Differential proliferation regulates multi-tissue morphogenesis during embryonic axial extension: integrating viscous modeling and experimental approaches.

A major challenge in biology is to understand how mechanical interactions and cellular behavior affect the shapes of tissues and embryo morphology. The extension of the neural tube and paraxial mesoderm, which form the spinal cord and musculoskeletal system, respectively, results in the elongated shape of the vertebrate embryonic body. Despite our understanding of how each of these tissues elongates independently of the others, the morphogenetic consequences of their simultaneous growth and mechanical interactions are still unclear. Our study investigates how differential growth, tissue biophysical properties and mechanical interactions affect embryonic morphogenesis during axial extension using a 2D multi-tissue continuum-based mathematical model. Our model captures the dynamics observed in vivo by time-lapse imaging of bird embryos, and reveals the underestimated influence of differential tissue proliferation rates. We confirmed this prediction in quail embryos by showing that decreasing the rate of cell proliferation in the paraxial mesoderm affects long-term tissue dynamics, and shaping of both the paraxial mesoderm and the neighboring neural tube. Overall, our work provides a new theoretical platform upon which to consider the long-term consequences of tissue differential growth and mechanical interactions on morphogenesis.

Persistent species relationships characterize migrating bird communities across stopover sites and seasons.

Global migrations of diverse animal species often converge along the same routes, bringing together seasonal assemblages of animals that may compete, prey on each other, and share information or pathogens. These interspecific interactions, when energetic demands are high and the time to complete journeys is short, may influence survival, migratory success, stopover ecology, and migratory routes. Numerous accounts suggest that interspecific co-migrations are globally distributed in aerial, aquatic, and terrestrial systems, although the study of migration to date has rarely investigated species interactions among migrating animals. Here, we test the hypothesis that migrating animals are communities engaged in networks of ecological interactions. We leverage over half a million records of 50 bird species from five bird banding sites collected over 8 to 23 y to test for species associations using social network analyses. We find strong support for persistent species relationships across sites and between spring and fall migration. These relationships may be ecologically meaningful: They are often stronger among phylogenetically related species with similar foraging behaviors and nonbreeding ranges even after accounting for the nonsocial contributions to associations, including overlap in migration timing and habitat use. While interspecific interactions could result in costly competition or beneficial information exchange, we find that relationships are largely positive, suggesting limited competitive exclusion at the scale of a banding station during migratory stopovers. Our findings support an understanding of animal migrations that consist of networked communities rather than random assemblages of independently migrating species, encouraging future studies of the nature and consequences of co-migrant interactions.

Nationwide law enforcement impact on the pet bird trade in China.

Conservation enforcement is a direct strategy to combat illegal wildlife trade in open markets. Yet, its large-scale effectiveness has not been widely assessed due to the lack of extensive market data. Between August 2016 and June 2017, a national coordinated enforcement campaign led by the leading Chinese authority to combat illegal migratory bird trade coincided with the largest-ever pet bird market survey across China by voluntary birdwatchers before and after the enforcement, which served as a unique natural experiment. Across 73 markets from 22 Chinese provinces, the dataset contains 140,723 birds of 346 species from 48 families and recorded a drastic decline in bird abundance traded after enforcement. Notably, species protected under China's Wildlife Protection Law declined significantly, while commercially bred species increased, although responses to enforcement were spatially heterogeneous. Our model showed that the national protection level was the best predictor for the trend of traded species, even after accounting for confounding factors such as regional baseline enforcement pressure and wild native bird populations. However, the widely traded native songbirds were not offered adequate national protection. Future policies should consider the pet bird trade patterns, target key areas of trade, and develop a more systematic market survey design to monitor trade.

Genomes, fossils, and the concurrent rise of modern birds and flowering plants in the Late Cretaceous.

