Amazonian birds in more dynamic habitats have less population genetic structure and higher gene flow.

Understanding the factors that govern variation in genetic structure across species is key to the study of speciation and population genetics. Genetic structure has been linked to several aspects of life history, such as foraging strategy, habitat association, migration distance, and dispersal ability, all of which might influence dispersal and gene flow. Comparative studies of population genetic data from species with differing life histories provide opportunities to tease apart the role of dispersal in shaping gene flow and population genetic structure. Here, we examine population genetic data from sets of bird species specialized on a series of Amazonian habitat types hypothesized to filter for species with dramatically different dispersal abilities: stable upland forest, dynamic floodplain forest, and highly dynamic riverine islands. Using genome-wide markers, we show that habitat type has a significant effect on population genetic structure, with species in upland forest, floodplain forest, and riverine islands exhibiting progressively lower levels of structure. Although morphological traits used as proxies for individual-level dispersal ability did not explain this pattern, population genetic measures of gene flow are elevated in species from more dynamic riverine habitats. Our results suggest that the habitat in which a species occurs drives the degree of population genetic structuring via its impact on long-term fluctuations in levels of gene flow, with species in highly dynamic habitats having particularly elevated gene flow. These differences in genetic variation across taxa specialized in distinct habitats may lead to disparate responses to environmental change or habitat-specific diversification dynamics over evolutionary time scales.

A compreensão dos fatores que governam a variação da estrutura genética entre as espécies é fundamental para o estudo da especiação e da genética das populações. A estrutura genética tem sido ligada a vários aspectos da história da vida, tais como estratégia de forrageio, associação ao habitat, distância de migração e capacidade de dispersão, os quais poderiam influenciar a dispersão e o fluxo gênico. Estudos comparativos usando espécies que diferem nas suas histórias de vida oferecem uma oportunidade para desvendar o papel da dispersão no estabelecimento do fluxo gênico e da estrutura genética da população. Aqui examinamos dados genéticos populacionais de diversas espécies de aves com diferentes capacidades de dispersão especializadas em três habitats amazônicos, incluindo florestas de terra-firme, florestas de várzea e ilhas fluviais, cujos ambientes ripários são altamente dinâmicos. Utilizando dados genômicos que incluem milhares de loci, mostramos que o tipo de habitat tem um efeito significativo na estruturação genética das populações; espécies de florestas de terra-firme, florestas de várzea e ilhas fluviais exibem níveis de estruturação progressivamente menores. Embora os traços morfológicos frequentemente usados como indicadores da capacidade de dispersão a nível individual não expliquem este padrão, as medidas genéticas populacionais de fluxo gênico são altas em espécies associadas a habitats ribeirinhos mais dinâmicos. Nossos resultados sugerem que o habitat no qual uma espécie é encontrada determina o grau de estruturação genética da população através de seu impacto nas flutuações de longo prazo do fluxo gênico, com espécies em habitats altamente dinâmicos tendo um fluxo gênico particularmente alto. As diferenças na variação genética dos táxons especializados em diferentes habitats podem resultar em respostas díspares às mesmas mudanças ambientais, ou dinâmicas de diversificação específicas a um determinado habitat ao longo de escalas de tempo evolutivas.

