Abstract
Rejection of parasitic eggs is the most common and effective defence used by hosts to mitigate the fitness costs imposed by avian brood parasites. Although egg rejection importantly relies on the cognitive abilities of parasitized individuals, both theoretical models and experimental studies have found that some hosts are able to modify their response according to the current conditions of parasitism, which reflects the existence of phenotypic plasticity in host defences. In environments in which the risk of parasitism is variable, plastic responses can be favoured by natural selection as they will allow hosts to avoid potential rejection costs under low risk of parasitism. In this chapter, we review the current evidence of plastic responses in egg rejection and discuss both the evolution and the long-term consequences of phenotypic plasticity for brood parasite–host coevolution. In addition, we suggest addressing the study of egg rejection as a complex process affected by multiple components and governed by decision-making and host motivation, which has important implications for host responses. Despite its apparent benefits, phenotypic plasticity is scarce among host species. Thus, the evolution of phenotypic plasticity in brood parasite–host systems deserves special attention as the maintenance or the loss of plastic responses involves important evolutionary consequences, affecting the long-term outcome of the interaction between brood parasites and their hosts. We conclude this chapter with some suggestions to deal with phenotypic plasticity in future egg-rejection studies.
Keywords
1 Introduction
Antagonistic interactions between avian brood parasites and their hosts usually result in a coevolutionary arms race in which adaptations and counteradaptations evolve on both sides (Davies 2000). The high fitness costs imposed by brood parasitism select for host defences at different stages of the breeding cycle: hosts attack brood parasites that approach their nests, reject the parasitic egg, remove the young parasitic chick or refuse to feed parasitic nestlings or fledglings (Soler 2014). However, recognition and rejection of parasitic eggs is the most common and effective strategy used by hosts against brood parasitism (Rothstein 1990; Davies 2000), which has led some brood parasites to evolve sophisticated egg mimicry and host species to fine-tune their abilities to recognize parasitic eggs (Brooke and Davies 1988).
Both theoretical models (Rothstein 1990; Takasu 1998; Robert et al. 1999; Servedio and Lande 2003) and empirical evidence (Martín-Gálvez et al. 2006, 2007) have pointed to the importance of the genetic component of hosts’ egg recognition abilities. In many host species, such abilities are maintained even after generations of allopatry with brood parasites (Lahti 2006; Hale and Briskie 2007; Peer et al. 2011; Soler 2014; Ruiz-Raya et al. 2016), while, in other cases, evolutionary change has led to a decline in the egg-rejection behaviour of some hosts after long period of isolation from parasites (Kuehn et al. 2014). There are occasions, however, when the decline of parasitism rate is accompanied by a decrease in rejection rates too rapid to reflect genetic change in populations (Soler et al. 2012a; Thorogood and Davies 2013). These findings suggest that egg rejection does not rely exclusively on genetically determined cognitive abilities, but hosts are able to modify their rejection decisions under different environmental contexts, such as the risk of parasitism (Stokke et al. 2005; Moskát and Hauber 2007; Soler et al. 2012b). Given the costs linked to the expression of antiparasitic behaviours, natural selection should favour the emergence of flexible host defences in circumstances in which the risk of parasitism is low. For example, highly mimetic parasitic eggs can lead hosts to eject their own eggs by mistake (recognition costs) or to break some eggs of their own during the ejection process (ejection costs) (Davies 2000). Furthermore, cuckoo-hawk mimicry (Davies and Welbergen 2008; Welbergen and Davies 2011) makes it dangerous to approach an intruder that might be a potentially lethal enemy. Thus, when the probability of being parasitized is low, phenotypic plasticity in host defences would allow individuals to avoid such costs.
Phenotypic plasticity can be defined as the property of a single genotype to produce different phenotypes in response to distinct environmental conditions (Pigliucci 2001), which has been evidenced for a large array of traits including morphological, physiological, life history and behavioural traits (West-Eberhard 2003; Pigliucci 2005; Nussey et al. 2007). This relationship between phenotype and environment is usually represented by “reaction norms” (Fig. 25.1), whose slope reflects the degree of plasticity of genotypes (Schlichting and Pigliucci 1998; Pigliucci 2005). Furthermore, in cases in which there is variation within the population for the slope of the reaction norm (non-parallel reaction norms), it can be said that population shows a G × E effect (i.e. genotype × environment) (Pigliucci 2005). This approach is also used to study between-individual variations in animal behaviour through the “behavioural reaction norms”, which are characterized not only by the individual slopes of reaction norms (plasticity) but also from individual differences in the elevation of reaction norms (personality) (Dingemanse et al. 2010; Dingemanse and Wolf 2013). In highly variable environments, individuals can obtain fitness benefits from their ability to respond plastically when compared with those that do not, so phenotypic plasticity can become adaptive (Ghalambor et al. 2007). Behavioural plasticity has been suggested to be particularly important in variable environments since the development and expression of animal behaviour may be immediate, reversible and especially sensitive to environmental changes (West-Eberhard 2003; Fordyce 2006; Snell-Rood 2013).
