Molecular Genetic Perspectives on Avian Brood Parasitism

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Molecular Genetic Perspectives on Avian Brood Parasitism1 MICHAEL D. SORENSON2,*,†

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ROBERT B. PAYNE†,‡

*Department of Biology, Boston University, Boston, Massachusetts 02215 †Museum of Zoology and ‡Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109

INTRODUCTION About 1% of all bird species are obligate brood parasites, reproducing only by laying eggs in the nests of other species. Brood parasites avoid much of the investment usually made in rearing young, while the foster parents (or ‘‘hosts’’) often suffer significantly reduced survival of their own young (Payne, 1977a, 1997a). Brood parasitism provides evolutionary biology with some of the best and clearest examples of reciprocal coevolution (Davies and Brooke, 1988; Rothstein, 1990; Lotem and Rothstein, 1995). Given the high costs of parasitism, there is often strong selection on hosts to recognize and reject parasitic eggs. In turn, counter-adaptations in parasites, such as egg or nestling mimicry, limit the ability of hosts to detect and discriminate against parasitic young. The adaptations of parasitic species to secure parental care from hosts and the counter-adaptations of hosts to avoid or reduce the effects of parasitism have been studied extensively in selected species (e.g., Davies and Brooke, 1988, 1989a, b; Soler and Møller, 1990; Lotem et al., 1992, 1995; Lotem, 1993; Soler et al., 1995, 1999a; Davies et al., 1996; Brooke et al., 1998; Kilner et al., 1999a, b). A variety of functional, mechanistic, and developmental questions about host and parasite behaviors have been considered (e.g., Rothstein, 1975, 1982a, b; Lotem et al., 1995; Sorenson, 1997), usually in studies centered around interactions at the host nest. Studies of the population biology of brood parasitism have generally focused on the negative effects of

parasitism on the host population (e.g., May and Robinson, 1985; Payne and Payne, 1998; Woodworth, 1999; Ward and Smith, 2000). Extensive research on cowbirds Molothrus spp. in particular has been motivated by concerns about the conservation of host species whose survival is threatened by parasitism (Ortega, 1998; Rothstein and Robinson, 1998). The population dynamics of brood parasites themselves and the population genetic and evolutionary consequences of their behavioral interactions with hosts have received much less attention. Recently, however, molecular studies on cuckoos (Gibbs et al., 1996, 2000a; Marchetti et al., 1998; Martinez et al., 1998a, b, 1999), cowbirds (Gibbs et al., 1997; Alderson et al., 1999a, b), and parasitic finches (Klein and Payne, 1998; Payne et al., 2002) have begun to complement behavioral studies in helping us to understand the evolutionary dynamics of brood parasitism. APPROACHES

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Molecular systematics In addition to simply establishing how many times obligate brood parasitism has originated, knowledge of the systematic relationships among brood parasites, their nearest nesting relatives, and their host species can provide insight into host-parasite coevolution (Payne, 1997a; Klein and Payne, 1998) and the ecological conditions under which brood parasitism evolved. For example, does brood parasitism typically originate with the parasitism of closely related hosts species that are more likely to provide appropriate parental care for parasitic chicks? Which parasitic lineages have switched to parasitizing more distantly related hosts and what are the relative ages of the different parasitic lineages among birds? Given that many

1 From the Symposium Living Together: The Dynamics of Symbiotic Interactions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois. 2 E-mail: [email protected]

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SYNOPSIS. Advances in molecular genetic techniques have provided new approaches for addressing evolutionary questions about brood parasitic birds. We review recent studies that apply genetic data to the systematics, population biology, and social systems of avian brood parasites and suggest directions for future research. Recent molecular systematics studies indicate that obligate brood parasitism has evolved independently in seven different avian lineages, a tally that has increased by one in cuckoos (Cuculiformes) and decreased by one in passeriforms (Passeriformes) as compared to conventional taxonomy. Genetic parentage analyses suggest that brood parasitic birds are less promiscuous than might be expected given their lack of nesting and parental care behavior. Host-specificity in brood parasites, which has important implications for host-parasite coevolution, has been evaluated using both population genetic and parentage analyses. Female lineages are faithful to particular host species over evolutionarily significant time scales in both common cuckoos (Cuculus canorus) and indigobirds (Vidua spp.), but differences in the host-specificity of male parasites has resulted in different patterns of diversification in these two lineages. Future research on brood parasitism will benefit from the availability of comprehensive molecular phylogenies for brood parasites and their hosts and from advances in functional genomics.

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of these questions require species-level phylogenies, mitochondrial DNA (mtDNA) sequences have been and will likely continue to be the primary source of data for phylogenetic analyses on parasitic birds, although independent sources of molecular data, such as nuclear intron sequences (e.g., Prychitko and Moore, 1997), may also be useful.

Parentage analyses Genetic parentage analyses provide a powerful approach to answering a variety of questions about parasitic birds. These include evaluations of host use by individual females, assessments of mating systems, and in the context of conspecific brood parasitism (CBP), identification of parasitic and nesting females and quantification of their reproductive success. Although protein electrophoresis and then multi-locus DNA fingerprinting (Burke and Bruford, 1987; Wetton et al., 1987) have been the standard approaches in avian studies, nuclear microsatellite markers offer much greater power to assign paternity to specific individuals (Blouin et al., 1996; Double et al., 1997), especially when ancillary information about putative parents is limited, as is likely to be the case when dealing with parasitic eggs laid in spatially dispersed host nests (e.g., Alderson et al., 1999b). The power of parentage analyses may be greatly improved by combining information from genetic markers with different modes of inheritance, including mtDNA haplotypes, nuclear microsatellite loci, and markers on the W and Z sex chromosomes. Mitochondrial data, for example, can be used to subdivide a population sample into groups of individuals from different maternal lineages and thereby greatly reduce the pool of potential mothers for