The phylogeny and divergence timing of the Neoavian radiation remain controversial despite recent progress. We analyzed the genomes of 124 species across all Neoavian orders, using data from 25,460 loci spanning four DNA classes, including 5,756 coding sequences, 12,449 conserved nonexonic elements, 4,871 introns, and 2,384 intergenic segments. We conducted a comprehensive sensitivity analysis to account for the heterogeneity across different DNA classes, leading to an optimal tree of Neoaves with high resolution. This phylogeny features a novel Neoavian dichotomy comprising two monophyletic clades: a previously recognized Telluraves (land birds) and a newly circumscribed Aquaterraves (waterbirds and relatives). Molecular dating analyses with 20 fossil calibrations indicate that the diversification of modern birds began in the Late Cretaceous and underwent a constant and steady radiation across the KPg boundary, concurrent with the rise of angiosperms as well as other major Cenozoic animal groups including placental and multituberculate mammals. The KPg catastrophe had a limited impact on avian evolution compared to the Paleocene-Eocene Thermal Maximum, which triggered a rapid diversification of seabirds. Our findings suggest that the evolution of modern birds followed a slow process of gradualism rather than a rapid process of punctuated equilibrium, with limited interruption by the KPg catastrophe. This study places bird evolution into a new context within vertebrates, with ramifications for the evolution of the Earth's biota.

How exceptional are the classic adaptive radiations of passerine birds?

We investigated whether celebrated cases of evolutionary radiations of passerine birds on islands have produced exceptional morphological diversity relative to comparable-aged radiations globally. Based on eight external measurements, we calculated the disparity in size and shape within clades, each of which was classified as being tropical or temperate and as having diversified in a continental or an island/archipelagic setting. We found that the distribution of disparity among all clades does not differ substantively from a normal distribution, which would be consistent with a common underlying process of morphological diversification that is largely independent of latitude and occurrence on islands. Disparity is slightly greater in island clades than in those from continents or clades consisting of island and noninsular taxa, revealing a small, but significant, effect of island occurrence on evolutionary divergence. Nonetheless, the number of highly disparate clades overall is no greater than expected from a normal distribution, calling into question the need to invoke key innovations, ecological opportunity, or other factors as stimuli for adaptive radiations in passerine birds.

Autumn stopover hotspots and multiscale habitat associations of migratory landbirds in the eastern United States.

Halting the global decline of migratory birds requires a better understanding of migration ecology. Stopover sites are a crucial yet understudied aspect of bird conservation, mostly due to challenges associated with understanding broad-scale patterns of transient habitat use. Here, we use a national network of weather radar stations to identify stopover hotspots and assess multiscale habitat associations of migratory landbirds across the eastern United States during autumn migration. We mapped seasonal bird densities over 5 y (2015 to 2019) from 60 radar stations covering 63.2 million hectares. At a coarse scale, we found that landbirds migrate across a broad front with small differences in migrant density between radar domains. However, relatively more birds concentrate along the Mississippi River and Appalachian Mountains. At a finer scale, we identified radar pixels that consistently harbored high densities of migrants for all 5 y, which we classify as stopover hotspots. Hotspot probability increased with percent cover of all forest types and decreased with percent cover of pasture and cultivated crops. Moreover, we found strong concentrating effects of deciduous forest patches within deforested regions. We also found that the prairie biome in the Midwest (now mostly cropland) is likely a migration barrier, with large concentrations of migrants at the prairie-forest boundary after crossing the agricultural Midwest. Overall, the broad-front migration pattern highlights the importance of locally based conservation efforts to protect stopover habitats. Such efforts should target forests, especially deciduous forests in highly altered landscapes. These findings demonstrate the value of multiscale habitat assessments for the conservation of migratory landbirds.

Diversified farms bolster forest-bird populations despite ongoing declines in tropical forests.

