Terrestrial Bird Migration and West Nile Virus Circulation, United States

Abstract

Host migration and emerging pathogens are strongly associated, especially with regard to zoonotic diseases. West Nile virus (WNV), a mosquitoborne pathogen capable of causing severe, sometimes fatal, neuroinvasive disease in humans, is maintained in highly mobile avian hosts. Using phylogeographic approaches, we investigated the relationship between WNV circulation in the United States and the flight paths of terrestrial birds. We demonstrated southward migration of WNV in the eastern flyway and northward migration in the central flyway, which is consistent with the looped flight paths of many terrestrial birds. We also identified 3 optimal locations for targeted WNV surveillance campaigns in the United States-Illinois, New York, and Texas. These results illustrate the value of multidisciplinary approaches to surveillance of infectious diseases, especially zoonotic diseases.

Keywords: United States; West Nile virus; bird migration; emerging pathogens; phylogeography; terrestrial birds; vector-borne infections; viruses; zoonoses.

Figure 1

Maximum-likelihood phylogeny generated with all West Nile virus sequences from New York, Virginia, Georgia, Illinois, North Dakota, South Dakota, Texas, and Colorado (n = 379) in study of terrestrial bird migration and West Nile virus circulation, United States. Sequence names include the 2-letter state abbreviation to indicate the origin of isolation, followed by the year. Multiple isolates collected from the same state within the same year are differentiated by letter. GenBank accession numbers are provided for all taxa that were not sequenced in this study. Scale bar indicates nucleotide substitutions per site.

Figure 2

Analysis of correlation between virus isolation date and genetic diversity in study of terrestrial bird migration and West Nile virus circulation, United States. Root-to-tip distances of all sequences were determined for each isolate by using the maximum-likelihood tree shown in Figure 1 (https://wwwnc.cdc.gov/EID/article/24/12/18-0382-F1.htm) and plotted against the year. Dots are colored by location of isolation. The correlation between the root-to-tip distance and year of isolation was determined with linear regression shown in blue. 95% CIs are shown in gray. The equation of the linear regression line was used to estimate the year of the most recent common ancestor (MRCA) and the mutation rate (m): y = mx + MRCA.

Figure 3

Bayesian phylogeny of West Nile virus isolates collected in representative regions along the Eastern and Central flyways between 2001 and 2009, United States. Maximum-clade credibility tree was obtained by using a Bayesian approach. The location of each isolate and the inferred location of each ancestor are depicted by color.

Figure 4

Summary of source/sink analysis in study of terrestrial bird migration and West Nile virus circulation, United States. Minimum number of migration events detected from A) the Eastern flyway, B) Illinois, and C) the Central flyway. Only events that occurred at least twice are depicted. Red arrows, northward migration; black arrows, southward migration; green arrow, lateral migration; dotted arrows, migration that could not be confirmed by incident-controlled downsampling because of an insufficient number of sequences.

Figure 5

Incidence-controlled phylogeny of Eastern and Central flyways, United States. Sequences were down-sampled such that the number of sequences was proportional to the annual incidence of West Nile neurologic disease incidence for each location between 2001 and 2009. Down-sampling was undertaken twice (A and B) to ensure that the reduction in sequences did not result in a substantial loss of diversity. Illinois, North Dakota, and South Dakota were not included in the incidence-control analysis because too few sequences were available to support down-sampling. Bayesian approaches were used to generate maximum-clade credibility trees. Scale bars indicate nucleotide substitutions per site.

Figure 6

Summary of Markov jump analysis performed on the incident-controlled phylogeny. A, B) The results of the Markov jump analysis for each down-sampled dataset are summarized as box plots. Box tops indicate third quartiles, box bottoms indicate first quartiles; horizontal bars within boxes indicate medians; error bars indicate maximums and minimums. Red, northward movement; teal, southward movement; purple, movement that is neither north nor south; dotted arrows, movement that was not observed in the incident-controlled down-sampling because of an insufficient number of sequences. C, D) Movement originating in the eastern and central United States. Only Markov jumps that occurred >2 times are depicted.

Figure 7

Model summarizing the general patterns of West Nile virus movement in the United States. Red, northward movement; teal, southward movement; dotted arrows, relationships that could not be confirmed in incident-controlled datasets because of an insufficient number of sequences.