The Auk 121(1):156–161, 2004 BEHAVIORAL AND GENETIC IDENTIFICATION OF A HYBRID VIDUA: MATERNAL ORIGIN AND MATE CHOICE IN A BROOD-PARASITIC FINCH R g B. P ~ 1,3 i M h D. S x 2 1Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA; and 2Department of Biology, Boston University, Boston, Massachuse s 02215, USA
Agx h .—Hybrid male Vidua were observed in the fi eld and recorded to document host song mimicry. The mtDNA of one male was sequenced to identify the maternal parent. The hybrid males mimicked songs of Melba Finch (Pytilia melba), the usual host of Long-tailed Paradise Whydah (V. paradisaea), but the mtDNA matched that of indigobirds (V. chalybeata or another species), which parasitize and mimic other estrildid fi nches. This combination of song behavior and genetics is consistent with a two-generation history that began with a female indigobird (e.g. V. chalybeata) laying in a Melba Finch nest rather than in a nest of her usual host (e.g. Red-billed Firefi nch [Lagonosticta senegala]). Her daughter, genetically an indigobird, imprinted on her Melba Finch foster parents and then mated with a male paradise whydah mimicking Melba Finch song. She also laid eggs in Melba Finch nests. Her son, the male hybrid carrying his grandmother’s indigobird mtDNA, learned and later mimicked Melba Finch song. Genetic identifi cation of the maternal species origin of this hybrid supports a model of mate choice based on mimetic song in the Vidua fi nches. Received 15 February 2003, accepted 5 October 2003.
R xz .—Se observaron machos híbridos del género Vidua en el campo y se grabaron sus vocalizaciones para documentar la imitación del canto de su hospedero. También se secuenció el ADN mitocondrial (ADNmt) de uno de los machos para identifi car a la especie madre. Los machos híbridos imitaron el canto de la especie Pytilia melba, el hospedero usual de Vidua para- disaea, pero el ADNmt coincidió con el de una viuda (V. chalybeata u otra especie) que parasita e imita el canto de otros pinzones estríldidos. Esta combinación del comportamiento de canto y la genética es consistente con una historia de dos generaciones que comenzó con una viuda hembra (e.g. V. chalybeata) que puso un huevo en un nido de P. melba y no en un nido de su hospedero habitual, Lagonosticta senegala. Su hij a, genéticamente una viuda, se improntó en sus padres putativos (P. melba) y luego se apareó con un macho de la especie V. paradisaea, que imitaba el canto de P. melba. Ella también puso huevos en nidos de P. melba. Su hij o, el macho híbrido que llevaba el ADNmt de viuda de su abuela, aprendió y más tarde imitó el canto de P. melba. La identifi cación genética de la especie materna que originó a este híbrido apoya un modelo de selección de pareja basado en cantos miméticos en el género Vidua.
B brood-parasitic of a diff erent host (1) if other male traits (e.g. fi nches of the genus Vidua provides a mechanism plumage, fl ight displays) are more important for reproductive isolation of populations associ- than song in female choice, (2) if female choice is ated with diff erent host species. Males learn and constrained by the availability of males singing mimic the songs of their host (Nicolai 1973, Payne the appropriate host song, or (3) if males engage et al. 1998) and females use male song mimicry to in unsolicited copulation with females of other discriminate among potential mates, preferring parasitic species. Unsolicited copulation leads to males reared by the same host species (Nicolai extrapair fertilizations in other songbirds (Payne 1964, Payne et al. 2000). Occasional hybridiza- and Payne 1989, Westneat 1990, Westneat et al. tion may occur when females do not actively 1990). Alternatively, behavioral imprinting could choose their mate on the basis of song. Females lead to hybridization (Grant and Grant 1997) if may reproduce with males mimicking the songs female Vidua imprint on an alternative host dur- ing the period of parental care and as a result actively choose to mate with males of another 3E-mail: [email protected] species.
