Evolutionary trajectory of fish Piscine novirhabdovirus (=Viral Hemorrhagic Septicemia Virus) across its Laurentian Great Lakes history: Spatial and temporal diversification

Authors: STEPIEN, CAROL - University Of Toledo; NINER, MEGAN - University Of Toledo

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2020
Publication Date: N/A
Citation: N/A
DOI: https://doi.org/10.1002/ece3.6611

Interpretive Summary: Finfish Viral Hemorrhagic Septicemia Virus (VHSV) first appeared in the Great Lakes with large outbreaks from 2005 to 2006, as a new sub-group (called VHSV-IVb) that killed >30 fish species. Surveillance continues, but there have been no reports of outbreaks or positives from 2018-2020. Using various genetics approaches while surveilling the virus, we evaluated the evolutionary trajectory of the VHSV G-gene sequence variation. Results show continued diversification of the VHSV G-gene into many variants, which appear to have remained geographically constrained to the Great Lakes region and surrounding areas. Continuing diversification of the VHSV-IVb pathogen likely allowed the virus to persist at low levels in resident fish populations, and may facilitate its potential for further and future spread to new water bodies in a multispecies pattern.

Technical Abstract: Piscine novirhabdovirus = Viral Hemorrhagic Septicemia Virus (VHSV) first appeared in the Laurentian Great Lakes with large outbreaks from 2005 to 2006, as a new and novel RNA rhabdovirus subgenogroup (IVb) that killed >30 fish species. Interlude periods punctuated smaller more localized outbreaks in 2007, 2010, and 2017, although some fishes tested positive in the intervals. There have not been reports of outbreaks or positives from 2018, 2019, or 2020. Here, we employ a combined population genetics and phylogenetic approach to evaluate spatial and temporal evolutionary trajectory on its G-gene sequence variation, in comparison with wholegenome sequences (11,083 bp) from a subset of 44 individual isolates (including 40 newly sequenced ones). Our results show that IVb (N = 184 individual fish isolates) diversified into 36 G-gene haplotypes from 2003 to 2017, stemming from two originals (“a” and “b”). G-gene haplotypes “a” and “b” differed by just one synonymous single-nucleotide polymorphism (SNP) substitution, remained the most abundant until 2011, then disappeared. Group “a” descendants (14 haplotypes) remained most prevalent in the Upper and Central Great Lakes, with eight (51%) having nonsynonymous substitutions. Group “b” descendants primarily have occurred in the Lower Great Lakes, including 22 haplotypes, of which 15 (68%) contained nonsynonymous changes. Evolutionary patterns of the whole-genome sequences (which had 34 haplotypes among 44 isolates) appear congruent with those from the G-gene. Virus populations significantly diverged among the Upper, Central, and Lower Great Lakes, diversifying over time. Spatial divergence was apparent in the overall patterns of nucleotide substitutions, while amino acid changes increased temporally. VHSV-IVb thus significantly differentiated across its less than two decades in the Great Lakes, accompanied by declining outbreaks and virulence. Continuing diversification likely allowed the virus to persist at low levels in resident fish populations, and may facilitate its potential for further and future spread to new habitats and nonacclimated hosts.