The radiation of New Zealand's skinks and geckos is associated with distinct viromes

Abstract

Background: New Zealand is home to over 120 native endemic species of skinks and geckos that radiated over the last 20-40 million years, likely driven by the exploitation of diverse habitats formed during the Miocene. The recent radiation of animal hosts may facilitate cross-species virus transmission, likely reflecting their close genetic relationships and therefore relatively low barriers for viruses to emerge in new hosts. Conversely, as animal hosts adapt to new niches, even within specific geographic locations, so too could their viruses. Consequently, animals that have niche-specialised following radiations may be expected to harbour genetically distinct viruses. Through a metatranscriptomic analysis of eight of New Zealand's native skink and gecko species, as well as the only introduced lizard species, the rainbow skink (Lampropholis delicata), we aimed to reveal the diversity of viruses in these hosts and determine whether and how the radiation of skinks and geckos in New Zealand has impacted virus diversity and evolution.

Results: We identified a total of 15 novel reptilian viruses spanning 11 different viral families, across seven of the nine species sampled. Notably, we detected no viral host-switching among the native animals analysed, even between those sampled from the same geographic location. This is compatible with the idea that host speciation has likely resulted in isolated, niche-constrained viral populations that have prevented cross-species transmission. Using a protein structural similarity-based approach, we further identified a highly divergent bunya-like virus that potentially formed a new family within the Bunyavirales.

Conclusions: This study has broadened our understanding of reptilian viruses within New Zealand and illustrates how niche adaptation may limit viral-host interactions.

Keywords: Gecko; Host radiation; Metatranscriptomics; New Zealand; Skink; Viral co-divergence; Virome.

Fig. 1

a Map of New Zealand indicating the four sites where skinks and geckos were sampled. b Cladogram illustrating the evolutionary relationship of geckos in the family Diplodactylidae compared to skinks in the family Scincidae [41], and the evolution of New Zealand skinks and geckos [9, 11]. c Venn diagram depicting the number of skink and gecko species shared between the four sampling sites

Fig. 2

a Heatmap of relative viral abundance (%) across libraries. Information regarding pooled RNA sampling sites is denoted by coloured dots and in the key, while information regarding introduced vs native species and host species is noted above and below the heatmap respectively. b Dual plot of average viral family richness across lizard species (left y-axis) and average raw reads across libraries of lizard species (right y-axis). Error bars represent standard deviation values. c Log scale dual plot of average viral abundance (reads per 100 million) across lizard species (left y-axis) and average raw reads across libraries of lizard species (right y-axis). Error bars represent standard deviation values

Fig. 3

Bipartite network depicting the connections between viral families shared between skinks and geckos sampled. Branch thickness is weighted by the standardised abundance in reads per million of viral transcripts within a given host species

Fig. 4

Phylogenetic trees of negative-sense RNA viruses. Maximum likelihood phylogenetic trees of representative viral transcripts containing the RdRp from negative-sense RNA viral families (a) Amnoonviridae, (b) Hantaviridae and (c) Chuviridae. Skink viruses identified in this study are bolded while known genera and subfamilies are highlighted. Branches are scaled to the number of amino acid substitutions per site. All phylogenetic trees were midpoint-rooted. Nodes with ultrafast bootstrap values of > 70% are noted by a red circle. If near full-length genomes of skink viruses were uncovered a nt alignment (black) and the predicted ORFs (orange) of the skink virus along with a representative complete viral genome from the same family is shown below the respective phylogenetic trees

Fig. 5

Phylogenetic trees of positive-sense RNA viruses. Maximum likelihood phylogenetic trees of representative viral transcripts containing the RdRp from positive-sense RNA families (a) Caliciviridae, (b) Astroviridae, (c) Hepeviridae, (d) Picornaviridae. Skink and gecko viruses identified in this study are bolded while known genera and subfamilies are highlighted. Branches are scaled to the number of amino acid substitutions per site. All phylogenetic trees were midpoint rooted. Nodes with ultrafast bootstrap values of > 70% are noted by a red circle. If near full-length genomes of skink or gecko viruses were uncovered a nt alignment (black) and the predicted ORFs (orange) of the skink or gecko virus along with a representative complete viral genome from the same family is shown below the respective phylogenetic trees

Fig. 6

Phylogenetic trees of DNA viruses. Maximum likelihood phylogenetic trees of representative viral transcripts containing the replicase, DNA polymerase or nonstructural protein 1 from the families (a) Circoviridae, (b) Adenoviridae and (c) Parvoviridae. Skink and gecko viruses identified in this study are bold while known genera and subfamilies are highlighted. Branches are scaled to the number of amino acid substitutions per site. All phylogenetic trees were midpoint rooted. Nodes with ultrafast bootstrap values of > 70% are noted by a red circle

Fig. 7

Maximum likelihood unrooted phylogenetic tree of representative viral transcripts containing the RdRp from the Bunyavirales. Viruses identified in this study and the termite virus identified by screening the TSA are bolded while families are highlighted. Branches are scaled to the number of amino acid substitutions per site. Nodes with ultrafast bootstrap values of > 70% are noted by a red circle. Below the phylogeny is an alignment of Bunyavirales RdRp amino acid sequences. Conserved Bunyavirales A-E RdRp motifs are shown while the Raukawa gecko associated bunya-like virus and the Termite associated bunya-like virus are bolded