Complexity of avian evolution revealed by family-level genomes.

Despite tremendous efforts in the past decades, relationships among main avian lineages remain heavily debated without a clear resolution. Discrepancies have been attributed to diversity of species sampled, phylogenetic method and the choice of genomic regions1-3. Here we address these issues by analysing the genomes of 363 bird species4 (218 taxonomic families, 92% of total). Using intergenic regions and coalescent methods, we present a well-supported tree but also a marked degree of discordance. The tree confirms that Neoaves experienced rapid radiation at or near the Cretaceous-Palaeogene boundary. Sufficient loci rather than extensive taxon sampling were more effective in resolving difficult nodes. Remaining recalcitrant nodes involve species that are a challenge to model due to either extreme DNA composition, variable substitution rates, incomplete lineage sorting or complex evolutionary events such as ancient hybridization. Assessment of the effects of different genomic partitions showed high heterogeneity across the genome. We discovered sharp increases in effective population size, substitution rates and relative brain size following the Cretaceous-Palaeogene extinction event, supporting the hypothesis that emerging ecological opportunities catalysed the diversification of modern birds. The resulting phylogenetic estimate offers fresh insights into the rapid radiation of modern birds and provides a taxon-rich backbone tree for future comparative studies.

Dense sampling of bird diversity increases power of comparative genomics.

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1-4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families-including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species.

Reconstructing locomotor ecology of extinct avialans: a case study of Ichthyornis comparing sternum morphology and skeletal proportions.

Avian skeletal morphology is associated with locomotor function, including flight style, swimming and terrestrial locomotion, and permits informed inferences on locomotion in extinct taxa. The fossil taxon Ichthyornis (Avialae: Ornithurae) has long been regarded as highly aerial, with flight similar to terns or gulls (Laridae), and skeletal features resembling foot-propelled diving adaptations. However, rigorous testing of locomotor hypotheses has yet to be performed on Ichthyornis, despite its notable phylogenetic position as one of the most crownward stem birds. We analysed separate datasets of three-dimensional sternal shape (geometric morphometrics) and skeletal proportions (linear measurements across the skeleton), to examine how well these data types predict locomotor traits in Neornithes. We then used this information to infer locomotor capabilities of Ichthyornis. We find strong support for both soaring and foot-propelled swimming capabilities in Ichthyornis. Further, sternal shape and skeletal proportions provide complementary information on avian locomotion: skeletal proportions allow better predictions of the capacity for flight, whereas sternal shape predicts variation in more specific locomotor abilities such as soaring, foot-propelled swimming and escape burst flight. These results have important implications for future studies of extinct avialan ecology and underscore the importance of closely considering sternum morphology in investigations of fossil bird locomotion.

Confidence intervals in molecular dating by maximum likelihood.

Molecular dating has been widely used to infer the times of past evolutionary events using molecular sequences. This paper describes three bootstrap methods to infer confidence intervals under a penalized likelihood framework. The basic idea is to use data pseudoreplicates to infer uncertainty in the branch lengths of a phylogeny reconstructed with molecular sequences. The three specific bootstrap methods are nonparametric (direct tree bootstrapping), semiparametric (rate smoothing), and parametric (Poisson simulation). Our extensive simulation study showed that the three methods perform generally well under a simple strict clock model of molecular evolution; however, the results were less positive with data simulated using an uncorrelated or a correlated relaxed clock model. Several factors impacted, possibly in interaction, the performance of the confidence intervals. Increasing the number of calibration points had a positive effect, as well as increasing the sequence length or the number of sequences although both latter effects depended on the model of evolution. A case study is presented with a molecular phylogeny of the Felidae (Mammalia: Carnivora). A comparison was made with a Bayesian analysis: the results were very close in terms of confidence intervals and there was no marked tendency for an approach to produce younger or older bounds compared to the other.

AVONET: morphological, ecological and geographical data for all birds.

Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.

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 relationship between sternum variation and mode of locomotion in birds.

