Incomplete reproductive isolation following host shift in brood parasitic indigobirds

Behavioural and molecular studies suggest that brood parasitic indigobirds (Vidua spp.) rapidly diversified through a process of speciation by host shift. However, behavioural imprinting on host song, the key mechanism promoting speciation in this system, may also lead to hybridization and gene flow among established indigobird species when and if female indigobirds parasitize hosts already associated with other indigobird species. It is therefore not clear to what extent the low level of genetic differentiation among indigobird species is due to recent common ancestry versus ongoing gene flow. We tested for reproductive isolation among three indigobird species in Cameroon, one of which comprises two morphologically indistinguishable host races. Mimicry of host songs corresponded with plumage colour in 184 male indigobirds, suggesting that females rarely parasitize the host of another indigobird species. Paternity analyses, however, suggest that imperfect specificity in host and/or mate choice allows for continuing gene flow between recently formed host races of the Cameroon Indigobird Vidua camerunensis; while 63 pairs of close relatives were associated with the same host, two strongly supported father-son pairs included males mimicking the songs of the two different hosts of V. camerunensis. Thus, complete reproductive isolation is not necessarily an automatic consequence of host shifts, a result that suggests an important role for natural and/or sexual selection in indigobird speciation.     

Song mimicry of Black-bellied Firefinch Lagonosticta rara and other finches by the brood-parasitic Cameroon Indigobird Vidua camerunensis in West Africa

Brood-parasitic finches Vidua spp. mimic songs of their foster species, with most Vidua species both mimicking songs and parasitizing nests of a single estrildid finch species. We describe a behavioural radiation in the Cameroon Indigobird Vidua camerunensis . Local populations are polymorphic in behaviour, each male mimicking songs of a single species, with certain males mimicking songs of one species and other males mimicking songs of another host species. The species most often mimicked in song are Black-bellied Firefinch Lagonosticta rara and African Firefinch L. rubricata ; other species mimicked in song are Brown Twinspot Clytospiza monteiri and Dybowski's Twinspot Euschistospiza dybowskii . Indigobirds in the different mimicry song populations do not differ morphologically in plumage colour or size. The lack of morphological differences between male indigobirds with different mimicry songs is consistent with a recent behavioural radiation through host shifts, perhaps facilitated by environmental change associated with prehistoric cultivation of grain. The mimicry song populations of indigobirds, behaviourally imprinted upon different host species, support the idea of a process of speciation driven by a shift to new host species.     

Genetic continuity of brood-parasitic indigobird species

Speciation in brood-parasitic indigobirds (genus Vidua) is a consequence of behavioural imprinting in both males and females. Mimicry of host song by males and host fidelity in female egg laying result in reproductive isolation of indigobirds associated with a given host species. Colonization of new hosts and subsequent speciation require that females occasionally lay eggs in the nests of novel hosts but the same behaviour may lead to hybridization when females parasitize hosts already associated with other indigobird species. Thus, retained ancestral polymorphism and ongoing hybridization are two alternative explanations for the limited genetic differentiation among indigobird species. We tested for genetic continuity of indigobird species using mitochondrial sequences and nuclear microsatellite data. Within West Africa and southern Africa, allopatric populations of the same species are generally more similar to each other than to sympatric populations of different species. Likewise, a larger proportion of genetic variation is explained by differences between species than by differences between locations in alternative hierarchical AMOVAS, suggesting that the rate of hybridization is not high enough to homogenize sympatric populations of different species or prevent genetic differentiation between species. Broad sharing of genetic polymorphisms among species, however, suggests that some indigobird species trace to multiple host colonization events in space and time, each contributing to the formation of a single interbreeding population bound together by songs acquired from the host species.     

A new species of firefinch Lagonosticta from northern Nigeria and its association with the Jos Plateau Indigobird Vidua maryae

A firefinch of the Jos Plateau, northern Nigeria, is described as a new species, Rock Fire-finch Lagonosticta sanguinodorsalis. This firefinch has distinctive songs and a distinctive habitat—bushy and grassy rocky outcrops on the plateau and inselbergs to the north and east. It has a blue-grey bill, red back in the male and reddish brown back in the female and juvenile and broad primaries in both the adult and juvenile. It appears most closely related to the Mali Firefinch Lagonosticta virata and the Chad Firefinch Lagonosticta umbrinodorsalis. Its songs are mimicked by the brood-parasitic Jos Plateau Indigobird Vidua maryae , which occurs within the range of the firefinch and whose songs led to the discovery of the firefinch. The songs of the firefinch, the song mimicry of the indigobird and the apparent continuity of song mimicry across 27 years indicate a unique association of this distinct pair of species.     

