Approaching a state shift in Earth's biosphere.

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale 'tipping point' highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

Multi-locus phylogenetic inference among New World Vultures (Aves: Cathartidae).

New World Vultures are large-bodied carrion feeding birds in the family Cathartidae, currently consisting of seven species from five genera with geographic distributions in North and South America. No study to date has included all cathartid species in a single phylogenetic analysis. In this study, we investigated the phylogenetic relationships among all cathartid species using five nuclear (nuc; 4060bp) and two mitochondrial (mt; 2165bp) DNA loci with fossil calibrated gene tree (27 outgroup taxa) and coalescent-based species tree (2 outgroup taxa) analyses. We also included an additional four nuclear loci (2578bp) for the species tree analysis to explore changes in nodal support values. Although the stem lineage is inferred to have originated ∼69 million years ago (Ma; 74.5-64.9 credible interval), a more recent basal split within Cathartidae was recovered at ∼14Ma (17.1-11.1 credible interval). Two primary clades were identified: (1) Black Vulture (Coragyps atratus) together with the three Cathartes species (Lesser C. burrovianus and Greater C. melambrotus Yellow-headed Vultures, and Turkey Vulture C. aura), and (2) King Vulture (Sarcoramphus papa), California (Gymnogyps californianus) and Andean (Vultur gryphus) Condors. Support for taxon relationships within the two basal clades were inconsistent between analyses with the exception of Black Vulture sister to a monophyletic Cathartes clade. Increased support for a yellow-headed vulture clade was recovered in the species tree analysis using the four additional nuclear loci. Overall, these results are in agreement with cathartid life history (e.g. olfaction ability and behavior) and contrasting habitat affinities among sister taxa with overlapping geographic distributions. More research is needed using additional molecular loci to further resolve the phylogenetic relationships within the two basal cathartid clades, as speciation appeared to have occurred in a relatively short period of time.

Rapid diversification of falcons (Aves: Falconidae) due to expansion of open habitats in the Late Miocene.

Understanding how and why lineages diversify is central to understanding the origins of biological diversity. The avian family Falconidae (caracaras, forest-falcons, falcons) has an uneven distribution of species among multiple well-supported clades, and provides a useful system for testing hypotheses about diversification rate and correlation with environmental changes. We analyzed eight independent loci for 1-7 individuals from each of the 64 currently recognized Falconidae species, together with two fossil falconid temporal calibrations, to assess phylogeny, absolute divergence times and potential shifts in diversification rate. Our analyses supported similar diversification ages in the Early to Middle Miocene for the three traditional subfamilies, Herpetotherinae, Polyborinae and Falconinae. We estimated that divergences within the subfamily Falconinae began about 16mya and divergences within the most species-rich genus, Falco, including about 60% of all Falconidae species, began about 7.5mya. We found evidence for a significant increase in diversification rate at the basal phylogenetic node for the genus Falco, and the timing for this rate shift correlates generally with expansion of C4 grasslands beginning around the Miocene/Pliocene transition. Concomitantly, Falco lineages that are distributed primarily in grassland or savannah habitats, as opposed to woodlands, and exhibit migratory, as opposed to sedentary, behavior experienced a higher diversification rate.

Response to Bakker et al.

Robinson and colleagues respond to the points raised about their paper by Bakker et al.

Pliocene diversification within the South American Forest falcons (Falconidae: Micrastur).

The Neotropics are one of the most species rich regions on Earth, with over 3150 species of birds. This unrivaled biodiversity has been attributed to higher proportions of mountain ranges, tropical rain forest or rain fall in the forest than in any other major biogeographic regions. Five primary hypotheses aim to explain processes of diversification within the Neotropics; (1) the Pleistocene refuge hypothesis, (2) the riverine barrier hypothesis, (3) the Miocene marine incursions hypothesis, (4) the ecological gradient hypothesis, and (5) the impact of the last Andean uplift serving as a barrier between eastern and western population Andean populations. We assessed these hypotheses to see which best explained the species richness of the forest-falcons (Micrastur), a poorly known lineage of birds that inhabit lowland and mid-elevation humid forest. Our analyses suggest all speciation events within the genus Micrastur probably occurred in the last 2.5-3.6 myrs, at or before the Pliocene/Pleistocene boundary, with the basal split within the genus being 7 myrs old. Hence our data allow us to formerly reject the classical Pleistocene refuge for Micrastur, Our divergence time estimates are younger that dates for the Miocene marine incursions, the riverine barrier and the Andean uplift hypotheses.

Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.

Due to their small population sizes, threatened and endangered species frequently suffer from a lack of genetic diversity, potentially leading to inbreeding depression and reduced adaptability.1 During the latter half of the twentieth century, North America's largest soaring bird,2 the California condor (Gymnogyps californianus; Critically Endangered3), briefly went extinct in the wild. Though condors once ranged throughout North America, by 1982 only 22 individuals remained. Following decades of captive breeding and release efforts, there are now >300 free-flying wild condors and ∼200 in captivity. The condor's recent near-extinction from lead poisoning, poaching, and loss of habitat is well documented,4 but much about its history remains obscure. To fill this gap and aid future management of the species, we produced a high-quality chromosome-length genome assembly for the California condor and analyzed its genome-wide diversity. For comparison, we also examined the genomes of two close relatives: the Andean condor (Vultur gryphus; Vulnerable3) and the turkey vulture (Cathartes aura; Least Concern3). The genomes of all three species show evidence of historic population declines. Interestingly, the California condor genome retains a high degree of variation, which our analyses reveal is a legacy of its historically high abundance. Correlations between genome-wide diversity and recombination rate further suggest a history of purifying selection against linked deleterious alleles, boding well for future restoration. We show how both long-term evolutionary forces and recent inbreeding have shaped the genome of the California condor, and provide crucial genomic resources to enable future research and conservation.

Population structure and plumage polymorphism: The intraspecific evolutionary relationships of a polymorphic raptor, Buteo jamaicensis harlani.

BACKGROUND: Phenotypic and molecular genetic data often provide conflicting patterns of intraspecific relationships confounding phylogenetic inference, particularly among birds where a variety of environmental factors may influence plumage characters. Among diurnal raptors, the taxonomic relationship of Buteo jamaicensis harlani to other B. jamaicensis subspecies has been long debated because of the polytypic nature of the plumage characteristics used in subspecies or species designations. RESULTS: To address the evolutionary relationships within this group, we used data from 17 nuclear microsatellite loci, 430 base pairs of the mitochondrial control region, and 829 base pairs of the melanocortin 1 receptor (Mc1r) to investigate molecular genetic differentiation among three B. jamaicensis subspecies (B. j. borealis, B. j. calurus, B. j. harlani). Bayesian clustering analyses of nuclear microsatellite loci showed no significant differences between B. j. harlani and B. j. borealis. Differences observed between B. j. harlani and B. j. borealis in mitochondrial and microsatellite data were equivalent to those found between morphologically similar subspecies, B. j. borealis and B. j. calurus, and estimates of migration rates among all three subspecies were high. No consistent differences were observed in Mc1r data between B. j. harlani and other B. jamaicensis subspecies or between light and dark color morphs within B. j. calurus, suggesting that Mc1r does not play a significant role in B. jamaicensis melanism. CONCLUSIONS: These data suggest recent interbreeding and gene flow between B. j. harlani and the other B. jamaicensis subspecies examined, providing no support for the historical designation of B. j. harlani as a distinct species.

Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle.

The critically endangered Madagascar fish-eagle (Haliaeetus vociferoides) is considered to be one of the rarest birds of prey globally and at significant risk of extinction. In the most recent census, only 222 adult individuals were recorded with an estimated total breeding population of no more than 100-120 pairs. Here, levels of Madagascar fish-eagle population genetic diversity based on 47 microsatellite loci were compared with its sister species, the African fish-eagle (Haliaeetus vocifer), and 16 of these loci were also characterized in the white-tailed eagle (Haliaeetus albicilla) and the bald eagle (Haliaeetus leucocephalus). Overall, extremely low genetic diversity was observed in the Madagascar fish-eagle compared to other surveyed Haliaeetus species. Determining whether this low diversity is the result of a recent bottleneck or a more historic event has important implications for their conservation. Using a Bayesian coalescent-based method, we show that Madagascar fish-eagles have maintained a small effective population size for hundreds to thousands of years and that its low level of neutral genetic diversity is not the result of a recent bottleneck. Therefore, efforts made to prevent Madagascar fish-eagle extinction should place high priority on maintenance of habitat requirements and reducing direct and indirect human persecution. Given the current rate of deforestation in Madagascar, we further recommend that the population be expanded to occupy a larger geographical distribution. This will help the population persist when exposed to stochastic factors (e.g. climate and disease) that may threaten a species consisting of only 200 adult individuals while inhabiting a rapidly changing landscape.

Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages.

BACKGROUND: Determining an absolute timescale for avian evolutionary history has proven contentious. The two sources of information available, paleontological data and inference from extant molecular genetic sequences (colloquially, 'rocks' and 'clocks'), have appeared irreconcilable; the fossil record supports a Cenozoic origin for most modern lineages, whereas molecular genetic estimates suggest that these same lineages originated deep within the Cretaceous and survived the K-Pg (Cretaceous-Paleogene; formerly Cretaceous-Tertiary or K-T) mass-extinction event. These two sources of data therefore appear to support fundamentally different models of avian evolution. The paradox has been speculated to reflect deficiencies in the fossil record, unrecognized biases in the treatment of genetic data or both. Here we attempt to explore uncertainty and limit bias entering into molecular divergence time estimates through: (i) improved taxon (n = 135) and character (n = 4594 bp mtDNA) sampling; (ii) inclusion of multiple cladistically tested internal fossil calibration points (n = 18); (iii) correction for lineage-specific rate heterogeneity using a variety of methods (n = 5); (iv) accommodation of uncertainty in tree topology; and (v) testing for possible effects of episodic evolution. RESULTS: The various 'relaxed clock' methods all indicate that the major (basal) lineages of modern birds originated deep within the Cretaceous, although temporal intraordinal diversification patterns differ across methods. We find that topological uncertainty had a systematic but minor influence on date estimates for the origins of major clades, and Bayesian analyses assuming fixed topologies deliver similar results to analyses with unconstrained topologies. We also find that, contrary to expectation, rates of substitution are not autocorrelated across the tree in an ancestor-descendent fashion. Finally, we find no signature of episodic molecular evolution related to either speciation events or the K-Pg boundary that could systematically mislead inferences from genetic data. CONCLUSION: The 'rock-clock' gap has been interpreted by some to be a result of the vagaries of molecular genetic divergence time estimates. However, despite measures to explore different forms of uncertainty in several key parameters, we fail to reconcile molecular genetic divergence time estimates with dates taken from the fossil record; instead, we find strong support for an ancient origin of modern bird lineages, with many extant orders and families arising in the mid-Cretaceous, consistent with previous molecular estimates. Although there is ample room for improvement on both sides of the 'rock-clock' divide (e.g. accounting for 'ghost' lineages in the fossil record and developing more realistic models of rate evolution for molecular genetic sequences), the consistent and conspicuous disagreement between these two sources of data more likely reflects a genuine difference between estimated ages of (i) stem-group origins and (ii) crown-group morphological diversifications, respectively. Further progress on this problem will benefit from greater communication between paleontologists and molecular phylogeneticists in accounting for error in avian lineage age estimates.

Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles.

BACKGROUND: Birds of prey (raptors) are dominant apex predators in terrestrial communities, with hawks (Accipitriformes) and falcons (Falconiformes) hunting by day and owls (Strigiformes) hunting by night. RESULTS: Here, we report new genomes and transcriptomes for 20 species of birds, including 16 species of birds of prey, and high-quality reference genomes for the Eurasian eagle-owl (Bubo bubo), oriental scops owl (Otus sunia), eastern buzzard (Buteo japonicus), and common kestrel (Falco tinnunculus). Our extensive genomic analysis and comparisons with non-raptor genomes identify common molecular signatures that underpin anatomical structure and sensory, muscle, circulatory, and respiratory systems related to a predatory lifestyle. Compared with diurnal birds, owls exhibit striking adaptations to the nocturnal environment, including functional trade-offs in the sensory systems, such as loss of color vision genes and selection for enhancement of nocturnal vision and other sensory systems that are convergent with other nocturnal avian orders. Additionally, we find that a suite of genes associated with vision and circadian rhythm are differentially expressed in blood tissue between nocturnal and diurnal raptors, possibly indicating adaptive expression change during the transition to nocturnality. CONCLUSIONS: Overall, raptor genomes show genomic signatures associated with the origin and maintenance of several specialized physiological and morphological features essential to be apex predators.

Northern Spotted Owl (Strix occidentalis caurina) Genome: Divergence with the Barred Owl (Strix varia) and Characterization of Light-Associated Genes.