BACKGROUND: The origin of powered avian flight was a locomotor innovation that expanded the ecological potential of maniraptoran dinosaurs, leading to remarkable variation in modern birds (Neornithes). The avian sternum is the anchor for the major flight muscles and, despite varying widely in morphology, has not been extensively studied from evolutionary or functional perspectives. We quantify sternal variation across a broad phylogenetic scope of birds using 3D geometric morphometrics methods. Using this comprehensive dataset, we apply phylogenetically informed regression approaches to test hypotheses of sternum size allometry and the correlation of sternal shape with both size and locomotory capabilities, including flightlessness and the highly varying flight and swimming styles of Neornithes. RESULTS: We find evidence for isometry of sternal size relative to body mass and document significant allometry of sternal shape alongside important correlations with locomotory capability, reflecting the effects of both body shape and musculoskeletal variation. Among these, we show that a large sternum with a deep or cranially projected sternal keel is necessary for powered flight in modern birds, that deeper sternal keels are correlated with slower but stronger flight, robust caudal sternal borders are associated with faster flapping styles, and that narrower sterna are associated with running abilities. Correlations between shape and locomotion are significant but show weak explanatory power, indicating that although sternal shape is broadly associated with locomotory ecology, other unexplored factors are also important. CONCLUSIONS: These results display the ecological importance of the avian sternum for flight and locomotion by providing a novel understanding of sternum form and function in Neornithes. Our study lays the groundwork for estimating the locomotory abilities of paravian dinosaurs, the ancestors to Neornithes, by highlighting the importance of this critical element for avian flight, and will be useful for future work on the origin of flight along the dinosaur-bird lineage.

Species coexistence and the dynamics of phenotypic evolution in adaptive radiation.

Interactions between species can promote evolutionary divergence of ecological traits and social signals, a process widely assumed to generate species differences in adaptive radiation. However, an alternative view is that lineages typically interact when relatively old, by which time selection for divergence is weak and potentially exceeded by convergent selection acting on traits mediating interspecific competition. Few studies have tested these contrasting predictions across large radiations, or by controlling for evolutionary time. Thus the role of species interactions in driving broad-scale patterns of trait divergence is unclear. Here we use phylogenetic estimates of divergence times to show that increased trait differences among coexisting lineages of ovenbirds (Furnariidae) are explained by their greater evolutionary age in relation to non-interacting lineages, and that--when these temporal biases are accounted for--the only significant effect of coexistence is convergence in a social signal (song). Our results conflict with the conventional view that coexistence promotes trait divergence among co-occurring organisms at macroevolutionary scales, and instead provide evidence that species interactions can drive phenotypic convergence across entire radiations, a pattern generally concealed by biases in age.

Phylogeographic variation within the Buff-browed Foliage-gleaner (Aves: Furnariidae: Syndactyla rufosuperciliata) supports an Andean-Atlantic forests connection via the Cerrado.

We evaluated whether the Andean and the Atlantic forests acted as refugia during the Quaternary, and tested biogeographic hypotheses about the regions involved in the connectivity between those biomes (through the Chaco or the Cerrado). To achieve these goals we selected the Buff-browed Foliage-gleaner Syndactyla rufosuperciliata (Aves, Furnariidae) as a study system, a taxon distributed between the Andean and Atlantic forest. We first explored the historical connectivity between regions through niche modeling. We subsequently used DNA sequences (n = 71 individuals) and genomic analyses (ddRADseq, n = 33 individuals) to evaluate population genetic structure and gene flow within this species. Finally, we performed population model selection using Approximate Bayesian Computation. Our findings indicate that the Andean and the Atlantic forests acted as refugia, and that the populations of the focal species from both regions contacted through the Cerrado region, thus suggesting that the historical dynamics of Andean and Atlantic forests are important for the evolution of forest birds in the region. The results are in agreement with studies of other organisms and may indicate a more general pattern of connectivity among biomes in the Neotropics. Finally, we recommend recognizing both the Andean and the Altantic forests lineages of S. rufosuperciliata as independent species.

Early procurement of scarlet macaws and the emergence of social complexity in Chaco Canyon, NM.

High-precision accelerator mass spectrometer (AMS) (14)C dates of scarlet macaw (Ara macao) skeletal remains provide the first direct evidence from Chaco Canyon in northwestern New Mexico that these Neotropical birds were procured from Mesoamerica by Pueblo people as early as ∼ A.D. 900-975. Chaco was a prominent prehistoric Pueblo center with a dense concentration of multistoried great houses constructed from the 9th through early 12th centuries. At the best known great house of Pueblo Bonito, unusual burial crypts and significant quantities of exotic and symbolically important materials, including scarlet macaws, turquoise, marine shell, and cacao, suggest societal complexity unprecedented elsewhere in the Puebloan world. Scarlet macaws are known markers of social and political status among the Pueblos. New AMS (14)C-dated scarlet macaw remains from Pueblo Bonito demonstrate that these birds were acquired persistently from Mesoamerica between A.D. 900 and 1150. Most of the macaws date before the hypothesized apogeal Chacoan period (A.D. 1040-1110) to which they are commonly attributed. The 10th century acquisition of these birds is consistent with the hypothesis that more formalized status hierarchies developed with significant connections to Mesoamerica before the post-A.D. 1040 architectural florescence in Chaco Canyon.

