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(Anas Platyrhynchos) in the Spread of Avian Influenza

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(Anas Platyrhynchos) in the Spread of Avian Influenza The Role of Mallard (Anas platyrhynchos) in the Spread of Avian In uenza: GENOMICS, POPULATION GENETICS, AND FLYWAYS. Robert H. Kraus The Role of Mallard (Anas platyrhynchos) in the Spread of Avian Influenza: GENOMICS, POPULATION GENETICS, AND FLYWAYS. Robert H. Kraus THESIS COMMITTEE THESIS SUPERVISORS Prof. dr. H.H.T. Prins Professor of Resource Ecology, Wageningen University Prof. dr. R.C. Ydenberg Professor of Fauna Management and Conservation, Wageningen University Professor of Behavioural Ecology, Simon Frasier University, Canada THESIS CO-SUPERVISOR Dr. W.F. van Hooft Assistant professor, Resource Ecology Group Wageningen University OTHER MEMBERS Prof. dr. B.J. Zwaan, Wageningen University Prof. dr. C. Dreyer, MPI for developmental Biology, Tübingen, Germany Prof. dr. C. Schlötterer, University of Veterinary Medicine, Vienna, Austria Prof. dr. R. Tiedemann, University of Potsdam, Golm, Germany This research was conducted under the auspices of the C.T. de Wit Graduate School Production Ecology & Resource Conservation The Role of Mallard (Anas platyrhynchos) in the Spread of Avian Influenza: GENOMICS, POPULATION GENETICS, AND FLYWAYS. Robert H. Kraus THESIS submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Tuesday 13 December 2011 at 1.30 p.m. in the Aula Robert H. Kraus The Role of Mallard (Anas platyrhynchos) in the Spread of Avian Influenza: Genomics, Population Genetics, and Flyways. 143 pages. Thesis, Wageningen University, Wageningen, NL (2011) With references, with summaries in Dutch and English ISBN 978-94-6173-028-2 Table of Contents CHAPTER 1 — General Introduction . 6 CHAPTER 2 — Evolution and connectivity in the world-wide migration system of the mallard: Inferences from mitochondrial DNA . .11 CHAPTER 3 — Genome wide SNP discovery, analysis and evaluation in mallard....................................31 CHAPTER 4 — Global panmixia in a cosmopolitan bird? Model selection with hundreds of genome-wide single nucleotide polymorphisms reveals world- wide gene pool connectivity . .46 CHAPTER 5 — Widespread horizontal genomic exchange does not erode species barriers among duck species . .66 CHAPTER 6 — Avian Influenza surveillance: on the usability of FTA® cards to solve biosafety and transport issues . .90 CHAPTER 7 — Avian Influenza surveillance with FTA® cards: Field methods, biosafety, and transportation issues solved . .96 CHAPTER 8 — Synthesis . .105 References ..............................................113 Summary ...............................................135 Samenvatting ............................................136 Acknowledgements .......................................137 5 CHAPTER 1 General Introduction 6 General Introduction Birds, in particular poultry and ducks, are a source of many zoonotic diseases, such as those caused by corona and influenza viruses1,2. These viruses are a threat not only to these birds themselves but also to poultry farming and human health, as forms that can infect humans are known to have evol- ved1,2. It is believed that migratory birds, and water birds in particular, play an important role in the global spread of Avian Influenza (AI)3. However, it is still debated how large this role precisely is and whether other modes of spread may be more important2,4. Migratory birds with separate breeding and wintering grounds are interesting model species for studying disease transmission. The mallard The mallard (Anas platyrhynchos) is a member of the order of the Anseriformes (ducks, geese and swans)5,6, and is generally bound to open waters and wetland habitats. Mallards are omnivorous, and their diet consists not only of small invertebrates, which they collect with their bill by “da- bbling” under water with their tail up (the characteristic feeding behaviour of the sub-family dabbling ducks, the Anatini7), but also tadpoles, small fish, or all sorts of plant material. In the family of ducks (Anatidae) the mallard is the largest bird with a weight of around 1 kg and a body size of 50 cm in both females and males8. Mallards display sexual dimorphism: males have bright plumage to display to females during courtship9, females are dull-brown camouflaged to facilitate secretive life-style, especially during breeding season. The mallard is the most numerous and well-known waterfowl (Anseriformes) species with a Holarctic distribution. For instance, in Europe it is absent only in January from upland areas and those areas affected by prolonged freezing10. Most mallards are migratory without clear geo- graphic directionality, and spring and fall flights can exceed thousands of