Demographic and environmental drivers of metagenomic viral diversity in vampire bats

Abstract

Viruses infect all forms of life and play critical roles as agents of disease, drivers of biochemical cycles and sources of genetic diversity for their hosts. Our understanding of viral diversity derives primarily from comparisons among host species, precluding insight into how intraspecific variation in host ecology affects viral communities or how predictable viral communities are across populations. Here we test spatial, demographic and environmental hypotheses explaining viral richness and community composition across populations of common vampire bats, which occur in diverse habitats of North, Central and South America. We demonstrate marked variation in viral communities that was not consistently predicted by a null model of declining community similarity with increasing spatial or genetic distances separating populations. We also find no evidence that larger bat colonies host greater viral diversity.Instead, viral diversity follows an elevational gradient, is enriched by juvenile-biased age structure, and declines with local anthropogenic food resources as measured by livestock density. Our results establish the value of linking the modern influx of metagenomic sequence data with comparative ecology, reveal that snapshot views of viral diversity are unlikely to be representative at the species level, and affirm existing ecological theories that link host ecology not only to single pathogen dynamics but also to viral communities. K E Y W O R D SChiroptera, community assembly, demography, Desmodus rotundus, elevational gradient, infectious diseases, population structure, shotgun metagenomics, virome, wildlife disease | 27 BERGNER Et al.

Host age shapes virome abundance and diversity in birds

“…This observation is consistent with previous studies of virus ecology, in which influenza A viruses exhibit higher prevalence in juveniles compared to adults [7,8], and juveniles have a greater number of infections and diversity of subtypes over an autumn season compared to adult birds [22]. Similarly, caves hosting a larger proportion of juvenile bats had a larger viral diversity as compared to those hosting a low proportion of juvenile bats [47].…”

“…Based on studies of the ecology of both avian influenza A virus [1, 7,8], and more recently, of virus communities in bats [47], we predicted that juvenile birds would have high viral abundance and diversity compared to adult birds. During the non-breeding period, Ruddy Turnstones on King Island, Tasmania spend time in small (~50 birds) groups comprising both adult and juvenile birds, and are often restricted to small stretches of coastline (~1 km).…”

Diversification of mammalian deltaviruses by host shifting

“…Initial virus discovery efforts in Peruvian vampire bats used metagenomic datasets generated from bats captured at 23 colonies between 2013 and 2016 (46,47). For studies on DrDV prevalence in vampire bats, we studied 12 focal sites in three departments of Peru between 2016-2017 (Fig 2A).…”

Accounting for imperfect detection reveals role of host traits in structuring viral diversity of a wild bat community

“…Using calipers, forearm length was measured to the nearest 0.01 millimeter from the distal tip of the radius to the distal tip of the olecranon process. Ectoparasite intensity was measured from visual inspection of the number of individual ecotparasites and represented as a categorical variable: low (< 5), medium (5)(6)(7)(8), high (9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19), and extreme (>19). A categorical measure of intensity was used instead of abundance because best practices to quantify exact abundance require host anesthesia [2].…”

“…Emerging infectious viruses, such as SARS-CoV or Zika, represent single pathogen species embedded within multi-host, multi-pathogen systems. Community ecology -at the scale of host communities, and also at the scale of viral communities -is increasingly recognized as a productive framework with which to dissect such complex dynamics, illuminating risk factors associated with pathogen transmission, host switching, and spillover from wildlife to humans, among others [1,2,3,4,5,6]. However, viral community ecology is limited by two major quantitative obstacles.…”