Behavioral Ecology Advance Access originally published online on November 30, 2005
Behavioral Ecology 2006 17(2):196-205; doi:10.1093/beheco/arj013
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On the origin of brood parasitism in altricial birds
Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel
Address correspondence to E. Geffen. E-mail: geffene{at}post.tau.ac.il.
Received 23 April 2004; revised 29 September 2005; accepted 31 October 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The probability that obligate interspecific brood parasitism (OP), among altricial birds evolved directly from the normal breeding (no parasitism, NP) mode or indirectly through intraspecific nest parasitism (INP) was examined by using maximum-likelihood and parsimony approaches. We examined the probability of ancestral states at 24 key nodes in order to test our hypotheses. The state of the most basal node in a tree of 565 genera of altricial birds is equivocal; however, the state probability of NP at this node is about 5.5-fold more likely than the state of obligate parasite. A similar trend was observed for basal nodes of most families examined. The INP state was supported only in the Hirundinidae. The high incidence of INP among martins and swallows explains this finding. Contrary to our predictions, even in other groups where there is a high incidence of INP and OP, such as in the tribe Icteri and the Old World finches, the probability of NP being ancestral was very high. We conclude that in all cases but one (Hirundinidae) obligate, and probably facultative, brood parasitism evolved directly from normal breeding mode rather than indirectly through some other form of parasitism.
Key words: altricial birds, intraspecific brood parasitism, obligate brood parasitism.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Intraspecific nest parasitism (INP) is widespread among birds, and a recent review (Yom-Tov, 2001
) put the number at 234 species or about 2.4% of all birds, occurring in 16 orders. In comparison, obligate interspecific brood parasitism (OP) is rarer, occurring in about 100 species (1.0%) and only in four orders—Cuculiformes, Piciformes (honeyguides), Passeriformes, and Anseriformes (one species; Davies, 2000). Recent studies based on molecular systematics suggest that OP has evolved independently in seven avian lineages, ducks, honeyguides, cowbirds, finches, cuckoos (three; Sorenson and Payne, 2002), while INP has evolved in many more lineages (Davies, 2000; Petrie and Moller, 1991). The quantitative difference between the two forms of parasitism might be due to the fact that while OP involves various adaptations by the parasite (Kruger and Davies, 2002), fewer adaptations are required for intraspecific parasites, whose characters resemble those of their conspecifics.
Brood parasitism occurs in insects, fish and birds. Among fish the species involved are mostly facultative parasites, exploiting their own species, and only one species is known to be an obligate parasite (Sato, 1986). Intraspecific nest parasitism (INP) is also widespread among insects, where it occurs in ants, beetles, lace bugs, wasps, and bees. However, certain species parasitize other species, some of which belong to different orders (Hölldobler and Wlison, 1994).
Interspecific parasitism may evolve directly without an intermediate stage, particularly when parasites exploit hosts smaller than themselves or species with longer incubation periods (Slagsvold, 1998). The evolutionary transition from the normal mode of breeding (no parasitism, NP) to OP may include INP, takeover or use of nests built by other species, and communal laying by cooperative species (Payne, 1998). Several studies have dealt with the questions of what form of parasitism, inter- or intraspecific, was ancestral and which indirect pathway to OP via INP is considered more likely (Hamilton and Orians, 1965; Payne, 1977). Quantitative genetic models show that INP may serve as an intermediate step from purely parental reproduction to OP and conclude that it is unlikely that OP is ancestral, while INP may be ancestral (Cichon, 1995; Magali and Gabriele, 2001; Sorci, 2001; Yamaguchi, 1995). On the other hand, Aragon et al. (1999) following Hughes (1996) suggested that the ancestral state for the clade that includes the genera Coccyzus (where INP was observed) and Clamator (an OP genus) might have been OP. This suggestion seems to be a somewhat remote possibility because it requires lineages descended from OP to have developed normal nesting behavior. Davies (2000) suggested that INP might have been the ancestral state of OP in the cuckoos and the black-headed duck (Heteronetta atricapilla). Hence, various authors have suggested that OP evolved directly from either NP or INP, that INP evolved from NP, and even that an OP lineage had regained normal breeding behavior. Another possible route from NP to either INP or OP is the widespread behavior (particularly among estrildids and ploceids) of using an old nest, an explanation favored by Sorenson and Payne (2001).
