The Complete Genome Sequences of 23 Finch Species (Fringillidae, Passeriformes).

We present complete genome sequences of 23 species of finches from 6 genera.

The Evolution of Multiple Color Mechanisms Is Correlated with Diversification in Sunbirds (Nectariniidae).

How and why certain groups become speciose is a key question in evolutionary biology. Novel traits that enable diversification by opening new ecological niches are likely important mechanisms. However, ornamental traits can also promote diversification by opening up novel sensory niches and thereby creating novel inter-specific interactions. More specifically, ornamental colors may enable more precise and/or easier species recognition and may act as key innovations by increasing the number of species-specific patterns and promoting diversification. While the influence of coloration on diversification is well-studied, the influence of the mechanisms that produce those colors (e.g., pigmentary, nanostructural) is less so, even though the ontogeny and evolution of these mechanisms differ. We estimated a new phylogenetic tree for 121 sunbird species and combined color data of 106 species with a range of phylogenetic tools to test the hypothesis that the evolution of novel color mechanisms increases diversification in sunbirds, one of the most colorful bird clades. Results suggest that: (1) the evolution of novel color mechanisms expands the visual sensory niche, increasing the number of achievable colors, (2) structural coloration diverges more readily across the body than pigment-based coloration, enabling an increase in color complexity, (3) novel color mechanisms might minimize trade-offs between natural and sexual selection such that color can function both as camouflage and conspicuous signal, and (4) despite structural colors being more colorful and mobile, only melanin-based coloration is positively correlated with net diversification. Together, these findings explain why color distances increase with an increasing number of sympatric species, even though packing of color space predicts otherwise.

Genomic signatures of convergent shifts to plunge-diving behavior in birds.

Understanding the genetic basis of convergence at broad phylogenetic scales remains a key challenge in biology. Kingfishers (Aves: Alcedinidae) are a cosmopolitan avian radiation with diverse colors, diets, and feeding behaviors-including the archetypal plunge-dive into water. Given the sensory and locomotor challenges associated with air-water transitions, kingfishers offer a powerful opportunity to explore the effects of convergent behaviors on the evolution of genomes and phenotypes, as well as direct comparisons between continental and island lineages. Here, we use whole-genome sequencing of 30 diverse kingfisher species to identify the genomic signatures associated with convergent feeding behaviors. We show that species with smaller ranges (i.e., on islands) have experienced stronger demographic fluctuations than those on continents, and that these differences have influenced the dynamics of molecular evolution. Comparative genomic analyses reveal positive selection and genomic convergence in brain and dietary genes in plunge-divers. These findings enhance our understanding of the connections between genotype and phenotype in a diverse avian radiation.

The Complete Genome Sequences of 19 Species of Snipes (Scolopacidae, Charadriiformes, Aves).

We present the complete genome sequences of 19 species of snipes from 7 genera. Illumina sequencing was performed on genetic material from museum specimens. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data are publicly available via Genbank.

Complex plumages spur rapid color diversification in kingfishers (Aves: Alcedinidae).

Colorful signals in nature provide some of the most stunning examples of rapid phenotypic evolution. Yet, studying color pattern evolution has been historically difficult owing to differences in perceptual ability of humans and analytical challenges with studying how complex color patterns evolve. Island systems provide a natural laboratory for testing hypotheses about the direction and magnitude of phenotypic change. A recent study found that plumage colors of island species are darker and less complex than continental species. Whether such shifts in plumage complexity are associated with increased rates of color evolution remains unknown. Here, we use geometric morphometric techniques to test the hypothesis that plumage complexity and insularity interact to influence color diversity in a species-rich clade of colorful birds-kingfishers (Aves: Alcedinidae). In particular, we test three predictions: (1) plumage complexity enhances interspecific rates of color evolution, (2) plumage complexity is lower on islands, and (3) rates of plumage color evolution are higher on islands. Our results show that more complex plumages result in more diverse colors among species and that island species have higher rates of color evolution. Importantly, we found that island species did not have more complex plumages than their continental relatives. Thus, complexity may be a key innovation that facilitates evolutionary response of individual color patches to distinct selection pressures on islands, rather than being a direct target of selection itself. This study demonstrates how a truly multivariate treatment of color data can reveal evolutionary patterns that might otherwise go unnoticed.

