Robert B. Payne

Song learning and social interaction in indigo buntings

Abstract Indigo buntings ( Passerina cyanea ) isolated as individuals from 60 days of age developed abnormal songs. Birds isolated in groups for 9 to 10 months and then individually isolated developed slightly more normal songs but lacked the adult song figures. Birds copied the songs of adult tutors with whom they interacted socially. Birds with two tutors copied the songs of tutors that they could see and join in supplanting behaviour, but not songs of tutors from which they were visually isolated. One song was transmitted culturally across three generations under experimental conditions. The importance of social factors in song development of yearling buntings explains the development of local groups of males that share songs or dialects with each other in the field.

Speciation by host switch in brood parasitic indigobirds

A growing body of empirical and theoretical work supports the plausibility of sympatric speciation, but there remain few examples in which all the essential components of the process are well understood. The African indigobirds Vidua spp. are host-specific brood parasites. Indigobird nestlings are reared along with host young, and mimic the mouth markings of their respective hosts. As adults, male indigobirds mimic host song, whereas females use these songs to choose both their mates and the nests they parasitize. These behavioural mechanisms promote the cohesion of indigobird populations associated with a given host species, and provide a mechanism for reproductive isolation after a new host is colonized. Here we show that all indigobird species are similar genetically, but are significantly differentiated in both mitochondrial haplotype and nuclear allele frequencies. These data support a model of recent sympatric speciation. In contrast to the cuckoo Cuculus canorus, in which only female lineages are faithful to specific hosts, host switches have led to speciation in indigobirds because both males and females imprint on their hosts.

Local Song Traditions in Indigo Buntings: Cultural Transmission of Behavior Patterns Across Generations

Songs of indigo buntings were recorded at the E. S. George Reserve in southeastern Michigan from 1963 to 1980. A computer program was developed for the recognition of similar song patterns, using a catalog of audiospectrogram song figures and the sequence of the song figures. Neighboring buntings often matched their songs, usually with no more than five birds having the same song. Buntings from remote populations rarely matched the song of the George Reserve buntings. The probability of survival of song traditions was estimated from the historical data on the local songs. Most bunting songs of the 1960s no longer occur locally and either have disappeared or have altered beyond recognition by cultural drift. A few song types nevertheless have persisted in the local population for 15 years. Song types of adult buntings had an estimated annual exponential decay rate of 0.18 and an exponential half-life of 3.8 years. Estimated survival rates of songs were higher when more liberal criteria were used to recognize cases of matching songs, indicating that certain song traditions have changed through the accumulation of learning errors in cultural evolution. Survival of marked individual adult buntings was only a third of the survival of their song types. Survival of songs was similar whether estimated forward in time from the early samples or backward from the last samples. The equivalence is consistent with a random neutral substitution model of cultural evolution rather than with a competitive model that resembles an intense natural selection leading to many descendants being derived from a few founders. The local songs of adult indigo buntings are relatively long-lived behavior traditions that persist by social song learning outside of any family kinship line across several generations.

BIOLOGICAL AND CULTURAL SUCCESS OF SONG MEMES IN INDIGO BUNTINGS

Song behavior, breeding success, and survival of individuals and the survival of their local song traditions or memes were compared in two populations of Indigo Buntings (Passerina cyanea) in southern Michigan. First-year males were less successful than older males. First-year males with the song of a neighboring adult tended to be more successful in mating and in fledging young than were 1st-yr males that retained an individualistic song. Adults that were members of a local song neighborhood tended to be more successful than adults that were not. Reproductive and survival success of individual birds did not vary with the number of males in the meme. The different song traditions (memes) are equivalent in biological terms to mating success, breeding success, and survival of their bearers. Memes are successful in a cultural sense if they survive from year to year. Meme survival is determined largely by the number of individual birds in the song group; chances are high that at least one male with the song will return in the larger groups. Songs are learned outside the family context, kin usually do not have the same song, and a female selects a mate independently of whether his song is the same as her fathers. The change over time in the local meme pool is independent of any obviously associated genetic traits, and cultural extinction of song memes is described in probabilistic terms of meme size.

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.

A SINGLE ANCIENT ORIGIN OF BROOD PARASITISM IN AFRICAN FINCHES: IMPLICATIONS FOR HOST-PARASITE COEVOLUTION

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 phylogenetic hypotheses for the two genera of African brood‐parasitic finches, Anomalospiza and Vidua, using mitochondrial 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 finches rather than twice, as has been the conventional view. In addition, the parasitic finches (Viduidae) are not recently derived from either weavers (Ploceidae) or grassfinches (Estrildidae), but represent a third distinct lineage. Among these three groups, the parasitic finches 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‐specificity 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 finch 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 significantly faster rate of DNA sequence evolution in parasitic finches 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 finches, ancestral estrildids must have been parasitized well before the diversification of extant Vidua, suggesting a long history of coevolution between these lineages preceding more recent interactions between specific hosts and parasites.