Occasionally, birds lay eggs in other species' nests ("egg dumping"), sometimes even in nests of species that are unlikely to raise their chicks to fledglings due to substantial differences in their biology (Johnsgard, 1997). For example, insectivorous cowbirds opportunistically lay eggs in nests of birds that feed their chicks with a low-protein diet of seeds and fruits (Kozlovic et al., 1996), and the insectivorous black-winged stilt (Himantopus himantopus) lays eggs in a the nest of the piscivorous common tern (Sterna hirundo; Paz and Eshbol, 2002). This behavior, termed facultative interspecific nest parasitism (FIP), is common in precocial species, particularly Anseriformes (Lyon and Eadie, 2000) and in some altricial species, notably in the cuckoo family (Aragon et al., 1999; Nolan and Thompson, 1975). FIP might be a possible ancestral state for the evolution of OP, either through INP or directly so. However, FIP has been reported only occasionally, and to our knowledge, there is only one short review of this phenomenon (Lyon and Eadie, 2000); thus, we have included it in our analysis only in the case of cuckoos.
Slagsvold (1998) suggested that the comparative method may be useful in testing the hypotheses on the origin of parasitism when sufficient details are known on the biology and phylogeny of the species involved. However, as far as we know, no quantitative study has tested the probabilities of the origin of either OP or INP among birds, which, if any, was the ancestral state to brood parasitism. In this study we used a maximum-likelihood approach to calculate the probability that brood parasitism (either OP or INP) among altricial birds evolved either directly from the normal breeding mode or indirectly through intraspecific or obligate brood parasitism. We predicted that the normal breeding (NP) would predominate, with a significantly smaller probability that INP would be ancestral; that the probability of INP being ancestral would increase in nodes where it occurs; and that OP would be ancestral only at the base of nodes where it occurs. The results of this study may have an implication also for the understanding of brood parasitism among nonavian groups. We are aware that the biology of many species have not been studied, and it is likely that in the future more cases of INP will be reported, especially among tropical species. As more data become available, our present conclusion might change accordingly.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The bird species used in the analyses were categorized into three groups: obligate interspecific brood parasites (OP; Davies, 2000
), intraspecific nest parasites (INP; Yom-Tov, 2001), and nonparasite species (NP). We constructed a phylogenetic tree for 550 genera of altricial birds by a modification of the Sibley and Ahlquist (1990) tree. These genera include all genera of altricial obligate parasites (Davies, 2000) and all but one known INP genera in the orders Passeriformes (32 genera), Apodiformes (2 genera), Cuculiformes (2 genera), and Coraciiformes (1 genus; Yom-Tov, 2001). We included in the analysis all the altricial genera outlined on the Sibley and Ahlquist (1990) tree, starting at the basal node of the first clade holding OP species (Indicatoridae). Our tree does not include nonaltricial orders or the altricial orders Procellarifomes (one genus), Ciconiiformes (five genera), Accipiteriformes (one genus), and Columbiformes (four genera). Branch lengths used were as specified by Sibley and Ahlquist (1990). We collapsed species branches into a single genus branch. Further, 15 genera were added by placing each of the following recently published topologies and setting the branch length similar to that of their sister taxa. The genera added were Euphagus, Molothrus, Quiscalus, Scaphidura (Ericson and Johansson, 2003; Johnson and Lanyon, 1999; Klicka et al., 2000; Sorenson and Payne, 2001), Tachycineta (Whittingham et al., 2002), Passerculus (Grapputo et al., 2001), Anomalopsiza (Sorenson and Payne, 2001), Caprimulgus, Cercococcyx, Clamator, Dromococcyx, Neomorphus, Phaenicophaeus, Surinculus, and Tapera (Aragon et al., 1999; Sorenson and Payne, 2002).