Birds are among the most colorful animals on Earth. The different patterns and colors displayed on their feathers help them to identify their own species, attract mates or hide from predators. The bright plumages of birds are achieved through either pigments (such as reds and yellows) or structures (such as blues, greens or ultraviolet) inside feathers, or through a combination of both pigments and structures. Variation in the diversity of color patterns over time can give a helpful insight into the rate of evolution of a species. For example, structural colors evolve more quickly than pigment-based ones and can therefore be a key feature involved in species recognition or mate attraction. Studying the evolution of plumage patterns has been challenging due to differences in the vision of humans and birds. However, recent advances in technology have enabled researchers to map the exact wavelengths of the colors that make up the patterns, allowing for rigorous comparison of plumage color patterns across different individuals and species. To gain a greater understanding of how plumage color patterns evolve in birds, Eliason et al. studied kingfishers, a group of birds known for their complex and variable color patterns, and their worldwide distribution. The experiments analyzed the plumage color patterns of 72 kingfisher species (142 individual museum specimens) from both mainland and island populations by quantifying the amount of different wavelengths of light reflecting from a feather and accounting for relationships among species and among feather patches. The analyzes showed that having more complex patterns leads to a greater accumulation of plumage colors over time, supporting the idea that complex plumages provide more traits for natural or sexual selection to act upon. Moreover, in upper parts of the bodies, such as the back, the plumage varied more across the different species and evolved faster than in ventral parts, such as the belly or throat. This indicates that sexual selection may be the evolutionary force driving variation in more visible areas, such as the back, while patterns in the ventral part of the body are more important for kin recognition. Eliason et al. further found no differences in plumage complexity between kingfishers located in island or mainland habitats, suggesting that the isolation of the island and the different selection pressures this may bring does not impact the complexity of color patterns. However, kingfisher species located on islands did display higher rates of color evolution. This indicates that, regardless of the complexity of the plumage, island-specific pressures are driving rapid color diversification. Using a new multivariate approach, Eliason et al. have unearthed a pattern in plumage complexity that may otherwise have been missed and, for the first time, have linked differences in color pattern on individual birds with evolutionary differences across species. In doing so, they have provided a framework for future studies of color evolution. The next steps in this research would be to better understand why the island species are evolving more rapidly even though they do not have more complex plumage patterns and how the observed color differences relate to rapid rates of speciation.

Interspecific hybridization explains rapid gorget colour divergence in Heliodoxa hummingbirds (Aves: Trochilidae).

Hybridization is a known source of morphological, functional and communicative signal novelty in many organisms. Although diverse mechanisms of established novel ornamentation have been identified in natural populations, we lack an understanding of hybridization effects across levels of biological scales and upon phylogenies. Hummingbirds display diverse structural colours resulting from coherent light scattering by feather nanostructures. Given the complex relationship between feather nanostructures and the colours they produce, intermediate coloration does not necessarily imply intermediate nanostructures. Here, we characterize nanostructural, ecological and genetic inputs in a distinctive Heliodoxa hummingbird from the foothills of eastern Peru. Genetically, this individual is closely allied with Heliodoxa branickii and Heliodoxa gularis, but it is not identical to either when nuclear data are assessed. Elevated interspecific heterozygosity further suggests it is a hybrid backcross to H. branickii. Electron microscopy and spectrophotometry of this unique individual reveal key nanostructural differences underlying its distinct gorget colour, confirmed by optical modelling. Phylogenetic comparative analysis suggests that the observed gorget coloration divergence from both parentals to this individual would take 6.6-10 My to evolve at the current rate within a single hummingbird lineage. These results emphasize the mosaic nature of hybridization and suggest that hybridization may contribute to the structural colour diversity found across hummingbirds.