We report here the assembly of a northern spotted owl (Strix occidentalis caurina) genome. We generated Illumina paired-end sequence data at 90× coverage using nine libraries with insert lengths ranging from ∼250 to 9,600 nt and read lengths from 100 to 375 nt. The genome assembly is comprised of 8,108 scaffolds totaling 1.26 × 109 nt in length with an N50 length of 3.98 × 106 nt. We calculated the genome-wide fixation index (FST) of S. o. caurina with the closely related barred owl (Strix varia) as 0.819. We examined 19 genes that encode proteins with light-dependent functions in our genome assembly as well as in that of the barn owl (Tyto alba). We present genomic evidence for loss of three of these in S. o. caurina and four in T. alba. We suggest that most light-associated gene functions have been maintained in owls and their loss has not proceeded to the same extent as in other dim-light-adapted vertebrates.

The rise and fall of the CR1 subfamily in the lineage leading to penguins.

The evolution of penguins has been investigated extensively, although inconclusively, by morphologists, biogeographers and molecular phylogeneticists. We investigated this issue using retroposon analysis of insertions of CR1, which is a member of the LINE (long interspersed element) family, in the genomes of penguins and penguin relatives. The retroposon method is a powerful tool for identifying monophyletic groups. Because retroposons often show different relative frequencies of retroposition during evolution, it is first necessary to identify a certain subgroup that was specifically active during the period when the species in question diverged. Hence, we systematically analyzed many CR1 members isolated from penguin and penguin-related genomes. These CR1s are divided into at least three distinct subgroups that share diagnostic nucleotide insertions and/or deletions, namely, penguin CR1 Sph I, Sph II type A and Sph II type B. The analysis of the inserted retroposons by PCR revealed that different CR1 subfamilies or types had amplified at different rates among different periods during penguin evolution. Namely, the penguin CR1 Sph I subfamily had higher rates of retroposition in a common ancestor of all orders examined in this study or at least in a common ancestor of all extant penguins, and the subfamily Sph II type A also had the same tendency. Therefore, these CR1 members can be used to elucidate the phylogenetic relationships of Sphenisciformes (penguins) among different avian orders. In contrast, the penguin CR1 Sph II type B subfamily had higher rates of retroposition just before and after the emergence of the extant genera in Spheniscidae, suggesting that they are useful for elucidating the intra-relationships among extant penguins. This is the first report for the characterization among the members of CR1 family in avian genomes excluding those of chickens. Hence, this work will be a cornerstone for elucidating the phylogenetic relationships in penguin evolution using the retroposon method.

Prioritizing species conservation: does the Cape Verde kite exist?

The Cape Verde kite (Milvus milvus fasciicauda) is considered to be one of the rarest birds of prey in the world and at significant risk of extinction. For this reason there is great interest in both the taxonomic and the population status of this group. To help resolve its taxonomic status, we provide phylogenetic analyses based on three mitochondrial genes for a sampling of kites in the genus Milvus, including a broad geographical sampling of black kites (Milvus migrans), red kites (Milvus milvus), Cape Verde kite museum specimens collected between 1897 and 1924, and five kites trapped on the Cape Verde Islands during August 2002. We found that the historical Cape Verde kites, including the type specimen, were non-monophyletic and scattered within a larger red kite clade. The recently trapped kites from the Cape Verde Islands were all phylogenetically diagnosed as black kites. Our findings suggest that the traditional Cape Verde kite is not a distinctive evolutionary unit, and the case for species status, as recently suggested by others, is not supported. We do find support for recognition of at least one clade of yellow-billed kites, traditionally considered as a black kite subspecies, as a distinctive phylogenetic species.

Isolation of a Complete Circular Virus Genome Sequence from an Alaskan Black-Capped Chickadee (Poecile atricapillus) Gastrointestinal Tract Sample.

We report here the genome sequence of a circular virus isolated from samples of an Alaskan black-capped chickadee (Poecile atricapillus) gastrointestinal tract. The genome is 2,152 bp in length and is most similar (30 to 44.5% amino acid identity) to the genome sequences of other single-stranded DNA (ssDNA) circular viruses belonging to the gemycircularvirus group.

Response to Comment on "Whole-genome analyses resolve early branches in the tree of life of modern birds".

