Genomic phylogeography of the White-crowned Manakin Pseudopipra pipra (Aves: Pipridae) illuminates a continental-scale radiation out of the Andes.

The complex landscape history of the Neotropics has generated opportunities for population isolation and diversification that place this region among the most species-rich in the world. Detailed phylogeographic studies are required to uncover the biogeographic histories of Neotropical taxa, to identify evolutionary correlates of diversity, and to reveal patterns of genetic connectivity, disjunction, and potential differentiation among lineages from different areas of endemism. The White-crowned Manakin (Pseudopipra pipra) is a small suboscine passerine bird that is broadly distributed through the subtropical rainforests of Central America, the lower montane cloud forests of the Andes from Colombia to central Peru, the lowlands of Amazonia and the Guianas, and the Atlantic forest of southeast Brazil. Pseudopipra is currently recognized as a single, polytypic biological species. We studied the effect of the Neotropical landscape on genetic and phenotypic differentiation within this species using genomic data derived from double digest restriction site associated DNA sequencing (ddRAD), and mitochondrial DNA. Most of the genetic breakpoints we identify among populations coincide with physical barriers to gene flow previously associated with avian areas of endemism. The phylogenetic relationships among these populations imply a novel pattern of Andean origination for this group, with subsequent diversification into the Amazonian lowlands. Our analysis of genomic admixture and gene flow reveals a complex history of introgression between some western Amazonian populations. These reticulate processes confound our application of standard concatenated and coalescent phylogenetic methods and raise the question of whether a lineage in the western Napo area of endemism should be considered a hybrid species. Lastly, analysis of variation in vocal and plumage phenotypes in the context of our phylogeny supports the hypothesis that Pseudopipra is a species-complex composed of at least 8, and perhaps up to 17 distinct species which have arisen in the last ~2.5 Ma.

A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing.

Although reconstruction of the phylogeny of living birds has progressed tremendously in the last decade, the evolutionary history of Neoaves--a clade that encompasses nearly all living bird species--remains the greatest unresolved challenge in dinosaur systematics. Here we investigate avian phylogeny with an unprecedented scale of data: >390,000 bases of genomic sequence data from each of 198 species of living birds, representing all major avian lineages, and two crocodilian outgroups. Sequence data were collected using anchored hybrid enrichment, yielding 259 nuclear loci with an average length of 1,523 bases for a total data set of over 7.8 × 10(7) bases. Bayesian and maximum likelihood analyses yielded highly supported and nearly identical phylogenetic trees for all major avian lineages. Five major clades form successive sister groups to the rest of Neoaves: (1) a clade including nightjars, other caprimulgiforms, swifts, and hummingbirds; (2) a clade uniting cuckoos, bustards, and turacos with pigeons, mesites, and sandgrouse; (3) cranes and their relatives; (4) a comprehensive waterbird clade, including all diving, wading, and shorebirds; and (5) a comprehensive landbird clade with the enigmatic hoatzin (Opisthocomus hoazin) as the sister group to the rest. Neither of the two main, recently proposed Neoavian clades--Columbea and Passerea--were supported as monophyletic. The results of our divergence time analyses are congruent with the palaeontological record, supporting a major radiation of crown birds in the wake of the Cretaceous-Palaeogene (K-Pg) mass extinction.

An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.

Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector-transmitted parasites. Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity of Leucocytozoon (an avian blood parasite) at site and species levels across the New World. To explore spatial patterns in infection probability and lineage diversity for Leucocytozoon parasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high-resolution satellite remote-sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly. Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence of Leucocytozoon parasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected with Leucocytozoon increased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes. Whereas temperature partially constrains Leucocytozoon diversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, for Leucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector-transmitted parasites. Unlike other vector-transmitted diseases, our results show that Leucocytozoon diversity and prevalence will likely decrease with warming temperatures.

Genomic Signature of an Avian Lilliput Effect across the K-Pg Extinction.

