The Evolutionary Dynamics of Influenza A Viruses Circulating in Mallards in Duck Hunting Preserves in Maryland, USA

Duck hunting preserves (DHP) have resident populations of farm-raised mallard ducks, which create potential foci for the evolution of novel influenza A viruses (IAVs). Through an eleven-year (2003–2013) IAV surveillance project in seven DHPs in Maryland, USA, we frequently identified IAVs in the resident, free-flying mallard ducks (5.8% of cloacal samples were IAV-positive). The IAV population had high genetic diversity, including 12 HA subtypes and 9 NA subtypes. By sequencing the complete genomes of 290 viruses, we determined that genetically diverse IAVs were introduced annually into DHP ducks, predominantly from wild birds in the Anatidae family that inhabit the Atlantic and Mississippi flyways. The relatively low viral gene flow observed out of DHPs suggests that raised mallards do not sustain long-term viral persistence nor do they serve as important sources of new viruses in wild birds. Overall, our findings indicate that DHPs offer reliable samples of the diversity of IAV subtypes, and could serve as regional sentinel sites that mimic the viral diversity found in local wild duck populations, which would provide a cost-efficient strategy for long-term IAV monitoring. Such monitoring could allow for early identification and characterization of viruses that threaten bird species of high economic and environmental interest.

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Reassortment and persistence of influenza A viruses from diverse geographic origins within Australian wild birds: evidence from a small, isolated population of Ruddy turnstones

Journal of Virology ◽

10.1128/jvi.02193-20 ◽

2021 ◽

Author(s):

Bethany J. Hoye ◽

Celeste M. Donato ◽

Simeon Lisovski ◽

Yi-Mo Deng ◽

Simone Warner ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Birds ◽

Influenza Viruses ◽

Low Density ◽

Isolated Population ◽

Influenza A Viruses ◽

Geographic Origins ◽

Eastern Australia

Australian lineages of avian influenza A viruses (AIVs) are thought to be phylogenetically distinct from those circulating in Eurasia and the Americas, suggesting the circulation of endemic viruses seeded by occasional introductions from other regions. However, processes underlying the introduction, evolution and maintenance of AIVs in Australia remain poorly understood. Waders (Order Charadriiformes, Family Scolopacidae) may play a unique role in the ecology and evolution of AIVs, particularly in Australia, where ducks, geese and swans (Order Anseriformes, Family Anatidae) rarely undertake intercontinental migrations. Across a five-year surveillance period (2011–2015), Ruddy turnstones (Arenaria interpres) that ‘overwinter’ during the Austral summer in south eastern Australia showed generally low levels of AIV prevalence (0–2%). However, in March 2014 we detected AIVs in 32% (95% CI; 25–39%) of individuals in a small, low-density, island population 90km from the Australian mainland. This epizootic comprised three distinct AIV genotypes, each of which represent a unique reassortment of Australian, recently introduced Eurasian, and recently introduced American-lineage gene segments. Strikingly, the Australian-lineage gene segments showed high similarity to H10N7 viruses isolated in 2010 and 2012 from poultry outbreaks 900–1500km to the north. Together with the diverse geographic origins of the American and Eurasian gene segments, these findings suggest extensive circulation and reassortment of AIVs within Australian wild birds over vast geographic distances. Our findings indicate that long-term surveillance in waders may yield unique insights into AIV gene flow, especially in geographic regions like Oceania where Anatidae do not display regular inter- or intracontinental migration. IMPORTANCE High prevalence of avian influenza viruses (AIVs) was detected in a small, low-density, isolated population of Ruddy turnstones in Australia. Analysis of these viruses revealed relatively recent introductions of viral gene segments from both Eurasia and North America, as well as long-term persistence of introduced gene segments in Australian wild birds. These data demonstrate that the flow of viruses into Australia may be more common than initially thought and that, once introduced, these AIVs have the potential to be maintained within the continent. These findings add to a growing body of evidence suggesting Australian wild birds are unlikely to be ecologically-isolated from the highly pathogenic H5Nx viruses circulating among wild birds throughout the northern hemisphere.

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Characterization of Subtype H6 Avian Influenza A Viruses Isolated From Wild Birds in Poyang Lake, China

Frontiers in Veterinary Science ◽

10.3389/fvets.2021.685399 ◽

2021 ◽

Vol 8 ◽

Author(s):

Zhimin Wan ◽

Qiuqi Kan ◽

Zhehong Zhao ◽

Hongxia Shao ◽

Thomas J. Deliberto ◽

...