each offspring sampled. Molecular sexing (Griffiths et al., 1998) can provide an added benefit, especially for sexually monomorphic species (e.g., Martinez et al., 1998a). Genetic checks of maternity assignments based on egg characteristics usually show good agreement between egg morphology and genetic markers (Fleischer, 1985; McRae and Burke, 1996; Jones et al., 1997). In some cases, however, the eggs of individual females may be more variable than assumed, resulting in an overestimate of parasitism rate (in the case of CBP) or in the number of parasitic females laying in a nest or area if egg characteristics alone are used to assess maternity (McRae, 1997; Martinez et al., 1998a). Ideally, the availability of genetic information will not be viewed as a substitute for careful field-based observations, or vice versa. Microsatellite markers recently have been developed for cuckoos, including Cuculus canorus (Gibbs et al., 1996, 1998) and Clamator glandarius (Martinez et al., 1998a), brown-headed cowbirds Molothrus ater (Alderson et al., 1999a; Longmire et al., 2001) and indigobirds Vidua spp. (Sefc et al., 2001). In each case, the utility of these markers is likely to extend at least to other species in the same genera (Primmer et al., 1996). Additional information on collecting different kinds of molecular data and their application to questions in ecology and evolution can be found in recent volumes edited by DeSalle and Schierwater (1998) and Baker (2000). Power (1998) considers issues of data quality and provides guidelines for the sampling design of field studies in which molecular methods are used to assess the frequency of conspecific brood parasitism. THE ORIGINS OF OBLIGATE BROOD PARASITISM Recent views on avian relationships suggest seven independent origins of obligate brood-parasitism (Sibley and Ahlquist, 1990; Sibley and Monroe, 1990; Payne, 1997a). These include 1) a single origin in the Old World honeyguides (family Indicatoridae), which comprises 17 parasitic species; 2) a single species of waterfowl (Anatidae), the black-headed duck Heteronetta atricapilla of South America; 3) two independent origins in Old World and New World cuckoos (Cuculidae), respectively; and 4) three independent origins within Passeriformes, including the New World cowbirds (Icteridae), and two origins in African finches, represented by the genera Vidua and Anomalospiza, respectively. Recent molecular systematic studies, however, require us to increase this tally by one for cuckoos and reduce it by one for African finches. Cuckoos We are working on a comprehensive molecular phylogeny for the cuckoos to resolve uncertain taxonomic relationships and to address questions about biogeography and the origins of brood parasitism. Figure 1 presents a preliminary analysis for selected cuckoos based on sequences of the mitochondrial NADH de-

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Phylogeography and population genetics Perhaps the most interesting questions about brood parasitic birds concern the coevolution of brood parasites and their hosts and the potential for diversification of parasitic lineages through their association with different hosts species. These questions lie at the interface of systematics and population genetics, making a variety of molecular markers and analytical approaches potentially valuable. Comparative phylogeographic studies, for example, may lend insight into the historical duration of interactions between brood parasites and their hosts. Population genetic analyses allow assessments of gene flow (or the lack thereof) among the geographic populations or host races of a particular parasitic species as compared to its host(s), patterns which may have important consequences for local adaptation in the coevolution of parasites and hosts (e.g., Martinez et al., 1999; Soler et al., 1999b). The combined analysis of rapidly evolving mtDNA control region sequences and length variation in nuclear microsatellite loci (e.g., Gibbs et al., 2000a) is the current state of the art, but new genetic markers such as single nucleotide polymorphisms (SNPs) may offer new ways of examining the history of populations (Cann, 2001).

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hydrogenase subunit 2 (ND2) gene. One unexpected result in this analysis is that the Old World brood parasites (tribe Cuculini) fall into two distinct clades. Representatives of Clamator, which includes four parasitic species, are included within a clade of nesting species previously placed in Phaenicophaeinae (e.g., Ceuthmochares, Phanicophaeus) and Coccyzinae (Piaya, Saurothera, Coccyzus) (Payne, 1997b). The other Old World parasites sampled here form a separate, well-supported clade. The New World parasites, Dromococcyx and Tapera, are sister to the New World ground cuckoos (Neomorphus and Geococcyx). These results lead to the clear inference that obligate brood parasitism evolved independently in three different cuckoo lineages. Aragon et al. (1999) obtained similar results based on a somewhat smaller mtDNA data set. Following Hughes (1996), they suggested that the ancestral state for the clade including both Clamator and Coccyzus, which is noted for facultative brood parasitism (Nolan and Thompson, 1975; Fleischer et al., 1985), may have been obligate brood parasitism. This is a remarkable proposition in that it would require lineages descended from an obligate brood parasite ancestor to regain nesting and parental care behaviors. Although it is possible to construct ad hoc arguments in favor of this scenario (Aragon et al., 1999; Hughes, 2000), independent gains (not losses) of parasitic behavior is the only ten-