While some agricultural landscapes can support wildlife in the short term, it is uncertain how well they can truly sustain wildlife populations. To compare population trends in different production systems, we sampled birds along 48 transects in mature forests, diversified farms, and intensive farms across Costa Rica from 2000 to 2017. To assess how land use influenced population trends in the 349 resident and 80 migratory species with sufficient data, we developed population models. We found, first, that 23% of species were stable in all three land use types, with the rest almost evenly split between increasing and decreasing populations. Second, in forest habitats, a slightly higher fraction was declining: 62% of the 164 species undergoing long-term population changes; nearly half of these declines occurred in forest-affiliated invertivores. Third, in diversified farms, 49% of the 230 species with population changes were declining, with 60% of these declines occurring in agriculture-affiliated species. In contrast, 51% of the species with population changes on diversified farms showed increases, primarily in forest-affiliated invertivores and frugivores. In intensive farms, 153 species showed population changes, also with similar proportions of species increasing (50%) and decreasing (50%). Declines were concentrated in agriculture-affiliated invertivores and forest-affiliated frugivores; increases occurred in many large, omnivorous species. Our findings paint a complex picture but clearly indicate that diversified farming helps sustain populations of diverse, forest-affiliated species. Despite not fully offsetting losses in forest habitats, diversified farming practices help sustain wildlife in a critical time, before possible transformation to nature-positive policies and practices.

Space weather disrupts nocturnal bird migration.

Space weather, including solar storms, can impact Earth by disturbing the geomagnetic field. Despite the known dependence of birds and other animals on geomagnetic cues for successful seasonal migrations, the potential effects of space weather on organisms that use Earth's magnetic field for navigation have received little study. We tested whether space weather geomagnetic disturbances are associated with disruptions to bird migration at a macroecological scale. We leveraged long-term radar data to characterize the nightly migration dynamics of the nocturnally migrating North American avifauna over 22 y. We then used concurrent magnetometer data to develop a local magnetic disturbance index associated with each radar station (ΔBmax), facilitating spatiotemporally explicit analyses of the relationship between migration and geomagnetic disturbance. After controlling for effects of atmospheric weather and spatiotemporal patterns, we found a 9 to 17% decrease in migration intensity in both spring and fall during severe space weather events. During fall migration, we also found evidence for decreases in effort flying against the wind, which may represent a depression of active navigation such that birds drift more with the wind during geomagnetic disturbances. Effort flying against the wind in the fall was most reduced under both overcast conditions and high geomagnetic disturbance, suggesting that a combination of obscured celestial cues and magnetic disturbance may disrupt navigation. Collectively, our results provide evidence for community-wide avifaunal responses to geomagnetic disturbances driven by space weather during nocturnal migration.

Upper bound for broadband radiofrequency field disruption of magnetic compass orientation in night-migratory songbirds.

Night-migratory songbirds have a light-dependent magnetic compass sense, the mechanism of which is thought to depend on the photochemical formation of radical pairs in cryptochrome (Cry) proteins located in the retina. The finding that weak radiofrequency (RF) electromagnetic fields can prevent birds from orienting in the Earth's magnetic field has been regarded as a diagnostic test for this mechanism and as a potential source of information on the identities of the radicals. The maximum frequency that could cause such disorientation has been predicted to lie between 120 and 220 MHz for a flavin-tryptophan radical pair in Cry. Here we show that the magnetic orientation capabilities of Eurasian blackcaps (Sylvia atricapilla) are not affected by RF noise in the frequency bands 140 to 150 MHz and 235 to 245 MHz. From a consideration of its internal magnetic interactions, we argue that RF field effects on a flavin-containing radical-pair sensor should be approximately independent of frequency up to 116 MHz and that birds' sensitivity to RF disorientation should fall by about two orders of magnitude when the frequency exceeds 116 MHz. Taken together with our earlier finding that 75 to 85 MHz RF fields disrupt the magnetic orientation of blackcaps, these results provide compelling evidence that the magnetic compass of migratory birds operates by a radical pair mechanism.

Farmland practices are driving bird population decline across Europe.