The strength of interactions between brood parasites and their hosts shows a remarkable spatiotemporal heterogeneity, and some hosts have been found able to adjust their defences accordingly (see below). Such flexible defences are important from an evolutionary perspective as they can determine the result of ecological interactions (Fordyce 2006). The existence of flexible defences in hosts has been documented regarding nest vigilance (Davies et al. 2003; Feeney and Langmore 2015), mobbing to adult parasites and nest defence (Lindholm and Thomas 2000; Welbergen and Davies 2009, 2012; Langmore et al. 2012; Thorogood and Davies 2013; Kuehn et al. 2016), egg rejection (see Table 25.1) and chick rejection (Langmore et al. 2009a). Throughout this chapter, we review the current evidences of flexible defences in hosts of obligate brood parasites by focusing on the egg-rejection behaviour and the host decision-making. In addition, we discuss both the evolutionary origin and the main consequences of phenotypic plasticity on the coevolutionary history between brood parasites and their hosts.
2 Evidence of Phenotypic Plasticity in Egg Rejection
The existence of a conditional component in egg-rejection behaviour has been predicted by several theoretical models, which widely describe the importance of both the risk of parasitism and potential rejection costs on host responses (Davies et al. 1996; Rodríguez-Gironés and Lotem 1999; Holen and Johnstone 2006; Stokke et al. 2007). In addition to theoretical predictions, many empirical studies (see below) have suggested that phenotypic plasticity is behind the variations in rejection rates found among both host populations and individuals, especially those cases where there is a variable risk of parasitism.
Ecological interactions between brood parasites and their hosts show spatial heterogeneity resulting in the emergence of both “coevolutionary hot spots” (population with intense interactions between parasites and hosts) and “cold spots” (populations showing scarce or absent interactions) (Thompson 2005; Møller and Soler 2012). As a result, host populations vary in the extent of local adaptations against brood parasitism, leading to differences in egg-rejection behaviour among populations (Davies and Brooke 1989; Soler and Møller 1990; Briskie et al. 1992; Soler et al. 1999a). Although such differences may reflect genotypic differences (Martín-Gálvez et al. 2007), studies on metapopulation dynamics have revealed the importance of phenotypic plasticity in explaining variations in rejection rates among host populations. For example, the presence of common cuckoo Cuculus canorus (cuckoo hereafter) parasitism has been proven to be the main predictor to explain the spatial variation in host resistance existing among different populations of reed warbler Acrocephalus scirpaceus across Europe (Stokke et al. 2008). In British populations of this species that are not genetically isolated, individuals from unparasitized populations reject eggs at lower rates and show a less aggressive response towards cuckoos than those from parasitized populations (Lindholm and Thomas 2000). Most importantly, reed warblers from both parasitized and unparasitized populations were able to recognize (individuals from all populations pecked the model eggs) and eject experimental model eggs, but they differ in their tendency to reject them, confirming that phenotypic plasticity was responsible for the differences in host responses between nearby populations (Lindholm 2000). Similarly, some hosts of the shiny cowbird Molothrus bonariensis, such as the village weavers Ploceus cucullatus on Hispaniola, show higher rejection rates in those areas where the parasites are present (Cruz et al. 2008), confirming that differences between host population can be explained by the spatial distribution of brood parasites.
In addition to geographic variations, risk of parasitism also varies across a temporal scale as the result of changes in the density of parasite populations over the time (reviewed in Møller and Soler 2012). In some cases, when parasitism pressure increases in a certain area, or brood parasites expand their geographical ranges, some hosts respond by increasing their egg-rejection rate. In Guadix, southern Spain, the increase in parasitism rate by great spotted cuckoos Clamator glandarius over a decade was followed by a marked increase of egg rejection by common magpies Pica pica (Soler et al. 1994, 1998). A similar increase in host defences was also found in one of the major hosts of the common cuckoo in Japan, the azure-winged magpie Cyanopica cyana, which was also related to a strong increase in cuckoo parasitism (Nakamura et al. 1998). In other cases, parasite populations experience significant declines over a few years as a result of various ecological factors, and, in such circumstances, host defences can show a rapid decrease within host populations as parasitism rate decreases. The most extreme response to such decline in parasitism was that found by Soler et al. (2012a) in Los Palacios, southern Spain, where rufous-tailed scrub robins Cercotrichas galactotes drastically reduced their egg-rejection rate from about 64.7% to 0% within 10 years following the cuckoos’ disappearance from the area. These results are similar to those previously found on Wicken Fen, England, where a decline in cuckoo parasitism from 16% to 2–6% over a 12-year period resulted in a significant decline in egg-rejection behaviour by reed warblers from 75% to 25% during the same period of time (Brooke et al. 1998). Interestingly, this trend has been maintained in this English population during the subsequent 15 years, and it may reflect a phenomenon common to other reed warbler populations across Europe (Thorogood and Davies 2013).
