Population genetics of fruit bat reservoir informs the dynamics, distribution and diversity of Nipah virus.

Kevin J Olival1 Alice Latinne1 Ariful Islam1 Jonathan H Epstein1 Rebecca Hersch2 Rachel C Engstrand2 Emily S Gurley3 George Amato2 Stephen P Luby3 Peter Daszak1
Affiliations 3 institutions
  1. EcoHealth Alliance, New York, NY, USA.
  2. Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY, USA.
  3. ICDDR,b, Dhaka, Bangladesh.

Abstract

The structure and connectivity of wildlife host populations may influence zoonotic disease dynamics, evolution and therefore spillover risk to people. Fruit bats in the genus Pteropus, or flying foxes, are the primary natural reservoir for henipaviruses-a group of emerging paramyxoviruses that threaten livestock and public health. In Bangladesh, Pteropus medius is the reservoir for Nipah virus-and viral spillover has led to human fatalities nearly every year since 2001. Here, we use mitochondrial DNA and nuclear microsatellite markers to measure the population structure, demographic history and phylogeography of P. medius in Bangladesh. We combine this with a phylogeographic analysis of all known Nipah virus sequences and strains currently available to better inform the dynamics, distribution and evolutionary history of Nipah virus. We show that P. medius is primarily panmictic, but combined analysis of microsatellite and morphological data shows evidence for differentiation of two populations in eastern Bangladesh, corresponding to a divergent strain of Nipah virus also found in bats from eastern Bangladesh. Our demographic analyses indicate that a large, expanding population of flying foxes has existed in Bangladesh since the Late Pleistocene, coinciding with human population expansion in South Asia, suggesting repeated historical spillover of Nipah virus likely occurred. We present the first evidence of mitochondrial introgression, or hybridization, between P. medius and flying fox species found in South-East Asia (P. vampyrus and P. hypomelanus), which may help to explain the distribution of Nipah virus strains across the region.

Supporting text Virus Host Location
Chiroptera 376 dispersal 1 emerging infectious disease 11 phylogeography 35 population genetic structure 1 Pteropus giganteus 1 zoonoses 477 Genetics, Population 2 Animals 1948 Bangladesh 25 Chiroptera 371 DNA, Mitochondrial 5 Female 289 Male 224 Microsatellite Repeats 2 Nipah Virus 45 Phylogeography 30

Evidence records

4 total
Zoonotic Surveillance
2 records · 1 evidence types
Evidence type
2 records
OVE3474
Key finding

Pteropus medius acts as the natural reservoir host maintaining Nipah virus circulation in Bangladesh.

Virus
Host
Location
Supporting text

In Bangladesh, Pteropus medius is the reservoir for Nipah virus—and viral spillover has led to human fatalities nearly every year since 2001.

Method
mitochondrial DNA analysis | nuclear microsatellite markers | phylogeographic analysis
Geographic raw
Bangladesh
Country inferred
BGD
OVE3477
Key finding

Mitochondrial introgression or hybridization between Pteropus medius and other flying fox species (P. vampyrus and P. hypomelanus) is linked to the distribution of Nipah virus strains across South-East Asia, indicating potential viral exchange among these bat species.

Virus
Host
Location
Supporting text

We present the first evidence of mitochondrial introgression, or hybridization, between P. medius and flying fox species found in South-East Asia (P. vampyrus and P. hypomelanus), which may help to explain the distribution of Nipah virus strains across the region.

Method
mitochondrial DNA analysis | microsatellite analysis
Geographic raw
South-East Asia
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE3473
Key finding

Nipah virus has repeatedly spilled over from Pteropus medius to humans in Bangladesh, resulting in human fatalities nearly every year since 2001.

Virus
Host
Location
Supporting text

In Bangladesh, Pteropus medius is the reservoir for Nipah virus—and viral spillover has led to human fatalities nearly every year since 2001.

Method
field surveillance | epidemiologic linkage of human cases to bat reservoir
Study design
epidemiological observation of natural spillover
Transmission direction
animal-to-human
Geographic raw
Bangladesh
Country inferred
BGD
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE3475
Key finding

Phylogenetic and host genetic analyses revealed a divergent strain of Nipah virus associated with differentiated Pteropus medius bat populations in eastern Bangladesh.

Virus
Host
Location
Not specified
Supporting text

Combined analysis of microsatellite and morphological data shows evidence for differentiation of two populations in eastern Bangladesh, corresponding to a divergent strain of Nipah virus also found in bats from eastern Bangladesh.

Analysis methods
phylogeographic analysis | microsatellite analysis | morphological data comparison