Genomic Architecture Predicts Tree Topology, Population Structuring, and Demographic History in Amazonian Birds.

Geographic barriers are frequently invoked to explain genetic structuring across the landscape. However, inferences on the spatial and temporal origins of population variation have been largely limited to evolutionary neutral models, ignoring the potential role of natural selection and intrinsic genomic processes known as genomic architecture in producing heterogeneity in differentiation across the genome. To test how variation in genomic characteristics (e.g. recombination rate) impacts our ability to reconstruct general patterns of differentiation between species that cooccur across geographic barriers, we sequenced the whole genomes of multiple bird populations that are distributed across rivers in southeastern Amazonia. We found that phylogenetic relationships within species and demographic parameters varied across the genome in predictable ways. Genetic diversity was positively associated with recombination rate and negatively associated with species tree support. Gene flow was less pervasive in genomic regions of low recombination, making these windows more likely to retain patterns of population structuring that matched the species tree. We further found that approximately a third of the genome showed evidence of selective sweeps and linked selection, skewing genome-wide estimates of effective population sizes and gene flow between populations toward lower values. In sum, we showed that the effects of intrinsic genomic characteristics and selection can be disentangled from neutral processes to elucidate spatial patterns of population differentiation.

Changes in parrot diversity after human arrival to the Caribbean.

Humans did not arrive on most of the world's islands until relatively recently, making islands favorable places for disentangling the timing and magnitude of natural and anthropogenic impacts on species diversity and distributions. Here, we focus on Amazona parrots in the Caribbean, which have close relationships with humans (e.g., as pets as well as sources of meat and colorful feathers). Caribbean parrots also have substantial fossil and archaeological records that span the Holocene. We leverage this exemplary record to showcase how combining ancient and modern DNA, along with radiometric dating, can shed light on diversification and extinction dynamics and answer long-standing questions about the magnitude of human impacts in the region. Our results reveal a striking loss of parrot diversity, much of which took place during human occupation of the islands. The most widespread species, the Cuban Parrot, exhibits interisland divergences throughout the Pleistocene. Within this radiation, we identified an extinct, genetically distinct lineage that survived on the Turks and Caicos until Indigenous human settlement of the islands. We also found that the narrowly distributed Hispaniolan Parrot had a natural range that once included The Bahamas; it thus became "endemic" to Hispaniola during the late Holocene. The Hispaniolan Parrot also likely was introduced by Indigenous people to Grand Turk and Montserrat, two islands where it is now also extirpated. Our research demonstrates that genetic information spanning paleontological, archaeological, and modern contexts is essential to understand the role of humans in altering the diversity and distribution of biota.

Genomes of the extinct Bachman's warbler show high divergence and no evidence of admixture with other extant Vermivora warblers.

Bachman's warbler1 (Vermivora bachmanii)-last sighted in 1988-is one of the only North American passerines to recently go extinct.2,3,4 Given extensive ongoing hybridization of its two extant congeners-the blue-winged warbler (V. cyanoptera) and golden-winged warbler (V. chrysoptera)5,6,7,8-and shared patterns of plumage variation between Bachman's warbler and hybrids between those extant species, it has been suggested that Bachman's warbler might have also had a component of hybrid ancestry. Here, we use historic DNA (hDNA) and whole genomes of Bachman's warblers collected at the turn of the 20th century to address this. We combine these data with the two extant Vermivora species to examine patterns of population differentiation, inbreeding, and gene flow. In contrast to the admixture hypothesis, the genomic evidence is consistent with V. bachmanii having been a highly divergent, reproductively isolated species, with no evidence of introgression. We show that these three species have similar levels of runs of homozygosity (ROH), consistent with effects of a small long-term effective population size or population bottlenecks, with one V. bachmanii outlier showing numerous long ROH and a FROH greater than 5%. We also found-using population branch statistic estimates-previously undocumented evidence of lineage-specific evolution in V. chrysoptera near a pigmentation gene candidate, CORIN, which is a known modifier of ASIP, which is in turn involved in melanic throat and mask coloration in this family of birds. Together, these genomic results also highlight how natural history collections are such invaluable repositories of information about extant and extinct species.

Convergent genomic signatures of local adaptation across a continental-scale environmental gradient.

Convergent local adaptation offers a glimpse into the role of constraint and stochasticity in adaptive evolution, in particular the extent to which similar genetic mechanisms drive adaptation to common selective forces. Here, we investigated the genomics of local adaptation in two nonsister woodpeckers that are codistributed across an entire continent and exhibit remarkably convergent patterns of geographic variation. We sequenced the genomes of 140 individuals of Downy (Dryobates pubescens) and Hairy (Dryobates villosus) woodpeckers and used a suite of genomic approaches to identify loci under selection. We showed evidence that convergent genes have been targeted by selection in response to shared environmental pressures, such as temperature and precipitation. Among candidates, we found multiple genes putatively linked to key phenotypic adaptations to climate, including differences in body size (e.g., IGFPB) and plumage (e.g., MREG). These results are consistent with genetic constraints limiting the pathways of adaptation to broad climatic gradients, even after genetic backgrounds diverge.