Declines in European bird populations are reported for decades but the direct effect of major anthropogenic pressures on such declines remains unquantified. Causal relationships between pressures and bird population responses are difficult to identify as pressures interact at different spatial scales and responses vary among species. Here, we uncover direct relationships between population time-series of 170 common bird species, monitored at more than 20,000 sites in 28 European countries, over 37 y, and four widespread anthropogenic pressures: agricultural intensification, change in forest cover, urbanisation and temperature change over the last decades. We quantify the influence of each pressure on population time-series and its importance relative to other pressures, and we identify traits of most affected species. We find that agricultural intensification, in particular pesticides and fertiliser use, is the main pressure for most bird population declines, especially for invertebrate feeders. Responses to changes in forest cover, urbanisation and temperature are more species-specific. Specifically, forest cover is associated with a positive effect and growing urbanisation with a negative effect on population dynamics, while temperature change has an effect on the dynamics of a large number of bird populations, the magnitude and direction of which depend on species' thermal preferences. Our results not only confirm the pervasive and strong effects of anthropogenic pressures on common breeding birds, but quantify the relative strength of these effects stressing the urgent need for transformative changes in the way of inhabiting the world in European countries, if bird populations shall have a chance of recovering.

Bayesian phylodynamics reveals the transmission dynamics of avian influenza A(H7N9) virus at the human-live bird market interface in China.

In 2013 to 2017, avian influenza A(H7N9) virus has caused five severe epidemic waves of human infections in China. The role of live bird markets (LBMs) in the transmission dynamics of H7N9 remains unclear. Using a Bayesian phylodynamic approach, we shed light on past H7N9 transmission events at the human-LBM interface that were not directly observed using case surveillance data-based approaches. Our results reveal concurrent circulation of H7N9 lineages in Yangtze and Pearl River Delta regions, with evidence of local transmission during each wave. Our results indicate that H7N9 circulated in humans and LBMs for weeks to months before being first detected. Our findings support the seasonality of H7N9 transmission and suggest a high number of underreported infections, particularly in LBMs. We provide evidence for differences in virus transmissibility between low and highly pathogenic H7N9. We demonstrate a regional spatial structure for the spread of H7N9 among LBMs, highlighting the importance of further investigating the role of local live poultry trade in virus transmission. Our results provide estimates of avian influenza virus (AIV) transmission at the LBM level, providing a unique opportunity to better prepare surveillance plans at LBMs for response to future AIV epidemics.

Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod.

The dinosaur-bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as Troodon, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we applied dual clumped isotope (Δ47 and Δ48) thermometry, a technique that resolves mineralization temperature and other nonthermal information recorded in carbonates, to eggshells from Troodon, modern reptiles, and modern birds. Troodon eggshells show variable temperatures, namely 42 and 29 ± 2 °C, supporting the hypothesis of an endothermic thermophysiology with a heterothermic strategy for this extinct taxon. Dual clumped isotope data also reveal physiological differences in the reproductive systems between Troodon, reptiles, and birds. Troodon and modern reptiles mineralize their eggshells indistinguishable from dual clumped isotope equilibrium, while birds precipitate eggshells characterized by a positive disequilibrium offset in Δ48. Analyses of inorganic calcites suggest that the observed disequilibrium pattern in birds is linked to an amorphous calcium carbonate (ACC) precursor, a carbonate phase known to accelerate eggshell formation in birds. Lack of disequilibrium patterns in reptile and Troodon eggshells implies these vertebrates had not acquired the fast, ACC-based eggshell calcification process characteristic of birds. Observation that Troodon retained a slow reptile-like calcification suggests that it possessed two functional ovaries and was limited in the number of eggs it could produce; thus its large clutches would have been laid by several females. Dual clumped isotope analysis of eggshells of extinct vertebrates sheds light on physiological information otherwise inaccessible in the fossil record.

Spatiotemporal genotype replacement of H5N8 avian influenza viruses contributed to H5N1 emergence in 2021/2022 panzootic.

