Audubon's Warbler Research Articles

Comparing divergence landscapes from reduced-representation and whole genome resequencing in the yellow-rumped warbler (Setophaga coronata) species complex.

Researchers seeking to generate genomic data for non-model organisms are faced with a number of trade-offs when deciding which method to use. The selection of reduced representation approaches versus whole genome resequencing will ultimately affect the marker density, sequencing depth, and the number of individuals that can multiplexed. These factors can affect researchers' ability to accurately characterize certain genomic features, such as landscapes of divergence-how FST varies across the genomes. To provide insight into the effect of sequencing method on the estimation of divergence landscapes, we applied an identical bioinformatic pipeline to three generations of sequencing data (GBS, ddRAD, and WGS) produced for the same system, the yellow-rumped warbler species complex. We compare divergence landscapes generated using each method for the myrtle warbler (Setophaga coronata coronata) and the Audubon's warbler (S. c. auduboni), and for Audubon's warblers with deeply divergent mtDNA resulting from mitochondrial introgression. We found that most high-FST peaks were not detected in the ddRAD data set, and that while both GBS and WGS were able to identify the presence of large peaks, WGS was superior at a finer scale. Comparing Audubon's warblers with divergent mitochondrial haplotypes, only WGS allowed us to identify small (10-20kb) regions of elevated differentiation, one of which contained the nuclear-encoded mitochondrial gene NDUFAF3. We calculated the cost per base pair for each method and found it was comparable between GBS and WGS, but significantly higher for ddRAD. These comparisons highlight the advantages of WGS over reduced representation methods when characterizing landscapes of divergence.

Exploring the hybrid speciation continuum in birds.

Hybridization is increasingly recognized as a creative evolutionary force contributing to adaptation and speciation. Homoploid hybrid speciation—the process in which hybridization results in a stable, fertile, and reproductively isolated hybrid lineage where there is no change in ploidy—has been documented in several taxa. Hybridization can directly contribute to reproductive isolation or reinforce it at a later stage. Alternatively, hybridization might not be related to the evolution of reproductive isolation. To account for these different scenarios, I propose to discriminate between two types of hybrid speciation: type I where reproductive isolation is a direct consequence of hybridization and type II where it is the by‐product of other processes. I illustrate the applicability of this classification scheme with avian examples. To my knowledge, seven hybrid bird species have been proposed: Italian sparrow, Audubon's warbler, Genovesa mockingbird, Hawaiian duck, red‐breasted goose, golden‐crowned manakin, and a recent lineage of Darwin's finches on the island of Daphne Major (“Big Bird”). All studies provide convincing evidence for hybridization, but do not always confidently discriminate between scenarios of hybrid speciation and recurrent introgressive hybridization. The build‐up of reproductive isolation between the hybrid species and their parental taxa is mainly driven by premating isolation mechanisms and comparable to classical speciation events. One hybrid species can be classified as type I (“Big Bird”) while three species constitute type II hybrid species (Italian sparrow, Audubon's warbler, and golden‐crowned manakin). The diversity in hybrid bird species across a range of divergence times also provides an excellent opportunity to study the evolution of hybrid genomes in terms of genome stabilization and adaptation.

Similar hybrid composition among different age and sex classes in the Myrtle–Audubon's warbler hybrid zone

ABSTRACT Hybrid zones provide a key natural context within which to study the barriers between incipient species. In some avian hybrid zones, there is indirect evidence of selection against hybrid offspring, yet the source of that selection is often unclear. We examined the frequency distribution of hybrids between Myrtle Warblers (Setophaga coronata coronata) and Audubon's Warblers (S. c. auduboni), using data to quantify—for the first time at a genomic scale—the composition of hybrids in this hybrid zone. We sampled birds during the breeding season and during fall migration and compared the frequencies of hybrids of different sex and age classes. Specifically, we tested for evidence of early-generation hybrids being significantly under- or over-represented in any of these classes, as would be expected if hybrids have lower or higher fitness than non-hybrids. We found that the genomic composition of birds in the hybrid zone spans the full ancestry spectrum. Across all our sampling periods, we found an ex...