Vocal mimicry of the paraside whydahs (Vidua) and response of female whydahs to the songs of their hosts (Pytilia) and their mimics

Parasitic paradise whydahs (Vidua paradisaea) mimic the vocalizations of their hosts, Pytilia melba. Photostimulated female whydahs isolated in large aviaries responded to broadcasts of recorded song. Approach occurred significantly more often to songs of the host species P. melba than to the similar P. phoenicoptera. Females approached with equal frequency the songs recorded from their hosts and the mimetic songs of the male whydahs. No significant differences were found between the responses of females to songs of sympatric and allopatric forms of their host. It is suggested that mimetic songs of males and the responses of females are behavioural isolating mechanisms among species of whydahs.     

Behavioural and genetic evidence of a recent population switch to a novel host species in brood-parasitic indigobirds Vidua chalybeata

We describe a population of Village Indigobirds Vidua chalybeata on the Zambezi River that parasitizes the nests and mimics the songs of a novel host species, Brown Firefinch Lagonosticta nitidula , yet coexists with a population that mimics the usual host species of this indigobird, Red-billed Firefinch L. senegala . Male indigobirds mimicking the song of L. nitidula are morphologically indistinguishable from those that mimic songs of the usual host, L. senegala . Likewise, nestling indigobirds in broods of L. nitidula and L. senegala are similar in having mouth markings that mimic the nestlings of L. senegala rather than those of the novel host. Molecular genetic evidence indicates that the host switch to L. nitidula has involved at least four different indigobird matrilines. Indigobirds that are associated with L. nitidula are genetically similar to the indigobirds associated with sympatric L. senegala , and not to the indigobirds associated with west African Bar-breasted Firefinch L. rufopicta , the species that is most closely related to L. nitidula . Because field and experimental studies show that female indigobirds prefer males that mimic the songs of their own foster species, and females choose the same host to parasitize, the indigobirds reared by a novel host form a distinct breeding population. Taken together, behavioural, morphological and genetic evidence indicates a recent host switch by indigobirds in the Zambezi region from their old host L. senegala to a new host L. nitidula .     

Song of the finch Lagonosticta senegala: Interspecific mimicry by its brood-parasite Vidua chalybeata and the role of song in the host's social context

The African village indigobird Vidua chalybeata mimics the song of its brood-host, the Senegal firefinch Lagonosticta senegala. Firefinches in large aviaries did not respond to mimicry of their song and calls by indigobirds in the same aviaries. The lack of agonistic reaction by the firefinches is related to the non-agonistic meaning of song in the social behaviour of the firefinches. Song was not given during experimentally induced aggressive behaviour in the firefinches, but was given during courtship and by both male and female firefinches separated from their mates. Thus the main communicative function of song in L. senegala is in pair-bond maintenance.     

Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata

Brood-parasitic village indigobirds, Vidua chalybeata, were bred in captivity and foster-reared by their normal host species, the red-billed firefinch, Lagonosticta senegala, or by an experimental foster species, the Bengalese finch, Lonchura striata. Captive-reared female indigobirds were tested as adults for mate choice and for host choice. In tests of mate choice, female indigobirds responded preferentially towards mimicry songs of male indigobirds that were similar to those of the females' own foster parents. Females reared by Bengalese finches responded to male songs that mimicked Bengalese finch song rather than to male songs that mimicked their normal host species, the firefinch. In tests of host choice, females reared by Bengalese finches laid in the nests of Bengalese finches, and females reared by firefinches laid in the nests of firefinches. Wild-caught females showed the same behaviours as captive-bred females reared by firefinches. A female indigobird's social companions (firefinch or Bengalese) following her independence of her foster parents had no effect on her sexual response to male mimicry song or her choice of a host species in brood parasitism. The results support the predictions of a model of imprinting-like behaviour development in which young indigobirds focus their attention on their foster parents, rather than a model of innate bias for songs and nests of their normal host species, or a null model of nonspecific brood parasitism and differential survival. The results provide experimental support for the recent origin of brood parasite-host associations and the significance of imprinting in speciation in these brood parasites. Copyright 2000 The Association for the Study of Animal Behaviour.     