Although changes in host defences as those described above could also be due to rapid evolutionary change, the fact that hosts are able to modify their rejection behaviour in response to changes in parasitism pressure within the same breeding season supports the idea that these variations are due to phenotypic plasticity. For instance, rufous-tailed scrub robins show a drastic decline in rejection rate when cuckoos leave the breeding area to go to their winter quarters (Álvarez 1996; Soler et al. 2012a). Other host species, such as reed warblers, have been also found to weaken their rejection response as the breeding season progresses (Brooke et al. 1998; Lindholm 2000; Thorogood and Davies 2013); although the opposite effect, an increase in rejection rates later in the breeding season, has also been described in some host species of the brown-headed cowbird Molothrus ater (Lang et al. 2014), which could also be explained by phenotypic plasticity. Of course, this seasonal decline in rejection rates could be the consequence of factors linked to life history traits instead of changes in parasitism pressure, such as inexperienced individuals breeding later (Lotem et al. 1992) or lower chances of renesting at the end of the breeding season (Burgham and Picman 1989). However, rufous-tailed scrub robins did not show differences in their rejection rates between young and experienced individuals (Soler et al. 2000), which suggests that phenotypic plasticity is behind the within-season changes in the egg-rejection behaviour found in some host species.
Flexible responses to brood parasitism are also observable within populations as individuals may respond differently to parasitism and show variations in their individual level of defence, which could be considered valuable evidence of phenotypic plasticity. Several studies have shown that the presentation of a female cuckoo model increases the likelihood of egg rejection in several host species, such as reed warblers (Davies and Brooke 1988), meadow pipits Anthus pratensis (Moksnes and Røskaft 1989; Moksnes et al. 1993) and great reed warblers Acrocephalus arundinaceus (Bartol et al. 2002) (but see Lindholm 2000; Soler et al. 2012a), meaning that individuals exposed to greater risk of parasitism are more likely to reject parasitic eggs, at least in the mentioned species. In fact, naturally parasitized reed warblers reject the parasitic egg more frequently when they discover the cuckoo near the nest (Moksnes et al. 2000). In other cases, individuals show lack of consistency in their rejection behaviour, and they vary their response to experimental parasitism as a consequence of the balance between cost and benefits of egg rejection (Soler et al. 2000). In response to repeated parasitism, individual yellow warblers Setophaga petechia may either accept or reject the parasitic egg after recognizing it (Guigueno and Sealy 2012). This individual lack of consistency in subsequent parasitism events has been documented even in rarely parasitized species, such as the common grackle Quiscalus quiscula (Peer and Rothstein 2010).
One of the most striking examples of conditional host behaviours is that exhibited in response to the mafia tactics used by some parasites, which have been particularly studied in the great spotted cuckoo-magpie system. After parasitism, great spotted cuckoos systematically punish rejecter magpies by predating those nests where the parasitic egg has disappeared, drastically reducing the reproductive success of hosts and, therefore, the advantage of egg rejection (Soler et al. 1995). The benefit obtained by the great spotted cuckoo is a greater probability of acceptance of the parasite egg since punished magpies change their behaviour from rejection to acceptance in subsequent parasitism events (Soler et al. 1999b). Thus, magpie response to the great spotted cuckoos’ mafia tactics reveals the ability of hosts to adjust their response based on previous experience. These changes in the host response are more frequent in areas with a high density of brood parasites in which hosts are likely to be parasitized by several cuckoos, which means that magpies can plastically adjust their response according to the risk of suffering a second retaliation (Soler et al. 1999b; Chap. 15).
Host defences are often costly since rejection behaviour may involve the desertion of the complete clutch, recognition errors during egg ejection, accidental breaking of some own eggs or even retaliation by the parasite. As mentioned earlier, flexible defences can be favoured by natural selection in order to avoid such costs under certain ecological conditions, such as a low risk of parasitism. The use of video cameras in recognition experiments has made possible the detailed study of host responses to parasitic eggs, and it has shown that hosts can recognize more eggs than they finally reject, thus confirming the complex nature of the egg-rejection process. Antonov et al. (2009) found that eastern olivaceous warblers Hippolais pallida pecked the experimental egg very often, but they did not always eject it because of physical restrictions that made ejection harder, such as the impossibility shown by olivaceous warblers to puncture strong egg shells. But acceptance of previously recognized eggs is not always the outcome of ejection failure, as was revealed by the fact that some host species such as rufous-tailed scrub robins, which can easily eject parasitic eggs, frequently peck the experimental egg but they finally accept it (Soler et al. 2012b). According to the authors, acceptance may occur if hosts do not have the necessary motivation to assume the potential costs associated with egg ejection, perhaps due to a low risk of parasitism in the area. Thus, an increase in potential costs of egg ejection would lead to higher acceptance rates, even if hosts have previously recognized the parasitic egg. Recent studies have experimentally demonstrated that hosts can decide to accept foreign eggs due to physical constraints imposed by certain characteristics of the parasitic egg that do not affect recognition but hinder egg ejection (Ruiz-Raya et al. 2015; Soler et al. 2017).
