Diversity and cross-species transmission of viruses in a remote island ecosystem: implications for wildlife conservation

Abstract

The ability of viruses to emerge in new species is influenced by aspects of host biology and ecology, with some taxa harbouring a high diversity and abundance of viruses. However, how these factors shape virus diversity at the ecosystem scale is often unclear. To better understand the pattern and determinants of viral diversity within an ecosystem, and to describe the novel avian viruses infecting an individual avian community, we performed a metagenomic snapshot of the virome from the entire avian community on remote Pukenui/Anchor Island in Aotearoa New Zealand. Through total RNA sequencing of 18 bird species, we identified 50 avian viruses from 9 viral families, of which 96% were novel. Of note, passerines (perching birds) exhibited high viral abundance and diversity, with viruses found across all nine viral families identified. We also identified numerous viruses infecting seabirds on the Island, including megriviruses, hepaciviruses, and hepatoviruses, while parrots exhibited an extremely low diversity of avian viruses. Within passerines, closely related astroviruses and hepatoviruses, and multiple identical hepe-like viruses, were shared among host species. Phylogenetic reconciliation analysis of these viral groups revealed a mixture of co-divergence and cross-species transmission, with virus host-jumping relatively frequent among passerines. In contrast, there was no evidence for recent cross-species virus transmission in parrots or seabirds. The novel pegiviruses and a flavivirus identified here also pose intriguing questions regarding their origins, pathogenicity, and potential impact on vertebrate hosts. Overall, these results highlight the importance of understudied remote island ecosystems as refugia for novel viruses, as well as the intricate interplay between host ecology and behaviour in shaping viral communities.

Keywords: birds; cross-species transmission; evolution; metatranscriptomics; virus.

Figure 1.

(a) Total number of reads in each library. (b) Abundance of viral reads. (c) Abundance of non-avian viral reads. (d) Abundance of avian viral reads. For all graphs the y-axis is a log scale. For panels (b–d), the abundance is expressed as RPM. Green = passerine, red = seabird, blue = parrot, black = other.

Figure 2.

Boxplots showing the differences in (a) log viral abundance (RPM) and (b) Shannon index across the three species groups. Brackets show P-value significance, * <.05, ** <.01. Raw data (jittered) is shown using empty circles.

Figure 3.

(a) Phylogeny of the Astroviridae (representative viruses only, n = 33 including collapsed clades) based on the nonstructural polyprotein (alignment length of 374 amino acids post-trimming). Coloured circles depict the host species for each virus found as shown in the key (for passerine astrovirus 1–4 the host species is unknown). (b) Phylogeny of the Caliciviridae (representative viruses only, n = 25 including collapsed clades) using the polyprotein gene (alignment length of 1693 amino acids post-trimming). Coloured text denotes viruses found in this study, with related viruses shown in black. Black circles on nodes show bootstrap support values of >90%. Branches are scaled according to the number of amino acid substitutions per site, shown in the scale bar. The trees are midpoint rooted for purposes of clarity only. Silhouettes were adapted from Microsoft 365 icons.

Figure 4.

Phylogenetic analysis of the Hepeviridae (representative viruses only, n = 67 including collapsed clades) based on the nonstructural polyprotein (alignment length of 762 amino acids post-trimming). Green coloured text denotes viruses found in this study, while related viruses are shown in black. In the avian clade, coloured circles show the host species for each virus found in the study as shown in the key. Black circles on nodes show bootstrap support values of >90%. Branches are scaled according to the number of amino acid substitutions per site, shown in the scale bar. The tree is midpoint rooted for purposes of clarity only. Silhouettes were adapted from Microsoft 365 icons.

Figure 5.

(a) Phylogenetic analysis of the genus Orthoflavivirus (Flaviviridae) (representative viruses only, n = 36 including collapsed clade) based on the polyprotein (alignment length 2486 amino acids post trimming). (b) Phylogenetic analysis of the Flaviviridae (representative viruses only, n = 139 including collapsed clades) based on the polyprotein (alignment length 1562 amino acids post trimming). Green/red text and icons denote the novel viruses found in this study. Related viruses are shown in black. Black circles on nodes show bootstrap support values of >90%. Branches are scaled according to the number of amino acid substitutions per site, shown in the scale bar. The tree is midpoint rooted for purposes of clarity only. Silhouettes were adapted from Microsoft 365 icons.

Figure 6.

Phylogenetic analysis of two Picornaviridae genera: (a) the genus Hepatovirus (representative viruses only, n = 44) based on the polyprotein (alignment length 1699 amino acids post-trimming). (b) The genus Megrivirus (representative viruses only, n = 27) based on the polyprotein (alignment length 2063 amino acids). Shading shows clustering according to host; grey = mammalian-infecting viruses, green = passerine-infecting viruses, red = mottled petrel-infecting viruses. Coloured text and black icons denote viruses found in this study, while related viruses are shown in black. Black circles on nodes show bootstrap support values of >90%. Branches are scaled according to the number of amino acid substitutions per site, shown in the scale bar. The tree is midpoint rooted for purposes of clarity only. Silhouettes were adapted from Microsoft 365 icons.

Figure 7.

Median maximum parsimony reconciliation phylogenies for avian viruses in the Hepatovirus (a), Avastrovirus (b) genera, and the hepe-like viruses (c) group. The host phylogenies are shown in black with binomial names of each host in black text. The viral phylogenies are overlaid in blue, with no tip labels. Symbols on the nodes of the viral phylogenies denote the evolutionary event inferred.