Award ID: 31672303
                Award Recipient :
                Funded by: National Natural Science Foundation of China (CN)
                Award ID: 31660617
                Award ID: 31960105
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Animal science & Zoology
                avian brood parasitism,cuculus canorus,parasitism pressure,prinia inornata,rejection motivation

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