BEHAVIORAL AND GENETIC IDENTIFICATION OF A HYBRID VIDUA: MATERNAL ORIGIN AND MATE CHOICE IN A BROOD-PARASITIC FINCH

Auk, The, Jan 2004 by Payne, Robert B, Sorenson, Michael D

ABSTRACT.-Hybrid male Vidua were observed in the field 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 finches. 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 Firefinch [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 identification of the maternal species origin of this hybrid supports a model of mate choice based on mimetic song in the Vidua finches. Received 15 February 2003, accepted 5 October 2003.

RESUMEN.-Se observaron machos hibridos del genero Vidua en el campo y se grabaron sus vocalizaciones para documentar la imitacion del canto de su hospedero. Tambien se secuencio el ADN mitocondrial (ADNmt) de uno de los machos para identificar a la especie madre. Los machos hibridos imitaron el canto de la especie Pytilia melba, el hospedero usual de Vidua paradisaea, pero el ADNmt coincidio con el de una viuda (V. chalybeata u otra especie) que parasita e imita el canto de otros pinzones estrildidos. Esta combinacion del comportamiento de canto y la genetica es consistente con una historia de dos generaciones que comenzo 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 habituai, Lagonosticta senegala. Su hija, geneticamente una viuda, se impronto en sus padres putativos (P. melba) y luego se apareo con un macho de la especie V. paradisaea, que imitaba el canto de P. melba. Ella tambien puso huevos en nidos de P. melba. Su hijo, el macho hibrido que llevaba el ADNmt de viuda de su abuela, aprendio y mas tarde imito el canto de P. melba. La identificacion genetica de la especie materna que origino a este hibrido apoya un modelo de seleccion de pareja basado en cantos mimeticos en el genero Vidua.

BEHAVIORAL IMPRINTING IN brood-parasitic finches of the genus Vidua provides a mechanism for reproductive isolation of populations associated with different host species. Males learn and mimic the songs of their host (Nicolai 1973, Payne et al. 1998) and females use male song mimicry to discriminate among potential mates, preferring males reared by the same host species (Nicolai 1964, Payne et al. 2000). Occasional hybridization may occur when females do not actively choose their mate on the basis of song. Females may reproduce with males mimicking the songs of a different host (1) if other male traits (e.g. plumage, flight displays) are more important than song in female choice, (2) if female choice is constrained by the availability of males singing the appropriate host song, or (3) if males engage in unsolicited copulation with females of other parasitic species. Unsolicited copulation leads to extrapair fertilizations in other songbirds (Payne and Payne 1989, Westneat 1990, Westneat et al. 1990). Alternatively, behavioral imprinting could lead to hybridization (Grant and Grant 1997) if female Vidua imprint on an alternative host during the period of parental care and as a result actively choose to mate with males of another species.

Two hybrid male Vidua were observed and tape-recorded at Lochinvar National Park in Zambia in 1973 (Payne 1980). judging from morphology, those males were the product of a cross between a Long-tailed Paradise Whydah (V. paradisaea), the specialist broodparasite of Melba Finch (Pytilia melba; Nicolai 1969), and one of three indigobird species in the area: Purple Indigobird (V. purpurascens), Village Indigobird (V. chalybeata), or Twinspot Indigobird (V. codringtoni). The male hybrids mimicked Melba Finch song and not the songs of any normal indigobird host species, and therefore must have been reared in Melba Finch nests (Payne 1980). Because male indigobirds were seen to engage in unsolicited matings with female whydahs, Payne (1980) reasoned that the mother of the hybrids was a whydah that was fertilized by an indigobird and then laid eggs in nests of her usual host, the Melba Finch.

Employing a method common in studies of songbird hybridization (Gelter et al. 1992, Joseph and Moritz 1993, jung et al. 1994, Rohwer 1994), we used mitochondrial DNA (mtDNA) to identify the maternal origin of a hybrid male Vidua, testing the expectation that it would have paradise whydah mtDNA. The unexpected result of the genetic analysis, in combination with data on the hybrid's song, supports a two-generation model of hybridization in which female mate choice based on male song leads to hybridization in the generation after a female Vidua lays in the nest of an alternative host. We discuss the implications of this result for understanding mate choice and egg-laying behavior in parasitic finches and patterns of genetic variation among Vidua species.