Comprender los factores que rigen la variación de la estructura genética entre especies es clave para el estudio de la especiación y la genética de poblaciones. La estructura genética se ha relacionado con varios aspectos de la historia vital, como la estrategia de búsqueda de alimento, la asociación de hábitats, la distancia de migración y la capacidad de dispersión, factores todos ellos que podrían influir en la dispersión y el flujo genético. Los estudios comparativos de datos genéticos poblacionales de especies con historias vitales diferentes ofrecen la oportunidad de desentrañar el papel de la dispersión en la conformación del flujo genético y la estructura genética poblacional. En este trabajo examinamos los datos genéticos de poblaciones de especies de aves especializadas en una serie de hábitats amazónicos que, según la hipótesis, filtran especies con capacidades de dispersión radicalmente diferentes: bosques estables de tierras altas, bosques dinámicos de llanuras aluviales e islas fluviales altamente dinámicas. Utilizando marcadores genómicos, demostramos que el tipo de hábitat tiene un efecto significativo en la estructura genética de la población, y que las especies de los bosques de tierras altas, los bosques inundables y las islas fluviales presentan niveles de estructura progresivamente más bajos. Aunque los rasgos morfológicos utilizados como indicadores de la capacidad de dispersión individual no explican este patrón, las medidas genéticas poblacionales del flujo genético son más elevadas en las especies de hábitats fluviales más dinámicos. Nuestros resultados sugieren que el hábitat en el que se encuentra una especie determina el grado de estructuración genética de la población a través de su impacto en las fluctuaciones a largo plazo de los niveles de flujo genético, siendo las especies de hábitats muy dinámicos las que presentan un flujo genético particularmente elevado. Estas diferencias en la variación genética entre taxones especializados en hábitats distintos pueden dar lugar a respuestas dispares al cambio ambiental o a dinámicas de diversificación específicas del hbitat a lo largo de escalas temporales evolutivas.

Earth history and the passerine superradiation.

Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.

The demography of extinction in eastern North American birds.

Species are being lost at an unprecedented rate during the Anthropocene. Progress has been made in clarifying how species traits influence their propensity to go extinct, but the role historical demography plays in species loss or persistence is unclear. In eastern North America, five charismatic landbirds went extinct last century, and the causes of their extinctions have been heavily debated. Although these extinctions are most often attributed to post-colonial human activity, other factors such as declining ancestral populations prior to European colonization could have made these species particularly susceptible. We used population genomic data from these extinct birds and compared them with those from four codistributed extant species. We found extinct species harboured lower genetic diversity and effective population sizes than extant species, but both extinct and non-extinct birds had similar demographic histories of population expansion. These demographic patterns are consistent with population size changes associated with glacial-interglacial cycles. The lack of support for overall population declines during the Pleistocene corroborates the view that, although species that went extinct may have been vulnerable due to low diversity or small population size, their disappearance was driven by human activities in the Anthropocene.

Investigating the utility of traditional and genomic multi-locus datasets to resolve relationships in Lipaugus and Tijuca (Cotingidae).

Rapid diversification limits our ability to resolve evolutionary relationships and examine diversification history, as in the case of the Neotropical cotingas. Here we present an analysis with complete taxon sampling for the cotinga genera Lipaugus and Tijuca, which include some of the most range-restricted (e.g., T. condita) and also the most widespread and familiar (e.g., L. vociferans) forest birds in the Neotropics. We used two datasets: (1) Sanger sequencing data sampled from eight loci in 34 individuals across all described taxa and (2) sequence capture data linked to 1,079 ultraconserved elements and conserved exons sampled from one or two individuals per species. Phylogenies estimated from the Sanger sequencing data failed to resolve three nodes, but the sequence capture data produced a well-supported tree. Lipaugus and Tijuca formed a single, highly supported clade, but Tijuca species were not sister and were embedded within Lipaugus. A dated phylogeny confirmed Lipaugus and Tijuca diversified rapidly in the Miocene. Our study provides a detailed evolutionary hypothesis for Lipaugus and Tijuca and demonstrates that increasing genomic sampling can prove instrumental in resolving the evolutionary history of recent radiations.

Correction: A latitudinal phylogeographic diversity gradient in birds.

[This corrects the article DOI: 10.1371/journal.pbio.2001073.].

A latitudinal phylogeographic diversity gradient in birds.