Bird Songs and Avian Systematics

Song has been used widely in the systematic study of bird species and their relationships in the past two decades. The similarity of songs among different populations provides a test of the species identity of isolated or remote populations. As song is used in social and sexual behavior, we can test whether different populations respond to each other’s behavior. Systematists have used song differences and experiments to determine species limits among remote populations (Rowley, 1970; Lanyon, 1978; Martens, 1980, 1982; Payne, 1973a, 1982). The conditions under which song is a reliable guide to species relationships have not generally been considered. How similar must songs be for populations to be considered conspecific, or how different to support a hypothesis of species distinctiveness? How reliable are song playback experiments? How adequate are studies that compare songs alone? What effect does song learning have on the usefulness of song as a guide to species limits? In addition, systematists are interested in song as a guide to relationships among species. Several reviews of song in systematics have indicated that song may be more useful at the species level than at higher levels (Mayr, 1956; Lohrl, 1963; Thielcke, 1964; Lanyon, 1969; Selander, 1971). Is song a reliable guide to the phylogenetic history of speciation? Has cultural evolution within related species obscured their biological relationships?

MICROSATELLITE AMPLIFICATION FROM MUSEUM FEATHER SAMPLES: EFFECTS OF FRAGMENT SIZE AND TEMPLATE CONCENTRATION ON GENOTYPING ERRORS

Abstract We address the problem of microsatellite genotyping errors associated with polymerase chain reaction (PCR) amplification from degraded and dilute template DNA and provide suggestions for improving the accuracy of genotype data in studies using older museum specimens as a source of DNA. In the course of a population genetics study of African indigobirds (Vidua spp.), we used replicate PCR to evaluate genotyping reliability for nine microsatellite loci in relation to PCR fragment length and DNA template concentration (DNA extracted from the calamus of one vs. two wing feathers). Complete amplification failure and the dropout of one allele from heterozygous genotypes were the predominant problems encountered. For samples with heterozygous genotypes, allele dropout occurred in 19.2 and 12.1% of PCR using extracts derived from one and two feathers, respectively. The amplification of artifact bands was less frequent (affecting 4.9 and 1% of positive PCR reactions with one- and two-feather extracts, respectively). Those results indicate that multiple replicates per sample and locus are required to obtain accurate genotype data from museum feather samples. Although higher DNA concentration improved success, PCR fragment size had a much stronger influence on the success and repeatability of microsatellite amplification, which suggests that the accuracy and efficiency of genotyping can be improved most easily by designing primers that amplify smaller DNA fragments.

Parental care in estrildid finches: experimental tests of a model of Vidua brood parasitism

To assess the potential success of a brood parasite with a novel host, we tested whether three species of African estrildid finches provide foster parental care only to young with normal conspecific appearance and behaviour or also to other young in their nests. One (red-billed firefinch, Lagonosticta senegala) has a mimetic brood parasite in the field, one (goldbreast, Amandava subflava) has a nonmimetic brood parasite and one (blue-capped cordon-bleu, Uraeginthus cyanocephalus) has no brood parasite. All three species sometimes reared nestlings of other species to fledging, and all three reared the brood parasite of the firefinch, the village indigobird, Vidua chalybeata. Finches were more successful in rearing young of their own than young of other species, however, firefinches were as likely to rear young indigobirds as to rear their own young. Nestling mimicry gives young Vidua brood parasites a survival advantage in receiving care from firefinch foster parents. Firefinches were more likely to rear their own young in a mixed-species brood if the other species matched the appearance of their own young. There was no difference in reproductive success between novice and experienced pairs of finches rearing a brood of their own or the other species. Because these nesting species reared alien young, which were vicariant experimental stand-ins of young brood parasites, and these nesting species also reared the young indigobird, we conclude that the nestling appearance and behaviour does not completely prevent the colonization of a new host species by a brood parasite. The experimental results are consistent with molecular genetic estimates of colonization histories of estrildid hosts by Vidua brood parasites.

Nuclear DNA does not reconcile 'rocks' and 'clocks' in Neoaves: a comment on Ericson et al.

The discrepancy between fossil- and molecular-based age estimates for the diversification of modern birds has persisted despite increasingly large datasets on both sides ([Penny & Phillips 2004][1]). For the purpose of addressing this discrepancy, [Ericson et al. (2006)][2] recently generated a