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able hypothesis in light of the phylogeny in Figure 1 and an objective criterion of parsimony. We note, however, that Hughes’ (1996, 2000) morphological analyses provide a substantially different view of cuckoo relationships. Her data supported a tree topology in which Coccyzus is nested within a single clade comprising all of the parasitic cuckoos. This result suggests a single origin of parasitic behavior and leads reasonably to the inference that obligate parasitism was lost and nesting behaviors were regained in Coccyzus. Future analyses will seek to resolve the apparent conflict between molecular and morphological information and provide a clearer conclusion about the evolution of parasitism in cuckoos. At present, we think the molecular tree is more consistent with biogeographic considerations and suspect that further analysis will support our conclusion that obligate brood parasitism originated three separate times within cuckoos. Interesting differences in parasitic behavior are observed among these three lineages. Host nestling ejection, observed in most of the Old World parasites, is absent in Clamator which is generally reared along with young of the host (Davies, 2000). In contrast, the New World parasites have been observed to kill host young directly with sharp bill hooks (Morton and Farabaugh, 1979). Parasitic finches Twenty species of African finches are obligate brood parasites (Payne, 1996, 1997a, c, 1998). These include 10 species of indigobirds and 9 species of long-tailed whydahs in the genus Vidua plus the cuckoo finch Anomalospiza imberbis. Although various hypotheses for the relationships of these two genera have been proposed, they have generally been thought to represent two independent origins of parasitism (e.g., Friedmann, 1960). Recent classifications place Vidua with the estrildid finches and Anomalospiza with the ploceid finches (e.g., Sibley and Monroe, 1990). Our analysis of mtDNA sequence data for parasitic finches (Sorenson and Payne, 2001) strongly supported a sister relationship between Anomalospiza and Vidua, leading to the inference that parasitism evolved only once in African finches (Fig. 2). In addition, a very deep split between these two genera suggests an ancient origin of parasitism. Analysis of genetic distances, corrected for differences in evolutionary rate between lineages, suggests an origin of obligate parasitism perhaps as long as 20 million years ago and predating the most recent common ancestor of all 140 extant estrildid species in Africa, Asia, and Australia (Sorenson and Payne, 2001). This provides a striking contrast to the very recent origin of extant indigobird species within Vidua (see below). Another key finding of this study was a substantially faster rate of mtDNA sequence evolution in parasitic finches than in their sister group, the estrildid finches. Given their common ancestry and similar generation times, rate differences associated with metabolic rate or germ-line replication rate (e.g., Martin and Palumbi, 1993; Nunn and Stanley, 1998)

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FIG. 1. A phylogeny of selected cuckoo species based on complete sequences of the mitochondrial ND2 gene and showing three separate origins of obligate brood parasitism (arrows). Obligate brood parasites are indicated by asterisks and outlined branches on the tree. The single most parsimonious tree (length 5 4,541, CI 5 0.29) for an analysis giving equal weight to all characters and changes is shown. Bremer support indices (Bremer, 1988) and bootstrap values are indicated above and below each branch, respectively. The outgroup included sequences for 13 other avian taxa.

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are unlikely. The fixation of nearly-neutral mutations (Ohta, 1992) during repeated population bottlenecks associated with the colonization of new hosts (see below) during the evolutionary history of parasitic finches provides a potential alternative explanation. The young of most Vidua mimic the elaborate mouth markings of their estrildid hosts. The sister relationship between parasitic finches and estrildids suggests that similar mouth markings may have been present in the common ancestor of these two lineages, but the species-specificity of these markings in extant parasites has clearly evolved in response to interactions with their current hosts. The relatively frequent use of old nests of other species by a variety of estrildids suggests that this behavior may have been a starting point in the evolution of parasitism in this group (Payne, 1998; Davies, 2000; Sorenson and Payne, 2001). The first parasitic finches very likely used closely related host species in which the behavior and parental care requirements of nestlings were very similar to their own. The cuckoo finch, which parasitizes Prinia and Cisticola warblers (Vernon, 1964), subsequently switched to relatively distantly related hosts. Cowbirds Recent studies have confirmed the monophyly of the brood parasitic cowbirds (Lanyon, 1992; Lanyon and Omland, 1999; Johnson and Lanyon, 1999) and show that the bay-winged cowbird Molothrus badius, a nesting species and primary host of the screaming cowbird M. rufoaxillaris, is the sister taxon of the Bolivian blackbird Oreospars bolivianus. This pair of species (badius and bolivianus) is nested within a large clade of non-parasitic blackbirds and is only distantly related to the five parasitic species. Previously, M. badius was thought to be very closely related to its specialist parasite, M. rufoaxillaris (Friedmann, 1963). The distant relationship of M. badius to the parasitic cowbirds has two important implications for previous hypotheses about the evolution of parasitism (Lanyon, 1992).

First, the remarkable nestling mimicry of badius by rufoaxillaris (Hudson, 1874) must be attributed to host-parasite coevolution rather than just common ancestry. Second, nest parasitism (the use of old nests of other species) by badius can no longer be viewed as a transitional stage in the evolutionary progression from nesting to obligate parasitism in cowbirds. While this route to parasitism is still a plausible hypothesis for the parasitic cowbirds, this behavior evolved independently in the distantly related badius. Among the five parasitic cowbirds, the host-specialist M. rufoaxillaris is basal to the giant cowbird, M. (Scaphidura) orizyvorus, which is know to parasitize seven cacique Cacicus and oropendola Psarocolius species, whereas the increasingly generalist M. aeneus, M. bonariensis, and M. ater, with 82, 214, and 226 recorded hosts, respectively (Ortega, 1998), are more recently derived. Lanyon (1992) argued that these relationships provide evidence of an evolutionary progression in cowbirds from species that are host specialists to those that are host generalists. Honeyguides Sibley and Ahlquist (1990) placed the honeyguides (Indicatoridae) as the sister taxon of woodpeckers (Picidae) on the basis of DNA-DNA hybridization evidence. Also included in the Piciformes are the African barbets (Lybiidae), which together with woodpeckers are the most frequent honeyguide hosts. A comprehensive test of honeyguide relationships using DNA sequence data has not been completed, but existing hypotheses again suggest an origin of parasitism in which ancestral parasites used closely related host species. In addition, the shared habit of hole-nesting between parasites and hosts may help to explain the evolution of parasitism in this clade (see Eadie et al., 1988). Black-headed duck The waterfowl (Anatidae), which is distinguished by a high frequency of both inter-specific and conspecific facultative brood parasitism (Eadie et al., 1988; Rohwer and Freeman, 1989; Sorenson, 1992), includes a single obligate brood parasite, the black-headed duck Heteronetta atricapilla. This species represents a relatively recent origin of obligate parasitism and recent molecular analyses suggest it is most closely related to stifftails, Oxyurinae (McCracken et al., 1999), consistent with morphological evidence (Livezey, 1995). The black-headed duck most often parasitizes other waterfowl and marsh-nesting birds (Weller, 1968). SOCIAL SYSTEMS OF OBLIGATE BROOD PARASITES Lacking incubation and parental care behavior, the breeding biology of obligate brood parasites poses a variety of interesting questions. Are brood parasites more likely, for example, to be polygynous or promiscuous (e.g., Yokel, 1986)? Do female brood parasites defend exclusive laying territories? How many eggs do individual females lay and how are these eggs

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FIG. 2. Relationships among Old World finch families based on a phylogenetic analysis of over 3,000 bases of mtDNA sequence data for 43 representative taxa (tree topology based on the results of Sorenson and Payne [2001]). Obligate brood parasitism evolved only once and the parasitic finches (Viduidae), comprising the genera Anomalospiza and Vidua, are sister to Estrildidae, the family that includes the hosts of all Vidua species.

