Abstract
The diversity of viruses probably exceeds biodiversity of eukaryotes, but little is known about the origin and emergence of novel virus species. Experimentation and disease outbreak investigations have allowed the characterization of rapid molecular virus adaptation. However, the processes leading to the establishment of functionally distinct virus taxa in nature remain obscure. Here, we demonstrate that incipient speciation in a natural host species has generated distinct ecological niches leading to adaptive isolation in an RNA virus. We found a very strong association between the distributions of two major phylogenetic clades in Tula orthohantavirus (TULV) and the rodent host lineages in a natural hybrid zone of the European common vole (Microtus arvalis). The spatial transition between the virus clades in replicated geographic clines is at least eight times narrower than between the hybridizing host lineages. This suggests a strong barrier for effective virus transmission despite frequent dispersal and gene flow among local host populations, and translates to a complete turnover of the adaptive background of TULV within a few hundred meters in the open, unobstructed landscape. Genetic differences between TULV clades are homogenously distributed in the genomes and mostly synonymous (93.1%), except for a cluster of nonsynonymous changes in the 5′ region of the viral envelope glycoprotein gene, potentially involved in host-driven isolation. Evolutionary relationships between TULV clades indicate an emergence of these viruses through rapid differential adaptation to the previously diverged host lineages that resulted in levels of ecological isolation exceeding the progress of speciation in their vertebrate hosts.
Highlights
Evolutionary diversification has resulted in a myriad of virus species [1,2], but—despite their great importance as agents of diseases of humans, crops, and livestock—our understanding of their functional partitioning and distribution across hosts is strongly limited
Phylogenetic analyses with reference sequences spanning the known Tula orthohantavirus (TULV) distribution assigned them to the two most recently diverged virus clades (Fig 2). We termed these TULV clades Central South (TULV-CEN.S) and Eastern South (TULV-EST.S) given their spatial association with different common vole host lineages and their respective geographic distribution relative to other, more diverged TULV clades in the northern range of the same host lineages (Fig 2)
Sequences from the western parts of both transects (n = 111) were all most closely related with TULV strains found within the geographic distribution of the Central host lineage, whereas sequences from the eastern parts (n = 195) were all most similar to strains associated with the Eastern host lineage ([12]; Figs 1 and 2)
Summary
Evolutionary diversification has resulted in a myriad of virus species [1,2], but—despite their great importance as agents of diseases of humans, crops, and livestock—our understanding of their functional partitioning and distribution across hosts is strongly limited. The evolution of novel viral features and their molecular basis is best understood in laboratory and medical settings in which new virus types can arise quickly through genetic adaptation to specific host environments [3,4] Such adaptive processes may lead to ecological isolation of specialized virus types due to their reduced ability to use alternative hosts [5]. Heterogeneity in the environment of a virus population, e.g., through the simultaneous presence of different hosts, can drive differential adaptation to divergent ecological niches resulting in “sympatric speciation” [6] These principles of virus diversification have been demonstrated under controlled experimental conditions, our knowledge of the mechanisms that generate and maintain functionally distinct viruses in nature is very scarce [7]. The ecological conditions that promote virus divergence and potentially lead to the emergence of new virus species in nature are generally unclear
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