High tropical species diversity is often attributed to evolutionary dynamics over long timescales. It is possible, however, that latitudinal variation in diversification begins when divergence occurs within species. Phylogeographic data capture this initial stage of diversification in which populations become geographically isolated and begin to differentiate genetically. There is limited understanding of the broader implications of intraspecific diversification because comparative analyses have focused on species inhabiting and evolving in restricted regions and environments. Here, we scale comparative phylogeography up to the hemisphere level and examine whether the processes driving latitudinal differences in species diversity are also evident within species. We collected genetic data for 210 New World bird species distributed across a broad latitudinal gradient and estimated a suite of metrics characterizing phylogeographic history. We found that lower latitude species had, on average, greater phylogeographic diversity than higher latitude species and that intraspecific diversity showed evidence of greater persistence in the tropics. Factors associated with species ecologies, life histories, and habitats explained little of the variation in phylogeographic structure across the latitudinal gradient. Our results suggest that the latitudinal gradient in species richness originates, at least partly, from population-level processes within species and are consistent with hypotheses implicating age and environmental stability in the formation of diversity gradients. Comparative phylogeographic analyses scaled up to large geographic regions and hundreds of species can show connections between population-level processes and broad-scale species-richness patterns.

The drivers of tropical speciation.

Since the recognition that allopatric speciation can be induced by large-scale reconfigurations of the landscape that isolate formerly continuous populations, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers, landscape change has been viewed as a primary driver of biological diversification. This process is referred to in biogeography as vicariance. In the most species-rich region of the world, the Neotropics, the sundering of populations associated with the Andean uplift is ascribed this principal role in speciation. An alternative model posits that rather than being directly linked to landscape change, allopatric speciation is initiated to a greater extent by dispersal events, with the principal drivers of speciation being organism-specific abilities to persist and disperse in the landscape. Landscape change is not a necessity for speciation in this model. Here we show that spatial and temporal patterns of genetic differentiation in Neotropical birds are highly discordant across lineages and are not reconcilable with a model linking speciation solely to landscape change. Instead, the strongest predictors of speciation are the amount of time a lineage has persisted in the landscape and the ability of birds to move through the landscape matrix. These results, augmented by the observation that most species-level diversity originated after episodes of major Andean uplift in the Neogene period, suggest that dispersal and differentiation on a matrix previously shaped by large-scale landscape events was a major driver of avian speciation in lowland Neotropical rainforests.

Positive association between population genetic differentiation and speciation rates in New World birds.

An implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, but its significance as a rate-limiting control on phylogenetic speciation dynamics remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. By pairing population genetics datasets from 173 New World bird species (>17,000 individuals) with phylogenetic estimates of speciation rate, we show that the population differentiation rates within species are positively correlated with their speciation rates over long timescales. Although population differentiation rate explains relatively little of the variation in speciation rate among lineages, the positive relationship between differentiation rate and speciation rate is robust to species-delimitation schemes and to alternative measures of both rates. Population differentiation occurs at least three times faster than speciation, which suggests that most populations are ephemeral. Speciation and population differentiation rates are more tightly linked in tropical species than in temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest that the processes responsible for population differentiation are tied to those that underlie broad-scale patterns of diversity.

Evolutionary dynamics of hybridization and introgression following the recent colonization of Glossy Ibis (Aves: Plegadis falcinellus) into the New World.

Geographic range shifts can cause secondary contact and hybridization between closely related species, revealing mechanisms of species formation and integrity. These dynamics typically play out in restricted geographic regions, but highly vagile species may experience major distributional changes resulting in broad areas of contact. The Glossy Ibis (Plegadis falcinellus) is a dispersive waterbird of the Old World and Australia that colonized eastern North America in the early 19th century and came into contact with the native White-faced Ibis (P. chihi). Putative hybrids between the two species have been observed across North America. To examine the population genomic consequences of this natural invasion, we sequenced 4,616 ultraconserved elements from 66 individuals sampled across the distributions of falcinellus, chihi, and the Puna Ibis (P. ridgwayi) of South America. We found genomic differentiation among the three species. Loci with high sequence divergence were often shared across all pairwise species comparisons, were associated with regions of high nucleotide diversity, and were concentrated on the Z chromosome. We detected signals of genetic admixture between chihi and falcinellus in individuals both near and far from their core area of sympatry. Genomic cline analyses revealed evidence of greater introgression into falcinellus from chihi, but we found little evidence for selection against hybrids. We also found signals of admixture between ridgwayi and South American populations of chihi. Our results indicate vagile species can experience pervasive introgression upon secondary contact, although we suggest these dynamics may be more ephemeral than the stable hybrid zones often observed in less dispersive organisms.