Survivorship following major mass extinctions may be associated with a decrease in body size-a phenomenon called the Lilliput Effect. Body size is a strong predictor of many life history traits (LHTs), and is known to influence demography and intrinsic biological processes. Pronounced changes in organismal size throughout Earth history are therefore likely to be associated with concomitant genome-wide changes in evolutionary rates. Here, we report pronounced heterogeneity in rates of molecular evolution (varying up to $\sim$20-fold) across a large-scale avian phylogenomic data set and show that nucleotide substitution rates are strongly correlated with body size and metabolic rate. We also identify potential body size reductions associated with the Cretaceous-Paleogene (K-Pg) transition, consistent with a Lilliput Effect in the wake of that mass extinction event. We posit that selection for reduced body size across the K-Pg extinction horizon may have resulted in transient increases in substitution rate along the deepest branches of the extant avian tree of life. This "hidden" rate acceleration may result in both strict and relaxed molecular clocks over-estimating the age of the avian crown group through the relationship between life history and demographic parameters that scale with molecular substitution rate. If reductions in body size (and/or selection for related demographic parameters like short generation times) are a common property of lineages surviving mass extinctions, this phenomenon may help resolve persistent divergence time debates across the tree of life. Furthermore, our results suggest that selection for certain LHTs may be associated with deterministic molecular evolutionary outcomes.

A comprehensive multilocus phylogeny of the Neotropical cotingas (Cotingidae, Aves) with a comparative evolutionary analysis of breeding system and plumage dimorphism and a revised phylogenetic classification.

The Neotropical cotingas (Cotingidae: Aves) are a group of passerine birds that are characterized by extreme diversity in morphology, ecology, breeding system, and behavior. Here, we present a comprehensive phylogeny of the Neotropical cotingas based on six nuclear and mitochondrial loci (∼7500 bp) for a sample of 61 cotinga species in all 25 genera, and 22 species of suboscine outgroups. Our taxon sample more than doubles the number of cotinga species studied in previous analyses, and allows us to test the monophyly of the cotingas as well as their intrageneric relationships with high resolution. We analyze our genetic data using a Bayesian species tree method, and concatenated Bayesian and maximum likelihood methods, and present a highly supported phylogenetic hypothesis. We confirm the monophyly of the cotingas, and present the first phylogenetic evidence for the relationships of Phibalura flavirostris as the sister group to Ampelion and Doliornis, and the paraphyly of Lipaugus with respect to Tijuca. In addition, we resolve the diverse radiations within the Cotinga, Lipaugus, Pipreola, and Procnias genera. We find no support for Darwin's (1871) hypothesis that the increase in sexual selection associated with polygynous breeding systems drives the evolution of color dimorphism in the cotingas, at least when analyzed at a broad categorical scale. Finally, we present a new comprehensive phylogenetic classification of all cotinga species.

The pace of mitochondrial molecular evolution varies with seasonal migration distance.

Animals that engage in long-distance seasonal migration experience strong selective pressures on their metabolic performance and life history, with potential consequences for molecular evolution. Species with slow life histories typically show lower rates of synonymous substitution (dS) than "fast" species. Previous research suggests long-distance seasonal migrants have a slower life history strategy than short-distance migrants, raising the possibility that rates of molecular evolution may covary with migration distance. Additionally, long-distance migrants may face strong selection on metabolically-important mitochondrial genes due to their long-distance flights. Using over 1,000 mitochondrial genomes, we assessed the relationship between migration distance and mitochondrial molecular evolution in 39 boreal-breeding migratory bird species. We show that migration distance correlates negatively with dS, suggesting that the slow life history associated with long-distance migration is reflected in rates of molecular evolution. Mitochondrial genes in every study species exhibited evidence of purifying selection, but the strength of selection was greater in short-distance migrants, contrary to our predictions. This result may indicate effects of selection for cold tolerance on mitochondrial evolution among species overwintering at high latitudes. Our study demonstrates that the pervasive correlation between life history and molecular evolutionary rates exists in the context of differential adaptations to seasonality.

The genomic landscape, causes, and consequences of extensive phylogenomic discordance in Old World mice and rats.

A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is often widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents (Old World mice and rats) - a large and ecologically diverse group that gave rise to the mouse and rat model systems. Combining new linked-read genome assemblies for seven murine species with eleven published rodent genomes, we first used ultra-conserved elements (UCEs) to infer a robust species tree. We then used whole genomes to examine finer-scale patterns of discordance and found that phylogenies built from proximate chromosomal regions had similar phylogenies. However, there was no relationship between tree similarity and local recombination rates in house mice, suggesting that genetic linkage influences phylogenetic patterns over deeper timescales. This signal may be independent of contemporary recombination landscapes. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to less discordance, while genes experiencing positive selection showed more discordant and variable phylogenetic signals. Finally, we show that assuming a single species tree can result in high error rates when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.