Keyword(s):

Genetic Diversity ◽

Avian Influenza ◽

Mammalian Cells ◽

Influenza A ◽

Poyang Lake ◽

Wild Birds ◽

Mouse Lung ◽

Influenza A Viruses ◽

Domestic Poultry ◽

History Of

Subtype H6 avian influenza A viruses (IAVs) are enzootic and genetically diverse in both domestic poultry and wild waterfowl and may cause spillovers in both pigs and humans. Thus, it is important to understand the genetic diversity of H6 IAVs in birds and their zoonotic potential. Compared with that in domestic poultry, the genetic diversity of H6 viruses in wild birds in China has not been well-understood. In this study, five H6 viruses were isolated from wild birds in Poyang Lake, China, and genetic analyses showed that these isolates are clustered into four genotypes associated with reassortments among avian IAVs from domestic poultry and wild birds in China and those from Eurasia and North America and that these viruses exhibited distinct phenotypes in growth kinetics analyses with avian and mammalian cells lines and in mouse challenge experiments. Of interest is that two H6 isolates from the Eurasian teal replicated effectively in the mouse lung without prior adaptation, whereas the other three did not. Our study suggested that there are variations in the mammalian viral replication efficiency phenotypic among genetically diverse H6 IAVs in wild birds and that both intra- and inter-continental movements of IAVs through wild bird migration may facilitate the emergence of novel H6 IAV reassortants with the potential for replicating in mammals, including humans. Continued surveillance to monitor the diversity of H6 IAVs in wild birds is necessary to increase our understanding of the natural history of IAVs.

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Pathogens from Wild Birds at the Wildlife–Agriculture Interface

10.1093/oso/9780198746249.003.0011 ◽

2021 ◽

pp. 207-228

Author(s):

Alan B. Franklin ◽

Sarah N. Bevins ◽

Susan A. Shriner

Keyword(s):

Disease Ecology ◽

Influenza A ◽

Wild Birds ◽

Avian Species ◽

Influenza A Viruses ◽

Agricultural Health ◽

Bird Populations ◽

Food Borne ◽

Global Movement ◽

Agricultural Operations

Birds are known to carry pathogens affecting human and agricultural health. Conversely, agricultural operations can serve as sources of pathogens that affect wild bird populations. This chapter provides guidelines to identify focal avian species that frequently use agricultural operations. These guidelines are coupled with identifying host types, such as maintenance and bridge hosts, and potential direct and indirect pathways for pathogen contamination from wild birds to agricultural operations, including patterns of spillover and spillback. The chapter also identifies major bacterial and viral pathogens of concern that are prevalent in birds and that affect human and agricultural health. These pathogens are then used to illustrate disease ecology concepts important at the wildlife–agriculture interface. These microorganisms include food-borne bacteria, influenza A viruses, and Newcastle disease virus. The chapter introduces the concept of contamination potential for categorizing avian species in terms of the risk they pose to contamination of agricultural operations with pathogens of concern. Finally, the chapter examines long-distance movements of wild birds in relation to pathogen introduction and illustrates this with global movement of influenza A viruses by wild birds.

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Non-Uniform and Non-Random Binding of Nucleoprotein to Influenza A and B Viral RNA

Viruses ◽

10.3390/v10100522 ◽

2018 ◽

Vol 10 (10) ◽

pp. 522 ◽

Cited By ~ 10

Author(s):

Valerie Le Sage ◽

Adalena Nanni ◽

Amar Bhagwat ◽

Dan Snyder ◽

Vaughn Cooper ◽

...

Keyword(s):

Influenza A ◽

Gene Segment ◽

Influenza Viruses ◽

Viral Rna ◽

Influenza B Virus ◽

Viral Gene ◽

Influenza B ◽

Influenza A Viruses ◽

Binding Profile ◽

Random Manner

The genomes of influenza A and B viruses have eight, single-stranded RNA segments that exist in the form of a viral ribonucleoprotein complex in association with nucleoprotein (NP) and an RNA-dependent RNA polymerase complex. We previously used high-throughput RNA sequencing coupled with crosslinking immunoprecipitation (HITS-CLIP) to examine where NP binds to the viral RNA (vRNA) and demonstrated for two H1N1 strains that NP binds vRNA in a non-uniform, non-random manner. In this study, we expand on those initial observations and describe the NP-vRNA binding profile for a seasonal H3N2 and influenza B virus. We show that, similar to H1N1 strains, NP binds vRNA in a non-uniform and non-random manner. Each viral gene segment has a unique NP binding profile with areas that are enriched for NP association as well as free of NP-binding. Interestingly, NP-vRNA binding profiles have some conservation between influenza A viruses, H1N1 and H3N2, but no correlation was observed between influenza A and B viruses. Our study demonstrates the conserved nature of non-uniform NP binding within influenza viruses. Mapping of the NP-bound vRNA segments provides information on the flexible NP regions that may be involved in facilitating assembly.