3 Why Have Flexible Defences Evolved in Hosts?
Evidence of flexible behaviours described in the previous section reveals that hosts can adjust their response to the current conditions of brood parasitism. But what ecological conditions make plastic responses adaptive for hosts? Why have plastic responses been described in just a few host species? Behaviour, like any phenotypic trait, is either favoured or penalized by natural selection as a result of a fitness trade-off between associated costs and benefits under certain ecological contexts. However, ecological conditions are often highly variable, and no behavioural trait can be considered consistently optimal, so behavioural plasticity will allow individuals to track rapid environmental changes and respond appropriately. According to Mery and Burns (2010), the evolution of behavioural plasticity requires four conditions: (1) environmental heterogeneity, (2) reliable cues, (3) that benefits of plasticity outweigh the costs, and (4) the existence of genetic basis to plasticity. Throughout this section, we will discuss the importance of these conditions for the evolution of plastic responses by hosts.
3.1 Environmental Heterogeneity
Environmental changes force both individuals and populations to rapidly respond and adapt to the current ecological context. This response may occur through genetic changes within populations resulting from microevolutionary processes guided by natural selection. However, environmental heterogeneity sometimes involves variation on such a fine spatiotemporal scale that individuals respond too rapidly to represent genetic changes within populations. Brood parasite populations are usually variable in space and time, so hosts are likely to experience wide fluctuations in parasitism rates. This variation would make phenotypic plasticity adaptive for hosts and would explain the presence of plastic responses in some host populations. For example, populations of common cuckoo parasitizing reed warblers are usually restricted to small patches in wetland, which makes them prone to local extinction; as a consequence, parasitism rates frequently vary between reed warbler populations and years (Lindholm 1999). On the other hand, after dispersion, young reed warblers probably occupy territories where the rate of parasitism will be different from that suffered by their parents. But variation in risk of parasitism may also result from annual cuckoo movements among host populations, which might be an adaptive behaviour allowing cuckoos to increase the probability of finding naïve hosts with less effective defences (Lotem et al. 1995; Langmore et al. 2009a, 2012). Recently, the existence of spatiotemporal variation in host use due to habitats constraints has been revealed in the great spotted cuckoo, indicating that parasitism pressure differs among environments for host species (Baglione et al. 2017). Given this temporal and spatial heterogeneity in parasitism rates, hosts would benefit from the ability to assess changes in the local risk of parasitism and adjust their defences accordingly, leading to the emergence of behavioural plasticity in some host populations.
3.2 Reliable Cues of Parasitism
The ability to rapidly respond to variations in parasitism conditions implies that hosts effectively assess the risk of parasitism in their area. Thus, the evolution of plastic defences requires the use of reliable cues that make possible an accurate monitoring of changes in the risk of parasitism. But how do hosts assess the risk of parasitism to which they are subjected? Hosts might assess the risk of parasitism from direct encounters with parasites. Several studies have found that some hosts increased their rejection rate after observing the parasite near the nest (Davies and Brooke 1988; Moksnes et al. 2000; Bartol et al. 2002); however, this response has been documented in a few species, while, in other cases, the presence of the parasite does not seem to be enough to modify the host behaviour (Lindholm 2000; Soler et al. 2012a). Furthermore, some brood parasites such as the cuckoo show secretive habits that make encounters with parasites unlikely (Davies 2000), as well as cuckoo-hawk mimicry makes any inspection approach potentially lethal to hosts (Davies and Welbergen 2008; Welbergen and Davies 2011). Another possibility is that hosts are able to assess the activity of parasites in their own territories and adjust their behaviour based on such information. Brooke et al. (1998) evaluated the effect of proximity to naturally parasitized nests, where parasite activity will be easier to detect, on the rejection rate of reed warblers. Although they did not find greater rejection rates in nests located near parasitized nests, reed warblers from a small unparasitized population just 11 km away did not show rejection behaviour, which suggests that hosts were able to track the cuckoo activity. Given the scarce and potentially risky nature of direct encounters with parasites, it has been suggested that some hosts may use both direct and indirect cues to assess specific risk of parasitism. Welbergen and Davies (2012) found that nest defence by reed warblers declined with distance to potential cuckoo perches (indirect cue), places from where cuckoos usually locate the host nests and whose distance to the host nest is related to the risk of parasitism (Øien et al. 1996). Interestingly, this effect was found both in parasitized and unparasitized sites, suggesting that direct cues of parasitism, such as the cuckoo presence, can be modulated by the use of indirect cues (Welbergen and Davies 2012).
The existence of reliable cues of parasitism is therefore a necessary condition for the evolution of plastic defences, which could explain the lower degree of plastic responses shown by hosts of other brood parasites. As was suggested by Thorogood and Davies (2013), the degree of specialization between the common cuckoo and its hosts is so high that parasite activity may be a more reliable cue for cuckoo’s hosts than for hosts of more generalist parasites. For instance, parasite activity alone might not be a reliable indicator of the risk of parasitism for any particular host species of the brown-headed cowbird given the more generalist nature of this brood parasite, which could difficult the evolution of plastic responses in these host species. It is clear (Table 25.1) that documented cases of plasticity in brown-headed cowbird hosts are much scarcer (only three species) than in common cuckoo hosts (seven species). This should not be surprising considering that most cowbird hosts are acceptors and phenotypic plasticity would be adaptive later, once egg-rejection ability has evolved and, mainly, when the risk of parasitism is highly variable (Soler 2014).
