Behavioral Ecology Vol. 14 No. 6: 917-923
© 2003 International Society for Behavioral Ecology
The impact of learning foster species' song on the evolution of specialist avian brood parasitism
Institute of Evolutionary and Ecological Sciences, Leiden University, Kaiserstraat 63, 2311 GP Leiden, The Netherlands
Address correspondence to J.B. Beltman. E-mail: beltman{at}rulsfb.leidenuniv.nl.
Received 7 August 2002; revised 23 January 2003; accepted 5 February 2003.
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ABSTRACT |
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Obligate interspecific avian brood parasites do not build nests of their own but lay their eggs in the nests of other species. It has been proposed that a flexible song learning mechanism (copying the heterospecific songs of the foster species) facilitates the evolution of brood-parasitic behavior. Some sort of song copying is common to all songbirds; hence, to better understand the evolution of brood parasitism it is important to study the role of song learning. The proposed hypothesis does not take into account that flexible song learning might make mate acquisition more difficult because males that are preferred by brood-parasitic females would be initially rare. We examine this by means of two population dynamic models. By using a recurrence equation model of brood parasites competing with their nestbuilding ancestors, we show that flexible song learning is indeed an obstacle to the evolution of brood parasitism. Results from a more realistic, individual-based model, in which the brood-parasitic trait can evolve more gradually, confirm this finding. However, we also show that the obstacle of flexible song learning can be overcome quite easily when males also are carriers of the brood-parasitic trait. This is probably because brood parasitism is a neutral trait in males, which increases the number of mutants carrying genes for brood parasitism, and thus makes the female task of finding suitable partners easier.
Key words: brood parasitism, sexual imprinting, song learning, Viduidae.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMODELSRESULTSDISCUSSIONREFERENCES |
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It has been estimated that about 1% of all bird species are interspecific brood parasites who do not build nests of their own but lay their eggs in the nests of other species (Payne, 1977
). Most of the studies on brood parasitism have focused on the costs and benefits of parasitism (Winfree, 1999; Payne, 1997), on the arms race between host and parasite (Davies, 2000; Takasu et al., 1993), and on the possible starting points of the evolution of brood parasitism (facultative conspecific brood parasitism, cooperative nesting, the use or takeover of nests of other species; Payne, 1977; Robert and Sorci, 2001; Slagsvold, 1998; Sorenson and Payne, 2001; Yamauchi, 1995).
An issue that received relatively little attention is the possible influence of learning processes like sexual imprinting and song learning on the evolution of brood parasitism. Sexual imprinting is the acquisition of mate preferences through learning the characteristics of parents or siblings early in life (Lorenz, 1937). It is widespread among birds (ten Cate and Vos, 1999) and has been suggested as playing a major role in evolutionary processes such as hybridization (ten Cate and Vos, 1999), sexual selection (Laland, 1994b; ten Cate and Bateson, 1988), and speciation (Aoki et al., 2001; Grant and Grant, 1997; Irwin and Price, 1999; Laland, 1994a; Owens et al., 1999).
Some researchers have suggested that because brood parasites are raised by another species, sexual imprinting will affect the future behavior of the cross-fostered young (Payne et al., 2000; Rowley and Chapman, 1986; Slagsvold, 1998). For instance, the young might obtain a preference for visual characteristics of the foster species and, as a result, have difficulties in finding a suitable partner. For this reason, sexual imprinting could form an obstacle to the evolution of brood parasitic behavior (Slagsvold and Hansen, 2001; Sorenson, 1994). A possible solution to the problem of finding a conspecific partner is to imprint on the song characteristics of the foster species (ten Cate and Vos, 1999). For males, this would mean learning to produce the heterospecific songs; for females, learning to recognize and prefer these songs. Such song learning might be a solution because males cannot adopt the visual characteristics of the foster species, but they could learn to sing the heterospecific songs of the foster species and thus attract conspecific females who are imprinted on these heterospecific songs. The latter situation occurs in finches of the genus Vidua (whydahs and indigobirds), which are African songbirds that parasitize estrildid finches. At a young age, the males copy the songs of their foster father (Payne, 1973a; Payne et al., 1998), and the females develop a mating preference for males singing a song resembling that of their foster father (Payne, 1973b; Payne et al., 2000). Furthermore, mature females preferably lay their eggs in the nests of individuals that sing songs similar to those of their foster father (Payne et al., 2000).