Habitat Association Predicts Genetic Diversity and Population Divergence in Amazonian Birds.

The ecological traits of organisms may predict their genetic diversity and population genetic structure and mediate the action of evolutionary processes important for speciation and adaptation. Making these ecological-evolutionary links is difficult because it requires comparable genetic estimates from many species with differing ecologies. In Amazonian birds, habitat association is an important component of ecological diversity. Here, we examine the link between habitat association and genetic parameters using 20 pairs of closely related Amazonian bird species in which one member of the pair occurs primarily in forest edge and floodplains and the other occurs in upland forest interior. We use standardized geographic sampling and data from 2,416 genomic markers to estimate genetic diversity, population genetic structure, and statistics reflecting demographic and evolutionary processes. We find that species of upland forest have greater genetic diversity and divergence across the landscape as well as signatures of older histories and less gene flow than floodplain species. Our results reveal that species ecology in the form of habitat association is an important predictor of genetic diversity and population divergence and suggest that differences in diversity between floodplain and upland avifaunas in the Amazon may be driven by differences in the demographic and evolutionary processes at work in the two habitats.

Sequence Capture versus Restriction Site Associated DNA Sequencing for Shallow Systematics.

Sequence capture and restriction site associated DNA sequencing (RAD-Seq) are two genomic enrichment strategies for applying next-generation sequencing technologies to systematics studies. At shallow timescales, such as within species, RAD-Seq has been widely adopted among researchers, although there has been little discussion of the potential limitations and benefits of RAD-Seq and sequence capture. We discuss a series of issues that may impact the utility of sequence capture and RAD-Seq data for shallow systematics in non-model species. We review prior studies that used both methods, and investigate differences between the methods by re-analyzing existing RAD-Seq and sequence capture data sets from a Neotropical bird (Xenops minutus). We suggest that the strengths of RAD-Seq data sets for shallow systematics are the wide dispersion of markers across the genome, the relative ease and cost of laboratory work, the deep coverage and read overlap at recovered loci, and the high overall information that results. Sequence capture's benefits include flexibility and repeatability in the genomic regions targeted, success using low-quality samples, more straightforward read orthology assessment, and higher per-locus information content. The utility of a method in systematics, however, rests not only on its performance within a study, but on the comparability of data sets and inferences with those of prior work. In RAD-Seq data sets, comparability is compromised by low overlap of orthologous markers across species and the sensitivity of genetic diversity in a data set to an interaction between the level of natural heterozygosity in the samples examined and the parameters used for orthology assessment. In contrast, sequence capture of conserved genomic regions permits interrogation of the same loci across divergent species, which is preferable for maintaining comparability among data sets and studies for the purpose of drawing general conclusions about the impact of historical processes across biotas. We argue that sequence capture should be given greater attention as a method of obtaining data for studies in shallow systematics and comparative phylogeography.

The Mouse-colored Tyrannulet (Phaeomyias murina) is a species complex that includes the Cocos Flycatcher (Nesotriccus ridgwayi), an island form that underwent a population bottleneck.

Simultaneous examination of evolutionary history in island forms and closely related mainland relatives can provide reciprocal insight into the evolution of island and mainland faunas. The Cocos Flycatcher (Nesotriccus ridgwayi) is a small tyrant flycatcher (Tyrannidae) endemic to Cocos Island, an oceanic island in the eastern Pacific Ocean. We first established its close relationship to the mainland species Mouse-colored Tyrannulet (Phaeomyias murina) using a phylogeny from genome-wide ultraconserved elements and exons. We then used mitochondrial DNA to explore the relationships between Nesotriccus and Phaeomyias populations from across its distribution in Central and South America. We found that Nesotriccus is nested within the Phaeomyias evolutionary tree, and that Phaeomyias represents a complex of at least four evolutionarily distinct species that differ in plumage, voice, and habitat association. Nesotriccus underwent a population bottleneck subsequent to its divergence from Central American and northern South American Phaeomyias populations in the middle Pleistocene. The 46 UCE loci containing alleles that are fixed between the two species are widely distributed across the genome, which suggests that selective or neutral processes responsible for divergence have occurred genome-wide. Overall, our simultaneous examination of Phaeomyias and Nesotriccus revealed divergent levels of genetic diversity and evolutionary histories between island and mainland forms.