156 January 2004] Identifi cation of a Hybrid Vidua 157
Two hybrid male Vidua were observed and H6313 (Sorenson et al. 1999). Sequences reported here tape-recorded at Lochinvar National Park in have been deposited in GenBank (accession numbers: Zambia in 1973 (Payne 1980). Judging from AF407022, AF407108, AY322693, AY323559, AY323565, morphology, those males were the product AY324263). of a cross between a Long-tailed Paradise R xz x Whydah (V. paradisaea), the specialist brood- parasite of Melba Finch (Pytilia melba; Nicolai The hybrid males were morphologically inter- 1969), and one of three indigobird species in mediate between V. paradisaea and indigobirds the area: Purple Indigobird (V. purpurascens), (see Payne 1980 for photographs). The hybrid Village Indigobird (V. chalybeata), or Twinspot male that was collected was all black, with a long Indigobird (V. codringtoni). The male hybrids tail that consisted of inner rectrices 170 mm in mimicked Melba Finch song and not the songs length and rectrices number 2 that were 194 mm of any normal indigobird host species, and in length and enclosed the inner pair. Rectrices therefore must have been reared in Melba Finch number 2 were slender and shaped like those nests (Payne 1980). Because male indigobirds of V. paradisaea rather than those of Broad-tailed were seen to engage in unsolicited matings with Paradise Whydah (V. obtusa), the other species female whydahs, Payne (1980) reasoned that the of paradise whydah at Lochinvar. Wing length mother of the hybrids was a whydah that was of the hybrid was 75 mm, intermediate between fertilized by an indigobird and then laid eggs in wing lengths of V. paradisaea and indigobirds nests of her usual host, the Melba Finch. (Payne 1980). Employing a method common in studies The Long-tailed Paradise Whydah mimics of songbird hybridization (Gelter et al. 1992, the songs of Melba Finch, its estrildid fi nch host Joseph and Moritz 1993, Jung et al. 1994, species, and those songs are unlike those of fi re- Rohwer 1994), we used mitochondrial DNA fi nches (Lagonosticta senegala and L. rhodopareia) (mtDNA) to identify the maternal origin of a or Peters’ Twinspot (Hypargos niveogu atus), the hybrid male Vidua, testing the expectation that hosts of the three indigobird species that breed it would have paradise whydah mtDNA. The at Lochinvar (Payne et al. 1993). The songs of unexpected result of the genetic analysis, in the hybrid Vidua clearly matched those of Melba combination with data on the hybrid’s song, Finch, the usual host species of V. paradisaea (see supports a two-generation model of hybridiza- Payne 1980 for audiospectrograms). tion in which female mate choice based on male Contrary to expectation, mtDNA sequences song leads to hybridization in the generation from the hybrid specimen were clearly indi- aV er a female Vidua lays in the nest of an alter- gobird sequences and not paradise whydah native host. We discuss the implications of this sequences for both the control region and ND2 result for understanding mate choice and egg- (Fig. 1). Because mtDNA is maternally inher- laying behavior in parasitic fi nches and pa erns ited, the mother of the hybrid was therefore an of genetic variation among Vidua species. indigobird rather than a paradise whydah. The identity of the mother’s species within the in- M ix digobird species complex is uncertain, because One of the hybrid males was collected and pre- the indigobirds breeding at Lochinvar and else- pared as a specimen in 1973 (UMMZ 219770). A single where in southern Africa are only marginally primary feather was plucked from that specimen diff erentiated in mtDNA haplotype frequencies and DNA was extracted from the calamus using a and a number of closely related haplotypes are QIAamp Tissue Kit (Qiagen, Valencia, California) shared among species (Klein and Payne 1998, supplemented with 30 µL of 100 mg mL–1 dithiothrei- Sorenson et al. 2003). Mitochondrial DNA nu- tol (DTT) added to the tissue digestion buff er (Cooper cleotide sequences, however, clearly distinguish 1994). The 5’ half of the control region was ampli- indigobirds from paradise whydahs (Fig. 1) and fi ed and sequenced using primers IndigoC1F1 and FinchC1R1 (Sorenson and Payne 2001). The resulting all other Vidua species (Sorenson et al. 2003). sequence was compared to those for all Vidua species. The unexpected result was confi rmed by repeating the D xhzxx entire process with a second feather, the extract from which was used to amplify the 3’ half of NADH dehy- The combined data on morphology, mi- drogenase subunit 2 (ND2) using primers L5758 and metic song behavior, and mtDNA allow a 158 P ~ i S x [Auk, Vol. 121