Postbreeding elevational movements of western songbirds in Northern California and Southern Oregon

Migratory species employ a variety of strategies to meet energetic demands of postbreeding molt. As such, at least a few species of western Neotropical migrants are known to undergo short‐distance upslope movements to locations where adults molt body and flight feathers (altitudinal molt migration). Given inherent difficulties in measuring subtle movements of birds occurring in western mountains, we believe that altitudinal molt migration may be a common yet poorly documented phenomenon. To examine prevalence of altitudinal molt migration, we used 29 years of bird capture data in a series of linear mixed‐effect models for nine commonly captured species that breed in northern California and southern Oregon. Candidate models were formulated a priori to examine whether elevation and distance from the coast can be used to predict abundance of breeding and molting birds. Our results suggest that long‐distance migrants such as Orange‐crowned Warbler (Oreothlypis celata) moved higher in elevation and Audubon's Warbler (Setophaga coronata) moved farther inland to molt after breeding. Conversely, for resident and short‐distance migrants, we found evidence that birds either remained on the breeding grounds until they finished molting, such as Song Sparrow (Melospiza melodia) or made small downslope movements, such as American Robin (Turdus migratorius). We conclude that altitudinal molt migration may be a common, variable, and complex behavior among western songbird communities and is related to other aspects of a species’ natural history, such as migratory strategy.

Linking the wintering and breeding grounds of warblers along the Pacific Flyway.

Long‐distance migration is a behavior that is exhibited by many animal groups. The evolution of novel migration routes can play an important role in range expansions, ecological interactions, and speciation. New migration routes may evolve in response to selection in favor of reducing distance between breeding and wintering areas, or avoiding navigational barriers. Many migratory changes are likely to evolve gradually and are therefore difficult to study. Here, we attempt to connect breeding and wintering populations of myrtle warblers (Setophaga coronata coronata) to better understand the possible evolution of distinct migration routes within this species. Myrtle warblers, unlike most other warblers with breeding ranges primarily in eastern North America, have two disjunct overwintering concentrations—one in the southeastern USA and one along the Pacific Coast—and presumably distinct routes to‐and‐from these locations. We studied both myrtle and Audubon's warblers (S. c. auduboni) captured during their spring migration along the Pacific Coast, south of the narrow region where these two taxa hybridize. Using stable hydrogen isotopes and biometric data, we show that those myrtle warblers wintering along the southern Pacific Coast of North America are likely to breed at high latitudes in Alaska and the Yukon rather than in Alberta or further east. Our interpretation is that the evolution of this wintering range and migration route along the Pacific Coast may have facilitated the breeding expansion of myrtle warblers into northwestern North America. Moreover, these data suggest that there may be a migratory divide within genetically similar populations of myrtle warblers.

MIGRATION, MITOCHONDRIA, AND THE YELLOW-RUMPED WARBLER

Discordance between mitochondrial and nuclear DNA has been noted in many systems. Asymmetric introgression of mitochondria is a common cause of such discordances, although in most cases the drivers of introgression are unknown. In the yellow-rumped warbler, evidence suggests that mtDNA from the eastern, myrtle warbler, has introgressed across much of the range of the western form, the Audubon's warbler. Within the southwestern United States myrtle mtDNA comes into contact with another clade that occurs in the Mexican black-fronted warbler. Both northern forms exhibit seasonal migration, whereas black-fronted warblers are nonmigratory. We investigated the link between mitochondrial introgression, mitochondrial function, and migration using novel genetic, isotopic, biochemical, and phenotypic data obtained from populations in the transition zone. Isotopes suggest the zone is coincident with a shift in migration, with individuals in the south being resident and populations further north becoming increasingly more migratory. Mitochondrial respiration in flight muscles demonstrates that myrtle-type individuals have a significantly greater acceptor control ratio of mitochondria, suggesting it may be more metabolically efficient. To our knowledge this is the first time this type of intraspecific variation in mitochondrial respiration has been measured in wild birds and we discuss how such mitochondrial adaptations may have facilitated introgression.