Learning heterospecific songs was suggested to have played a role in two evolutionary processes in the Viduidae: (1) it may have been the mechanism responsible for fast speciation because it enabled the colonization of new host species (Klein and Payne, 1998; Payne, 1973a; Payne and Payne, 1995; Payne et al., 1998, 2000; Sorenson and Payne, 2001; ten Cate, 2000), and (2) it may have promoted the evolution of brood-parasitic behavior according to the following hypothetical scenario (Nicolai, 1964; ten Cate and Vos, 1999). Initially, a few females laid some eggs in the nests of another species instead of building their own nests. Assuming that the eggs were accepted and the young chicks were raised by the species owning the nest, the cross-fostered males copied the heterospecific songs, and the females developed a preference for males singing heterospecific songs. Consequently, when the males and females attained adulthood, they chose each other as mates, maybe after having been rejected by the foster species. Furthermore, cross-fostered females were biased to lay their eggs in the nests of the foster species. The result of these hypothetical events would be an interspecific brood-parasitic species that is intimately associated with its host species.
An obvious question that comes to mind when considering the latter hypothetical scenario is whether this mechanism has played a role in Viduidae. However, we are interested in the more general question of whether flexible song learning can indeed promote the evolution of specialist brood-parasitic behavior. This is important to investigate because some sort of song copying is common to all songbirds (passerines). Many songbirds have the ability to learn to produce heterospecific song, although they may still have a perceptual bias for conspecific song when given the choice between two songs, at least in tape-tutoring experiments (Marler and Sherman, 1985; Marler and Peters, 1988; Nelson, 2000; Whaling et al., 1997; Soha and Marler, 2000). The mentioned scenario presumes that among specialist brood parasites, preference for heterospecific song facilitates mate finding. However, even though flexible song learning may facilitate mate finding when compared with sexual imprinting on visual characteristics in such species, mate acquisition may still be more difficult than in a species in which recognition of conspecifics is based on some nonlearned mechanism. This might be owing to the initial scarcity of males singing heterospecific songs, which are preferred by brood-parasitic females. Species that do not learn their song, or that have such a strong perceptual bias that they will only learn conspecific song, may have fewer difficulties in finding a mate.
In this article, we study the influence of flexible song learning on the evolution of specialist brood-parasitic behavior, by using population dynamical models. We compare model predictions for species that vary in the flexibility of song learning. The model parameter that represents song learning flexibility refers to hypothetical species in which (1) song is learned from foster parents (complete flexibility), or (2) there is a perceptual bias for conspecific song. The model for the latter situation is identical to a model for situations in which song is not learned at all (as in the nonpasserine, brood-parasitic cuckoos), or for situations in which song learning is extended until independence from the foster parents (as in brood-parasitic cowbirds). The results of a recurrence equation model and an individual-based simulation model show that flexible song learning forms an obstacle to the evolution of brood-parasitic behavior, because brood-parasitic females would find partners less easily. However, the obstacle can be overcome quite easily when males also are carriers of the brood-parasitic trait.
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MODELS |
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Recurrence equation model
The model considers a population of a bird species that consists of a mixture of birds that build nests of their own (nestbuilders) and birds that are brood-parasitic. A population of a second species consists of hosts of the brood parasites. The host species is not modelled explicitly: It is assumed that there are always nests available for parasitization. The aim of the model is to investigate under what conditions the brood parasites can maintain themselves in the population, while competing with the nestbuilders. We assume non-overlapping generations, although this assumption does not influence the results qualitatively (data not shown).
Brood-parasitic (or nestbuilding) behavior of the young is inherited from the mother. It is assumed that there exist no individuals that only occasionally behave as a brood parasite. In the individual-based model (see below), we will relax both assumptions.
Each bird is characterized by a particular song, which can be either conspecific or heterospecific. Males express their song by singing; females, by having a mating preference for males singing their song. Females always mate with encountered males that sing the preferred song, and they mate with chance m with encountered males that sing the nonpreferred song (0 
m 1). Hence, the relative preference of females for males singing their favorite song is 1/m.
