Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host
TL;DR: This is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them, and results show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoos eggs may avoid rejection by means of their unusually high structural strength.
Abstract: Given the high costs of avian obligate brood parasitism, host individuals are selected to reject parasitic eggs they recognize as foreign. We show that rejection may not necessarily follow egg discrimination when selective removal of the parasitic egg is difficult. We studied egg rejection behaviour in a small host of the common cuckoo Cuculus canorus, the eastern olivaceous warbler Hippolais pallida, by experimental parasitism with model and real non-mimetic cuckoo eggs and video recordings of host behaviour. Hosts pecked 87 per cent (20 out of 23) of the model eggs but eventually accepted 43.5 per cent (10 out of 23) of them. A similar pattern was found for real cuckoo eggs, which were all pecked, but as many as 47 per cent (7 out of 15) of them were accepted. To our knowledge, this is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them. Our results also show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoo eggs may avoid rejection by means of their unusually high structural strength.
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TL;DR: The twin hurdles of effective trickery in the face of evolving host defences and difficulties of tuning into another species' life history may together explain why obligate brood parasitism is relatively rare.
Abstract: I suggest that the cuckoo's parasitic adaptations are of two kinds: ‘trickery’, which is how adult cuckoos and cuckoo eggs and chicks evade host defences, and involves adaptations that have co-evolved with host counter-adaptations, and ‘tuning’, which is how, once accepted, cuckoo egg and chick development are then attuned to host incubation and provisioning strategies, and which might not always provoke co-evolution. Cuckoo trickery involves adaptations to counter successive lines of host defence and includes: tricks for gaining access to host nests, egg trickery and chick trickery. In some cases, particular stages of host defences, and hence their corresponding cuckoo tricks, are absent. I discuss three hypotheses for this curious mixture of exquisite adaptation and apparent lack of adaptation: different defences best for different hosts, strategy blocking and time for evolution of defence portfolios. Cuckoo tuning includes adaptations involving: host choice and monitoring of host nests, efficient incubation of the cuckoo egg, efficient provisioning and protection of the cuckoo chick, and adaptations to avoid misimprinting on the wrong species. The twin hurdles of effective trickery in the face of evolving host defences and difficulties of tuning into another species' life history may together explain why obligate brood parasitism is relatively rare.
205 citations
Cites background from "Evidence for egg discrimination pre..."
...They may decide to accept if cuckoo eggs are difficult to distinguish with certainty (Antonov et al., 2009) or if acceptance is not too costly, because the cuckoo egg is often laid too late, or some host young can be raised alongside a cuckoo chick (Krüger, 2011)....
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...They may decide to accept if cuckoo eggs are difficult to distinguish with certainty (Antonov et al., 2009) or if acceptance is not too costly, because the cuckoo egg is often laid too late, or some host young can be raised alongside a cuckoo chick (Krüger, 2011)....
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TL;DR: An adaptive explanation of co‐evolution between brood parasites and their hosts is proposed, which centres on the relative strength of two opposing processes: strategy‐facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy‐blocking, which may relax selection on another so completely that it causes it to decay.
Abstract: Avian parents and social insect colonies are victimized by interspecific brood parasites-cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter-strategies in the parasite, thus setting in motion antagonistic co-evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co-evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co-evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co-evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co-evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co-evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co-evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co-evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy-facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy-blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy-facilitation outweighs strategy-blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.
178 citations
Cites background from "Evidence for egg discrimination pre..."
...The largest hosts can potentially reject a parasitic egg by grasping the whole egg within their bill, but this is impossible for smaller hosts (Antonov et al., 2009; Spaw & Rohwer, 1987) who constitute the majority of avian brood parasite victims....
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TL;DR: The incorporation of frontline interactions in empirical and theoretical investigations of brood parasite–host arms races are advocated to provide a more holistic understanding of the coevolutionary processes in these systems.
151 citations
Cites background from "Evidence for egg discrimination pre..."