Molt and Body Condition of Myrtle and Audubon's Warblers During Migration-Stopover in Portland, Oregon

Among Yellow-rumped Warblers (Dendroica coronata)1 banded in Portland, Oregon, in the spring migration seasons of 2007 through 2010, prealternate molt was found in 40.0% of the Myrtle subspecies group (D. c. coronata group) but just 5.9% of the Audubon's subspecies group (D. c. auduboni group). The peak of molt frequency occurred prior to the peak of abundance for both subspecies groups, but that of the Myrtle Warbler substantially overlapped its peak in abundance and represented 82.4% of individuals captured. Twenty-two Yellow-rumped Warblers (1.4%) were recaptured. The mean stopover time for those recaptured within the same season was 8.27 d. Most of the same-season recaptures gained fat or became no leaner during their stay. Molting birds had lower fat scores than prior to and after completion of molt. Fat scores continued to increase following completion of molt. Multiple lines of inference point to the importance of Smith and Bybee Lakes Preserve and its vicinity as a migratory stopover site for the Yellow-rumped Warblers. Prealternate molt at a migratory stopover site to the extent shown by the Myrtle Warbler subspecies group has not previously been documented for any species.

A cryptic contact zone between divergent mitochondrial DNA lineages in southwestern North America supports past introgressive hybridization in the yellow-rumped warbler complex (Aves: Dendroica coronata)

Using genetic data to study the process of population divergence is central to understanding speciation, yet distinguishing between recent divergence and introgressive hybridization is challenging. In a previous study on the phylogeography of the yellow-rumped warbler complex using mitochondrial (mt)DNA data, we reported limited sequence divergence and a lack of reciprocal monophyly between myrtle and Audubon's warblers (Dendroica coronata and Dendroica auduboni, respectively), suggesting very recent isolation. In the present study, we report the results obtained from a subsequent sampling of Audubon's warbler in Arizona and Utah (‘memorabilis’ race), which shows that, although this taxon is similar to auduboni in plumage colour, most memorabilis individuals sampled (93%) carry haplotypes that belong to the divergent black-fronted warbler lineage (Dendroica nigrifrons) of Mexico. Furthermore, the auduboni and nigrifrons lineages mix in southern Utah at a narrow, yet apparently ‘cryptic’ contact zone. Newly-available evidence from nuclear markers indicating marked differentiation between auduboni and coronata has focused attention on the possibility of mtDNA introgression in the absence of nuclear gene flow, and the results of the present study are consistent with the hypothesis that the mtDNA of auduboni was indeed historically introgressed from the coronata lineage. Analysis of morphological traits shows that memorabilis is significantly differentiated from auduboni and nigrifrons in some traits, yet is overall intermediate between the two, which is consistent with a shared common ancestor for the auduboni/memorabilis/nigrifrons group. The striking, unexpected mtDNA pattern reported in the present study reveals a complex evolutionary history of the yellow-rumped warbler complex, and cautions against the exclusive use of mtDNA to infer evolutionary relationships. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 696–706.

Increasing evidence of the role of gene flow in animal evolution: hybrid speciation in the yellow-rumped warbler complex

In this issue of Molecular Ecology, Brelsford et al. (2011) present strong evidence for a case of hybrid speciation within the yellow-rumped warbler complex. Although homoploid hybrid speciation has now been documented in many animals (Mallet 2007), it seems rare in tetrapods (Mavárez & Linares 2008) and it has barely even been mentioned in birds (Price 2008). Brelsford and colleagues thus present the first detailed molecular evidence suggesting that hybrid speciation can occur in birds. Brelsford et al. (2011) posit that Audubon's warbler (Dendroica auduboni) constitutes a hybrid species originating from the admixture of two distinct parental lineages, represented today by myrtle warbler (D. coronata) and black-fronted warbler (D. nigrifrons). The authors present three major lines of molecular evidence suggesting that this is not simply a case of a hybrid swarm or limited introgression.