Ecological selectivity and the evolution of mammalian substrate preference across the K-Pg boundary.

The Cretaceous-Paleogene (K-Pg) mass extinction 66 million years ago was characterized by a worldwide ecological catastrophe and rapid species turnover. Large-scale devastation of forested environments resulting from the Chicxulub asteroid impact likely influenced the evolutionary trajectories of multiple clades in terrestrial environments, and it has been hypothesized to have biased survivorship in favour of nonarboreal lineages across the K-Pg boundary. Here, we evaluate patterns of substrate preferences across the K-Pg boundary among crown group mammals, a group that underwent rapid diversification following the mass extinction. Using Bayesian, likelihood, and parsimony reconstructions, we identify patterns of mammalian ecological selectivity that are broadly similar to those previously hypothesized for birds. Models based on extant taxa indicate predominant K-Pg survivorship among semi- or nonarboreal taxa, followed by numerous independent transitions to arboreality in the early Cenozoic. However, contrary to the predominant signal, some or all members of total-clade Euarchonta (Primates + Dermoptera + Scandentia) appear to have maintained arboreal habits across the K-Pg boundary, suggesting ecological flexibility during an interval of global habitat instability. We further observe a pronounced shift in character state transitions away from plesiomorphic arboreality associated with the K-Pg transition. Our findings are consistent with the hypothesis that predominantly nonarboreal taxa preferentially survived the end-Cretaceous mass extinction, and emphasize the pivotal influence of the K-Pg transition in shaping the early evolutionary trajectories of extant terrestrial vertebrates.

Complex coevolution of wing, tail, and vocal sounds of courting male bee hummingbirds.

Phenotypic characters with a complex physical basis may have a correspondingly complex evolutionary history. Males in the "bee" hummingbird clade court females with sound from tail-feathers, which flutter during display dives. On a phylogeny of 35 species, flutter sound frequency evolves as a gradual, continuous character on most branches. But on at least six internal branches fall two types of major, saltational changes: mode of flutter changes, or the feather that is the sound source changes, causing frequency to jump from one discrete value to another. In addition to their tail "instruments," males also court females with sound from their syrinx and wing feathers, and may transfer or switch instruments over evolutionary time. In support of this, we found a negative phylogenetic correlation between presence of wing trills and singing. We hypothesize this transference occurs because wing trills and vocal songs serve similar functions and are thus redundant. There are also three independent origins of self-convergence of multiple signals, in which the same species produces both a vocal (sung) frequency sweep, and a highly similar nonvocal sound. Moreover, production of vocal, learned song has been lost repeatedly. Male bee hummingbirds court females with a diverse, coevolving array of acoustic traits.

Early Evolution of Modern Birds Structured by Global Forest Collapse at the End-Cretaceous Mass Extinction.

The fossil record and recent molecular phylogenies support an extraordinary early-Cenozoic radiation of crown birds (Neornithes) after the Cretaceous-Paleogene (K-Pg) mass extinction [1-3]. However, questions remain regarding the mechanisms underlying the survival of the deepest lineages within crown birds across the K-Pg boundary, particularly since this global catastrophe eliminated even the closest stem-group relatives of Neornithes [4]. Here, ancestral state reconstructions of neornithine ecology reveal a strong bias toward taxa exhibiting predominantly non-arboreal lifestyles across the K-Pg, with multiple convergent transitions toward predominantly arboreal ecologies later in the Paleocene and Eocene. By contrast, ecomorphological inferences indicate predominantly arboreal lifestyles among enantiornithines, the most diverse and widespread Mesozoic avialans [5-7]. Global paleobotanical and palynological data show that the K-Pg Chicxulub impact triggered widespread destruction of forests [8, 9]. We suggest that ecological filtering due to the temporary loss of significant plant cover across the K-Pg boundary selected against any flying dinosaurs (Avialae [10]) committed to arboreal ecologies, resulting in a predominantly non-arboreal post-extinction neornithine avifauna composed of total-clade Palaeognathae, Galloanserae, and terrestrial total-clade Neoaves that rapidly diversified into the broad range of avian ecologies familiar today. The explanation proposed here provides a unifying hypothesis for the K-Pg-associated mass extinction of arboreal stem birds, as well as for the post-K-Pg radiation of arboreal crown birds. It also provides a baseline hypothesis to be further refined pending the discovery of additional neornithine fossils from the Latest Cretaceous and earliest Paleogene.