3.3 Benefits and Costs of Plastic Responses
Evolution of behavioural plasticity in host responses is necessarily subject to a trade-off between costs and benefits of plasticity, which explains the current variation in the occurrence of flexible defences among species, populations or individuals. As suggested above, benefits of phenotypic plasticity become noticeable in changing environments, so environmental variation is considered the main selective force for phenotypic plasticity (Moran 1992; Ghalambor et al. 2007; Hendry 2016). Regarding behaviour, we can differentiate two forms of plasticity. On the one hand, activational behavioural plasticity, or “innate” plasticity, allows individual to express a particular behaviour in response to the external context, so that, different environmental conditions will result in the expression of different behaviours (Snell-Rood 2013). Developmental behavioural plasticity, on the other hand, refers to the expression of different behavioural phenotypes in different contexts as a consequence of different developmental trajectories, which includes modifications of behaviour as a result of experience (learning) (Mery and Burns 2010; Snell-Rood 2013). The characteristics of the environmental variation will determine the relative benefits of each of these two types of behavioural plasticity. When individuals have to cope with variations within their lifetime, reversible activational plasticity will be favoured. In contrast, in those situations where environmental variations occur between generations or exceed the dispersal capacity of individuals but remain relatively constant within generations, learning costs would be minimized and irreversible plasticity would be favoured (Mery and Burns 2010; Snell-Rood 2013). Some host species may experience significant variations in the rate of parasitism throughout their lifetime, so evolution could favour the appearance of flexible responses (reversible) in such species. On the other hand, when the parasitism pressure remains stable over time, the level of defence could be maintained in the population according to such invariable risk of parasitism (Zölei et al. 2015).
As we mentioned, behavioural plasticity has been proved to be advantageous for hosts when facing environments with variable risk of parasitism. So why do most host species lack this capacity? Given that no trait is infinitely or ideally plastic, the most likely response is that there are restrictions both for the evolution of plasticity and for its maintenance. Studies on the evolution of phenotypic plasticity have suggested the existence of two main types of constraints on the evolution and maintenance of plasticity: costs, which lead to lower fitness when a feature is produced through plasticity rather than constitutively, and limits, referring to the impossibility of reaching the optimal trait value (DeWitt et al. 1998; Murren et al. 2015). Specifically, costs linked to activational behavioural plasticity may be related to the maintenance of the sensory and regulatory mechanisms to detect environmental changes and a further development of possible motor responses (Snell-Rood 2013). Unlike activational behavioural plasticity, which is usually an immediate response to environmental variations, selection of developmental behavioural plasticity, in particular learning, is usually linked to a trial-and-error process. This involves a period of suboptimal behaviour that is usually costly since it requires a considerable investment in time and energy, as well as making errors, what is known as “costs of being naïve” (Mery and Burns 2010; Snell-Rood 2013). In addition, learning has been also shown to involve important constitutive costs since it requires a remarkable neurobiological and morphological reorganization (Mery and Burns 2010). Therefore, if environmental conditions fail to favour phenotypic plasticity, the costs of plasticity per se could lead to the loss of plastic responses.
Individual experience can enhance the host ability to respond against brood parasitism and results in more effective defences. In some cases, experience is the result of the interaction with other individuals, which can also modify the behaviour and lead to plastic responses. It has been suggested that social transmission of defences (social learning) represents an additional factor in the rapid acquisition of defences by some hosts. For instance, social learning is especially important in the transmission of mobbing behaviour towards cuckoos in reed warblers, which acquire information by observing conspecific from adjacent territories (Davies and Welbergen 2009; Campobello and Sealy 2011). These cues will allow hosts to track fine-scale variations in parasitism risk and respond accordingly in future encounters with parasites. In the case of egg rejection, a similar mechanism of social transmission is unlikely to evolve due to the difficulty for individuals to witness an egg-rejection event on the part of their conspecifics. However, other mechanisms of social transmission have been suggested to explain the extraordinarily rapid increase in rejection rates observed in some host species. Such mechanisms might be based on communicative systems, and they would be especially important in species with remarkable cognitive abilities such as the common magpie or the azure-winged magpie (Soler 2011); however, further studies are needed to prove the existence of such mechanisms. Unlike individual learning, social transmission of defences would allow hosts to track environmental changes in risk of parasitism while avoiding the potential costs associated with trial-and-error processes (Mery and Burns 2010).
