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

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.

Climate change will drive novel cross-species viral transmission

“…Even non-migratory bats can regularly travel hundreds of kilometers within a lifetime, far exceeding what small mammals might be able to cover in 50 years; half of all bat population genetic studies have failed to find any evidence for isolation by distance 46 . This unique dispersal capacity has inevitable epidemiological implications, with recent evidence suggesting that continental panmixia may be common for zoonotic reservoirs, and allow viral circulation at comparable scales 43,44,47 . We found that a staggering number of studies have also identified ongoing rapid range expansions in bat species around the world 45,48,49,50,51,52,53,54,55 , with little mention in the broader climate change or emerging disease literature.…”

When are pathogen dynamics likely to reflect host population genetic structure?

“…Interspecific transmission among Pteropodid reservoir species may occur through coroosting where species' geographical ranges overlap. Evidence of interspecific transmission among Pteropodid NiV reservoirs was discovered by Olival et al (2020)—historical mitochondrial hybridization of P. medius with P. lylei and P. vampyrus —further supporting this theory. Indeed, Olival et al's study suggests that NiV isolates currently circulating in Bangladesh may have been introduced recently (1941, 95% highest posterior density 1887–1994) through coroosting, which is much more recent than the estimated arrival time of P. medius in the region (Late Pleistocene).…”

“…Congruence of host and pathogen genetic structure, however, relies on the coupling between the spatial scale of host movement (which produces spatial genetic structure), and a pattern of pathogen transmission events (which will be considerably more contemporary) having sufficient evolutionary signature for detection. To illustrate this with a contrasting example, and cited by Olival et al (2020), bobcats occasionally cross Interstate 5 south of Los Angeles from an inland (Santa Ana Mountain) population to a coastal (San Joaquin Hills) population (Fountain‐Jones et al, ; Lee et al, ). Bobcats encounter other individuals and transmit their FIV, but rarely establish in the coastal population (probably dying following unsuccessful attempts to establish a territory), resulting in incongruous host and pathogen genetic structure.…”

“…In this issue of Molecular Ecology , Olival et al (2020) present a well‐reasoned range of mechanisms to explain their pattern of IHPC. The dominant mechanism driving IHPC in their study may be the interface between host movement and transmission.…”

“…This was exemplified by the panmixia observed in the genetic structure of P. medius . Olival et al (2020) suggest that individual heterogeneity in the movement of bats among roosts may lead to host metapopulation dynamics as a driving mechanism of Nipah virus (NiV) panmictic structure and persistence at the population scale. Where some host genetic structure was detected (between the Nipah belt and sites to the east) it was matched by structure in NiV, suggesting barriers to both host and viral movement (and hence IHPC).…”