Dispersal has inhibited avian diversification in Australasian archipelagoes.

Different models of speciation predict contrasting patterns in the relationship between the dispersal ability of lineages and their diversification rates. This relationship is expected to be negative in isolation-limited models and positive in founder-event models. In addition, the combination of negative and positive effects of dispersal on speciation can result in higher diversification rates at intermediate levels of dispersal ability. Using molecular phylogenies to estimate diversification rates, and wing morphology to estimate dispersal ability, we analysed the influence of dispersal on diversification in the avifauna of Australasian archipelagoes. Contrary to expectations given the fragmented nature of island systems, the relationship between dispersal ability and diversification rate was monotonically negative. While multiple mechanisms could generate this pattern, they all share a phase of range expansion that is decoupled from speciation.

Phylogenetic relationships among Synallaxini spinetails (Aves: Furnariidae) reveal a new biogeographic pattern across the Amazon and Paraná river basins.

Relationships among genera in the tribe Synallaxini have proved difficult to resolve. In this study, I investigate relationships among Synallaxis, Certhiaxis and Schoeniophylax using DNA sequences from the mitochondrion and three nuclear regions. I implemented novel primers and protocols for amplifying and sequencing autosomal and sex-linked introns in Furnariidae that resolved basal relationships in the Synallaxini with strong support. Synallaxis propinqua is sister to Schoeniophylax phryganophilus, and together they form a clade with Certhiaxis. The results are robust to analytical approaches when all genomic regions are analyzed jointly (parsimony, maximum likelihood, and species-tree analysis) and the same basal relationships are recovered by most genomic regions when analyzed separately. A sister relationship between S. propinqua, an Amazonian river island specialist, and S. phryganophilus, from the Paraná River basin region, reveals a new biogeographic pattern shared by at least other four pairs of taxa with similar distributions and ecologies. Estimates of divergence times for these five pairs span from the late Miocene to the Pleistocene. Identification of the historical events that produced this pattern is difficult and further advances will require additional studies of the taxa involved and a better understanding of the recent environmental history of South America. A new classification is proposed for the Synallaxini, including the description of a new genus for S. propinqua.

Neotropics as a Cradle for Adaptive Radiations.

Neotropical ecosystems are renowned for numerous examples of adaptive radiation in both plants and animals resulting in high levels of biodiversity and endemism. However, we still lack a comprehensive review of the abiotic and biotic factors that contribute to these adaptive radiations. To fill this gap, we delve into the geological history of the region, including the role of tectonic events such as the Andean uplift, the formation of the Isthmus of Panama, and the emergence of the Guiana and Brazilian Shields. We also explore the role of ecological opportunities created by the emergence of new habitats, as well as the role of key innovations, such as novel feeding strategies or reproductive mechanisms. We discuss different examples of adaptive radiation, including classic ones like Darwin's finches and Anolis lizards, and more recent ones like bromeliads and lupines. Finally, we propose new examples of adaptive radiations mediated by ecological interactions in their geological context. By doing so, we provide insights into the complex interplay of factors that contributed to the remarkable diversity of life in the Neotropics and highlight the importance of this region in understanding the origins of biodiversity.

No Signs of Adaptations for High Flight Intensity in the Mitochondrial Genome of Birds.

Mitochondrial genomes are expected to show adaptations for optimizing aerobic respiration in birds that make intense use of flight. However, there is limited empirical evidence of such a relationship. We here examine correlates of several mitochondrial genome characteristics and flight use across a diverse sample of 597 bird species. We developed an index of flight use intensity that ranged from 0 in flightless species to 9 in migratory hummingbirds and examined its association with nucleobase composition, amino acid class composition, and amino acid site allelic variation using phylogenetic comparative methods. We found no evidence of mitochondrial genome adaptations to flight intensity. Neither nucleotide composition nor amino acid properties showed consistent patterns related to flight use. While specific sites in mitochondrial genes exhibited variation associated with flight intensity, there was limited association between specific amino acid residues and flight intensity levels. Our findings suggest a complex genetic architecture for aerobic performance traits, where multiple genes in both mitochondria and the nucleus may contribute to overall performance. Other factors, such as gene expression regulation and anatomical adaptations, may play a more significant role in influencing flight performance than changes in mitochondrial genes. These findings highlight the need for comprehensive genomic analyses to unravel the intricate relationship between genetic variants and aerobic performance in birds.

Determinants of natal dispersal distances in North American birds.