...In response, brood parasites have evolved counteradaptations including mimicry of host eggs (Avilés et al. 2010; Spottiswoode & Stevens 2010; Stoddard & Stevens 2010), cryptic eggs (Marchant 1972; Langmore et al. 2009b) and thickened eggshells (Brooker & Brooker 1991; Antonov et al. 2009)....
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...2009b) and thickened eggshells (Brooker & Brooker 1991; Antonov et al. 2009)....
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TL;DR: Hosts rejected their own eggs and manipulated (‘parasitic’) eggs above control levels in experiments when manipulated eggs were in the majority but when clutches also included a minority of own eggs, supporting a mechanism of template-based egg discrimination.
Abstract: Many avian hosts have evolved antiparasite defence mechanisms, including egg rejection, to reduce the costs of brood parasitism. The two main alternative cognitive mechanisms of egg discrimination are thought to be based on the perceived discordancy of eggs in a clutch or the use of recognition templates by hosts. Our experiments reveal that the great reed warbler (Acrocephalus arundinaceus), a host of the common cuckoo (Cuculus canorus), relies on both mechanisms. In support of the discordancy mechanism, hosts rejected their own eggs (13%) and manipulated ('parasitic') eggs (27%) above control levels in experiments when manipulated eggs were in the majority but when clutches also included a minority of own eggs. Hosts that had the chance to observe the manipulated eggs daily just after laying did not show stronger rejection of manipulated eggs than when the eggs were manipulated at clutch completion. When clutches contained only manipulated eggs, in 33% of the nests hosts showed rejection, also supporting a mechanism of template-based egg discrimination. Rejection using a recognition template might be more advantageous because discordancy-based egg discrimination is increasingly error prone with higher rates of multiple parasitism.
86 citations
Cites background from "Evidence for egg discrimination pre..."
...…not always allow distinction between predictions and outcomes of the discordancy versus the template recognition mechanisms (Moskát et al., 2008c; Antonov et al., 2009), contemporary experiments are required that specifically aim to contrast the predictions of these alternative cognitive models…...
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TL;DR: Hosts can rely on comparisons of foreign egg colors against an internal recognition template of acceptable (own) egg phenotypes to reject foreign eggs, suggesting a role for discordancy and/or online self-referent phenotype matching.
Abstract: Many hosts have evolved diverse cognitive mechanisms to recognize and reduce the cost of social parasitism. For example, great reed warblers Acrocephalus arundinaceus can accurately reject closely mimetic eggs of brood parasitic common cuckoos Cuculus canorus. Yet, these same hosts are less effective at identifying and rejecting parasitism when the clutch is parasitized by multiple cuckoo eggs, suggesting a role for discordancy (the rejection of the egg type in the minority of the clutch) and/or online self-referent phenotype matching (the simultaneous viewing of cuckoo and own eggs in the nest) to reject foreign eggs. We tested whether the presence of host’s own eggs is required for the discrimination of foreign eggs by dyeing hosts’ own eggs with one of several colors so that clutches contained (a) 1 dyed and 4 unmanipulated eggs, (b) 3 dyed and 2 unmanipulated eggs, or 5 eggs dyed either (c1) differently or (c2) similarly. Rejection rates of dyed eggs varied widely between different colors and were highest in treatment (a), with 1 dyed egg, compared with treatments with the majority (b) or all (c1 and c2) dyed eggs. However, relative rejection rates of dyed eggs were also consistent among specific colors across treatments, including (c1) and (c2), where no unmanipulated own eggs were available for viewing and irrespective of whether eggs were dyed all different colors (c1) or the same colors (c2). We conclude that these hosts can rely on comparisons of foreign egg colors against an internal recognition template of acceptable (own) egg phenotypes.
58 citations
References
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TL;DR: It is tentatively concluded that resistance to laying damage has not been critical in favoring the evolution of thick shells in cowbird eggs, and it is shown that a puncture specialist, the Marsh Wren, has greater difficulty puncturingcowbird eggs than the thinner-shelled eggs of various other passerines.