Mitchell et al. argue that divergence-time estimates for our avian phylogeny were too young because of an "inappropriate" maximum age constraint for the most recent common ancestor of modern birds and that, as a result, most modern bird orders diverged before the Cretaceous-Paleogene mass extinction event 66 million years ago instead of after. However, their interpretations of the fossil record and timetrees are incorrect.

Phylogenomic analyses data of the avian phylogenomics project.

BACKGROUND: Determining the evolutionary relationships among the major lineages of extant birds has been one of the biggest challenges in systematic biology. To address this challenge, we assembled or collected the genomes of 48 avian species spanning most orders of birds, including all Neognathae and two of the five Palaeognathae orders. We used these genomes to construct a genome-scale avian phylogenetic tree and perform comparative genomic analyses. FINDINGS: Here we present the datasets associated with the phylogenomic analyses, which include sequence alignment files consisting of nucleotides, amino acids, indels, and transposable elements, as well as tree files containing gene trees and species trees. Inferring an accurate phylogeny required generating: 1) A well annotated data set across species based on genome synteny; 2) Alignments with unaligned or incorrectly overaligned sequences filtered out; and 3) Diverse data sets, including genes and their inferred trees, indels, and transposable elements. Our total evidence nucleotide tree (TENT) data set (consisting of exons, introns, and UCEs) gave what we consider our most reliable species tree when using the concatenation-based ExaML algorithm or when using statistical binning with the coalescence-based MP-EST algorithm (which we refer to as MP-EST*). Other data sets, such as the coding sequence of some exons, revealed other properties of genome evolution, namely convergence. CONCLUSIONS: The Avian Phylogenomics Project is the largest vertebrate phylogenomics project to date that we are aware of. The sequence, alignment, and tree data are expected to accelerate analyses in phylogenomics and other related areas.

SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of host-shifting.

The sudden appearance and potential lethality of severe acute respiratory syndrome associated coronavirus (SARS-CoV) in humans has focused attention on understanding its origins. Here, we assess phylogenetic relationships for the SARS-CoV lineage as well as the history of host-species shifts for SARS-CoV and other coronaviruses. We used a Bayesian phylogenetic inference approach with sliding window analyses of three SARS-CoV proteins: RNA dependent RNA polymerase (RDRP), nucleocapsid (N) and spike (S). Conservation of RDRP allowed us to use a set of Arteriviridae taxa to root the Coronaviridae phylogeny. We found strong evidence for a recombination breakpoint within SARS-CoV RDRP, based on different, well supported trees for a 5' fragment (supporting SARS-CoV as sister to a clade including all other coronaviruses) and a 3' fragment (supporting SARS-CoV as sister to group three avian coronaviruses). These different topologies are statistically significant: the optimal 5' tree could be rejected for the 3' region, and the optimal 3' tree could be rejected for the 5' region. We did not find statistical evidence for recombination in analyses of N and S, as there is little signal to differentiate among alternative trees. Comparison of phylogenetic trees for 11 known host-species and 36 coronaviruses, representing coronavirus groups 1-3 and SARS-CoV, based on N showed statistical incongruence indicating multiple host-species shifts for coronaviruses. Inference of host-species associations is highly sensitive to sampling and must be considered cautiously. However, current sampling suggests host-species shifts between mouse and rat, chicken and turkey, mammals and manx shearwater, and humans and other mammals. The sister relationship between avian coronaviruses and the 3' RDRP fragment of SARS-CoV suggests an additional host-species shift. Demonstration of recombination in the SARS-CoV lineage indicates its potential for rapid unpredictable change, a potentially important challenge for public health management and for drug and vaccine development.

Speciational Evolution: a Phylogenetic Test With Allozymes in Sceloporus (Reptilia).

Abstract- The potential role of speciation in accelerating evolutionary divergence remains controversial. Earlier tests based on genetic and morphologic distances which indicated an absence of speciational evolution rely on problematic assumptions. We provide a phylogenetic test in which amounts of discrete character change relative to an outgroup are compared between sister taxa. Although this test is constrained by a need to assume similar extinction rates in groups compared, it provides conceptual improvements regarding monophyly, equal age of taxa, and distribution of homoplasy. Based on analysis of 68 informative allozyme characters for 19 lizard species in the genus Sceloporus, significant speciational evolution and punctuational change is, at least, a viable explanation for the distribution of observed character changes.