Natal dispersal-the movement from birth site to first breeding site-determines demographic and population genetic dynamics and has important consequences for ecological and evolutionary processes. Recent work suggested that one of the main factors determining natal dispersal distances is the cost of locomotion. We evaluated this hypothesis using band recovery data to estimate natal dispersal distances for 50 North American bird species. We then analyzed the relationships between dispersal distances and a suite of morphological and ecological predictors, including proxies for the cost of locomotion (flight efficiency), using phylogenetic regression models. We found that flight efficiency, population size, and habitat influence natal dispersal distances. We discuss how the effects of population size and habitat can also be related to mobility and locomotion. Our findings are consistent with a predominant effect of adaptations for mobility on dispersal distances.

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

N/A.

New methods for estimating the total wing area of birds.

Dispersal is a fundamental process in evolution and ecology. Due to the predominant role of flight in bird movement, their dispersal capabilities can be estimated from their flight morphology. Most predictors of flight efficiency require an estimate of the total wing area, but the existing methods for estimating wing area are multi-stepped and prone to compounding error. Here, we validated a new method for estimating the total wing area that requires only the measurement of the wingspan plus two measurements from the folded wings of study skin specimens: wing length and wing width. We demonstrate that the new folded-wing method estimates total wing area with high precision across a variety of avian groups and wing shapes. In addition, the new method performs as well as the old method when used to estimate natal dispersal distances of North American birds. The folded-wing method will allow for estimates of the total wing to be readily obtained from thousands of specimens in ornithological collections, thus providing critical information for studies of flight and dispersal in birds.

La dispersión es un proceso fundamental en evolución y ecología. Debido al papel predominante del vuelo en el movimiento de las aves, su capacidad de dispersión puede estimarse a partir de su morfología de vuelo. La mayoría de los predictores de la eficiencia de vuelo requieren una estimación del área total del ala, pero los métodos existentes para estimar el área del ala requieren numerosos pasos y son propensos a errores compuestos. En este estudio validamos un nuevo método para estimar el área total del ala que requiere solo la medida de la envergadura y dos medidas de las alas plegadas que pueden tomarse de pieles del estudio: el largo y el ancho del ala. Demostramos que el nuevo método estima el área total del ala con alta precisión en una variedad de grupos de aves y formas de alas. Además, el nuevo método funciona tan bien como el anterior cuando se usa para estimar las distancias de dispersión natal de las aves de América del Norte. El nuevo método permitirá obtener fácilmente estimaciones del área alar total a partir de miles de especímenes en colecciones ornitológicas, beneficiando estudios de vuelo y dispersión en aves.

Ecological opportunity and diversification in a continental radiation of birds: climbing adaptations and cladogenesis in the Furnariidae.

Ecological theories of adaptive radiation predict that ecological opportunity stimulates cladogenesis through its effects on competitive release and niche expansion. Given that key innovations may confer ecological opportunity, we investigated the effect of the acquisition of climbing adaptations on rates of cladogenesis in a major avian radiation, the Neotropical bird family Furnariidae, using a species-level phylogeny. Morphological specializations for vertical climbing originated in the woodcreepers ∼23 million years ago, well before that adaptation occurred in woodpeckers (Picidae) or in other potential competitors in South America. This suggests that the acquisition of climbing adaptations conferred ample ecological opportunity to early woodcreepers. Nonetheless, we found that increases in speciation rates in Furnariidae did not coincide with the acquisition of climbing adaptations and that the relationship between the accumulation of climbing adaptations and rates of speciation was negative. In addition, we did not detect a diversity-dependent decline in woodcreeper diversification rates consistent with saturation of the trunk-climbing niche. These findings do not support the hypothesis that ecological opportunity related to trunk foraging stimulated cladogenesis in this radiation. The negative effect of climbing on diversification may be mediated by an indirect positive effect of climbing on dispersal ability, which may reduce speciation rates over evolutionary timescales.

High dispersal ability inhibits speciation in a continental radiation of passerine birds.

Dispersal can stimulate speciation by facilitating geographical expansion across barriers or inhibit speciation by maintaining gene flow among populations. Therefore, the relationship between dispersal ability and speciation rates can be positive or negative. Furthermore, an 'intermediate dispersal' model that combines positive and negative effects predicts a unimodal relationship between dispersal and diversification. Because both dispersal ability and speciation rates are difficult to quantify, empirical evidence for the relationship between dispersal and diversification remains scarce. Using a surrogate for flight performance and a species-level DNA-based phylogeny of a large South American bird radiation (the Furnariidae), we found that lineages with higher dispersal ability experienced lower speciation rates. We propose that the degree of fragmentation or permeability of the geographical setting together with the intermediate dispersal model are crucial in reconciling previous, often contradictory findings regarding the relationship between dispersal and diversification.