Because finches and cuckoos are the only large group of birds for which all three states are each present in multiple members, we also calculated ancestral states for five key nodes on a tree of the superfamily Passeroidea published recently by Sorenson and Payne (2001, Figure 5) and four key nodes on the tree of the Cuculiformes (Sorenson and Payne, 2002, Figure 1). These two trees were composed by cladistic analysis of mitochondrial DNA sequence and most likely provide better estimates for topology and branch length than the Sibley and Ahlquist (1990) phylogeny.
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Few altricial species are facultative interspecific nest parasites (FIP; Aragon et al., 1999
; Payne, 1998), but this phenomenon is widespread among the precocial waterfowl (Lyon and Eadie, 1991). We considered the FIP state because it was suggested to be an intermediate state leading from NP to OP (Payne, 1998). For this analysis, we defined FIP species as any species that even occasionally lay their eggs in the nests of other species. However, as far as we are aware there is no review of this phenomenon among altricial species at large, although Aragon et al. (1999) provided data on the occurrence of IFP among the Cuculidea, a group for which a considerable proportion of species show FIP (Aragon et al., 1999). We thus added this fourth state only to the ancestral state analysis of the Cuculidea.
Ancestral states were traced on the phylogenetic tree using Mesquite (Maddison WP and Maddison DR, 2003). Ancestral state reconstruction was calculated using the maximum-likelihood and parsimony approaches. Maximum likelihood tests the hypotheses about trait evolution by summation of the probabilities over all possible states at each node of the tree (Pagel, 1999). The advantage of this approach is that uncertainty in the ancestral state reconstructions is automatically taken into account in all likelihood calculations. The asymmetrical Markov k-state two-parameter model is used in estimating transition rates among all possible pairs of states. These transition rates are then used for calculating the probability of states for each branch, given its length (Pagel, 1999). The program Mesquite lists the probability of all states per node, and those states that are significantly better supported than the others at that site are indicated by an asterisk. We used the value of 2.0 as the minimum significant difference between any two-state log likelihoods (Pagel, 1999). In using a probabilistic model we assumed that character states changed in the same manner throughout the tree. Such an assumption may be oversimplistic, however, because of heterogeneity among bird lineages. Further, likelihood calculations make use of branch lengths; thus, large deviations in length may generate an error in state reconstruction. Therefore, we also reconstructed the ancestral states using parsimony. The parsimony reconstruction method finds the ancestral states that minimize the number of steps of character change on the tree. Because our character is categorical, we assigned one step for every change (the unordered state option).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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To test our hypotheses, we examined the probability of states at 24 key nodes on the tree constructed based on the Sibley and Ahlquist tree (Figure 1), five nodes in the Sorenson and Payne (2001
, Figure 5) tree of finches (Figure 2), and four nodes in the Sorenson and Payne (2002, Figure 1) tree of cuckoos (Figure 3). The state of the most basal node in the tree of 565 genera of altricial birds is equivocal (NP: 0.827*, INP: 0.024, and OP: 0.149*); the state probability of no parasite at this node is about 5.5-fold more likely than the state of obligate parasite (Figure 1). Similar trends were observed for basal nodes of the Indicatoridae, Picidae, Lybiidae, Coliinae, and Cuculidae (Figure 1). Starting from the basal node of the Psittacidae and continuing with Apodiformes and Passeriformes, the OP state is no longer supported, even in the two clades where it occurs (Passeridae and Fringillidae).