Population genomics of the island thrush elucidates one of earth's great archipelagic radiations.

Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world's most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush's success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.

Demography and linked selection interact to shape the genomic landscape of codistributed woodpeckers during the Ice Age.

The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape.

Phylogenomic Analysis of the Parrots of the World Distinguishes Artifactual from Biological Sources of Gene Tree Discordance.

Gene tree discordance is expected in phylogenomic trees and biological processes are often invoked to explain it. However, heterogeneous levels of phylogenetic signal among individuals within data sets may cause artifactual sources of topological discordance. We examined how the information content in tips and subclades impacts topological discordance in the parrots (Order: Psittaciformes), a diverse and highly threatened clade of nearly 400 species. Using ultraconserved elements from 96% of the clade's species-level diversity, we estimated concatenated and species trees for 382 ingroup taxa. We found that discordance among tree topologies was most common at nodes dating between the late Miocene and Pliocene, and often at the taxonomic level of the genus. Accordingly, we used two metrics to characterize information content in tips and assess the degree to which conflict between trees was being driven by lower-quality samples. Most instances of topological conflict and nonmonophyletic genera in the species tree could be objectively identified using these metrics. For subclades still discordant after tip-based filtering, we used a machine learning approach to determine whether phylogenetic signal or noise was the more important predictor of metrics supporting the alternative topologies. We found that when signal favored one of the topologies, the noise was the most important variable in poorly performing models that favored the alternative topology. In sum, we show that artifactual sources of gene tree discordance, which are likely a common phenomenon in many data sets, can be distinguished from biological sources by quantifying the information content in each tip and modeling which factors support each topology. [Historical DNA; machine learning; museomics; Psittaciformes; species tree.].

The Genomic Landscapes of Desert Birds Form over Multiple Time Scales.

Spatial models show that genetic differentiation between populations can be explained by factors ranging from geographic distance to environmental resistance across the landscape. However, genomes exhibit a landscape of differentiation, indicating that multiple processes may mediate divergence in different portions of the genome. We tested this idea by comparing alternative geographic predctors of differentiation in ten bird species that co-occur in Sonoran and Chihuahuan Deserts of North America. Using population-level genomic data, we described the genomic landscapes across species and modeled conditions that represented historical and contemporary mechanisms. The characteristics of genomic landscapes differed across species, influenced by varying levels of population structuring and admixture between deserts, and the best-fit models contrasted between the whole genome and partitions along the genome. Both historical and contemporary mechanisms were important in explaining genetic distance, but particularly past and current environments, suggesting that genomic evolution was modulated by climate and habitat There were also different best-ftit models across genomic partitions of the data, indicating that these regions capture different evolutionary histories. These results show that the genomic landscape of differentiation can be associated with alternative geographic factors operating on different portions of the genome, which reflect how heterogeneous patterns of genetic differentiation can evolve across species and genomes.

Empirical and philosophical problems with the subspecies rank.

Species-level taxonomy derives from empirical sources (data and techniques) that assess the existence of spatiotemporal evolutionary lineages via various species "concepts." These concepts determine if observed lineages are independent given a particular methodology and ontology, which relates the metaphysical species concept to what "kind" of thing a species is in reality. Often, species concepts fail to link epistemology back to ontology. This lack of coherence is in part responsible for the persistence of the subspecies rank, which in modern usage often functions as a placeholder between the evolutionary events of divergence or collapse of incipient species. Thus, prospective events like lineages merging or diverging require information from unknowable future information. This is also conditioned on evidence that the lineage already has a detectably distinct evolutionary history. Ranking these lineages as subspecies can seem attractive given that many lineages do not exhibit intrinsic reproductive isolation. We argue that using subspecies is indefensible on philosophical and empirical grounds. Ontologically, the rank of subspecies is either identical to that of species or undefined in the context of evolutionary lineages representing spatiotemporally defined individuals. Some species concepts more inclined to consider subspecies, like the Biological Species Concept, are disconnected from evolutionary ontology and do not consider genealogy. Even if ontology is ignored, methods addressing reproductive isolation are often indirect and fail to capture the range of scenarios linking gene flow to species identity over space and time. The use of subspecies and reliance on reproductive isolation as a basis for an operational species concept can also conflict with ethical issues governing the protection of species. We provide a way forward for recognizing and naming species that links theoretical and operational species concepts regardless of the magnitude of reproductive isolation.

River network rearrangements promote speciation in lowland Amazonian birds.