Newborns either learn the song of the father who raises them, with chance s, or learn the conspecific song, with chance 1 - s. For a species in which song learning is maximally flexible (heterospecific song is always learned when raised by a foster parent), s = 1, whereas s < 1 represents a species in which a perceptual bias to learn conspecific song is present. An increase in s can be interpreted as more flexible song learning or, in other words, as a weaker perceptual bias for conspecific song. Note that at s = 0 (when the effect of the perceptual bias is strongest), the model corresponds to situations in which song acquisition is based on some nonlearned mechanism (as in cuckoos), or to situations in which song learning is extended until independence from the foster parents (as in cowbirds). We assume that the two processes of song production learning in males and song preference learning in females are similar (see, Riebel et al., 2002).
For mathematical convenience, we only follow the dynamics of the females and assume that those of males are equal. This means we assume that there is no differential survival between males and females and no differential production of males and females (sex ratio = 1 : 1). Nc, Nh, Bc, and Bh denote, respectively, the number of nestbuilding females with conspecific song, the number of nestbuilding females with heterospecific song, the number of brood-parasitic females with conspecific song, and the number of brood-parasitic females with heterospecific song. The numbers of males of these four types are the same as the numbers of females of these types. We denote frequencies of females (males) of the four types by corresponding lowercase letters. Furthermore, Eb denotes the number of surviving female (male) young of a brood-parasitic female; En, that of a nestbuilding female.
As an example, we will derive the equation for the frequency of nestbuilders with heterospecific song in the next generation, 
. Individuals of this type can be produced by female nestbuilders with either conspecific or heterospecific song, as long as they mate with males singing heterospecific song. We assume that the encounter chance with males of a specific type equals the frequency of such males. The expected number of matings between nest-building females with conspecific song and males with heterospecific song is mNc(nh + bh). The expected number of matings between nest-building females with heterospecific song and males with heterospecific song is Nh(nh + bh). Each mating produces En surviving females that have learned heterospecific song with chance s, so
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, , , , and subsequent simplification, Equation 3 can be rewritten to
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Individual-based model
The individual-based computer simulation model is based on similar assumptions. We assume a fixed population size of N females and N males. As before, individuals have either conspecific or heterospecific song. However, the assumption that individuals are either brood parasites or not is relaxed: individual birds are assigned a tendency p to lay their eggs parasitically.
The population is initialized with birds singing conspecific song and p = 0. Every generation, all individuals die and are replaced by newborns. The numbers of newborns of every type are determined in a similar way as in the recurrence equation model. The difference is that in that model parameters represent average population values and in the simulation model they correspond to probabilities that certain events (e.g., laying parasitically) occur. To create new young, a random pair is chosen. If they mate (which again depends on their songs and on the mating probability m), the female will produce with probability p on average Eb young, or else on average En young. This procedure is repeated until all N male and N female positions are filled up. The parasitization tendency of newborns either is inherited from the mother or is the average of both parents' p (depending on the case considered). In the latter case, the trait is obviously not expressed in males. The parasitization tendency of newborns mutates with probability µ, and the mutation step is drawn randomly from a normal distribution with average 0 and standard deviation 
. The resulting p becomes at most 1.0, and is at least 0.0. We study the evolution of p over many generations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMODELSRESULTSDISCUSSIONREFERENCES |
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Recurrence equation model
We analyzed the recurrence equation model using several approaches: We studied several equilibria and their stability analytically, used the software package Content (Kuznetsov and Levitin, 1997
) to perform a bifurcation analysis, and confirmed our results by numerical analysis. Because we are only interested in the long-term dynamical behavior, we focus on the stable equilibria. We found that the model yielded four possible outcomes regarding the stable population constitution at equilibrium: (1) all individuals are nestbuilders singing conspecific song (the Nest(con) equilibrium). Nestbuilders singing heterospecific song and brood parasites do not occur in this case. (2) Brood-parasitic birds singing conspecific song occur with frequency 1 - s and brood parasites singing heterospecific song occur with frequency s (the Par equilibrium). Nestbuilders are not present here. This equilibrium needs to be attained for brood parasitism to evolve and is thus important for the study of the hypothesis. (3) All individuals are nestbuilders singing either of the two possible songs (the Nest equilibrium). Brood parasites do not occur in this equilibrium. (4) Birds of all types exist in the population (the All equilibrium). Results are shown in Figure 1. Note that this is not the complete bifurcation diagram, because bifurcations involving unstable or negative equilibria are not included. There is some positive value for the payoff of brood parasitism (Eb/En) for which an equilibrium with brood parasites becomes stable; hence, the payoff represents a measure of the difficulty with which brood parasitism evolves. We show results for different values of m, the likelihood of mating between birds singing different songs. The parameter space is divided into areas in which different equilibria are stable (Figure 1).