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Brown-headed cowbirds Molothrus ater Fleischer (1985) was the first to use modern molecular techniques to study egg-laying in parasitic birds. Using protein electrophoresis to assay yolk proteins of maternal origin, he showed that individual brownheaded cowbirds laid parasitic eggs in the nests of multiple host species and that nests with more than one cowbird egg had usually been parasitized by two different females. Recently, Alderson et al. (1999b) used microsatellite data to determine the parentage of cowbird chicks at Delta Marsh, Manitoba. Genetic monogamy was the norm—the offspring produced by each female were fathered by a single male, although two males mated with more than one female. In this study, multiple parasitism was usually the result of one female laying two eggs in the same host nest, although two females sometimes laid in host nests at the boundaries of otherwise exclusive egg-laying areas. In contrast to previous studies, about half of the females parasitized only one host species—one female laid 13 eggs in red-winged blackbird Agelaius phoeniceus nests. These results suggest that some females might specialize on particular hosts, although it is not clear whether this is a function of host choice by the parasite or host availability within her egg-laying range (Davies, 2000). Despite intensive nest searching by the researchers, the number of cowbird chicks produced by each female was small (Alderson et al., 1999b), suggesting that realized reproductive success is much lower than estimates of the number of eggs laid by female cowbirds (Payne, 1965; Scott and Ankney, 1983). Hahn and Fleischer (1995) used DNA fingerprinting

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to test whether female and juvenile cowbirds trapped together at a feeding site were more closely related to each other than randomly selected pairs—although their sample size was small, band sharing coefficients in several instances were as high as those typically found between first order relatives, suggesting that females may associate with their own offspring after they gain independence from the host species. If so, this might help to explain how parasitic birds solve the potential problem of sexually imprinting on the host species. It would be particularly interesting to conduct a similar study on orange-rumped honeyguides Indicator xanthonotus in which females returning to feed at bee hives guarded by males were sometimes accompanied by immature birds (Cronin and Sherman, 1976). Great-spotted cuckoos Clamator glandarius Martinez et al. (1998a, b) combined information from microsatellite loci and a sex-linked marker to examine the social system of great-spotted cuckoos. Most offspring were from monogamous pairs, but a few cases consistent with polygyny by males or sequential polyandry by females were also found (Martinez et al., 1998a). The spatial pattern of egg-laying by great-spotted cuckoos provided no evidence for even short-term territoriality—females had broadlyoverlapping laying ranges and often shared individual host nests (Martinez et al., 1998b). The frequency of multiple parasitism involving different females was associated with seasonal changes in host availability, whereas multiple parasitism by the same female was not. Clamator cuckoos do not eject host young from the nest, such that the costs of multiple parasitism to parasitic females are relatively low. One female laid in carrion crow Corvus corone nests at the beginning and end of one season, when the preferred host, magpie Pica pica, was not available (Martinez et al., 1998a). Common cuckoos Cuculus canorus Jones et al. (1997) used a combination of singlelocus and multi-locus DNA fingerprinting to assess parentage for three series of cuckoo chicks (one in Britain and two in Japan), each presumed on the basis of egg markings to be the offspring of a single female cuckoo. The six to nine chicks in each series came from the nests of a single host species. Their data confirmed identifications based on egg markings and also indicated that each female mated with a single male, but that two females breeding at one site in Japan both mated with the same male. Marchetti et al. (1998) used microsatellite loci and a much larger sample of individual birds to examine the mating system of another Japanese cuckoo population. This study tested whether individual females specialized on only one of two primary host species in the area (azure-winged magpie Cyanopica cyana and great reed warbler Acrocephalus arundinaceus) and whether males mated with females using different hosts. Most females (22 of 24) pro-

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distributed among the nests of different host species? The issue of host-specificity, in particular, has important implications for understanding host-parasite coevolution in that high fidelity to individual host species may lead to the evolution of host-specific mimicry and/or diversification in the parasitic lineage. Egg laying patterns have been assessed previously by documenting sets of parasitic eggs with similar markings (e.g., Chance, 1922; Kattan, 1997; Lyon, 1997) and fecundity has been estimated by examining post-ovulatory follicles in females collected during the breeding season (e.g., Payne, 1965, 1973a, 1974, 1977b; Scott and Ankney, 1983). Molecular methods provide a powerful new approach to these kinds of questions and a variety of recent studies have sought to evaluate laying patterns, mating systems, and population structure using genetic data. One potential limitation of these studies is that researchers may include only parasitic eggs that hatch (or at least partially develop), such that information about the mating behavior and fecundity of parasitic females is lost. New methods, however, including fingerprinting of egg albumins (Andersson and Ahlund, 2001) and isolation of sperm from the perivitelline membrane (Carter et al., 2000), may allow both maternal and paternal genotypes to be obtained from infertile or unincubated eggs.

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duced offspring in the nests of only one host species, whereas male cuckoos were more likely (7 of 19) to produce offspring in the nests of two different host species (by mating with females using different hosts). This result has very important implications for understanding the genetic structure of cuckoo populations and the potential diversification of distinct host-races (see below).