Hybrid origin of Audubon’s warbler

Several animal species have recently been shown to have hybrid origins, but no avian examples have been documented with molecular evidence. We investigate whether the Audubon's warbler (Dendroica auduboni), one of four visually distinct species in the yellow-rumped warbler complex, has originated through hybridization between two other species in this group, the myrtle warbler (D.coronata) and black-fronted warbler (D.nigrifrons). Analysis of nuclear amplified fragment length polymorphism (AFLP) and sequence markers shows that Audubon's warblers are genetically intermediate and carry a mixture of alleles otherwise found only in one or the other of their putative parental species. Audubon's warblers also carry two deeply divergent mitochondrial DNA lineages, each shared with only one putative parental form. Broad clines between Audubon's and black-fronted warblers in AFLP markers call into question the validity of these two forms as full species; nevertheless, our results suggest that the Audubon's warbler probably originated through hybridization between two long-diverged species. It is likely that more cases of avian species of hybrid origin will be revealed by surveys of variation in nuclear DNA and other traits.

Honeydew foraging by birds in tropical montane forests and pastures of Mexico

Abstract:A honeydew-producing scale insect, Stigmacoccus garmilleri (Margarodidae), is associated with oak trees (Quercus spp.) in highland forests of Mexico. Although feeding by ants on scale-insect honeydew is more frequently documented in the literature, the honeydew produced by feeding instars of S. garmilleri is sufficient to provide nourishment for birds. This study elucidates bird use of honeydew in the tropical montane forests near Chiconquiaco, Veracruz, Mexico, and uncovers patterns in honeydew foraging. Over a 2-mo period, 40 trees harbouring scale insects, located in both forest and pasture areas, were intensely studied (160 h of bird-foraging observations along with quantitative measurements of honeydew production). Fifteen resident bird species and 18 migrant species were observed visiting observation trees. Approximately 72% of the resident bird species and 83% of the migrant bird species observed were recorded to forage on scale-insect honeydew. Audubon's warbler (Dendroica coronata auduboni) was the most active consumer and defender of the resource. Of 118 aggressive chases observed, only 9.65% occurred in forest observation trees, and 90.3% in pasture trees. Audubon's warbler demonstrated preferential defence and territorial patrolling of scale-insect honeydew in scattered pasture trees.

Speciation and rapid phenotypic differentiation in the yellow‐rumped warblerDendroica coronatacomplex

The relative importance of the Pleistocene glacial cycles in driving avian speciation remains controversial, partly because species limits in many groups remain poorly understood, and because current taxonomic designations are often based on phenotypic characteristics of uncertain phylogenetic significance. We use mtDNA sequence data to examine patterns of genetic variation, sequence divergence and phylogenetic relationships between phenotypically distinct groups of the yellow-rumped warbler complex. Currently classified as a single species, the complex is composed of two North American migratory forms (myrtle warbler Dendroica coronata coronata and Audubon's warbler Dendroica coronata auduboni), and two largely sedentary forms: Dendroica coronata nigrifrons of Mexico, and Dendroica coronata goldmani of Guatemala. The latter are typically considered to be races of the Audubon's warbler based on plumage characteristics. However, mtDNA sequence data reveal that sedentary Mesoamerican forms are reciprocally monophyletic to each other and to migratory forms, from which they show a long history of isolation. In contrast, migratory myrtle and Audubon's warblers form a single cluster due to high levels of shared ancestral polymorphism as evidenced by widespread sharing of mtDNA haplotypes despite marked phenotypic differentiation. Sedentary and migratory forms diverged in the early Pleistocene, whereas phenotypic differentiation between the two migratory forms has occurred in the Holocene and is likely the result of geographical isolation and subsequent range expansion since the last glaciation. Our results underscore the importance of Quaternary climatic events in driving songbird speciation and indicate that plumage traits can evolve remarkably fast, thus rendering them potentially misleading for inferring systematic relationships.