Randomization Analyses: Mimicry, Geographic Variation and Cultural Evolution of Song in Brood-Parasitic Straw-Tailed Whydahs, Vidua fischeri

Although bird song has been an important model for investigating questions of behavior development, cultural evolution and population differentiation, the quantitative methods of analysis have been problematic. Here we develop and apply quantitative randomization methods to test hypotheses about these processes in a natural population of birds. Songs of the African brood-parasitic straw-tailed whydahs ( Vidua fischeri ) and songs of their host species, the purple grenadier ( Granatina ianthinogaster ), were compared in audiospectrograms for similarity to test the following hypotheses: Whydahs mimic the songs of their host species, they have local song dialects, neighboring males match their song themes, local males match the songs of local hosts, remote populations have different songs according to their geographic distance, and songs undergo cultural evolution over time across generations. Randomization analyses were completed using (1) Mantel matrix statistics and (2) tree-based measures employing Sankoff optimization of Manhattan matrices and approximate randomizations. Our results provide evidence for song mimicry, local song dialects, matching song themes between neighboring males, song matching of local whydah mimics and grenadier song models, correspondence of song differences and geographic distance, and cultural continuity with change in song traditions within a local population. These randomization methods may be useful in other studies of animal communication, and they are sufficiently general for use both with distance matrices derived either from naturalistic impressions of song similarity as in our example or from acoustic measurements.     

Clade-limited colonization in brood parasitic finches (Vidua spp.)

The African brood parasitic finches (Vidua spp.) are host specialists that mimic the songs and nestling mouth markings of their finch hosts (family Estrildidae). Although recent molecular analyses suggest rapid speciation associated with host switches in some members of this group, the association of different Vidua lineages with particular host genera suggests the possibility of cospeciation at higher levels in the host and parasite phylogenies. We compared a phylogeny of all Vidua species with a phylogeny of their estrildid finch hosts and compared divergence time estimates for the two groups. Basal divergences among extant members of the Vidulidae and among Vidua species are more recent than those among host genera and species, respectively, allowing a model of cospeciation to be rejected at most or all levels of the Vidua phylogeny. Nonetheless, some tests for cospeciation indicated significant congruence between host and parasite tree topologies. This result may be an artifact of clade-limited colonization. Host switches in parasitic finches have most often involved new hosts in the same or a closely related genus, an effect that increases the apparent congruence of host and parasites trees.     

Genetic Control of Acoustic Behavior in Crickets

Evidence is presented that acoustic behavior in field cricketsis under firm genetic control. The calling song of adult malesis highly stereotyped and species specific. Hybrids can be madeby crossing two species of Teleogryllus with dissimilar callingsongs. The calling songs of the hybrids are uniquely differentfrom that of either parental species, and in addition the songsof the two reciprocal hybrids are different from each other.Genetic control of song production is polygenic and multichromosomal;sex-linkage of some song determinants is also indicated. Femalephonoresponse to calling song was measured on a Y-maze. Speciesspecificity of phonoresponse was confirmed and in addition,hybrid females prefer hybrid song to either parental song. Thepossibility that calling song production in the male and itsreception in the female are genetically coupled is discussed.     

SONG MIMICRY AND SPECIES STATUS OF THE GREEN WIDOWFINCH VIDUA CODRINGTONI

Summary

Payne, R. B., Payne, L. L. &; Nhlane, M. E. D. 1992. Song mimicry and species status of the Green Widowfinch Vidua codringtoni. Ostrich 63:86-97.