Genomic variation in a widespread Neotropical bird (Xenops minutus) reveals divergence, population expansion, and gene flow.

The demographic and phylogeographic histories of species provide insight into the processes responsible for generating biological diversity, and genomic datasets are now permitting the estimation of species histories with unprecedented accuracy. We used a genomic single nucleotide polymorphism (SNP) dataset generated using a RAD-Seq method to investigate the historical demography and phylogeography of a widespread lowland Neotropical bird (Xenops minutus). As expected, we found that prominent landscape features that act as dispersal barriers, such as Amazonian rivers and the Andes Mountains, are associated with the deepest phylogeographic breaks, and also that isolation by distance is limited in areas between these barriers. In addition, we inferred positive population growth for most populations and detected evidence of historical gene flow between populations that are now physically isolated. Although we were able to reconstruct the history of Xenops minutus with unprecedented resolution, we had difficulty conclusively relating this history to the landscape events implicated in many Neotropical diversification hypotheses. We suggest that even if many traditional diversification hypotheses remain untestable, investigations using genomic datasets will provide greater resolution of species histories in the Neotropics and elsewhere.

Target capture and massively parallel sequencing of ultraconserved elements for comparative studies at shallow evolutionary time scales.

Comparative genetic studies of non-model organisms are transforming rapidly due to major advances in sequencing technology. A limiting factor in these studies has been the identification and screening of orthologous loci across an evolutionarily distant set of taxa. Here, we evaluate the efficacy of genomic markers targeting ultraconserved DNA elements (UCEs) for analyses at shallow evolutionary timescales. Using sequence capture and massively parallel sequencing to generate UCE data for five co-distributed Neotropical rainforest bird species, we recovered 776-1516 UCE loci across the five species. Across species, 53-77% of the loci were polymorphic, containing between 2.0 and 3.2 variable sites per polymorphic locus, on average. We performed species tree construction, coalescent modeling, and species delimitation, and we found that the five co-distributed species exhibited discordant phylogeographic histories. We also found that species trees and divergence times estimated from UCEs were similar to the parameters obtained from mtDNA. The species that inhabit the understory had older divergence times across barriers, contained a higher number of cryptic species, and exhibited larger effective population sizes relative to the species inhabiting the canopy. Because orthologous UCEs can be obtained from a wide array of taxa, are polymorphic at shallow evolutionary timescales, and can be generated rapidly at low cost, they are an effective genetic marker for studies investigating evolutionary patterns and processes at shallow timescales.

Model selection as a tool for phylogeographic inference: an example from the willow Salix melanopsis.

Phylogeographic inference has typically relied on analyses of data from one or a few genes to provide estimates of demography and population histories. While much has been learned from these studies, all phylogeographic analysis is conditioned on the data, and thus, inferences derived from data that represent a small sample of the genome are unavoidably tenuous. Here, we demonstrate one approach for moving beyond classic phylogeographic research. We use sequence capture probes and Illumina sequencing to generate data from >400 loci in order to infer the phylogeographic history of Salix melanopsis, a riparian willow with a disjunct distribution in coastal and the inland Pacific Northwest. We evaluate a priori phylogeographic hypotheses using coalescent models for parameter estimation, and the results support earlier findings that identified post-Pleistocene dispersal as the cause of the disjunction in S. melanopsis. We also conduct a series of model selection exercises using IMa2, Migrate-n and ∂a∂i. The resulting ranking of models indicates that refugial dynamics were complex, with multiple regions in the inland regions serving as the source for postglacial colonization. Our results demonstrate that new sources of data and new approaches to data analysis can rejuvenate phylogeographic research by allowing for the identification of complex models that enable researchers to both identify and estimate the most relevant parameters for a given system.

Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales.

Although massively parallel sequencing has facilitated large-scale DNA sequencing, comparisons among distantly related species rely upon small portions of the genome that are easily aligned. Methods are needed to efficiently obtain comparable DNA fragments prior to massively parallel sequencing, particularly for biologists working with non-model organisms. We introduce a new class of molecular marker, anchored by ultraconserved genomic elements (UCEs), that universally enable target enrichment and sequencing of thousands of orthologous loci across species separated by hundreds of millions of years of evolution. Our analyses here focus on use of UCE markers in Amniota because UCEs and phylogenetic relationships are well-known in some amniotes. We perform an in silico experiment to demonstrate that sequence flanking 2030 UCEs contains information sufficient to enable unambiguous recovery of the established primate phylogeny. We extend this experiment by performing an in vitro enrichment of 2386 UCE-anchored loci from nine, non-model avian species. We then use alignments of 854 of these loci to unambiguously recover the established evolutionary relationships within and among three ancient bird lineages. Because many organismal lineages have UCEs, this type of genetic marker and the analytical framework we outline can be applied across the tree of life, potentially reshaping our understanding of phylogeny at many taxonomic levels.

A new genus for Philydor erythrocercum and P. fuscipenne (Aves: Furnariidae).

N/A.

Systematics of the Neopelminae (Aves: Passeriformes: Pipridae) with description of a new genus.

N/A.

Genomic Evidence for Rare Hybridization and Large Demographic Changes in the Evolutionary Histories of Four North American Dove Species.

Introductions and invasions provide opportunities for interaction and hybridization between colonists and closely related native species. We investigate this phenomenon using the mitochondrial DNA COI and 81,416 base-pairs of overlapping nuclear variation to examine the evolutionary histories and signatures of hybridization among introduced feral Rock Pigeon and Eurasian Collared-Dove and native White-winged and Mourning doves in southwestern North America. First, we report all four species to be highly divergent across loci (overall pair-wise species ΦST range = 0.17-0.70) and provide little evidence for gene flow at evolutionary timescales. Despite this, evidence from multiple population genetics analyses supports the presence of six putative contemporary late-stage hybrids among the 182 sampled individuals. These putative hybrids contain various ancestry combinations, but all involve the most populous species, the Mourning Dove. Next, we use a novel method to reconstruct demographic changes through time using partial genome sequence data. We identify recent, species-specific fluctuations in population size that are likely associated with changing environments since the Miocene and suggest that these fluctuations have influenced the genetic diversity of each dove species in ways that may impact their future persistence. Finally, we discuss the importance of using multiple marker types when attempting to infer complex evolutionary histories and propose important considerations when analyzing populations that were recently established or of domestic origins.

The dynamics of introgression across an avian radiation.

Hybridization and resulting introgression can play both a destructive and a creative role in the evolution of diversity. Thus, characterizing when and where introgression is most likely to occur can help us understand the causes of diversification dynamics. Here, we examine the prevalence of and variation in introgression using phylogenomic data from a large (1300+ species), geographically widespread avian group, the suboscine birds. We first examine patterns of gene tree discordance across the geographic distribution of the entire clade. We then evaluate the signal of introgression in a subset of 206 species triads using Patterson's D-statistic and test for associations between introgression signal and evolutionary, geographic, and environmental variables. We find that gene tree discordance varies across lineages and geographic regions. The signal of introgression is highest in cases where species occur in close geographic proximity and in regions with more dynamic climates since the Pleistocene. Our results highlight the potential of phylogenomic datasets for examining broad patterns of hybridization and suggest that the degree of introgression between diverging lineages might be predictable based on the setting in which they occur.