Palm Warbler in Guerrero and Comments on Audubon's Warbler in Costa Rica

Palm Warbler in Guerrero and Comments on Audubon's Warbler in Costa Rica

Audubon's Warbler in North Carolina

Audubon's Warbler in North Carolina

Audubon's Warbler and Red-Breasted Nuthatch Breeding in North Dakota

Audubon's Warbler and Red-Breasted Nuthatch Breeding in North Dakota

Possible Intergrades between the Myrtle and Audubon's Warbler

Possible Intergrades between the Myrtle and Audubon's Warbler

Audubon's Warbler in Ohio

Audubon's Warbler in Ohio

Audubon's Warbler in Northern Ohio

Audubon's Warbler in Northern Ohio

Audubon's Warbler near Minneapolis, Minn

Audubon's Warbler near Minneapolis, Minn

Great Destruction of Birds' Eggs and Nestlings in the Sierra Nevada

AS WE approached Cisco, Placer County, California, toward evening of June 7, 1912, the air seemed filled with the songs and call-notes of mountain birds. Observing that we had reached a section where birds were more numerous than is usual at so high an altitude as 5900 feet, I stopped my automobile at the only hotel in that charming resort and engaged accommodation for Mrs. Ingersoll and self. Knowing of no locality in the Sierras where small birds nested more plentifully than in that particular place, I anticipated the pleasure of adding much choice material to my collection of eggs. A few days' search, however, convinced me that I was not the only nest hunter, and that the Bluefronted Jays had a great advantage over one who collects full sets only. Jays were no more abundant than in similar places elsewhere, but these particular birds doubtless had an extra strong desire for eggs and naked birds. No jays were detected in the act of eating well-feathered young. Other natural enemies were doubtless the cause of some of the nests being tenantless. But as the jays were the only robbers caught in the act of taking eggs and young, the principal havoc is attributed to them and to an unseasonable snow fall. It is to be hoped that birds in the surrounding localities were more fortunate in raising their young. For a wide spread destruction like that at Cisco would tend to wipe some species out of existence. Following a week of delightful weather, a cold rain began falling on the morning of June 22, by night turning to sleet. At six o'clock on the morning of June 23 there was a depth of three and one-half inches of snow on the level. This snow was of a wet, clinging nature, weighing down every leaf and twig, and causing large branches and limbs of some deciduous trees to break. Clumps of bushes were generally weighted down to about half their height on the previous day. Many nests that were on flexible branches had their contents spilled out, while those built against trunks of small trees or between the main stems of bushes were later in the day bombarded with huge chunks of snow dislodged by the wind. This permitted branches to spring violently up to their accustomed position, a further cause of destruction. Horizontal branches of large fir trees drooped and crushed nests that chanced to be located between them. It is easy to imagine that many sleeping birds were crushed to death as the snow-laden branches quietly settled on them. Personally I know of two instances. A brooding Audubon Warbler was killed, and two of her three eggs broken, in the nest situated thirty feet above the ground on the branch of a fir. The other instance was that of a Western Wood Pewee picked up from the ground with nest on dead aspen limb that had broken off and fallen from a height of some twenty feet. Another Wood Pewee's nest destroyed in the same manner, was found later in the day. While searching a large pine stub for the nest of a Sierra Creeper, I discovered a female Calaveras Warbler under a partially detached piece of bark. Her feathers were quite wet, and as the crevice was rather dry, I presume this ground-nesting bird was flooded out of her home and sought shelter as death approached.