The Green Widowfinch Vidua codringtoni mimics the songs of the Redthroated Twinspot Hypargos niveoguttatus, its apparent foster species, in Zimbabwe, Zambia and Mala?i. Of 38 male Green Widowfinches, 37 mimicked the twinspot; one mimicked a firefinch and not the twinspot. A wild-captured juvenile developed mimicry of twinspot song after six months and retained its mimicry through the next year. Male Green Widowfinches have glossy breeding plumage (green to blue), black wings, white bill and bright orange feet, a colour combination unlike other widowfinches in their range in southern Africa. Females are marginally distinguishable from other widowfinch species. Green Widowfinches occur together locally with Black V. funerea nigerrima, Purple V. purpurascens and Steelblue V. chalybeata Widowfinches and do not interbreed with them. The four species of widowfinches in southern Africa each have distributional ranges within the limits of their foster species.     

Genetic and Molecular Analysis of the Love Song Preferences of Drosophila Females

The courtship songs of male Drosophila have been studied atthe behavioural, genetic and molecular levels. Less attentionhas been paid to the female's responses to these songs. Playbackexperiments are described which suggest that courtship songsare an important component of female mate choice. Some of theimplications of the behavioural responses of hybrid femalesbetween D. melanogaster and D. simulans are examined in thelight of theories concerning the mechanisms by which insectcommunication systems might evolve. The role of the period genein both male song production and in female song reception isconsidered, and the neural regions in the female which may beimportant for song integration are briefly discussed.     

Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance

The elaborateness of many bird songs is commonly presumed tohave evolved under the influence of sexual selection by femalemate choice. Thus, aspects of acoustic diversity, such as songrepertoire size, are seen as likely targets of female choice.In many songbird species with song repertoires, however, therepertoires are small. In such species, female choice mightbe based on song features other than, or in addition to, songdiversity. To investigate this conjecture, I assessed singingand paternity in a population of chestnut-sided warblers (Dendroicapensylvanica), a species in which song repertoires are of modestsize. Twenty-two song traits were evaluated to determine whichones best predicted male extrapair reproductive success. Thecandidate traits encompassed measures of song diversity (e.g.,song repertoire size), gross-scale song performance (e.g., singingrate), and fine-scale song performance (e.g., variability amongsongs in a bout). Regression analysis revealed that the bestpredictor of extrapair success was singing with little variability.In particular, the most successful males sang with consistentpitch and timing, as well as high pitch. The greater extrapairsuccess of males with more consistent vocal performance maybe due to female preference for such performance, which couldbe an indicator of male quality.     

Song Learning in Bengalese Finches: a Comparison with Zebra Finches

Male Bengalese finches, Lonchura striata var. domestica, learn their song from an adult male conspecific with whom they can interact at 35 to 70 days of age and normally-raised males fail to reproduce song which they have only heard before or after this time. Birds which have been raised by their mother alone and those which have been deprived of a song tutor during the learning phase produce abnormal songs with indistinct elements and little or no phrase structure; this is typical of males which fail to hear adult song during their development. These songs are unstable and are replaced by normal songs, if there is an opportunity to learn from an adult male conspecific. Presumably, this flexibility in the time when young males learn acts as a safeguard to ensure that normal conspecific song is produced. These results bear striking similarity to those on zebra finch song development. Differences between the two species, especially in the learning of call notes by female zebra finches, are discussed.     

Song mimicry and species associations of west African indigobirds Vidua with Quail-finch Ortygospiza atricollis, Goldbreast Amandava subflava and Brown Twinspot Clytospiza monteiri

The brood-parasitic indigobirds Vidua spp. mimic the songs of their foster species, which for many species of indigobirds are Lagonosticta firefinches. We report additional associations of indigobirds with estrildid finches in west Africa. Quail-finch Indigobirds Vidua nigeriae in northern Cameroon mimic the songs of Quail-finch Ortygospiza atricollis . Gold-breast Indigobirds Vidua raricola in Cameroon and Sierra Leone mimic the songs of Gold-breast Amandava subflava . Both indigobirds are distinct in male breeding plumage from other indigobirds. Also, a population of blue indigobirds Vidua sp. in Cameroon mimics the songs of Brown Twinspot Clytospiza monteiri . They are similar in colour and size to blue indigobirds associated with Dark Firefinch L. rubricata and Black-bellied Firefinch L. rara . Mouth patterns of fledged young Quail-finch Indigobirds and Goldbreast Indigobirds resemble those of their song-model and presumed foster species, but the mouth pattern of a fledged young associated with the Brown Twinspot mimic was not distinct from the mouth of young Black-bellied Firefinch. The field observations show associations of certain species of indigobirds with finches other than the firefinches. The results are consistent with mitochondrial DNA estimates of greater genetic similarity among indigobirds than among their foster species. The field observations support the hypothesis of evolutionary associations of the brood parasite and foster species by colonization with switching from one foster to another rather than by cospeciation.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions

Oscine songbirds are exposed to many more songs than they keep for their final song repertoire and little is known about how a bird selects the particular song(s) to sing as an adult. We simulated in the laboratory the key variables of the natural song learning environment and examined the song selection process in nine hand-reared male song sparrows, Melospiza melodia, a species in which males sing 5-11 song types. During their second and third months (their presumed sensitive period), subjects were rotated equally among four live adult male tutors that had been neighbours in the field. Tutors were housed in individual aviary 'territories' in four corners of the roof of a building; subjects could see only one tutor at a time, but they could hear the others at a short distance. Later in their first year (months 5-12), half the subjects were again rotated among all four tutors and the other half were randomly stationed next to just one tutor. Results from this experiment confirm and extend the findings from our two previous field studies of song learning in this species. Young males in this experiment (1) learned whole song types, (2) learned songs from multiple tutors, (3) preferentially learned songs that were shared among their tutors, (4) learned songs that other young males in their group also chose, and (5) learned more songs from the tutor they were stationed next to during the later stage (stationary subjects). These last two results support the late influence hypothesis that interactions after a bird's sensitive period affect song repertoire development. Copyright 2000 The Association for the Study of Animal Behaviour.     

Inferring performance in the songs of dark-eyed juncos (Junco hyemalis)

Within bird species, songs differ in their attractiveness tofemales or effectiveness in male–male interactions. Somesongs are more difficult to sing than others, and receiversmay use a singer's performance of difficult songs as a meansfor evaluating the quality of the singer. The concept of songperformance aims at quantifying how physiologically demandingare different songs. Using variation between song types of dark-eyedjuncos, Junco hyemalis, we show that some song traits tradeoff with costly aspects of song output—short intervalsbetween syllables or loud sound amplitude—suggesting thatthose traits are difficult to sing. First, after controllingfor other traits, long syllables require longer intervals forrecovery. This supports the idea that a measure of "respiratoryperformance" could be based on the relative lengths of syllablesand intervals. Second, some syllable traits trade off stronglywith sound amplitude, suggesting that these traits may be difficultto sing at high amplitudes. The ratio of frequency bandwidthand trill rate has been used to infer performance in other birdspecies, but we found no evidence that frequency bandwidth tradesoff with any aspect of song output in the junco. The negativeassociation of bandwidth with trill rate may instead be a passiveconsequence of syllable length, with longer syllables randomlyaccumulating frequency modulation. We conclude that bird receiversmay best evaluate how well a song is performed if they integratemultiple cues and discuss how researchers may similarly devisemeasures of song performance.     

SONG POPULATIONS AND DISPERSAL IN STEELBLUE AND PURPLE WIDOWFINCHES

Payne, R. B. 1985. Song populations and dispersal in Steelblue and Purple Widowfinches. Ostrich 56:135-146.

Songs of Steelblue Widowfinches Vidua chalybeata were recorded over eight years at Lochinvar National Park, Zambia. Neighbouring males share their song-type repertoires. Individual birds changed the structural details of all song types in their repertoire from year to year, and over 4–5 years the songs accumulated changes so that a song type could scarcely be recognized as the same. A few males in addition switched their song repertoires when they dispersed from one song population to another, or when their old neighbours disappeared and new neighbouring males sang a different song repertoire. Individual marked adult birds moved from one song neighbourhood to another. Purple Widowfinches had a similar song behaviour but only one song dialect was found in the study area.

An estimate of the proportion of immigrants was made from the proportion of birds with songs unlike their neighbours, and from birds that had a mixed song repertoire or that switched their song repertoires. Song populations were sampled at several localities in the Transvaal, Botswana, Zambia, Kenya, Tanzania, Cameroon, and Nigeria. An overall minimal estimate of dispersal between song neighbourhoods was 18 %. The incidence of observed dispersal and the movements indicated by the song differences among local widowfinches were considerable and more than sufficient to prevent genetic isoloation and differentiation of local song populations.