Large Amazonian rivers impede dispersal for many species, but lowland river networks frequently rearrange, thereby altering the location and effectiveness of river barriers through time. These rearrangements may promote biotic diversification by facilitating episodic allopatry and secondary contact among populations. We sequenced genome-wide markers to evaluate the histories of divergence and introgression in six Amazonian avian species complexes. We first tested the assumption that rivers are barriers for these taxa and found that even relatively small rivers facilitate divergence. We then tested whether species diverged with gene flow and recovered reticulate histories for all species, including one potential case of hybrid speciation. Our results support the hypothesis that river rearrangements promote speciation and reveal that many rainforest taxa are micro-endemic, unrecognized, and thus threatened with imminent extinction. We propose that Amazonian hyper-diversity originates partly from fine-scale barrier displacement processes-including river dynamics-which allow small populations to differentiate and disperse into secondary contact.

Microevolutionary dynamics show tropical valleys are deeper for montane birds of the Atlantic Forest.

Tropical mountains hold more biodiversity than their temperate counterparts, and this disparity is often associated with the latitudinal climatic gradient. However, distinguishing the impact of latitude versus the background effects of species history and traits is challenging due to the evolutionary distance between tropical and temperate assemblages. Here, we test whether microevolutionary processes are linked to environmental variation across a sharp latitudinal transition in 21 montane birds of the southern Atlantic Forest in Brazil. We find that effective dispersal within populations in the tropical mountains is lower and genomic differentiation is better predicted by the current environmental complexity of the region than within the subtropical populations. The concordant response of multiple co-occurring populations is consistent with spatial climatic variability as a major process driving population differentiation. Our results provide evidence for how a narrow latitudinal gradient can shape microevolutionary processes and contribute to broader scale biodiversity patterns.

Mining museums for historical DNA: advances and challenges in museomics.

Historical DNA (hDNA), obtained from museum and herbarium specimens, has yielded spectacular new insights into the history of organisms. This includes documenting historical genetic erosion and extinction, discovering species new to science, resolving evolutionary relationships, investigating epigenetic effects, and determining origins of infectious diseases. However, the development of best-practices in isolating, processing, and analyzing hDNA remain under-explored, due to the substantial diversity of specimen preparation types, tissue sources, archival ages, and collecting histories. Thus, for hDNA to reach its full potential, and justify the destructive sampling of the rarest specimens, more experimental work using time-series collections, and the development of improved methods to correct for data asymmetries and biases due to DNA degradation are required.

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.

The evolution of a tropical biodiversity hotspot.

The tropics are the source of most biodiversity yet inadequate sampling obscures answers to fundamental questions about how this diversity evolves. We leveraged samples assembled over decades of fieldwork to study diversification of the largest tropical bird radiation, the suboscine passerines. Our phylogeny, estimated using data from 2389 genomic regions in 1940 individuals of 1283 species, reveals that peak suboscine species diversity in the Neotropics is not associated with high recent speciation rates but rather with the gradual accumulation of species over time. Paradoxically, the highest speciation rates are in lineages from regions with low species diversity, which are generally cold, dry, unstable environments. Our results reveal a model in which species are forming faster in environmental extremes but have accumulated in moderate environments to form tropical biodiversity hotspots.

Spatial predictors of genomic and phenotypic variation differ in a lowland Middle American bird (Icterus gularis).

Spatial patterns of intraspecific variation are shaped by geographical distance among populations, historical changes in gene flow and interactions with local environments. Although these factors are not mutually exclusive and operate on both genomic and phenotypic variation, it is unclear how they affect these two axes of variation. We address this question by exploring the predictors of genomic and phenotypic divergence in Icterus gularis, a broadly distributed Middle American bird that exhibits marked geographical variation in body size across its range. We combined a comprehensive single nucleotide polymorphism and phenotypic data set to test whether genome-wide genetic and phenotypic differentiation are best explained by (i) isolation by distance, (ii) isolation by history or (iii) isolation by environment. We find that the pronounced genetic and phenotypic variation in I. gularis are only partially correlated and differ regarding spatial predictors. Whereas genomic variation is largely explained by historical barriers to gene flow, phenotypic diversity can be best predicted by contemporary environmental heterogeneity. Our genomic analyses reveal strong phylogeographical structure coinciding with the Chivela Pass at the Isthmus of Tehuantepec that was formed during the Pleistocene, when populations were isolated in north-south refugia. In contrast, we found a strong association between body size and environmental variables, such as temperature and precipitation. The relationship between body size and local climate is consistent with a pattern produced by either natural selection or environmental plasticity. Overall, these results provide empirical evidence for why phenotypic and genomic data are often in conflict in taxonomic and phylogeographical studies.

Uneven Missing Data Skew Phylogenomic Relationships within the Lories and Lorikeets.

