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: Any damage a host causes to its own eggs when ejecting a parasitic egg from its nest must be considered when attempting to make realistic predictions about optimal host response to parasitism, and the cost of puncture-ejecting cowbird eggs is estimated to be 0.26 oriole eggs for each cowbird egg ejected.
Abstract: Any damage a host causes to its own eggs when ejecting a parasitic egg from its nest must be considered when attempting to make realistic predictions about optimal host response to parasitism. We have assessed such damage for the Northern Oriole Icterus galbula, a species which puncture-ejects the eggs of Brown-headed Cowbirds Molothrus ater. We experimentally added genuine Brown-headed Cowbird eggs, which have substantially stronger shells than the eggs of comparable-sized passerines, to nests of the Northern Oriole. Orioles often damage some of their own eggs when ejecting a cowbird egg. The hatching success of damaged oriole eggs was less than 45%, while 99% of the undamaged eggs hatched. These results allow us to estimate that the cost of puncture-ejecting cowbird eggs is the death of 0.26 oriole eggs for each cowbird egg ejected. We also measured rearing costs in a limited number of nests into which we placed a newly hatched cowbird chick shortly after the oriole eggs hatched. When there were four oriole chicks in a nest, the cost of rearing a cowbird chick exceeded the cost of puncture ejection.
39 citations
"Evidence for egg discrimination pre..." refers background in this paper
...…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 et al. 1993; Antonov et al. 2006)....
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TL;DR: It is suggested that puncture-ejection may have evolved first, representing an initial selection pressure for cowbird eggshell strength.
35 citations
"Evidence for egg discrimination pre..." refers background in this paper
...It may be argued that acceptance rates may be overestimated for the model eggs, owing to their artificiality (e.g. Rothstein 1977; Underwood & Sealy 2006)....
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TL;DR: A metapopulation dynamics model for brood parasites and their hosts is used to investigate the validity of the "spatial habitat structure hypothesis," which states that a low level of parasite egg rejection in host populations is due to the immigration of acceptor individuals from nonparasitized populations.
Abstract: We used metapopulation dynamics to develop a mathematical simulation model for brood parasites and their hosts in order to investigate the validity of the "spatial habitat structure hypothesis," which states that a low level of parasite egg rejection in host populations is due to the immigration of acceptor individuals from nonparasitized populations. In our model, we varied dispersal rate and the relative carrying capacity of host individuals in parasitized and unparasitized patches. When both the relative carrying capacity in the parasite-free patch and the dispersal rate increase, the nonparasitized patch will provide more acceptor individuals to the parasite-prone patch. As the relative carrying capacity in the parasite-free patch increases, the equilibrium frequency of rejecters both in the parasite-prone and in the parasite-free patch decreases toward zero for intermediate levels of the dispersal rate. Although the rejecter strategy is more adaptive than the acceptor strategy in the parasite-prone patch, large numbers of acceptors are produced in the parasite-free patch dispersing to the parasitized patch. As the number of individuals in the parasite-free patch increases, parasitism rate can be maintained stable at a high equilibrium level in the parasite-prone patch. Copyright 2006.
35 citations
"Evidence for egg discrimination pre..." refers background in this paper
...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: This is the first in-depth study of brood parasitism in a warbler of the genus Hippolais, and cuckoos parasitizing olivaceous warblers probably represent a previously unknown gens.
Abstract: Coevolution is defined as specialized relationships between species that lead to a reciprocal evolutionary change. A particularly suitable model system for studying coevolution is the interactions between obligate avian brood parasites and their hosts. The common cuckoo (Cuculus canorus, hereafter cuckoo) is a well-known brood parasite, which utilizes a range of smaller passerines as hosts. However, warblers of the genus Hippolais have rarely been reported as being victims of cuckoos, and furthermore, few data exist on the occurrence of antiparasite defenses in these hosts. In this study, we examined possible host–parasite coevolution between cuckoos and eastern olivaceous warblers (Hippolais pallida elaeica, hereafter olivaceous warblers) in three closely situated areas in northwestern Bulgaria. The olivaceous warbler has never been reported to be a regular cuckoo host. However, the present study, carried out in 2001–2003 shows that the olivaceous warbler is regularly and heavily parasitized by the cuckoo in this area. Parasitism rate was high (26.6%, 34/128) and consistent among years, with some variation between areas. The cuckoo egg mimicry was moderately good, and olivaceous warbler rejection rate of such eggs was 50%. Cuckoo eggs laid in olivaceous warbler nests had a whitish to whitish-green ground color, and the majority appeared to be distinctly different from cuckoo eggs found in other host species in the area. The olivaceous warbler proved to be a rather good host for cuckoos as 20.6% (7/34) of cuckoo eggs laid produced fledglings, a breeding success comparable to other suitable hosts in Europe. This is the first in-depth study of brood parasitism in a warbler of the genus Hippolais, and cuckoos parasitizing olivaceous warblers probably represent a previously unknown gens.
31 citations
"Evidence for egg discrimination pre..." refers background in this paper
...This study was performed in northwestern Bulgaria where olivaceous warblers have been frequently parasitized by cuckoos (Antonov et al. 2007)....
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...Ejection also accounted for only a minority (12%, 2 out of 17) of rejections of naturally laid cuckoo eggs (Antonov et al. 2007)....
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23 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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...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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