F . 1. Comparison of control region and ND2 sequences for the hybrid Vidua (UMMZ 219770), V. purpurascens (UMMZ 231300), V. paradisaea (RBP.A81, specimen in National Museum of Malawi), and V. ob- tusa (UMMZ 231380). Only variable sites are shown. Nucleotides matching the hybrid are indicated by dots. In the control region and ND2 fragments, respectively, the hybrid differs from the V. purpurascens individual at 1 of 490 alignment positions (0.2%) and 3 of 549 positions (0.5%). By comparison, genetic divergence in the control region ranges ≤0.8% among southern indi- gobird haplotypes. The hybrid differs from the whyd- ahs at 31–32 positions in the control region (6.3-6.5%) F . 2. Two models for the origin of a male paradise and 64–65 positions in ND2 (11.7–11.8%). whydah × indigobird hybrid. See text for a descrip- tion of the events involved. Note that two reciprocal reconstruction of the events producing the hy- models produce male hybrids with the song of an in- brid male Vidua. The hybrid mimicked the song digobird host, but those are not relevant to the present of Melba Finch, the host of Long-tailed Paradise example in which the hybrid was already known to Whydah, whereas its mtDNA indicates that its have Melba Finch song. In addition, a model similar mother was an indigobird. The intermediate to that shown in (B) posits a male indigobird offspring in the first generation. If that male imprints on Melba male breeding plumage—between that of an Finches and sings Melba Finch song as an adult, it indigobird and a paradise whydah—therefore might attract a female Long-tailed Paradise Whydah indicates that the father was a paradise whydah. that would lay in a Melba Finch nest, producing a Figure 2 presents two alternative models for the hybrid son in the second generation that has Melba production of this hybrid. In the fi rst (Fig. 2A), Finch song and paradise whydah mtDNA, the same a female paradise whydah mates with a male combination as in (A). indigobird (whether by choice or coercion), then lays an egg in a nest of her usual host, Melba Finch rather than in the nest of her usual host, Finch. Her son, the male hybrid, learns Melba a fi refi nch (if the indigobird was V. purpura- Finch song from his foster parents and carries his scens or V. chalybeata) or a Peters’ Twinspot (if mother’s paradise whydah mtDNA. That model, the indigobird was V. codringtoni). In the next however, is inconsistent with the observation generation, her daughter (a bird that was not that the hybrid male has indigobird mtDNA. knowingly observed in the fi eld) is genetically In a second model consistent with all of an indigobird but imprints on her Melba Finch the empirical observations (Fig. 2B), a female foster parents and learns their songs. As a re- indigobird mates with a male indigobird as sult, she chooses to mate with a male paradise usual but lays an egg in the nest of a Melba whydah mimicking Melba Finch song and lays January 2004] Identifi cation of a Hybrid Vidua 159 her eggs in nests of Melba Finch, the host spe- explanation for both female mate choice (based cies on which she is imprinted (see Payne et al. on song) and egg-laying behavior in the second 2000). Her son, the male hybrid, learns and later generation. This model is consistent with ex- mimics Melba Finch song and also carries his perimental evidence that female Vidua choose grandmother’s indigobird mtDNA. males that mimic the songs of their own foster Captive cross-fostering experiments support species (Payne 1973a, b; Payne et al. 2000). the essential elements of the second model. Given that diff erent Vidua species mimic Young male indigobirds imprint on songs of the nestling mouth pa erns of their respective their foster species and sing the foster species’ hosts, our model requires that estrildid fi