Since 2020, clade 2.3.4.4b highly pathogenic avian influenza H5N8 and H5N1 viruses have swept through continents, posing serious threats to the world. Through comprehensive analyses of epidemiological, genetic, and bird migration data, we found that the dominant genotype replacement of the H5N8 viruses in 2020 contributed to the H5N1 outbreak in the 2021/2022 wave. The 2020 outbreak of the H5N8 G1 genotype instead of the G0 genotype produced reassortment opportunities and led to the emergence of a new H5N1 virus with G1's HA and MP genes. Despite extensive reassortments in the 2021/2022 wave, the H5N1 virus retained the HA and MP genes, causing a significant outbreak in Europe and North America. Furtherly, through the wild bird migration flyways investigation, we found that the temporal-spatial coincidence between the outbreak of the H5N8 G1 virus and the bird autumn migration may have expanded the H5 viral spread, which may be one of the main drivers of the emergence of the 2020-2022 H5 panzootic.IMPORTANCESince 2020, highly pathogenic avian influenza (HPAI) H5 subtype variants of clade 2.3.4.4b have spread across continents, posing unprecedented threats globally. However, the factors promoting the genesis and spread of H5 HPAI viruses remain unclear. Here, we found that the spatiotemporal genotype replacement of H5N8 HPAI viruses contributed to the emergence of the H5N1 variant that caused the 2021/2022 panzootic, and the viral evolution in poultry of Egypt and surrounding area and autumn bird migration from the Russia-Kazakhstan region to Europe are important drivers of the emergence of the 2020-2022 H5 panzootic. These findings provide important targets for early warning and could help control the current and future HPAI epidemics.

"Smart markets": harnessing the potential of new technologies for endemic and emerging infectious disease surveillance in traditional food markets.

Emerging and endemic zoonotic diseases continue to threaten human and animal health, our social fabric, and the global economy. Zoonoses frequently emerge from congregate interfaces where multiple animal species and humans coexist, including farms and markets. Traditional food markets are widespread across the globe and create an interface where domestic and wild animals interact among themselves and with humans, increasing the risk of pathogen spillover. Despite decades of evidence linking markets to disease outbreaks across the world, there remains a striking lack of pathogen surveillance programs that can relay timely, cost-effective, and actionable information to decision-makers to protect human and animal health. However, the strategic incorporation of environmental surveillance systems in markets coupled with novel pathogen detection strategies can create an early warning system capable of alerting us to the risk of outbreaks before they happen. Here, we explore the concept of "smart" markets that utilize continuous surveillance systems to monitor the emergence of zoonotic pathogens with spillover potential.IMPORTANCEFast detection and rapid intervention are crucial to mitigate risks of pathogen emergence, spillover and spread-every second counts. However, comprehensive, active, longitudinal surveillance systems at high-risk interfaces that provide real-time data for action remain lacking. This paper proposes "smart market" systems harnessing cutting-edge tools and a range of sampling techniques, including wastewater and air collection, multiplex assays, and metagenomic sequencing. Coupled with robust response pathways, these systems could better enable Early Warning and bolster prevention efforts.

Passive immunotherapies for the next influenza pandemic.

Influenzavirus is among the most relevant candidates for a next pandemic. We review here the phylogeny of former influenza pandemics, and discuss candidate lineages. After briefly reviewing the other existing antiviral options, we discuss in detail the evidences supporting the efficacy of passive immunotherapies against influenzavirus, with a focus on convalescent plasma.

Molecular parallelism in signaling function across different sexually selected ornaments in a warbler.

Extravagant ornaments are thought to signal male quality to females choosing mates, but the evidence linking ornament size to male quality is controversial, particularly in cases in which females prefer different ornaments in different populations. Here, we use whole-genome sequencing and transcriptomics to determine the genetic basis of ornament size in two populations of a widespread warbler, the common yellowthroat (Geothlypis trichas). Within a single subspecies, females in a Wisconsin population prefer males with larger black masks as mates, while females in a New York population prefer males with larger yellow bibs. Despite being produced by different pigments in different patches on the body, the size of the ornament preferred by females in each population was linked to numerous genes that function in many of the same core aspects of male quality (e.g., immunity and oxidative balance). These relationships confirm recent hypotheses linking the signaling function of ornaments to male quality. Furthermore, the parallelism in signaling function provides the flexibility for different types of ornaments to be used as signals of similar aspects of male quality. This could facilitate switches in female preference for different ornaments, a potentially important step in the early stages of divergence among populations.