Abstract: We directly measured the eggshell thickness of the three brood parasitic Molothrus cowbirds, 17 other icterids, and 13 additional passerines. By correcting these shell thickness measurements for variation attributable to interspecific differences in egg volume, we show that the Molothrus cowbirds lay eggs with shells that are 30% thicker than expected for their size. Our samples of nonparasitic icterids and of other passerines do not differ significantly in shell thickness values corrected for differences in egg volume. We evaluate two hypotheses for the evolution of unusually thick-shelled eggs in cowbirds. The first, an old idea proposed for parasitic cuckoos, is that thick shells resist damage to the parasite's egg at laying. From indirect tests we could find little or no evidence that the thin-shelled eggs of the hosts of cowbirds were damaged by impact when cowbird eggs were laid in their nests; thus, we tentatively conclude that resistance to laying damage has not been critical in favoring the evolution of thick shells in cowbird eggs. As an alternative hypothesis we propose that thick shells have evolved in cowbird eggs to resist puncture ejections by hosts that are too small to grasp whole cowbird eggs for ejection. We show that a puncture specialist, the Marsh Wren (Cistothorus palustris), has greater difficulty puncturing cowbird eggs than the thinner-shelled eggs of various other passerines. Implications of our hypothesis concerning resistance to puncture ejections are discussed.
138 citations
"Evidence for egg discrimination pre..." refers background in this paper
...Thus, the puncture resistance hypothesis, which was originally proposed to explain the adaptive significance of increased structural strength of cowbird eggs (Spaw & Rohwer 1987), may also be applicable to some hosts of the cuckoo in which puncture ejection is difficult or impossible....
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...Besides mimicry, the unusually strong shells of parasitic eggs (Spaw & Rohwer 1987; Picman & Pribil 1997) may render rejection especially costly for smallbilled hosts that have to puncture the parasitic egg in order to remove it (puncture ejection) or desert the clutch (Moksnes et al. 1991; Røskaft…...
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...Rejection costs involve recognition errors, accidental destruction of own eggs and/or simply energetic expenditure (Spaw & Rohwer 1987; Davies et al. 1996; Røskaft et al. 2002)....
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138 citations
"Evidence for egg discrimination pre..." refers background in this paper
...Furthermore, because rejection may be costly, some hosts also Received 6 November 2008 Accepted 2 December 2008 169 modify their rejection decisions according to the perceived risk of parasitism (Moksnes et al. 1993; Lindholm 2000; Soler et al. 2000)....
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...Video recordings showing strong pecking followed by desertion demonstrated that at least some of the desertions represent a failure at puncture ejection rather than nest abandonment in the first place (cf. Moksnes et al. 1993)....
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...Despite some indirect demonstrations of conditional host responses (Davies & Brooke 1989; Moksnes et al. 1993), there is very little direct evidence for acceptance of cuckoo eggs once host individuals have discriminated against them (Lindholm 2000; Soler et al. 2000)....
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TL;DR: Findings suggest that spatial variation in the level of host resistance to brood parasitism may depend on current and/or past selection pressure due to the parasite and individual differences linked to abilities for egg rejection.
Abstract: In the coevolutionary arms race between avian brood parasites and their hosts, several adaptations have evolved on both sides, the most prominent and important host defense being rejection of the parasitic egg. In the present study, we investigated possible predictors of egg rejection in 14 populations of reed warblers Acrocephalus scirpaceus across Europe differing in risk of parasitism by the common cuckoo Cuculus canorus, providing a test of factors associated with geographic variation in host resistance to parasitism. In a binomial general linear mixed model procedure, we quantified the possible influence of host clutch size, cuckoo parasitism in population (yes/no), height of the nest above ground, height of vegetation in the vicinity of the nest and distance to nearest vantage point on rejection of an experimentally added nonmimetic cuckoo sized egg. In addition, we entered ‘‘population’’ into the models as a random factor. Rejection rate varied significantly among populations (range 4.8–68.9%). The most parsimonious model, based on selection by the Akaike information criterion, included cuckoo parasitism in the population (yes/ no) and host clutch size; rejection rate was the highest in parasitized populations, and individuals laying larger clutches were the best rejecters. Furthermore, rejecters tended to breed in higher vegetation than acceptors. These findings suggest that spatial variation in the level of host resistance to brood parasitism may depend on current and/or past selection pressure due to the parasite and individual differences linked to abilities for egg rejection. Key words: Acrocephalus scirpaceus, brood parasitism, clutch size, coevolution, common cuckoo, Cuculus canorus, egg rejection, metapopulation, reed warbler. [Behav Ecol]
86 citations
"Evidence for egg discrimination pre..." refers background in this paper
...However, despite the apparent benefits of rejection, there is substantial variation both among and within host species used by cuckoos in their responses to foreign eggs (Davies & Brooke 1989; Moksnes et al. 1990; Martı́n-Gálvez et al. 2007; Stokke et al. 2008)....