HOST-PARASITE COEVOLUTION While additional studies on the social systems of parasitic birds are clearly needed, the contrasting results described above for cuckoos, cowbirds, and indigobirds have important implications for understanding the dynamics of host-parasite coevolution and the potential for the evolutionary diversification of parasitic lineages. Host egg mimicry in common cuckoos (Davies, 2000) and mimicry of host mouth patterns in Vidua finches (Nicolai, 1964; Payne, 1973b, 1982) provide two of the most remarkable and clearest examples of host-specific adaptations in parasitic birds, but these two systems provide an interesting contrast. In the common cuckoo, egg mimicry of several different host species seems to be maintained within a single parasitic species but in indigobirds, each parasitic species generally parasitizes and mimics a different host species. Recent genetic studies shed light on the different evolutionary dynamics of these systems. Common cuckoos Egg mimicry of several different hosts within the European population of common cuckoos has been a long-standing puzzle for evolutionary biologists. Jensen (1966; see also Punnett, 1933) suggested that cryptic host races or gentes might be maintained if the genes for egg mimicry reside on the female-specific

W chromosome (in birds, females are the heterogametic sex), such that females inherit from their mothers the genes for egg mimicry unaffected by recombination with paternal genes. Two recent genetic analyses sought to test this hypothesis by comparing patterns of variation in nuclear autosomal loci with maternally inherited mtDNA. If female lineages within the cuckoo population are faithful to particular host species, then host races should correspond to distinct mtDNA haplotype groups (which in turn should correspond to W-chromosome lineages). Gibbs et al. (1996) compared patterns of variation in three nuclear microsatellite loci with a microsatellite located in a small non-coding region of the mtDNA (see Mindell et al. [1998] for a description of a mtDNA gene rearrangement in cuckoos and other birds). This analysis found no significant differentiation in either nuclear or mtDNA markers among cuckoo chicks sampled from the nests of different host species in Britain. Sequence data from the mtDNA control region, however, revealed slight but significant differentiation in mtDNA haplotype frequencies among these same groups and also between common cuckoo chicks from two different hosts in Japan (Gibbs et al., 2000a). Using a larger sample of microsatellite loci, there was still no significant differentiation detected in nuclear markers. Perhaps the clearest result of this study is that female lineages within the cuckoo population are faithful to particular hosts over ecologically and evolutionarily significant time spans—long enough for significant differences in mtDNA haplotype frequencies to develop among host races. This strongly suggests some form of imprinting by female cuckoos on cues associated with their foster species, although the details of this process remain poorly understood (Brooke and Davies, 1991; Teuschl et al., 1998). In contrast, male cuckoos appear to mate with females irrespective of host race (Marchetti et al., 1998) and this apparently maintains the genetic continuity of common cuckoos as a single species. Significant differences in mtDNA among cuckoo host races are potentially consistent with egg mimicry genes residing on the W chromosome, but some difficulties remain. While the W chromosome hypothesis explains how mimicry of different hosts could be maintained within a single parasitic species, it also requires that egg mimicry evolve independently in each female lineage switching to a particular host species (given that there is presumably no recombination between the W chromosome and other nuclear loci). Because the mtDNA haplotypes in each cuckoo gens (or host race) are not monophyletic, however, multiple host switches by female lineages are required to explain the current distribution of haplotypes (Gibbs et al., 2000a). This implies that egg mimicry must have evolved independently after each of these host switches (assuming that mtDNA and W-chromosome histories, both of which should reflect only matrilineal inheritance, are perfectly parallel). The alternative is that segregating alleles at autosomal loci that code for egg

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Village indigobirds Vidua chalybeata In a similar vein, Payne et al. (2002) assessed parentage in a local population of village indigobirds in which some males mimicked the songs of red-billed firefinch Lagonosticta senegala, the usual host of this indigobird species, while other males mimicked the song of a novel host, the brown firefinch L. nitidula. Microsatellite analyses showed that three indigobird nestlings similar in appearance to red-billed firefinch nestlings but sampled from brown firefinch nests were the offspring of three different male indigobirds, all of which mimicked brown firefinch song. In addition, a female observed at the call site of one of these males was identified as the mother of one of the nestlings. None of the indigobirds associated with red-billed firefinch were closely related to individuals associated with brown firefinch, or vice versa. Although based on a limited sample, these results suggest a relatively recent host switch and are consistent with a model of speciation in indigobirds in which social imprinting results in assortative mating and reproductive isolation after the colonization of a new host species (see below).

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characteristics move through both males and females, obviating the need for de novo evolution of egg mimicry after every host switch by a female lineage. This model, however, evokes the classic problem of how any significant degree of mimicry could be maintained if male cuckoos are not also differentiated into host races. Perhaps the W-chromosome contains evolutionarily labile genes that regulate the expression of more conserved autosomal loci that determine alternative egg characteristics. Indigobirds Genetic analyses on indigobirds (Vidua spp.) suggest a similar pattern of host colonization by multiple female lineages, but a key difference in the social behavior of these birds has resulted in rapid speciation after the colonization of new hosts. Each of 10 very similar but morphologically distinct indigobird species generally parasitizes a different estrilid finch species. Unlike common cuckoos, young indigobirds are reared along with their hosts and they mimic the mouth markings of host nestlings (Nicolai, 1964; Payne, 1973b, 1982). Klein and Payne (1998) used mtDNA restriction fragment length polymorphism (RFLP) data to test alternative historical models for the evolution of these species-specific associations between parasites and hosts. A model of ancient cospeciation was sound-

ly rejected given the much greater time depth of the host phylogeny and a complete lack of parallel branching patterns in the host and parasitic lineages. We present here an expanded analysis of indigobird and indigobird host phylogenies based on mtDNA sequence data (Fig. 3). Comparison of these phylogenies clearly indicates that indigobirds colonized their current hosts long after the diversification of the host lineage—the maximum divergence among indigobird mtDNA haplotypes is substantially less than that observed within individual host species (e.g., L. rubricata and L. senegala) and is an order of magnitude less than the genetic divergence between the most distantly related hosts. These data indicate a very recent origin of extant indigobird species. Although mtDNA haplotypes are broadly shared among the species within each geographic region, the species in West Africa show highly significant differentiation in mtDNA haplotype frequencies, with an overall Fst value of 0.42 (unpublished data, M.D.S. et al.; Fst is an Fst analogue for haplotype data, Excoffier et al., 1992), suggesting a strong degree of current reproductive isolation. MtDNA differentiation among the four indigobird species in southern Africa is also statistically significant but is actually less than that found among common cuckoo host races (Gibbs et al., 2000a), yet these indigobirds (and those in West Africa) are diagnosable