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There are two regions in which one stable equilibrium is present. The other regions are bistable, which means that two equilibria are stable. Which of these will be attained depends on the initial population composition. If there is no mating preference (m = 1), either the Nest(con) equilibrium or the Par equilibrium is stable (Figure 1a). If females prefer to mate with males singing certain songs (m < 1), in addition, the Nest(con) equilibrium can be stable with either one of the three other mentioned equilibria (Figure 1b–d). Both the Nest(con) and the Par equilibrium are stable in the shaded areas of Figure 1. For high values of s and low values of Eb/En, the bistability is formed by the equilibria Nest(con) and Nest. In addition, there is a small region at intermediate values of s and Eb/En where the Nest(con) and the All equilibrium are both stable.
In areas with only one stable equilibrium, the dynamical behavior is clear: the population will evolve toward this equilibrium. In bistable regions, however, the final population composition depends on the initial conditions. Because we are studying the origin of brood parasitism, we consider what happens if the initial population consists of mostly nestbuilding birds with conspecific song and a few mutant brood parasites with heterospecific song. Although the fraction of initial mutants will be small, it is possible that the mutants accidentally increase in numbers despite having a fitness disadvantage and, consequently, reach the attracting region of another equilibrium. For very small percentages of initial mutants, the equilibrium with brood parasites can only be attained when parameter conditions are near the upper limit of the shaded areas in Figure 1. As an indication for how this changes for higher percentages of initial mutants, we show what equilibrium is attained when we start with 10% and with 50% brood parasites (see Figure 1b–d). This is only for later reference, when we compare these results with those of the individual-based model, and not because we assume them to be realistic percentages.
The main results of the recurrence equation model are (Figure 1):
- When the effect of the perceptual bias to learn conspecific song is strongest or when song learning is absent, namely, individuals sing or prefer conspecific song independent of experience (s = 0), the evolution of brood parasitism is possible only if brood parasites have more surviving offspring than do nestbuilding birds (Eb > En). This result does not depend on the mating preference 1/m.
- When song learning is more flexible (s > 0) but there is no mating preference based on song (m = 1), the condition for the evolution of brood parasitism remains Eb > En (Figure 1a).
- If there is a mating preference based on song (m < 1), then the results depend on the initial conditions as follows:
- (a) When the initial fraction of brood parasites is small, both more flexible song learning and stronger mating preferences result in more stringent conditions for the evolution of brood parasitism (Figure 1b–d, dotted lines).
- (b) When the initial fraction of brood parasites is high, the evolution of brood parasitism is most difficult for intermediate song learning flexibility, and relatively easy for extreme amounts of song learning flexibility. An increase in the mating preference makes the evolution of brood parasitism at intermediate values of s more difficult, but hardly affects the results for the extreme values of s (Figure 1b–d, dashed lines).
- (b) When the initial fraction of brood parasites is high, the evolution of brood parasitism is most difficult for intermediate song learning flexibility, and relatively easy for extreme amounts of song learning flexibility. An increase in the mating preference makes the evolution of brood parasitism at intermediate values of s more difficult, but hardly affects the results for the extreme values of s (Figure 1b–d, dashed lines).
- (a) When the initial fraction of brood parasites is small, both more flexible song learning and stronger mating preferences result in more stringent conditions for the evolution of brood parasitism (Figure 1b–d, dotted lines).