Intestinal microbiota of Nearctic-Neotropical migratory birds vary more over seasons and years than between host species.

Seasonal migration of Nearctic-Neotropical passerine birds may have profound effects on the diversity and abundance of their host-associated microbiota. Migratory birds experience seasonal change in environments and diets throughout the course of the annual cycle that, along with recurrent biological events such as reproduction, may significantly impact their microbiota. In this study, we characterize the intestinal microbiota of four closely related species of migratory Catharus thrushes at three time points of their migratory cycle: during spring migration, on the summer breeding territories and during fall migration. Using observations replicated over 3 years, we determined that microbial community diversity of Catharus thrushes was significantly different across distinct time periods of the annual cycle, whereas community composition was more similar within than across years. Elevated alpha diversity in the summer birds compared to either migratory period indicated that birds may harbour a reduced microbiota during active migration. We also found that community composition of the microbiota did not substantially differ between host species. Finally, we recovered two phyla, Cyanobacteria and Planctomycetota, which are not commonly described from birds, that were in relatively high abundance in specific years. This study contributes to our growing understanding of how microbiota in wild birds vary throughout disparate ecological conditions and reveals potential axes across which an animal's microbial flexibility adapts to variable environments and recurrent biological conditions throughout the annual cycle.

The Complete Genome Sequence of Cyanopsitta spixii, the Spix's Macaw.

The Spix's Macaw (Cyanopsitta spixii) is a critically endangered parrot that was once endemic to Brazil. We present the whole genome sequence of this species. Illumina sequencing was performed on a genetic sample from a single captive individual. The reads were assembled using a de novo method followed by a series of references from related species for finishing. The raw and assembled data is publicly available via Genbank: Sequence Read Archive (SRR15037507) and Assembly (GCA_024336845).

The Complete Genome Sequences of 94 Species of Parrots (Psittaciformes, Aves).

We present the complete genome sequences of 94 species of parrots from 40 genera. Illumina sequencing was performed on genetic material from single individuals. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data is publicly available via Genbank.

Genomic novelty within a "great speciator" revealed by a high-quality reference genome of the collared kingfisher (Todiramphus chloris collaris).

Islands are natural laboratories for studying patterns and processes of evolution. Research on island endemic birds has revealed elevated speciation rates and rapid phenotypic evolution in several groups (e.g. white-eyes, Darwin's finches). However, understanding the evolutionary processes behind these patterns requires an understanding of how genotypes map to novel phenotypes. To date, there are few high-quality reference genomes for species found on islands. Here, we sequence the genome of one of Ernst Mayr's "great speciators," the collared kingfisher (Todiramphus chloris collaris). Utilizing high molecular weight DNA and linked-read sequencing technology, we assembled a draft high-quality genome with highly contiguous scaffolds (scaffold N50 = 19 Mb). Based on universal single-copy orthologs, we estimated a gene space completeness of 96.6% for the draft genome assembly. The population demographic history analyses reveal a distinct pattern of contraction and expansion in population size throughout the Pleistocene. Comparative genomic analysis of gene family evolution revealed that species-specific and rapidly expanding gene families in the collared kingfisher (relative to other Coraciiformes) are mainly involved in the ErbB signaling pathway and focal adhesion. Todiramphus kingfishers are a species-rich group that has become a focus of speciation research. This draft genome will be a platform for future taxonomic, phylogeographic, and speciation research in the group. For example, target genes will enable testing of changes in sensory structures associated with changes in vision and taste genes across kingfishers.

Orthologous microsatellites, transposable elements, and DNA deletions correlate with generation time and body mass in neoavian birds.