3.4 Genetic Basis of Plasticity
Since phenotypic plasticity is a property of genotypes and it is subject to evolution, an underlying genetic basis would be expected in those host species showing plastic responses. From a general point of view, three models have been proposed to address the genetic basis of plasticity (Scheiner 1993): (1) overdominance, which states that plasticity is an inverse function of heterozygosity; (2) pleiotropy, which states that plasticity comes from the differential expression of genes in different environments; and (3) epistasis, which predicts that plasticity results from the interaction between genes that determine the magnitude of the response to environmental factors with genes that determine the mean expression of a trait. Empirical studies reveal that, while there is little evidence for the overdominance model, both pleiotropic and epistatic effects have been proved important in any plastic response, just as is probably the case with most of the phenotypic complex traits (Scheiner 1993; Pigliucci 2005). Therefore, current evidence suggests that specific properties of genotypes could favour the evolution of plastic responses also in hosts of avian brood parasites.
4 The Egg-Rejection Process: Decision-Making and the Role of Motivation
The lack of egg rejection exhibited by some host populations has been considered one of the most puzzling issues in the study of brood parasitism (Stokke et al. 2005), especially considering the high fitness costs linked to rearing the chick of many brood parasites. Over the last few decades, several hypotheses have been proposed to explain the acceptance of parasitic eggs within the framework of the coevolutionary arms race between brood parasites and hosts. Sometimes, lack of rejection might reflect an initial stage in the arms race between brood parasites and hosts resulting from a recent parasitism, so hosts would not have had enough time to evolve egg-rejection defences [evolutionary-lag hypothesis (Rothstein 1990; Davies 2000)]. Another possibility is that acceptance is adaptive under certain circumstances, which would occur whenever costs of maintaining egg rejection are higher than costs of parasitism [evolutionary-equilibrium hypothesis (Lotem et al. 1992, 1995; Lotem and Nakamura 1998)]. According to the metapopulation dynamics theory, the presence of acceptors within specific populations might also be due to gene flow of “acceptor alleles” from non-parasitized populations (Martínez et al. 1999; Soler et al. 1999a), as a possible consequence of the spatial structure of habitats (Røskaft et al. 2002, 2006). In other cases, the evolution of cryptic eggs by the parasite has prevented hosts to evolve recognition abilities, as occurs in some Australian cuckoos (Brooker et al. 1990; Langmore et al. 2009b). In addition, as some traits of parasite eggs such as the eggshell thickness can make ejection difficult, some species could accept due to the impossibility to puncture the parasitic egg, which would imply rejection failures instead of recognition failures (Antonov et al. 2009). On the other hand, egg acceptance could also be due to successful frontline defences blocking the evolution of egg-rejection behaviours (Britton et al. 2007). But there is one last possibility to be considered: in some cases, the absence of egg rejection might reflect acceptance decisions, which means that some hosts choose to accept the parasitic egg even after recognition (Soler et al. 2012b, 2017; Ruiz-Raya et al. 2015). Under this framework, host decision-making would play a central role in the egg-rejection process, being affected by the interaction of multiple elements such as clutch characteristics, recognition abilities of host, the presence of conditional stimuli and the host genotype (Stokke et al. 2005). The study of cognitive phenotypes in a “judgement and decision-making” framework has been suggested as an important point to gain a better understanding of the processes guiding animal decisions in behavioural ecology studies (Mendelson et al. 2016), which also includes egg-rejection studies in brood parasite–host systems (Ruiz-Raya and Soler 2018). Egg rejection can therefore be understood as a complex and potentially plastic process in which different stages are differentiated, namely, judgement, decision and action itself.
4.1 Judgement
Judgements allow hosts to arrive at an understanding of the environment, which is necessary to carry out a specific response towards the parasitic egg. Thus, egg rejection requires that hosts successfully assess information and realize that their nests have been parasitized; that is, recognition of the parasitic egg must occur. As suggested by Ruiz-Raya and Soler (2018), egg-rejection studies require the use of a unified and consistent terminology in which terms such as egg recognition deserve to be properly differentiated from other cognitive abilities affecting judgement, such as discrimination, categorization or evaluation. According to the authors, egg discrimination refers to the cognitive process by which hosts can distinguish two or more different stimuli from the parasitized clutch, and it therefore relies on the intensity of the stimulus and lead to the signal detection needed to initiate the decision-making process (Rodríguez-Gironés and Lotem 1999). Otherwise, egg recognition can be considered as the process leading to the host response, which implies that host has been able to identify the odd egg as a parasitic egg. Certain characteristics of the cognitive stimulus, such as the mimicry of the parasitic egg or the degree of intraclutch variation are determining factors that affect the host judgement. Thus, highly mimetic parasitic eggs will hinder egg discrimination, whereas high intraclutch variation will increase the likelihood of committing recognition errors (Stokke et al. 2005). On the other hand, cognitive abilities of hosts can also significantly affect egg recognition. Such cognitive abilities will be determined by the host genotype, and, at the population level, egg rejection will be partly affected by the frequencies of different genotypes present in that population. In accordance with the existing parasitism pressure and rejection costs, natural selection will favour or penalize certain genotypes and, along with metapopulation processes such as gene flow or drift, will determine the frequencies of “rejecters” and “acceptors” within populations. When the cognitive stimulus (i.e. the signal) is weak and/or the host’s cognitive abilities are not fine enough, the egg-rejection process can be wrecked in the recognition stage, and the outcome of the egg-rejection process will be egg acceptance.