nch songs as adults, even when the foster species is hosts at least occasionally rear brood-parasitic not their normal host (Nicolai 1973, Payne et al. Vidua with mouth colors and pa erns unlike 1998). Female Vidua also imprint on the songs of those of their own young. Red-billed Firefi nches a novel foster species and as adults are sexually (L. senegala), which are normally parasitized a racted to male Vidua that mimic those songs by a mimetic indigobird, will rear other spe- (Payne et al. 2000). In addition, those females cies in captivity, as will other estrildid fi nches parasitize nests of the species that reared them, (Immelmann et al. 1965, Goodwin 1982). In our even when active nests of their normal host spe- aviaries, L. senegala have successfully reared to cies are available in the same aviary (Payne et fl edging and independence nestlings of Blue- al. 2000). Thus, infrequent hybridization among capped Cordon-bleu (Uraeginthus cyanocepha- Vidua species may result from a two-generation lus) and Goldbreast (Amandava subfl ava), two process that begins with an egg-laying “mis- species that are likewise successful in rearing take” rather than mating between males and other estrildids as well as Vidua with mouth pat- females that are imprinted on diff erent hosts. terns diff erent from their own young (Payne et Throughout this process, females actively al. 2001). In addition, various combinations of choose to mate with males based on their host- estrildids, including both closely related species mimetic songs (Fig. 2B). and species in diff erent genera, produce hybrid Alternatively, female Vidua might choose off spring in captivity (Lynch 1989, Fehrer 1993). males on the basis of plumage (Barnard 1990, Nestlings of nearly all estrildid species have Oakes and Barnard 1994) rather than song. In diff erent palate marks and colors (Immelmann particular, female indigobirds might prefer et al. 1965, Goodwin 1982) and hybrid nestlings males with long tails like those of male para- have mouth pa erns unlike those of either par- dise whydahs, perhaps because they retain an ent species, yet hybrids are reared by mixed- ancestral sensory bias (Ryan and Rand 1993). species pairs to fl edging and independence. Phylogenetic analyses suggest that short-tailed The occurrence of hybrids between diff erent indigobirds may be derived from long-tailed estrildid species and successful cross-fostering ancestors (Klein and Payne 1998, Sorenson and demonstrate that parent fi nches can rear young Payne 2001). A hybrid with indigobird mtDNA with mouth pa erns and colors unlike those of could be produced by a female indigobird their own species. a racted to the long tail of a male paradise Perhaps the most interesting implication of whydah. That hybrid, however, would have the Lochinvar hybrid is that it serves as a model Melba Finch song only if his fi refi nch-reared of the usual mode of hybridization among in- mother also laid in a Melba Finch nest, a sec- digobirds, a species complex in which mtDNA ond unexpected event in the same generation. haplotypes are shared among morphologically Furthermore, there is no evidence that female distinct species (Sorenson et al. 2003). Hybrids indigobirds prefer males with long tails; female between two indigobird species are likely pro- indigobirds implanted with estradiol did not duced by essentially the same chain of events approach or solicit male indigobirds with ex- but go unnoticed because the species are similar perimentally elongated tails (R. B. Payne et al. in size and color and the females of some species unpubl. data). are not morphologically distinguishable (Payne The two-generation model presented above 1996). In contrast, the indigobird × whydah (Fig. 2B) requires a single unexpected event hybrid could be recognized by its unusual mor- in the fi rst generation (an indigobird laying phology. As in Figure 2B, the two-generation in a Melba Finch nest) and provides a clear process begins with a female indigobird laying 160 P ~ i S x [Auk, Vol. 121 in the nest of an estrildid host that is already laboratory at the University of Michigan Museum associated with another indigobird species. The of Zoology. R. 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