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FIG. 3. Mitochondrial DNA haplotype trees for individuals representing 10 indigobird species (left) and their host species (right). Lines connect indigobird species with their respective hosts. Indigobird and host trees are drawn to the same scale such that branch lengths are proportional to the number of substitutions per site (for gene regions common to both data sets) estimated using maximum likelihood with a molecular clock enforced (Swofford, 2001). Average genetic distances between sequences on either side of selected nodes (calculated using the method of Steel et al. [1996]) are shown: the upper value in each pair is the Kimura 2-parameter distance (Kimura, 1980); the lower value is the uncorrected transversion distance (percentage of sites that differ by a transversion). The indigobird tree is based on 1,100 bases of sequence comprising the ND6 gene, tRNA-glu, and the 59 half of the mtDNA control region. The tree shows relationships among 126 unique haplotypes found among 301 individuals and is rooted with sequences of the shaft-tailed whydah Vidua regia and straw-tailed whydah Vidua fischeri. Mitochondrial haplotypes are broadly shared among the indigobird species in each region, so it is not possible to identify monophyletic groups corresponding to individual species and there is not enough room in this figure to show the species identity of all 301 sampled birds. The host tree is based on the same gene regions plus an additional 545 bases from the ND2 gene and the flanking tRNA-trp. Note that many additional estrildid species not known to be indigobird hosts fall within the host phylogeny presented here.

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Brown-headed cowbirds Generalist laying patterns in brown-headed cowbirds suggest that there is relatively little scope for coevolution with individual host species or for the differentiation of host-specific races within the cowbird population. Consistent with this expectation, Gibbs et al. (1997) found no significant genetic differentiation in either mtDNA or nuclear microsatellite loci among groups of cowbird chicks sampled from the nests of different host species. Similar results seem likely for

the other host generalist cowbirds (M. bonariensis and M. aeneus). Great-spotted cuckoos Martinez et al. (1999) addressed host-parasite coevolution at a somewhat different level by comparing the population genetic structure of the great crested cuckoo with its principal host, the magpie Pica pica, across Europe. Both magpie and cuckoo populations showed a pattern of isolation by distance in analyses of microsatellite loci, although measures of gene flow were higher for the magpie, especially within the range of the cuckoo in Spain and southern France. Martinez et al. (1999) suggest that the negative effects of cuckoo parasitism might increase levels of gene flow among host populations by creating population sinks and, in turn, might promote the spread of anti-parasite adaptations such as egg recognition. Soler et al. (1999b) extended this analysis by correlating differences in egg rejection behavior with genetic distances among host populations. Differences between populations in the proportion of non-mimetic eggs that were rejected were positively correlated with genetic distances between populations, a result that is at least consistent with there being a genetic component to differences in egg rejection and the potential for this behavior to spread into allopatric host populations through gene flow. Host responses to mimetic eggs, however, were more strongly related to geographic distances, suggesting a role for flexible behavioral mechanisms in determining differences in rejection behavior among host populations (Alvarez, 1996; Moksnes et al., 1990; Davies and Brooke, 1989a; Brooke et al., 1998; Lotem et al., 1992, 1995; see also Payne, 1997a). Patterns of gene flow in the parasitic species may also affect the dynamics of the coevolutionary process, either preventing or promoting local adaptation to host populations and in turn determining the potential for host race formation. FACULTATIVE CONSPECIFIC BROOD PARASITISM Molecular genetic approaches are equally applicable to systems involving facultative CBP. Most studies to date have used genetic markers to assess only the incidence and frequency of CBP, a potentially difficult problem in that there are no obvious morphological differences between host and parasitic young. Careful observation of daily laying often in combination with an evaluation of egg characteristics has been used to detect CBP in several studies (e.g., Sorenson, 1993; Lyon, 1993a, b; Lyon and Everding, 1996; McRae and Burke, 1996), but genetic parentage analyses provide an additional source of information. One of the first studies documenting CBP using DNA-based markers was by Quinn et al. (1987), who used several singlelocus probes to evaluate RFLPs at specific loci in snow geese Anser caerulescens. CBP was documented in zebra finches Taeniopygia guttata by Birkhead et al. (1990) using multilocus probes (Jeffreys et al., 1985), the most common method in subsequent paternity

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as morphologically distinct species (Payne, 1973b, 1996). One explanation for these patterns is that the unique social system of indigobirds (and other Vidua) has resulted in a very recent and rapid diversification, such that the descendant species still retain genetic variation present in the ancestral population. In contrast to cuckoos, both male and female indigobirds imprint on their hosts. Based on extensive observation in the field (Payne 1973b, 1982; Payne et al., 1992; Payne and Payne, 1994, 1995) and a recent series of captive experiments (Payne et al., 1998, 2000), we know that male indigobirds learn the songs of their hosts species and mimic these songs as adults. Female indigobirds also imprint on their hosts and apparently use host song both to choose their mates and the nests they parasitize (Payne et al., 2000). These social mechanisms result in assortative mating of indigobirds associated with a particular host species and serve to maintain the genetic integrity of indigobird species. The same mechanisms, however, should also result in immediate reproductive isolation after the colonization of a new host species and, in turn, may facilitate the rapid evolution of host-specific mouth markings, which in contrast to egg markings are expressed by both male and female offspring. Taken at face value, the genetic similarity of indigobirds will raise questions for some about their status as distinct species, especially when contrasted with the ancient origin of parasitism in finches (see above). These results can be reconciled if extant indigobirds are simply the most recent products of a repeating process of host colonization, speciation, and extinction in the parasitic lineage (Sorenson and Payne, 2001). Behavioral and morphological evidence as well as significant genetic differentiation among indigobird species suggest limited gene flow between species at present and argue against an alternative model in which the parasitic clade has been in a perpetual state of incomplete speciation due to ongoing hybridization. Vidua also includes a number of genetically distinct clades (the whydahs) that are reciprocally monophyletic in their mtDNA and which may have passed through a stage similar to that currently observed in indigobirds. Regardless of species issues, the social system of indigobirds provides a clear mechanism for the reproductive isolation and morphological differentiation of populations associated with different host species and an interesting contrast to cuckoos.