4.2 Decision
Once the parasitic egg is recognized, hosts must choose among two different options before carrying out the action itself: they have to decide between acceptance and rejection of the parasitic egg. But how do individuals determine which strategy is optimal? During the decision stage, some hosts are able to integrate information from the judgement with that derived from conditional stimuli in a process that will determine their “tendency to rejection” or motivation. Motivation is revealed as a crucial concept in the psychology of decision-making, and it can be understood as the host’s tendency to assume the potential costs of egg rejection under certain parasitism conditions (i.e. trade-offs between costs of egg rejection and risk of parasitism) (Soler et al. 2012b). As previously seen, some hosts vary their response to parasitism according to the current risk of parasitism, their experience or the stage of the breeding season, which leads some of them to accept the parasitic egg. Of course, judgement and decision are deeply linked in the decision-making process since they both depend on the accuracy with which hosts evaluate the available information about parasitism. The combination of prior and new information will allow hosts to improve the evaluation of their current situation, a process known as “Bayesian updating” (Piersma and Gils 2011). As will be seen in the following section, the assessment of these potential costs is continuously updated, even in the last stage of the egg-rejection process (action itself), which can also significantly influence decision-making as it could result in new judgements and therefore new decisions.
4.3 Action
Action is the last stage of the egg-rejection process, and it can be defined as the specific behaviour resulting from the host decision-making. The egg-rejection process can also be interrupted in this last stage since some physical characteristics of parasitic eggs make ejection particularly hard. For example, unusual strong shells can make ejection difficult to small hosts (puncture ejectors) and can force the acceptance of previously recognized eggs (Antonov et al. 2009). During the action stage, hosts can assess the potential costs of ejection by gathering information on the physical characteristics of the parasite egg that may hinder ejection. For instance, Soler et al. (2012b) suggested that some hosts use weak touches to the parasitic egg as a mechanism to assess the shell strength and therefore the potential costs of egg puncture ejection. These behaviours contribute to the Bayesian updating process and allow hosts to add new information to the prior information on parasitism conditions, which might lead to new judgements and therefore modify the outcome of the decision-making process (Fig. 25.2). In this context, a low risk of parasitism would involve insufficient motivation to assume potential ejection costs, resulting in acceptance decisions. However, when the conditions of parasitism make the host’s motivation higher, hosts could increase the strength and frequency of their pecking in order to puncture the parasitic egg, assuming the possibility of breaking one of their own eggs in the attempt. At this point, if puncture ejection is not possible, higher motivation would be required to desert the nest as it is a much more costly strategy [see Fig. 6 in Soler et al. (2012b)]. In grasp ejectors, who eject the parasitic egg by grasping it with the beak and taking it out of the nest, the action stage can be affected by other egg traits such as egg size or mass. In fact, it has been recently shown how such traits can lead to acceptance of previously recognized eggs, or a delay in rejection decisions, when host motivation is not enough (Ruiz-Raya et al. 2015; Soler et al. 2017).
5 Phenotypic Plasticity and Brood Parasite–Host Coevolution
The existence of plastic responses makes it possible for individuals to rapidly respond to changes in ecological conditions affecting their environment. Importantly, these ecological conditions include phenotypes of other individuals with which they interact, so phenotypic plasticity has important consequences on both the strength of ecological interactions and the evolutionary trajectories of the species involved (Agrawal 2001; Fordyce 2006). In brood parasite–host interactions, the existence of fine-tuned plastic responses (i.e. close to the optimal phenotype) would allow some hosts to successfully respond to changes in parasitism pressure within populations. When a host is able to rapidly reach optimal behaviour after increases in parasitism rates, parasite fitness will be affected, and the potential outcome might be the host switching or the local extinction of the brood parasite. Phenotypic plasticity would allow certain hosts species, such as reed warbler, to retain their rejection abilities after periods of low parasitism pressure, even when the expression of their defences is reduced (Lindholm and Thomas 2000; Stokke et al. 2008; Thorogood and Davies 2013). This will make it difficult for a future reutilization of the host population by brood parasites since hosts will be able to rapidly respond to changes in the parasitism pressure.