Individual-based model
Next we study whether results are the same in the individual-based model, which is more realistic because brood parasitism can evolve more gradually in a mutation and selection process. We start simulations with all individuals being "pure" nestbuilders (p = 0) singing conspecific song. During evolution, mutants having different parasitization tendencies can occur, and they will accidentally increase or decrease in numbers. For this reason, the attracting region of the Par equilibrium might be reached. We calculate the average p that evolves after many generations for different parameter values (Figure 2). The parasitization tendency is inherited either from the mother (Figure 2a–d), or from both parents (Figure 2e–h).
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The first two results of the individual-based model are the same as results 1 and 2 of the recurrence equation model (Figure 2). Additional results of the individual based model are (Figure 2):
- Although during simulations individuals can have intermediate parasitization tendencies, after many generations the average parasitization tendency evolves to one of the extremes. Hence, for some parameter values, p evolves to approximately one, for others it remains close to zero. This is clearest when p is inherited from the mother (cf. the greyness of Figure 2a–d and Figure 2e–h).
- If there is a mating preference based on song (m < 1), then the results depend on the inheritance mode of p as follows:
- (a) When p is inherited from the mother, the evolution of brood-parasitic behavior is more difficult when song learning is more flexible and when the song-based mating preference is stronger (Figure 2a–d).
- (b) When p is inherited from both parents, the evolution of brood parasitism is most difficult for intermediate song learning flexibility, and relatively easy for extreme amounts of song learning flexibility (Figure 2e–h).
- (b) When p is inherited from both parents, the evolution of brood parasitism is most difficult for intermediate song learning flexibility, and relatively easy for extreme amounts of song learning flexibility (Figure 2e–h).
- (a) When p is inherited from the mother, the evolution of brood-parasitic behavior is more difficult when song learning is more flexible and when the song-based mating preference is stronger (Figure 2a–d).
- Increasing the population size or decreasing the mutation frequency result in a slightly larger obstacle for brood parasitism to evolve (not shown), but qualitatively, the results do not differ.
The results of the individual-based model are consistent with the recurrence equation model: Brood parasitism evolves exclusively in areas where the Par equilibrium is stable in the recurrence equation model. Furthermore, when p is inherited from the mother (Conclusion 2a), results are similar to those of the recurrence equation model when starting with a low percentage of initial brood parasites (see Conclusion 3a of those results). When p is inherited from both parents (Conclusion 2b), results are comparable to those of the recurrence equation model for a high fraction of initial mutants (see Conclusion 3b of those results).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMODELSRESULTSDISCUSSIONREFERENCES |
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We investigated how the learning of the foster species' song influences the evolution of specialist interspecific brood parasitism. Results depend on the fraction of initial brood parasites. For a small fraction of initial brood parasites, the flexibility of song learning forms an obstacle to the evolution of brood parasitism. If the initial fraction of brood parasites is large, however, the evolution of brood parasitism is most difficult for intermediate song learning flexibility. In evolutionary processes, there will normally be only a few mutants. However, we showed that a similar effect occurs if males carry (but do not express) the trait to lay eggs parasitically, which is probably owing to selection on the males. Because p is not expressed in males, there is no direct selection on this characteristic: a mutant male will, on average, have the same fitness as a resident male. Only when the parasitization tendency of a mutant male is passed on to his daughters, does selection occur. As a consequence, mutants can substantially increase in numbers, and the attracting region of another equilibrium will be more easily reached. In the same way, the neutrality of p in males can explain why the average parasitization tendency that evolves is not exactly zero or one (Figure 2e–h).