Increased neuron density in the midbrain of a foveate bird, pigeon, results from profound change in tissue morphogenesis.

The increase of brain neuron number in relation with brain size is currently considered to be the major evolutionary path to high cognitive power in amniotes. However, how changes in neuron density did contribute to the evolution of the information-processing capacity of the brain remains unanswered. High neuron densities are seen as the main reason why the fovea located at the visual center of the retina is responsible for sharp vision in birds and primates. The emergence of foveal vision is considered as a breakthrough innovation in visual system evolution. We found that neuron densities in the largest visual center of the midbrain - i.e., the optic tectum - are two to four times higher in modern birds with one or two foveae compared to birds deprived of this specialty. Interspecies comparisons enabled us to identify elements of a hitherto unknown developmental process set up by foveate birds for increasing neuron density in the upper layers of their optic tectum. The late progenitor cells that generate these neurons proliferate in a ventricular zone that can expand only radially. In this particular context, the number of cells in ontogenetic columns increases, thereby setting the conditions for higher cell densities in the upper layers once neurons did migrate.

Tree diversity enhances predation by birds but not by arthropods across climate gradients.

Tree diversity can promote both predator abundance and diversity. However, whether this translates into increased predation and top-down control of herbivores across predator taxonomic groups and contrasting environmental conditions remains unresolved. We used a global network of tree diversity experiments (TreeDivNet) spread across three continents and three biomes to test the effects of tree species richness on predation across varying climatic conditions of temperature and precipitation. We recorded bird and arthropod predation attempts on plasticine caterpillars in monocultures and tree species mixtures. Both tree species richness and temperature increased predation by birds but not by arthropods. Furthermore, the effects of tree species richness on predation were consistent across the studied climatic gradient. Our findings provide evidence that tree diversity strengthens top-down control of insect herbivores by birds, underscoring the need to implement conservation strategies that safeguard tree diversity to sustain ecosystem services provided by natural enemies in forests.

Functional reorganization of North American wintering avifauna.

Wintering birds serve as vital climate sentinels, yet they are often overlooked in studies of avian diversity change. Here, we provide a continental-scale characterization of change in multifaceted wintering avifauna and examine the effects of climate change on these dynamics. We reveal a strong functional reorganization of wintering bird communities marked by a north-south gradient in functional diversity change, along with a superimposed mild east-west gradient in trait composition change. Assemblages in the northern United States saw contractions of the functional space and increases in functional evenness and originality, while the southern United States saw smaller contractions of the functional space and stasis in evenness and originality. Shifts in functional diversity were underlined by significant reshuffling in trait composition, particularly pronounced in the western and northern United States. Finally, we find strong contributions of climate change to this functional reorganization, underscoring the importance of wintering birds in tracking climate change impacts on biodiversity.

Evolution and Spread of Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus in Wild Birds, South Korea, 2022-2023.

During October 2022-March 2023, highly pathogenic avian influenza (HPAI) A(H5N1) clade 2.3.4.4b virus caused outbreaks in South Korea, including 174 cases in wild birds. To understand the origin and role of wild birds in the evolution and spread of HPAI viruses, we sequenced 113 HPAI isolates from wild birds and performed phylogenetic analysis. We identified 16 different genotypes, indicating extensive genetic reassortment with viruses in wild birds. Phylodynamic analysis showed that the viruses were most likely introduced to the southern Gyeonggi-do/northern Chungcheongnam-do area through whooper swans (Cygnus cygnus) and spread southward. Cross-species transmission occurred between various wild bird species, including waterfowl and raptors, resulting in the persistence of HPAI in wild bird populations and further geographic spread as these birds migrated throughout South Korea. Enhanced genomic surveillance was an integral part of the HPAI outbreak response, aiding in timely understanding of the origin, evolution, and spread of the virus.