The resolution of the Tree of Life has accelerated with advances in DNA sequencing technology. To achieve dense taxon sampling, it is often necessary to obtain DNA from historical museum specimens to supplement modern genetic samples. However, DNA from historical material is generally degraded, which presents various challenges. In this study, we evaluated how the coverage at variant sites and missing data among historical and modern samples impacts phylogenomic inference. We explored these patterns in the brush-tongued parrots (lories and lorikeets) of Australasia by sampling ultraconserved elements in 105 taxa. Trees estimated with low coverage characters had several clades where relationships appeared to be influenced by whether the sample came from historical or modern specimens, which were not observed when more stringent filtering was applied. To assess if the topologies were affected by missing data, we performed an outlier analysis of sites and loci, and a data reduction approach where we excluded sites based on data completeness. Depending on the outlier test, 0.15% of total sites or 38% of loci were driving the topological differences among trees, and at these sites, historical samples had 10.9× more missing data than modern ones. In contrast, 70% data completeness was necessary to avoid spurious relationships. Predictive modeling found that outlier analysis scores were correlated with parsimony informative sites in the clades whose topologies changed the most by filtering. After accounting for biased loci and understanding the stability of relationships, we inferred a more robust phylogenetic hypothesis for lories and lorikeets.

Climatic dynamics and topography control genetic variation in Atlantic Forest montane birds.

Montane organisms responded to Quaternary climate change by tracking suitable habitat along elevational gradients. However, it is unclear whether these past climatic dynamics generated predictable patterns of genetic diversity in co-occurring montane taxa. To test if the genetic variation is associated with historical changes in the elevational distribution of montane habitats, we integrated paleoclimatic data and a model selection approach for testing the demographic history of five co-distributed bird species occurring in the southern Atlantic Forest sky islands. We found that changes in historical population sizes and current genetic diversity are attributable to habitat dynamics among time periods and the current elevational distribution of populations. Taxa with populations restricted to the more climatically dynamic southern mountain block (SMB) had, on average, a six-fold demographic expansion, whereas the populations from the northern mountain block (NMB) remained constant. In the current configuration of the southern Atlantic Forest montane habitats, populations in the SMB have more widespread elevational distributions, occur at lower elevations, and harbor higher levels of genetic diversity than NMB populations. Despite the apparent coupling of demographic and climatic oscillations, our data rejected simultaneous population structuring due to historical habitat fragmentation. Demographic modeling indicated that the species had different modes of differentiation, and varied in the timing of divergence and the degree of gene flow across mountain blocks. Our results suggest that the heterogeneous distribution of genetic variation in birds of the Atlantic Forest sky islands is associated with the interplay between topography and climate of distinct mountains, leading to predictable patterns of genetic diversity.

Macroevolutionary bursts and constraints generate a rainbow in a clade of tropical birds.

BACKGROUND: Bird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint. RESULTS: We found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst. CONCLUSIONS: Overall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.

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.

Species delimitation and biogeography of the gnatcatchers and gnatwrens (Aves: Polioptilidae).

The New World avian family Polioptilidae (gnatcatchers and gnatwrens) is distributed from Argentina to Canada and includes 15 species and more than 60 subspecies. No study to date has evaluated phylogenetic relationships within this family and the historical pattern of diversification within the group remains unknown. Moreover, species limits, particularly in widespread taxa that show geographic variation, remain unclear. In this study, we delimited species and estimated phylogenetic relationships using multilocus data for the entire family. We then used the inferred diversity along with alternative taxonomic classification schemes to evaluate how lumping and splitting of both taxa and geographical areas influenced biogeographic inference. Species-tree analyses grouped Polioptilidae into four main clades: Microbates, Ramphocaenus, a Polioptila guianensis complex, and the remaining members of Polioptila. Ramphocaenus melanurus was sister to the clade containing M. cinereiventris and M. collaris, which formed a clade sister to all species within Polioptila. Polioptila was composed of two clades, the first of which included the P. guianensis complex; the other contained all remaining species in the genus. Using multispecies coalescent modeling, we inferred a more than 3-fold increase in species diversity, of which 87% represent currently recognized species or subspecies. Much of this diversity corresponded to subspecies that occur in the Neotropics. We identified three polyphyletic species, and delimited 4-6 previously undescribed candidate taxa. Probabilistic modeling of geographic ranges on the species tree indicated that the family likely had an ancestral origin in South America, with all three genera independently colonizing North America. Support for this hypothesis, however, was sensitive to the taxonomic classification scheme used and the number of geographical areas allowed. Our study proposes the first phylogenetic hypothesis for Polioptilidae and provides genealogical support for the reclassification of species limits. Species limits and the resolution of geographical areas that taxa inhabit influence the inferred spatial diversification history.