Several investigators have suggested the opposite of our findings, namely, that flexible song learning promotes the evolution of specialist brood-parasitic behavior (Nicolai, 1964; ten Cate and Vos, 1999). However, they did not take into account that brood parasites are initially in the minority and that this decreases the chance to meet a preferred partner if song learning is more flexible. Our results confirm that this is an obstacle, and the disadvantage for brood parasites is larger if the song-based mating preference is stronger. This result relies on the assumption that female choosiness entails a cost that depends on the frequency of the preferred males. Female choosiness is often assumed to be costly, although the cost is not always assumed to depend on male frequencies (Gavrilets and Boake, 1998; Hall et al., 2000; Higashi et al., 1999; Janetos, 1980; Pomiankowski, 1987; Takimoto et al., 2000). In the case we study, this seems a reasonable assumption, because the conspecific and heterospecific songs are very different, which is likely to result in a high reluctance of females to mate with males singing nonpreferred songs. The exact form of the preference function we used assumes that choosiness is extremely costly to females. We also studied a variant of the presented models in which the cost of being choosy was absent (data not shown). As expected, in that case the flexibility of song learning had no effect on the evolution of brood-parasitic behavior, independent of the mating preference (results are always as in Figure 1a). Both these extreme cases are not very realistic. The cost of being choosy will depend on male frequencies, but the effect of male frequencies could be less than assumed here. This would, for example, be the case when females have a long search time for mates, or if adult birds tend to stay close to their native territory. On the other hand, females may also mistakenly approach heterospecific males, which reduces the encounter frequency with conspecific males. Although we ignored these effects in this article, other mate preference functions will not change our results qualitatively as long as they incorporate that female choosiness is costly and that the cost depends on male frequencies.
Vidua finches are brood parasites with a flexible song learning mechanism (they copy the heterospecific songs of the foster species). Recent molecular phylogenies (Sorenson and Payne, 2001, 2002) show that the flexible song learning of the Vidua finches may have evolved only after their brood-parasitic behavior had been established (Payne RB, personal communication). The closest relative of the Vidua finches is the cuckoo finch (genus Anomalospiza). This species is a generalist brood parasite, and it does not mimic the songs of its foster species (Davies, 2000). Furthermore, the species Vidua macroura and Vidua hypocherina, which are the basal clades in the phylogeny of the Vidua finches, are brood-parasitic but do not mimic the songs of their foster species (Klein and Payne, 1998; Nicolai, 1964).
By using our models, we compared the two possible scenarios: either flexible song learning was present from the onset of the brood-parasitic behavior (s = 1), or it evolved at a later time (s = 0). We show that if flexible song learning had been present from the onset of the brood-parasitic behavior, it would have been an obstacle for brood parasitism evolving. This fits the observation that among interspecific brood parasites, copying of the foster species' song occurs only in the Viduidae (Davies, 2000). In addition, according to our model results, it is most likely that the flexibility of song learning in the Vidua finches has evolved at a later stage than the brood-parasitic behavior.
If flexible song learning in the Vidua finches evolved only after brood parasitism had already been established, an open problem is why the song learning mechanism subsequently became more flexible. A possible explanation involves the evolution of defensive behaviors against brood parasitism by the foster species. This could be achieved by distinguishing between own and parasitic young on the basis of mouth patterns, which is known to occur in the contemporary estrildids (Payne et al., 2001). This in turn would have created a selection pressure for the brood parasites to specialize on particular host species by evolving mouth mimicry of the young. To succeed in this, mutant males and females that are better mimics of the host mouth patterns should mate with each other. A more flexible song learning mechanism may have helped in this process because it potentially generates assortative mating. Hence, flexible song learning may have evolved in parallel with mouth mimicry of the young (Payne RB, personal communication). Once the flexible song learning mechanism was in place, it may have been the driving force for colonisation of new host species followed by speciation (Klein and Payne, 1998; Payne, 1973a; Payne and Payne, 1995; Payne et al., 1998, 2000; Sorenson and Payne, 2001; ten Cate, 2000). The present model is not suitable for investigating these hypotheses. However, the problem that initially only few mates are available plays a role in the colonisation process as well.
In our model, the parameter s represents the strength of the perceptual bias for conspecific song. When the effect of this bias is maximally strong (at s = 0), an alternative interpretation of the model is that mate finding is based on some kind of nonlearned species recognition mechanism. This may occur in cuckoos, in which species recognition is probably based on nonlearned calls or visual characteristics. Cowbirds also belong to this category: they extend song learning until independence from the foster parents. For this reason, they probably need a nonlearned cue to find conspecifics (Hauber et al., 2001). Also, in the Vidua finches, a nonlearned cue is likely to be present, although it is not clear what this may be. Hence, it appears that in all the major bird families in which interspecific brood parasitism occurs, the evolutionary obstacle of potential misimprinting on the foster species has been circumvented by having a nonlearned species recognition mechanism. This suggests that if such a mechanism was unavailable, brood parasitism could not have evolved. Experiments by Slagsvold and Hansen (2001) and Slagsvold et al. (2002), who simulated parasitism in tits, support this idea. Such cross-fostering studies in the wild are necessary to evaluate the role of sexual imprinting and flexible song learning on the evolution of brood parasitism.