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Parsimony and maximum-likelihood reconstructions were in complete agreement on the Sibley & Ahlquist tree except in four cases (Figure 1). In the case of the Hirundinidae, maximum-likelihood reconstruction for the basal node of this clade supported INP as the ancestral state (INP: 0.616). However, the parsimony reconstruction favored the no parasitism as the ancestral state (Figure 1). Parsimony supported NP as the ancestral state for two nodes in the clade of the weavers and one node in the clade of the cowbirds, but the maximum likelihood favored obligate parasitism in all those cases (OP: 0.654, 0.688, and 0.879, respectively; Figure 1). To test the effect of adding 15 extra genera onto the Sibley and Ahlquist tree (see Methods), we reconstructed the ancestral state of the focal nodes using parsimony and the unmodified tree. All focal nodes on the modified tree had a similar ancestral state as in the unmodified tree, except the node of the Cuculidae. In the modified tree, the most probable state for that node was NP, but in the unmodified tree, the obligate parasitism state was most supported.
To address these inconsistencies, we also reconstructed ancestral states using better-supported trees for the cuckoos and finches (Figure 1 in Sorenson and Payne [2002], and Figure 5 in Sorenson and Payne [2001], respectively). Tracing the states on tree of finches of Sorenson and Payne (2001) showed that all basal nodes of that tree and the basal node for the Viduidae-Estrildidae clade significantly supported the NP origin (Figure 2). The ancestral states of the three most basal nodes on tree of cuckoos of Sorenson and Payne (2002) showed a significant support for NP. Only in the branch leading to the Eudynamys-Cuculus clade (Figure 3a) was the OP state supported. Adding the FIP state on the cuckoo tree did not change any of these results (Figure 3b).
The inclusion of FIP in the analysis of the cuckoos showed that this behavior was not supported as an ancestral state even for the Ceuthmochares-Saurothera clade, where most known FIP species are (the probability for NP was 1.0 at the basal node of this clade; Figure 3b). This does not exclude the possibility that FIP is the ancestral state in other groups of birds, particularly the Anseriformes, but we do not have evidence for this and thus cannot draw any general conclusions.
We expected that among groups where INP is common, the probability of it being the ancestral state would be very high. However, the INP state was supported only for the Hirundinidae, and this result is explained by the high incidence of INP among martins and swallows. Contrary to our prediction, INP as an ancestral state was unsupported in any other group. Even in those groups where there is a high incidence of both INP and OP, such as in the tribe Icteri and the Old World finches, the probabilities of NP being ancestral were very high (.996 and .999, respectively). These results contrast the various suggestions that OP has evolved via INP (Cichon, 1995; Davies, 2000; Magali & Gabriele, 2001; Yamaguchi, 1995) or that some ancestral OP Cuculidae have evolved NP species (Aragon et al., 1999; Hughes, 1996).
We thus conclude that all cases of obligate brood parasitism in altricial birds most probably evolved directly from normal breeding ancestors and not through INP or even facultative interspecific brood parasitism (at least among the cuckoos). However, we call the attention of the readers to the fact that phylogenetic relationships among the families of passerine birds have been the subject of many debates. Although the Sibley and Ahlquist (1990) phylogeny is by far the most comprehensive, the phylogenetic information obtained by DNA-DNA hybridization analysis is poor relative to cladistic analysis of DNA sequences. Some major divisions in the Sibley and Ahlquist (1990) phylogeny have been supported by recent analysis (e.g., Ericson and Johansson, 2003), while others have been refuted (e.g., Edwards and Boles, 2002; Sheldon and Gill, 1996). Further, it is highly likely that INP and FIP are underreported. These knowledge gaps are potential sources of bias in our analysis, and as more data become available, our present conclusion might change accordingly.
Finally, our analysis does not provide an indication of how OP was evolved or whether it evolved from cooperative breeding, through the takeover of nests of other species, (Payne, 1998) or through FIP, and this problem remains unsolved.
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ACKNOWLEDGEMENTS |
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YYT thanks Nick Davies for his hospitality during a sabbatical in Cambridge. We thank Nick Davies, Arnon Lotem, Steve Rothstein, and three anonymous referees for their useful comments, and to Naomi Paz for the editorial review. This work was partially supported by the Israel Cohen Chair for Environmental Zoology to YYT.
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