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TL;DR: This review considers several hypotheses set out to explain the apparent imperfect rejection behaviour against parasite eggs among hosts of brood parasites, and links these hypotheses with a consideration of various sources that can influence decision-making when hosts are faced with the possibility that a parasite egg is present in their nest.
Abstract: Coevolutionary dynamics allow revealing ongoing microevolutionary processes and adaptations. Interactions between obligate avian brood parasites and their hosts are suitable systems for the study of coevolution. This fascinating subject has interested both scientists and the common man for decades, but there are still many unanswered questions. One of the main puzzles is the apparent imperfect rejection behaviour against parasite eggs among hosts of brood parasites leading to a situation where many hosts experience severe costs of parasitism, which dramatically reduce their fitness. In order to lower these costs, hosts are expected to evolve counter-adaptations against parasitism. However, many host species show no rejection or only intermediate rejection rates against non-mimetic parasite eggs. In this review we consider several hypotheses set out to explain this phenomenon, and then we link these hypotheses with a consideration of various sources that can influence decision-making when hosts ar...
71 citations
"Evidence for egg discrimination pre..." refers background in this paper
...Nevertheless, the underlying mechanisms of rejection decisions within and across the different host species are still poorly understood (Davies et al. 1996; Stokke et al. 2005)....
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...Possible explanations invoke a lack of necessary genetic variation underpinning egg discrimination, or discrimination developing with age/experience or having only evolved in some host populations sympatric with the brood parasite (Rothstein & Robinson 1998; Stokke et al. 2005; Røskaft et al. 2006)....
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TL;DR: There was no evidence that egg damage was associated with cuckoo egg laying, and some support for the puncture resistance hypothesis for the occurrence of thick-shelled eggs in common cuckoos Cuculus canorus.
Abstract: Eggs of several brood parasites have thicker and stronger shells than expected for their size. The present study evaluated the puncture resistance hypothesis for the occurrence of thick-shelled eggs in common cuckoos Cuculus canorus by investigating costs of cuckoo egg ejection in four Acrocephalus warblers—the great reed warbler A. arundinaceus, reed warbler A. scirpaceus, marsh warbler A. palustris and sedge warbler A. schoenobaenus. The three latter species all suffered ejection costs, while ejection was not costly in the larger great reed warbler. The occurrence of ejection costs was negatively related to host bill size. In the marsh warbler, we compared ejection costs in naturally parasitized nests and two experimental treatments, in which broods were parasitized artificially with great reed warbler and conspecific eggs. Hosts damaged their own eggs significantly more often when ejecting the thick-shelled cuckoo eggs than when ejecting the similarly sized but thinner-shelled great reed warbler eggs, providing some support for the puncture resistance hypothesis. Ejection of conspecific eggs did not involve any costs. Furthermore, contrary to predictions derived from the laying damage hypothesis, there was no evidence that egg damage was associated with cuckoo egg laying. Hosts damaging their own eggs during ejection were more likely to subsequently desert their clutches than those that did not. The frequency of clutches smeared with the contents of the ejected egg were positively related to the hypothesized difficulty of foreign egg puncturing. Potential advantages of thicker shells in common cuckoo eggs are discussed.
52 citations