The rate of mutation accumulation in germline cells can be affected by cell replication and/or DNA damage, which are further related to life history traits such as generation time and body mass. Leveraging the existing datasets of 233 neoavian bird species, here, we investigated whether generation time and body mass contribute to the interspecific variation of orthologous microsatellite length, transposable element (TE) length, and deletion length and how these genomic attributes affect genome sizes. In nonpasserines, we found that generation time is correlated to both orthologous microsatellite length and TE length, and body mass is negatively correlated to DNA deletions. These patterns are less pronounced in passerines. In all species, we found that DNA deletions relate to genome size similarly as TE length, suggesting a role of body mass dynamics in genome evolution. Our results indicate that generation time and body mass shape the evolution of genomic attributes in neoavian birds.

The Complete Genome Sequence of Conuropsis carolinensis, the Carolina Parakeet.

The Carolina Parakeet (Conuropsis carolinensis) is an extinct species of parrot that was native to the eastern, midwest, and plains regions of the United States. We present the whole genome sequence of this species. Illumina sequencing was performed on a genetic sample from a single captive individual. The reads were assembled using a de novo method followed by a series of references from related species for finishing. The raw and assembled data is publicly available via Genbank: Sequence Read Archive (SRR21023482) and assembled genome (JAOBYI000000000).

Repeated sampling of individuals reveals impact of tropical and temperate habitats on microbiota of a migratory bird.

Migratory animals experiencing substantial change in diet and habitat across the annual cycle may have corresponding shifts in host-associated microbial diversity. Using automated telemetry and radio tags to recapture birds, we examined gut microbiota structure in the same population and often same individual of Kirtland's Warblers (Setophaga kirtlandii) initially sampled on their wintering grounds in The Bahamas and subsequently resampled within their breeding territories in Michigan, USA. Initial sampling occurred in March and April and resampling occurred in May, June and early July. The composition of the most abundant phyla and classes of the warblers' microbiota is similar to that of other migratory birds. However, we detected notable variation in abundance and diversity of numerous bacterial taxa, including a decrease in microbial richness and significant differences in microbial communities when comparing the microbiota of birds first captured in The Bahamas to that of birds recaptured in Michigan. This is observed at the individual and population level. Furthermore, we found that 22 bacterial genera exhibit heightened abundance within specific sampling periods and are probably associated with diet and environmental change. Finally, we described a small, species-specific shared microbial profile that spans multiple time periods and environments within the migratory cycle. Our research highlights that the avian gut microbiota is dynamic over time, most significantly impacted by changing environments associated with migration. These results support the need for full annual cycle monitoring of migratory bird microbiota to improve understanding of seasonal host movement ecologies and response to recurrent physiological stressors.

Accelerated Brain Shape Evolution Is Associated with Rapid Diversification in an Avian Radiation.

AbstractNiche expansion is a critical step in the speciation process. Large brains linked to improved cognitive ability may enable species to expand their niches and forage in new ways, thereby promoting speciation. Despite considerable work on ecological divergence in brain size and its importance in speciation, relatively little is known about how brain shape relates to behavioral, ecological, and taxonomic diversity at macroevolutionary scales. This is due in part to inherent challenges with quantifying brain shape across many species. Here we present a novel, semiautomated approach for rapidly phenotyping brain shape using semilandmarks derived from X-ray computed microtomography scans. We then test its utility by parsing evolutionary trends within a diverse radiation of birds: kingfishers (Aves: Alcedinidae). Multivariate comparative analyses reveal that rates of brain shape evolution (but not beak shape) are positively correlated with lineage diversification rates. Distinct brain shapes are further associated with changes in body size and foraging behavior, suggesting both allometric and ecological constraints on brain shape evolution. These results are in line with the idea of brains acting as a "master regulator" of critical processes governing speciation, such as dispersal, foraging behavior, and dietary niche.

Contrasting drivers of diversity in hosts and parasites across the tropical Andes.