kilometres11. Northern breeding birds are mostly migratory, wintering much further south, while birds breeding in temperate regions (most of Western Europe) are resident or merely dispersive12. Additionally, the level of “abmigration” (the switching of flyways) is thought to be very high in ducks species13 and thus a dense network-like connectivity between populations may exist. The large-scale migration systems of temperate waterfowl have been extensively studied us- ing ringing, telemetry, morphometrics, radar tracking and isotope analysis14. Migration routes are clearly defined12 for most waterfowl species and usually follow north-south directions, with populations travelling between northerly breeding areas and more southerly non-breeding areas. Many species follow similar routes and decades of studies on bird migration have led to the delin- eation of major waterfowl “flyways”12,15-17. In North-America especially, flyways are managerial units created by agreements between adjoining states and provinces, and thus are bounded by management requirements. In a population ecological sense true migratory pathways are much fuzzier. Populations and individuals within species may occupy different flyways, and many mi- grants are flexible in migration routing18, even though these migration routes have been in place for relatively long periods of time19,20. Mallards seem to display an extreme flexibility in their migration behaviour, when compared to the related species in their bird order, and it is unclear if biological reality would support their placement into a global waterfowl flyway system. Migra- tion in mallards is heavily studied but delineations of populations have been more tentative than in other waterfowl12,16,17. 7 Chapter 1 The foraging habitat of the mallard in shallow waters brings it into contact with a wide variety of pathogens and it may act as a reservoir and disperser for many of them. The mallard is consid- ered the primary natural reservoir of avian influenza due to its wide range and large population sizes21. Moreover, together with the black-headed gull (Larus ridibundus) it was identified as the species bearing the highest risk to transmit AI to farm-birds due to frequent contact with poul- try10. Post-breeding pre-migratory staging areas are thought to be important locations for viral acquisition22. Avian Influenza The Influenza viruses are a genus within the Orthomyxoviridae. They have a segmented negative sense single-stranded RNA-genome [(-)ssRNA]. Forms of the Influenza A virus can infect a wide range of host species including among others birds, pigs, horses, seals, whales and humans. There are eight RNA segments. Viral subtypes are classified using two of the encoded genes: the hemag- glutinin (HA) gene and the neuraminidase (NA) gene. These genes code for surface proteins that play a key role in host recognition and initial infection23. Sixteen HA-types24 and nine NA-types are recognised, giving rise to 144 (= 9 × 16) possible subtypes. These are described as, e.g., H5N1 (type 5 of HA, and type 1 of NA). The classification used to rely on immunoassays using standard procedures25-27. Nowadays it is also possible to sequence the genes of a virus using retrograde transcriptase PCR (RT-PCR) with a set of universal primers for all genes and all subtypes28 and compare the obtained cDNA sequence with databases such as GenBank29. Humans can be infected with all three species of Influenza viruses: A, B and C. Influenza A viruses are those referred to as Avian Influenza. In humans, the HA proteins H1-3 and NA types 1 and 2 of Influenza A viruses usually cause seasonal Influenza, but Influenza B and, less frequently, Influenza C viruses also circulate in humans30. However, human pandemics for which the medical histories have been reconstructed were all caused by Influenza A viruses31,32. It has been proposed that wild birds in general, and especially migratory waterfowl, are not only the reservoir, but also the vectors for the spread of Avian Influenza over large distances2. Highly pathogenic types of AI are thought to be easily spread through the flyways of waterfowl, because of these birds show no clinical signs of infection but transmit a form highly patho- genic to poultry or humans33-36, although this is not generally true for every highly pathogenic strain37-39. However, the evidence for this possible route of transport in cases of highly pathogenic strains is equivocal40-43. Alternatively, highly pathogenic strains might evolve from low pathogenic ones directly in poultry farms where the selective regime is different from the wild44. The molecular ecological approach The scientific discipline of ‘molecular ecology’ is characterised by the use of a certain type of data:
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