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ACKNOWLEDGEMENTS |
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We thank Marnix de Zeeuw for assistance with the simulations and Elizabeth van Ast, Andrew Bourke, Rob Lachlan, Bob Payne, and two anonymous referees for comments on the manuscript. This study was supported by the Research Council for Earth and Lifesciences (ALW), which is subsidized by the Netherlands Organization for Scientific Research (NWO).
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REFERENCES |
|---|
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TOPABSTRACTINTRODUCTIONMODELSRESULTSDISCUSSIONREFERENCES |
|---|
Aoki K, Feldman MW, Kerr B, 2001. Models of sexual selection on a quantitative genetic trait when preference is acquired by sexual imprinting. Evolution 55:25-32.[CrossRef][Web of Science][Medline]
Davies NB, 2000. Cuckoos, cowbirds and other cheats. London: T. & A. D. Poyser.
Gavrilets S, Boake CRB, 1998. On the evolution of premating isolation after a founder event. Am Nat 152:706-716.[CrossRef]
Grant PG, Grant RB, 1997. Hybridization, sexual imprinting, and mate choice. Am Nat 149:1-28.[CrossRef]
Hall DW, Kirkpatrick M, West B, 2000. Runaway sexual selection when female preferences are directly selected. Evolution 54:1862-1869.[CrossRef][Web of Science][Medline]
Hauber ME, Russo SA, Sherman PW, 2001. A password for species recognition in a brood-parasitic bird. Proc R Soc Lond B 268:1041-1048.[Medline]
Higashi M, Takimoto G, Yamamura N, 1999. Sympatric speciation by sexual selection. Nature 402:523-526.[CrossRef][Medline]
Irwin DE, Price T, 1999. Sexual imprinting, learning and speciation. Heredity 82:347-354.
Janetos CJ, 1980. Strategies of female mate choice: a theoretical analysis. Behav Ecol Sociobiol 7:107-112.
Klein NK, Payne RB, 1998. Evolutionary associations of brood parasitic finches (Vidua) and their host species: analyses of mitochondrial DNA restriction sites. Evolution 52:566-582.[CrossRef]
Kuznetsov YA, Levitin VV, 1995–1997. CONTENT: a multiplatform environment for analyzing dynamical systems. Dynamical Systems Laboratory, Centrum voor Wiskunde en Informatica, Amsterdam. Available at ftp.cwi.nl/pub/CONTENT.
Laland KN, 1994a. On the evolutionary consequences of sexual imprinting. Evolution 48:477-489.[CrossRef]
Laland KN, 1994b. Sexual selection with a culturally transmitted mating preference. Theor Popul Biol 45:1-15.[CrossRef][Web of Science][Medline]
Lorenz K, 1937. The companion in the bird's world. Auk 54:245-273.
Marler P, Peters S, 1988. The role of song phonology and syntax in vocal learning preferences in the song sparrow, Melospiza melodia. Ethology 77:125-149.
Marler P, Sherman V, 1985. Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song. Anim Behav 33:57-71.
Nelson DA, 2000. A preference for own-subspecies' song guides vocal learning in a song bird. Proc Natl Acad Sci USA 97:13348-13353.
Nicolai J, 1964. Der Brutparasitismus der Viduinae als ethologisches Problem. Z Tierpsychol 21:129-204.
Owens IP, Rowe C, Thomas AL, 1999. Sexual selection, speciation and imprinting: separating the sheep from the goats. Trends Ecol Evol 14:131-132.[CrossRef][Medline]
Payne RB, 1973a. Behaviour, mimetic songs and song dialects, and relationships of the parasitic indigobirds (Vidua) of Africa. Ornithol Monogr 11:1-333.