However, although plastic responses have been documented in several host species, phenotypic plasticity in egg rejection seems to be the exception rather than the rule. In most host species, rejection behaviour is a fixed trait retained in the absence of brood parasitism (even after speciation events; see references above), and continuous coevolutionary cycles have been shown to be absent in some brood parasite–host systems (Soler et al. 1998; Rothstein 2001; Peer et al. 2007). In fact, recent evidences have emphasized that the absence of coevolutionary cycles is the most frequent situation in host–brood parasite systems (Soler 2014). So what role does phenotypic plasticity play in most host species? Phenotypic plasticity is crucial to tolerate and then adapt to new environmental conditions, allowing populations to move more easily to another adaptive peak (Price et al. 2003; Ghalambor et al. 2007). Therefore, plastic responses would be especially important in the early stages of brood parasitism (Soler 2014), allowing hosts to benefit from the ability to adjust their behaviour to the new selection pressure. As long as the risk of parasitism is variable and unpredictable, hosts that show plastic responses will have higher fitness than those that do not, and phenotypic plasticity will be adaptive. By contrast, if the pressure or virulence of parasitism increases and is maintained over time, plastic responses may cease to be adaptive because of the costs of phenotypic plasticity itself, which would favour the evolution of the canalized phenotype (Pigliucci et al. 2006; Soler and Soler 2017), and the rejection behaviour would be fixed. This loss of plasticity can be understood as an alteration in the reaction norm (i.e. a flat reaction norm) derived from selection operating only in the new environment (Pigliucci et al. 2006; Ghalambor et al. 2007). In the absence of parasitism, the evolution of relaxed fixed host defences as response to reduced risk of parasitism will lead to coevolutionary cycles (Nuismer and Thompson 2006). However, egg-rejection behaviour will be maintained unless recognition errors and rejection costs are high, and recent studies have shown that the occurrence of such errors is low among host species (Stokke et al. 2016). Therefore, the maintenance of egg-rejection abilities shown by many species over long periods of time indicates that costs associated to the maintenance of such antiparasitic defence are insignificant, which has important implications in the evolutionary trajectory of brood parasites and their hosts: coevolutionary cycles are replaced by successful resistance as the main outcome of brood parasite–host coevolution (Rothstein 2001; Soler 2014). In fact, when the coevolutionary trajectories of brood parasite–host systems are reviewed, it was found that first, fixed responses and absence of coevolutionary cycles are frequent in host-brood parasite systems and, second, the few species showing phenotypic plasticity in their responses are usually involved in coevolutionary cycles, probably reflecting initial stages of parasitism (Soler 2014). According to Soler (2014), coevolutionary cycles are likely an intermediate phase of the interactions between brood parasites and their hosts, whose outcome will be the extinction or the acquisition of successful resistance by the host, forcing parasites to specialize in less suitable host species.
In some cases, phenotypic plasticity results in the emergence of reciprocal phenotypic changes among players in ecological interactions, which has important evolutionary implications (Agrawal 2001). In brood parasite–host systems, mathematical models suggest that emergence of some parasites’ strategies such as mafia behaviour might be promoted by the host’s plastic responses (Chakra et al. 2014). When retaliation occurrence is moderate, plastic responses will be beneficial for hosts and, at the same time, brood parasites will benefit from the existence of such plastic responses to force the acceptance of the egg parasites by punishing rejecter individuals. As the mafia strategy expands in the population, hosts would benefit from unconditional acceptance of parasitic eggs, leading the parasite population back to a non-mafia strategy. Thus, the occurrence of the mafia strategy within parasite population will oscillate in time, and plastic host responses would be crucial for its evolution. The magpies’ ability to express plastic defences is a determinant of the evolution of plastic virulence in parasites (e.g. retaliatory behaviours), while the existence of such plastic virulence will favour the maintenance of plastic defences in hosts (Soler and Soler 2017, Chap. 15).
Concluding Remarks and Future Directions
In this chapter, we have seen how some host species are able to modify their egg-rejection behaviour according to the perceived risk of parasitism, which reveals the existence of plastic defences against brood parasitism. Such plastic responses are favoured by natural selection under highly variable risk of parasitism since it allows hosts to avoid the expression of costly defences when the risk of parasitism is low. Future work should address the mechanisms used by hosts to accurately assess the risk of parasitism in their sites, which is crucial for the evolution of plastic defences. In addition, further studies should focus on the costs and limitations linked to the host plastic responses, which will determine the maintenance or loss of plasticity under low parasitism pressure. From a general perspective, studies on brood parasite–host coevolution should consider the potential effects of phenotypic plasticity on both the maintenance of host defences over the time and the long-term outcome of ecological interactions. Recent evidence that some potential host species may recognize more eggs than they eventually reject indicates that egg rejection can be viewed as a complex process in which multiple components interact and where decision-making and host motivation play a central role. Interestingly, the existence of phenotypic plasticity remains untested in many potential host species, so egg recognition experiments in different populations and/or under different risk of parasitism need to be carried out in most host species. These results, when available, will open a new avenue of research in which comparative studies would allow to answer crucial questions about the evolution of egg rejection. More work is also required to clarify the possible role of social learning on the defence acquisition by hosts and its importance on egg rejection. Finally, in view of the significant decline experienced by some parasites during the last years, phenotypic plasticity will be crucial to understand how host populations adapt to such changing environment.
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We greatly thank Naomi Langmore and Brian Peer, who provided useful comments which significantly improved this chapter.
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Ruiz-Raya, F., Soler, M. (2017). Phenotypic Plasticity in Egg Rejection: Evidence and Evolutionary Consequences. In: Soler, M. (eds) Avian Brood Parasitism. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-73138-4_25
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