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A Single Ancient Origin of Brood Parasitism in African Finches: Implications for Host-Parasite Coevolution

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A Single Ancient Origin of Brood Parasitism in African Finches: Implications for Host-Parasite Coevolution Evolution, 55(12), 2001, pp. 2550±2567 A SINGLE ANCIENT ORIGIN OF BROOD PARASITISM IN AFRICAN FINCHES: IMPLICATIONS FOR HOST-PARASITE COEVOLUTION MICHAEL D. SORENSON1,2,3 AND ROBERT B. PAYNE3,4,5 1Department of Biology, Boston University, Boston, Massachusetts 02215 2E-mail: [email protected] 3Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109 4Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109 5E-mail: [email protected] Abstract. Robust phylogenies for brood-parasitic birds, their hosts, and nearest nesting relatives provide the framework to address historical questions about host-parasite coevolution and the origins of parasitic behavior. We tested phy- logenetic hypotheses for the two genera of African brood-parasitic ®nches, Anomalospiza and Vidua, using mito- chondrial DNA sequence data from 43 passeriform species. Our analyses strongly support a sister relationship between Vidua and Anomalospiza, leading to the conclusion that obligate brood parasitism evolved only once in African ®nches rather than twice, as has been the conventional view. In addition, the parasitic ®nches (Viduidae) are not recently derived from either weavers (Ploceidae) or grass®nches (Estrildidae), but represent a third distinct lineage. Among these three groups, the parasitic ®nches and estrildids, which includes the hosts of all 19 Vidua species, are sister taxa in all analyses of our full dataset. Many characters shared by Vidua and estrildids, including elaborate mouth markings in nestlings, unusual begging behavior, and immaculate white eggs, can therefore be attributed to common ancestry rather than convergent evolution. The host-speci®city of mouth mimicry in Vidua species, however, is clearly the product of subsequent host-parasite coevolution. The lineage leading to Anomalospiza switched to parasitizing more distantly related Old World warblers (Sylviidae) and subsequently lost these characteristics. Substantial sequence divergence between Vidua and Anomalospiza indicates that the origin of parasitic behavior in this clade is ancient (;20 million years ago), a striking contrast to the recent radiation of extant Vidua. We suggest that the parasitic ®nch lineage has experienced repeated cycles of host colonization, speciation, and extinction through their long history as brood parasites and that extant Vidua species represent only the latest iterations of this process. This dynamic process may account for a signi®cantly faster rate of DNA sequence evolution in parasitic ®nches as compared to estrildids and other passerines. Our study reduces by one the tally of avian lineages in which obligate brood parasitism has evolved and suggests an origin of parasitism that involved relatively closely related species likely to accept and provide appropriate care to parasitic young. Given the ancient origin of parasitism in African ®nches, ancestral estrildids must have been parasitized well before the diversi®cation of extant Vidua, suggesting a long history of coevolution between these lineages preceding more recent interactions between speci®c hosts and parasites. Key words. Base composition, brood parasitism, mitochondrial DNA, optimization alignment, Passeriformes, phy- logeny, Vidua. Received August 23, 2000. Accepted August 30, 2001. Some of the clearest examples of coevolution are provided include: How many times has obligate brood parasitism by avian brood parasites and their hosts (Rothstein 1990; evolved? Are behavioral and morphological characters shared Payne 1997a). Adaptations of parasitic species to secure pa- by parasites and their hosts due to common ancestry or se- rental care from hosts and counter-adaptations of hosts to lection on parasites to mimic their hosts? What are the rel- avoid or reduce the negative effects of parasitism have been ative ages of different parasitic lineages? Researchers have studied extensively in selected species (e.g., Payne 1977; begun to address some of these historical questions for dif- Davies and Brooke 1988). These studies have considered a ferent groups of parasitic birds (e.g., Lanyon 1992; Hughes variety of functional, mechanistic, and developmental aspects 1996, 2000; Klein and Payne 1998; Aragon et al. 1999; Gibbs of host-parasite interactions (e.g., Rothstein 1982; Lotem et et al. 2000). al. 1995; Kilner et al. 1999), but questions about the evo- Molecular phylogenies for the parasitic cowbirds (Moloth- lutionary history of brood parasitism have received less at- rus spp.) and other icterids (Lanyon 1992; Johnson and Lan- tention. yon 1999; Omland et al. 1999) con®rm a single origin of Well-corroborated phylogenies