Payne RB, 1973b. Vocal mimicry of the paradise whydahs (Vidua) and response of female whydahs to the songs of their hosts (Pytilia) and their mimics. Anim Behav 21:762-771.[CrossRef]
Payne RB, 1977. The ecology of brood parasitism in birds. Rev Ecol Syst 8:1-28.
Payne RB, 1997. Host-parasite evolution. In: Avian brood parasitism (Clayton DH, Moore J, eds). Oxford: Oxford University Press; 338–369.
Payne RB, Payne LL, 1995. Song mimicry and association of brood-parasitic indigobirds (Vidua) with dybowski's twinspot (Eustichospiza dybowskii). Auk 112:649-658.
Payne RB, Payne LL, Woods JL, 1998. Song learning in brood-parasitic indigobirds Vidua chalybeata: song mimicry of the host species. Anim Behav 55:1537-1553.[CrossRef][Web of Science][Medline]
Payne RB, Payne LL, Woods JL, Sorenson MD, 2000. Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata. Anim Behav 59:69-81.[CrossRef][Web of Science][Medline]
Payne RB, Woods JL, Payne LL, 2001. Parental care in estrildid finches: experimental tests of a model of Vidua brood parasitism. Anim Behav 62:473-483.[CrossRef]
Pomiankowski A, 1987. The costs of choice in sexual selection. J Theor Biol 128:195-218.[CrossRef][Web of Science][Medline]
Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ, 2002. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc R Soc Lond B 269:729-733.[Medline]
Robert M, Sorci G, 2001. The evolution of obligate interspecific brood parasitism in birds. Behav Ecol 12:128-133.
Rowley I, Chapman G, 1986. Cross-fostering, imprinting and learning in two sympatric species of cockatoo. Behaviour 96:1-16.
Slagsvold T, 1998. On the origin and rarity of interspecific nest parasitism in birds. Am Nat 152:264-272.[CrossRef]
Slagsvold T, Hansen BT, 2001. Sexual imprinting and the origin of obligate brood parasitism in birds. Am Nat 158:354-367.[CrossRef]
Slagsvold T, Hansen BT, Johannessen LE, Lifjeld JT, 2002. Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc R Soc Lond B 269:1449-1455.[Medline]
Soha JA, Marler P, 2000. A species-specific acoustic cue for selective song learning in the white-crowned sparrow. Anim Behav 60:297-306.[CrossRef][Web of Science][Medline]
Sorenson MD, 1994. Is sexual imprinting an obstacle to the evolution of interspecific brood parasitism? In: Abstracts of the North American Ornithological Conference. Missoula, Montana: University of Montana; abstract 132.
Sorenson MD, Payne RB, 2001. A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution. Evolution 55:2550-2567.[CrossRef][Web of Science][Medline]
Sorenson MD, Payne RB, 2002. Molecular genetic perspectives on avian brood parasitism. Int Comp Biol 42:388-400.
Takasu F, Kawasaki K, Nakamura H, Cohen JE, Shigesada N, 1993. Modeling the population dynamics of a cuckoo-host association and the evolution of host defenses. Am Nat 142:819-839.[CrossRef]
Takimoto G, Higashi M, Yamamura N, 2000. A deterministic genetic model for sympatric speciation by sexual selection. Evolution 54:1870-1881.[CrossRef][Web of Science][Medline]
ten Cate C, 2000. How learning mechanisms might affect evolutionary processes. Trends Ecol Evol 15:179-181.[CrossRef][Medline]
ten Cate C, Bateson P, 1988. Sexual selection: the evolution of conspicuous characteristics in birds by means of imprinting. Evolution 42:1355-1358.[CrossRef]
ten Cate C, Vos DR, 1999. Sexual imprinting and evolutionary processes in birds: a reassessment. Adv Study Behav 28:1-31.
Whaling CS, Solis MM, Doupe AJ, Soha JA, Marler P, 1997. Acoustic and neural bases for innate recognition of song. Proc Natl Acad Sci USA 94:12694-12698.
Winfree R, 1999. Cuckoos, cowbirds and the persistence of brood parasitism. Trends Ecol Evol 14:338-343.[CrossRef][Medline]
Yamauchi A, 1995. Theory of evolution of nest parasitism in birds. Am Nat 145:434-456.[CrossRef]
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