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predictions depending on relative costs and benefits to host and parasite (Lyon and Eadie, 2000; Zink, 2000; Andersson, 2001). If costs to the host are high and a parasitic female has the ability to parasitize either kin or non-kin, she should prefer to impose the costs of parasitism on an unrelated individual. In contrast, if costs to the host are minimal and hosts are able to exclude parasitic females from their nests, then kin selection might favor the acceptance by hosts of parasitic eggs from related females. Alternatively, a bias towards parasitizing kin might simply reflect a more general advantage of interacting with familiar individuals. DIRECTIONS FOR FUTURE RESEARCH As with previous behavioral studies, genetic research on avian brood parasitism has focused on a few extensively studied species. Additional studies of other species that combine genetic analyses with careful observation and experimental manipulations in the field will contribute to our understanding of host-parasite coevolution and the social systems of brood parasitic birds. Issues of host-parasite coevolution may prove particularly interesting in speciose clades such as Cuculus and Chrysococcyx, and in parasitic species with variable eggs (e.g., Cuculus canorus, Chrysococcyx caprius, Molothrus bonariensis). In the context of conspecific brood parasitism, genetic markers will continue to provide a powerful approach to identifying parasitic individuals and measuring the reproductive success of alternative reproductive behaviors. While additional development of molecular markers such as microsatellite loci and single nucleotide polymorphisms is needed for some taxa, laboratory analyses for parentage and population studies have become routine. A greater challenge continues to be collecting sets of genetic samples in the field that are associated with relevant behavioral and/or morphological data from individual birds, such that hypotheses of interest can be tested. With respect to the analysis of population genetic data, there remains a general issue of how to develop and evaluate quantitative expectations for measures of genetic structure based on different kinds of molecular markers (e.g., mtDNA versus microsatellite loci) and under different historical models for host and parasite populations (see Goldstein et al., 1999; Gibbs et al., 2000b). Different population histories may lead to similar contemporary patterns of genetic variation among geographic populations or host races—retained ancestral polymorphism and recent gene flow, for example, may be particularly difficult to distinguish. With the increasing availability of comprehensive molecular phylogenies for different groups of birds will come new opportunities for comparative analyses of both obligate brood parasitism and CBP. For example, Payne (1974) compared egg size in parasitic and non-parasitic cuckoos and suggested hypotheses for why parasites lay relatively small eggs. Phylogenybased comparative methods that control for non-inde-

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studies. Power (1998) reviewed numerous avian parentage studies, including earlier work using allozyme markers. Many of these studies were primarily interested in extra-pair fertilizations but documented rare instances of CBP or ‘‘quasi-parasitism,’’ in which the resident male mates with the intruding parasitic female (e.g., Meek et al., 1994; Pinxten et al., 1993; Morton et al., 1990). For example, Alves and Bryant (1998) found that 14%, 2.4%, and 1.8% of 167 sand martins Riparia riparia chicks were the result of extra-pair fertilizations, quasi-parasitism, and CBP, respectively. They argued that the somewhat higher frequency of quasi-parasitism as compared to CBP was evidence that parasitic females mate with resident males more often that expected based on the observed frequency of extra-pair fertilizations and therefore that quasi-parasitism may be an adaptive female strategy. Perhaps a parasitic female gains access to a neighbor’s nest more easily if she mates with the resident male. One of the central issues in the study of CBP is the ultimate function of parasitic egg laying as a reproductive tactic in species that also nest in the typical fashion (e.g., Sorenson, 1991). A few recent studies have used genetic data to test alternative functional hypotheses. McRae and Burke (1996) used multilocus DNA fingerprinting to test whether female moorhens mate with the resident male of the nests they parasitized (quasi-parasitism) or if they parasitize close relatives, two alternative hypotheses that would help to explain the acceptance of parasitic eggs by hosts. Neither hypothesis was supported: parasitic females mated exclusively with the male on their home territory and although host and parasite were sometimes closely related due to philopatry, there was no evidence that females preferentially chose close relatives. Andersson and Ahlund (2000) used egg albumin to assess genetic relatedness between parasitic and host goldeneyes Bucephala islandica. This approach has two important advantages (Lyon and Eadie, 2000; Andersson and Ahlund, 2001): 1) eggs can be sampled in a non-destructive manner just after they are laid (at least for species with relatively large eggs), and 2) the dozen or more different proteins in albumin are maternal products and therefore allow the genotype of the female that laid the eggs to be sampled directly. This simplifies parentage analyses in which the goal is to study only the egg-laying patterns of females. Parasitic goldeneyes laid eggs in the nests of relatives slightly more often than expected by chance and also laid a larger number of parasitic eggs per nest when parasitizing close relatives than when parasitizing non-relatives (Andersson and Ahlund, 2000). Behavioral data suggested that females associate with and parasitize familiar individuals such as their social mother and sisters (individuals that are often but not always also genetic mothers and sisters), providing a mechanism for imperfect kin recognition. These data are consistent with hypotheses that suggest a role for kin selection in the evolution of CBP in ducks with female site fidelity. Theoretical models, however, lead to differing