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Molecular Characterization of a Novel Avian Influenza A (H2N9) Strain Isolated from Wild Duck in Korea in 2018

Viruses ◽

10.3390/v11111046 ◽

2019 ◽

Vol 11 (11) ◽

pp. 1046 ◽

Cited By ~ 4

Author(s):

Seon-Ju Yeo ◽

Duc-Duong Than ◽

Hong-Seog Park ◽

Haan Woo Sung ◽

Hyun Park

Keyword(s):

Influenza Virus ◽

Amino Acid ◽

Avian Influenza ◽

Avian Influenza Virus ◽

Influenza A ◽

Matrix Protein ◽

Sequence Similarity ◽

Wild Birds ◽

Structural Protein ◽

Wild Duck

A novel avian influenza virus (A/wild duck/Korea/K102/2018) (H2N9) was isolated from wild birds in South Korea in 2018, and phylogenetic and molecular analyses were conducted on complete gene sequences obtained by next-generation sequencing. Phylogenetic analysis indicated that the hemagglutinin (HA) and neuraminidase (NA) genes of the A/wild duck/Korea/K102/2018 (H2N9) virus belonged to the Eurasian countries, whereas other internal genes (polymerase basic protein 1 (PB1), PB2, nucleoprotein (NP), polymerase acidic protein (PA), matrix protein (M), and non-structural protein (NS)) belonged to the East Asian countries. A monobasic amino acid (PQIEPR/GLF) at the HA cleavage site, E627 in the PB2 gene, and no deletion of the stalk region in the NA gene indicated that the A/wild duck/Korea/K102/2018 (H2N9) isolate was a typical low pathogenicity avian influenza (LPAI). Nucleotide sequence similarity analysis of HA revealed that the highest homology (98.34%) is to that of A/duck/Mongolia/482/2015 (H2N3), and amino acid sequence of NA was closely related to that of A/duck/Bangladesh/8987/2010 (H10N9) (96.45%). In contrast, internal genes showed homology higher than 98% compared to those of other isolates derived from duck and wild birds of China or Japan in 2016–2018. The newly isolated A/wild duck/Korea/K102/2018 (H2N9) strain is the first reported avian influenza virus in Korea, and may have evolved from multiple genotypes in wild birds and ducks in Mongolia, China, and Japan.

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Avian Influenza Virus Prevalence and Subtype Diversity in Wild Birds in Shanghai, China, 2016–2018

Viruses ◽

10.3390/v12091031 ◽

2020 ◽

Vol 12 (9) ◽

pp. 1031

Author(s):

Ling Tang ◽

Wangjun Tang ◽

Xiaofang Li ◽

Chuanxia Hu ◽

Di Wu ◽

...

Keyword(s):

Influenza A ◽

Eastern China ◽

Wild Birds ◽

Influenza A Viruses ◽

Chain Reaction ◽

Virus Prevalence ◽

Total Prevalence ◽

Monitoring Group ◽

Polymerase Chain ◽

Common Teal

From 2016 to 2018, surveillance of influenza A viruses in wild birds was conducted in Shanghai, located at the East Asian–Australian flyway, China. A total of 5112 samples from 51 species of wild birds were collected from three different wetlands. The total three-year prevalence of influenza A viruses among them was 8.8%, as assessed using real-time polymerase chain reaction (PCR) methods, and the total prevalence was higher in Anseriformes (26.3%) than in the Charadriiformes (2.3%) and the other orders (2.4%) in the Chongmin wetlands. Anseriformes should be the key monitoring group in future surveillance efforts. The peak prevalence of influenza A viruses in Charadriiformes were in April and September, and in other bird orders, the peaks were in November and December. Twelve subtypes of haemagglutinin (HA; H1–H12) and eight subtypes of neuraminidase (NA; N1, N2, N4–N9) were identified in 21 different combinations. The greatest subtype diversity could be found in common teal, suggesting that this species of the bird might play an important role in the ecology and epidemiology of influenza A viruses in Shanghai. These results will increase our understanding of the ecology and epidemiology of influenza A viruses in wild bird hosts in eastern China, and provide references for subsequent surveillance of influenza A virus in wild birds in this area.