Geographic turnover in community composition is created and maintained by eco-evolutionary forces that limit the ranges of species. One such force may be antagonistic interactions among hosts and parasites, but its general importance is unknown. Understanding the processes that underpin turnover requires distinguishing the contributions of key abiotic and biotic drivers over a range of spatial and temporal scales. Here, we address these challenges using flexible, nonlinear models to identify the factors that underlie richness (alpha diversity) and turnover (beta diversity) patterns of interacting host and parasite communities in a global biodiversity hot spot. We sampled 18 communities in the Peruvian Andes, encompassing ∼1,350 bird species and ∼400 hemosporidian parasite lineages, and spanning broad ranges of elevation, climate, primary productivity, and species richness. Turnover in both parasite and host communities was most strongly predicted by variation in precipitation, but secondary predictors differed between parasites and hosts, and between contemporary and phylogenetic timescales. Host communities shaped parasite diversity patterns, but there was little evidence for reciprocal effects. The results for parasite communities contradicted the prevailing view that biotic interactions filter communities at local scales while environmental filtering and dispersal barriers shape regional communities. Rather, subtle differences in precipitation had strong, fine-scale effects on parasite turnover while host-community effects only manifested at broad scales. We used these models to map bird and parasite turnover onto the ecological gradients of the Andean landscape, illustrating beta-diversity hot spots and their mechanistic underpinnings.

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.

Morphological innovation and biomechanical diversity in plunge-diving birds.

Innovations in foraging behavior can drive morphological diversity by opening up new ways of interacting with the environment, or limit diversity through functional constraints associated with different foraging behaviors. Several classic examples of adaptive radiations in birds show increased variation in ecologically relevant traits. However, these cases primarily focus on geographically narrow adaptive radiations, consider only morphological evolution without a biomechanical approach, or do not investigate tradeoffs with other non-focal traits that might be affected by use of different foraging habitats. Here, we use X-ray microcomputed tomography, biomechanical modeling, and multivariate comparative methods to explore the interplay between foraging behavior and cranial morphology in kingfishers, a global radiation of birds with variable beaks and foraging behaviors, including the archetypal plunge-dive into water. Our results quantify covariation between the shape of the outer keratin covering (rhamphotheca) and the inner skeletal core of the beak, as well as highlight distinct patterns of morphospace occupation for different foraging behaviors and considerable rate variation among these skull regions. We anticipate these findings will have implications for inferring beak shapes in fossil taxa and inform biomimetic design of novel impact-reducing structures.

Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats.

Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from ∼900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Furthermore, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors convergently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.

Using Historical Biogeography Models to Study Color Pattern Evolution.

Color is among the most striking features of organisms, varying not only in spectral properties like hue and brightness, but also in where and how it is produced on the body. Different combinations of colors on a bird's body are important in both environmental and social contexts. Previous comparative studies have treated plumage patches individually or derived plumage complexity scores from color measurements across a bird's body. However, these approaches do not consider the multivariate nature of plumages (allowing for plumage to evolve as a whole) or account for interpatch distances. Here, we leverage a rich toolkit used in historical biogeography to assess color pattern evolution in a cosmopolitan radiation of birds, kingfishers (Aves: Alcedinidae). We demonstrate the utility of this approach and test hypotheses about the tempo and mode of color evolution in kingfishers. Our results highlight the importance of considering interpatch distances in understanding macroevolutionary trends in color diversity and demonstrate how historical biogeography models are a useful way to model plumage color pattern evolution. Furthermore, they show that distinct color mechanisms (pigments or structural colors) spread across the body in different ways and at different rates. Specifically, net rates are higher for structural colors than pigment-based colors. Together, our study suggests a role for both development and selection in driving extraordinary color pattern diversity in kingfishers. We anticipate this approach will be useful for modeling other complex phenotypes besides color, such as parasite evolution across the body.