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ism to catch up with long-standing models of genetic evolution (Rothstein, 1975; Kelly, 1987). ACKNOWLEDGMENTS Our work on indigobirds has been supported by National Science Foundation grants to R. B. P. and M. D. S. We thank Mary Beth Saffo for organizing this symposium. Steve Rothstein, Kristina Sefc, and two anonymous reviewers provided helpful comments on the manuscript. REFERENCES Alderson, G. W., H. L. Gibbs, and S. G. Sealy. 1999a. Parentage and kinship studies in an obligate brood parasitic bird, the brown-headed cowbird (Molothrus ater), using microsatellite DNA markers. J. Heredity 90:182–190. Alderson, G. W., H. L. Gibbs, and S. G. Sealy. 1999b. Determining the reproductive behaviour of individual brown-headed cowbirds using microsatellite DNA markers. Anim. Behav. 58:895– 905. Alvarez, F. 1996. Model cuckoo Cuculus canorus eggs accepted by rufous bush chats Cercotrichas galactotes during the parasite’s absence from the breeding area. Ibis 138:340–342. Alves, M. A. S. and D. M. Bryant. 1998. Brood parasitism in the sand martin, Riparia riparia: Evidence for two parasitic strategies in a colonial passerine. Anim. Behav. 56:1323–1331. Andersson, M. 2001. Relatedness and the evolution of conspecific brood parasitism. Am. Nat. 158:599–614. Andersson, M. and M. Ahlund. 2000. Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird. Proc. Natl. Acad. Sci. U.S.A. 97:13188–13193. Andersson, M. and M. Ahlund. 2001. Protein fingerprinting: A new technique reveals extensive conspecific brood parasitism. Ecology 82:1433–1442. Aragon, S., A. P. Møller, J. J. Soler, and M. Soler. 1999. Molecular phylogeny of cuckoos supports a polyphyletic origin of brood parasitism. J. Evol. Biol. 12:495–506. Baker, A. J. (ed.) 2000. Molecular methods in ecology. Blackwell Science, Oxford. Beauchamp, G. 1997. Determinants of intraspecific brood amalgamation in waterfowl. Auk 114:11–21. Beauchamp, G. 1998. The relationship between intra- and interspecific brood amalgamation in waterfowl. Condor 100:153–162. Birkhead, T. R., T. Burke, R. Zann, F. M. Hunter, and A. P. Krupa. 1990. Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting. Behav. Ecol. Sociobiol. 27:315–324. Blouin, M. S., M. Parsons, V. Lacaille, and S. Lotz. 1996. Use of microsatellite loci to classify individuals by relatedness. Mol. Ecol. 5:393–401. Bremer, K. 1988. The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803. Brooke, M. D. and N. B. Davies. 1991. A failure to demonstrate host imprinting in the cuckoo (Cuculus canorus) and alternative hypotheses for the maintenance of egg mimicry. Ethology 89: 154–166. Brooke, M. D., N. B. Davies, and D. G. Noble. 1998. Rapid decline of host defences in response to reduced cuckoo parasitism: Behavioural flexibility of reed warblers in a changing world. Proc. Roy. Soc. London B 265:1277–1282. Brown, P. O. and D. Botstein. 1999. Exploring the new world of the genome with DNA microarrays. Nature Genetics 21:33–37. Burke, T. and M. W. Bruford. 1987. DNA fingerprinting in birds. Nature 327:149–152. Cann, R. L. 2001. Genetic clues to dispersal in human populations: Retracing the past from the present. Science 291:1742–1748. Carter, K. L., B. C. Robertson, and B. Kempenaers. 2000. A differential DNA extraction method for sperm on the perivitelline membrane of avian eggs. Mol. Ecol. 9:2149–2150.

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pendence due to common ancestry can now be used to test some of these hypotheses—for example, an independent contrasts analysis (Felsenstein, 1985) could examine whether egg size among parasitic cuckoos changes in relation to the egg size of each species’ predominant host(s). Other issues to address in an explicitly phylogentic context include the ecological variables associated with the evolution of obligate parasitism and CBP (Rohwer and Freeman, 1989; Beauchamp, 1997, 1998; Poiani, 1998; Kru¨ger and Davies, 2002), host use in relation to host life history (Soler et al., 1999c), and behavioral or morphological traits that are presumed to have evolved either as adaptations for or defenses against parasitism (e.g., Soler and Møller, 1996; Hosoi and Rothstein, 2000; Kru ¨ger and Davies, 2002). Many studies of host-parasite coevolution have implicitly assumed that the relevant evolutionary time-scale is shorter than the history of the species involved, thus allowing correlation due to common ancestry to be ignored. Behaviors such as egg rejection, however, may include a historical component (e.g., Rothstein, 2001) that should be evaluated in the context of a comparative analysis. Perhaps the most exciting prospect in coming years will be the application of functional genomics and developmental genetics to the study of brood parasitism. Advancing technology may soon make feasible the identification and characterization of genetic loci that determine the interesting behavioral and morphological adaptations of brood parasites and their hosts. The mapping of quantitative trait loci using amplified fragment length polymorphisms (AFLPs) is one potential approach (Mueller and Wolfenbarger, 1999), although this will yield markers that are only linked to genes of potential interest. DNA chip technology (or gene expression arrays) perhaps offers the greatest potential for directly identifying genes that may play a role in specific traits (Brown and Botstein, 1999; Lockhart and Winzeler, 2000). Once specific genes and their actions are identified, allelic variation in these genes (or in their regulatory regions) among populations or species showing different behavior and morphology could be evaluated. In addition to providing a complete understanding of behavioral and morphological evolution from the ecology of the organism down to the DNA sequence level, the study of functional genes will allow new questions about coevolution to be addressed. For example, have allopatric populations of a parasitic species independently evolved egg or nestling mimicry of the same host species? Independent lineages might solve the same ecological problem in a slightly different way at the DNA sequence level (see Jessen et al. [1991] for an example involving hemoglobin). If segregating alleles that influence host rejection behavior, for example, can be identified, selection and the frequency of these alleles in host populations experiencing different rates and histories of parasitism could be measured, allowing empirical studies of brood parasit-

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