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Zoonotic Potential of Influenza A Viruses: A Comprehensive Overview

Viruses ◽

10.3390/v10090497 ◽

2018 ◽

Vol 10 (9) ◽

pp. 497 ◽

Cited By ~ 50

Author(s):

Ahmed Mostafa ◽

Elsayed Abdelwhab ◽

Thomas Mettenleiter ◽

Stephan Pleschka

Keyword(s):

Genetic Diversity ◽

Global Health ◽

Influenza A ◽

Viral Evolution ◽

Zoonotic Potential ◽

Influenza A Viruses ◽

Comprehensive Overview ◽

High Genetic Diversity ◽

Human Interface ◽

Animal Hosts

Influenza A viruses (IAVs) possess a great zoonotic potential as they are able to infect different avian and mammalian animal hosts, from which they can be transmitted to humans. This is based on the ability of IAV to gradually change their genome by mutation or even reassemble their genome segments during co-infection of the host cell with different IAV strains, resulting in a high genetic diversity. Variants of circulating or newly emerging IAVs continue to trigger global health threats annually for both humans and animals. Here, we provide an introduction on IAVs, highlighting the mechanisms of viral evolution, the host spectrum, and the animal/human interface. Pathogenicity determinants of IAVs in mammals, with special emphasis on newly emerging IAVs with pandemic potential, are discussed. Finally, an overview is provided on various approaches for the prevention of human IAV infections.

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ISOLATION OF ORTHO- AND PARAMYXOVIRUSES FROM WILD BIRDS IN WESTERN AUSTRALIA, AND THE CHARACTERIZATION OF NOVEL INFLUENZA A VIRUSES

Australian Journal of Experimental Biology and Medical Science ◽

10.1038/icb.1984.9 ◽

1984 ◽

Vol 62 (1) ◽

pp. 89-99 ◽

Cited By ~ 49

Author(s):

JS Mackenzie ◽

EC Edwards ◽

RM Holmes ◽

VS Hinshaw

Keyword(s):

Western Australia ◽

Influenza A ◽

Wild Birds ◽

Influenza A Viruses ◽

Novel Influenza A

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The evolutionary dynamics of influenza A virus adaptation to mammalian hosts

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0382 ◽

2013 ◽

Vol 368 (1614) ◽

pp. 20120382 ◽

Cited By ~ 27

Author(s):

S. Bhatt ◽

T. T. Lam ◽

S. J. Lycett ◽

A. J. Leigh Brown ◽

T. A. Bowden ◽

...

Keyword(s):

Avian Influenza ◽

Adaptive Evolution ◽

Influenza A ◽

Evolutionary Dynamics ◽

Adaptive Dynamics ◽

Swine Influenza ◽

Influenza Viruses ◽

Viral Fitness ◽

Influenza A Viruses ◽

Entire Genome

Few questions on infectious disease are more important than understanding how and why avian influenza A viruses successfully emerge in mammalian populations, yet little is known about the rate and nature of the virus’ genetic adaptation in new hosts. Here, we measure, for the first time, the genomic rate of adaptive evolution of swine influenza viruses (SwIV) that originated in birds. By using a curated dataset of more than 24 000 human and swine influenza gene sequences, including 41 newly characterized genomes, we reconstructed the adaptive dynamics of three major SwIV lineages (Eurasian, EA; classical swine, CS; triple reassortant, TR). We found that, following the transfer of the EA lineage from birds to swine in the late 1970s, EA virus genes have undergone substantially faster adaptive evolution than those of the CS lineage, which had circulated among swine for decades. Further, the adaptation rates of the EA lineage antigenic haemagglutinin and neuraminidase genes were unexpectedly high and similar to those observed in human influenza A. We show that the successful establishment of avian influenza viruses in swine is associated with raised adaptive evolution across the entire genome for many years after zoonosis, reflecting the contribution of multiple mutations to the coordinated optimization of viral fitness in a new environment. This dynamics is replicated independently in the polymerase genes of the TR lineage, which established in swine following separate transmission from non-swine hosts.

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