for brood parasitic species, brood parasitism in this group but also show that the bay- their hosts, and their closest nonparasitic relatives provide winged cowbird (``M.'' badius), a parental species that takes the basis for addressing a variety of questions about both the over other species' nests, is not closely related to the parasitic origins of parasitic behavior and host-parasite coevolution. cowbirds. Thus, the phylogeny provides no support for nest For example, Payne (1977, 1998a) suggested three possible takeover as a precursor to obligate brood parasitism in cow- precursors to obligate parasitism: (1) facultative parasitism birds. In addition, the nearly identical appearance of young of conspeci®cs and/or other species; (2) cooperative nesting; M. badius and M. rufoaxillaris, the specialist brood parasite and (3) the use or takeover of nests built by other species. of M. badius (Hudson 1874; Lichtenstein 2001), is clearly The presence or absence of these behaviors in the nesting the result of evolved mimicry rather than common ancestry relatives of brood parasitic birds provides a test of these (Lanyon 1992). Klein and Payne (1998) compared phylog- alternative hypotheses for the evolution of parasitism. Ad- enies of brood parasitic ®nches (Vidua spp.) with those of ditional questions that can be addressed using a phylogeny their estrildid hosts to test the hypothesis that these host- 2550 q 2001 The Society for the Study of Evolution. All rights reserved. PHYLOGENY OF BROOD-PARASITIC FINCHES 2551 have rarely been examined in a phylogenetic context. Chapin (1917, 1954), Friedmann (1960), and Kunkel (1969) reasoned that similar mouth markings in young Vidua and estrildids were evidence of their common ancestry. Other synapomor- phies of Vidua and estrildids include the absence of three muscles present in other Old World ®nches (Bentz 1979) and several plumage characters (Morlion 1980). Neunzig (1929), in contrast, argued for a relationship between Vidua and plo- ceids, reasoning that similarities in egg color, mouth mark- ings, and juvenile plumage between Vidua and their estrildid hosts were due to evolved mimicry rather than shared an- cestry. Nicolai (1964) described Vidua courtship displays and calls as being derived from those of ploceids, whereas Zis- wiler (1965, 1967) concluded that Vidua is more similar to the euplectines (Ploceidae) than to estrildids based on struc- FIG. 1. Phylogenetic hypothesis for Old World ®nches based on Sibley and Ahlquist (1990) and Sibley and Monroe (1990). Estril- tures of the horny palate and digestive tract. Small outer dini and Viduini were treated as tribes within Estrildinae (Sibley primaries (and long tails) in both Vidua and widowbirds (Eu- and Monroe 1990). This phylogeny implies independent origins of plectes spp.) have led various authors to group them together, obligate brood parasitism in Vidua and Anomalospiza. In this paper, either within Ploceidae (Delacour and Edmund-Blanc 1933± we treat most of the clades in this tree as family-level taxa (see 1934) or along with estrildids in Viduinae (as a subfamily Table 1). within Ploceidae, Sharpe 1890). By virtue of its yellow plumage, Anomalospiza was orig- speci®c parasites evolved in a process of host-parasite cospe- inally described as a cardueline canary and included in Frin- ciation. Their analysis indicated a very recent origin of the gillidae (e.g., Sharpe 1888). Chapin (1917, p. 259) grouped parasitic species, supporting a model of parasite speciation Anomalospiza with the estrildid ®nches, citing bill shape and through host colonization. the small outer primary, whereas Shelley (1905) included Current views on avian relationships suggest seven inde- both Vidua and Anomalospiza (along with estrildids and eu- pendent origins of obligate brood parasitism among birds plectines) in Viduidae. Anomalospiza also shares with Vidua (Sibley and Monroe 1990; Johnsgard 1997). This includes a common distribution in Africa, juvenile plumage that is three origins within Passeriformes: once in the New World distinct from the adult female's, and an unpneumatized fron- cowbirds (Icterinae) and twice in African ®nches, represented tal area in the skull of adults (Chapin 1954; Friedmann 1960; by the genera Vidua and Anomalospiza (Payne 1996, 1997a,b, Williams and Keith 1962), a trait found in estrildids that breed 1998a). The Vidua ®nches, including 10 indigobird species as early as three months of age (Morel 1973), but in few and nine long-tailed whydahs, are of particular interest be- adult ploceids (Disney 1980). Both genera are also obligate cause of their high degree of host speci®city and relatively brood parasites, although brood parasitism was not recog- benign effects on hosts as compared to other parasitic birds. nized in Anomalospiza until 1917 (Roberts 1917). Citing All Vidua parasitize estrildid ®nches (family
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