Increasing virulence, but not infectivity, associated with serially emergent virus strains of a fish rhabdovirus

Abstract

Surveillance and genetic typing of field isolates of a fish rhabdovirus, infectious hematopoietic necrosis virus (IHNV), has identified four dominant viral genotypes that were involved in serial viral emergence and displacement events in steelhead trout (Oncorhynchus mykiss) in western North America. To investigate drivers of these landscape-scale events, IHNV isolates designated 007, 111, 110, and 139, representing the four relevant genotypes, were compared for virulence and infectivity in controlled laboratory challenge studies in five relevant steelhead trout populations. Viral virulence was assessed as mortality using lethal dose estimates (LD50), survival kinetics, and proportional hazards analysis. A pattern of increasing virulence for isolates 007, 111, and 110 was consistent in all five host populations tested, and correlated with serial emergence and displacements in the virus-endemic lower Columbia River source region during 1980–2013. The fourth isolate, 139, did not have higher virulence than the previous isolate 110. However, the mG139M genotype displayed a conditional displacement phenotype in that it displaced type mG110M in coastal Washington, but not in the lower Columbia River region, indicating that factors other than evolution of higher viral virulence were involved in some displacement events. Viral infectivity, measured as infectious dose (ID50), did not correlate consistently with virulence or with viral emergence, and showed a narrow range of variation relative to the variation observed in virulence. Comparison among the five steelhead trout populations confirmed variation in resistance to IHNV, but correlations with previous history of virus exposure or with sites of viral emergence varied between IHNV source and sink regions. Overall, this study indicated increasing viral virulence over time as a potential driver for emergence and displacement events in the endemic Lower Columbia River source region where these IHNV genotypes originated, but not in adjacent sink regions.

Spatial and temporal heterogeneity of infectious hematopoietic necrosis virus in Pacific Northwest salmonids

“…However, it occurred slightly earlier, caused fewer juvenile infections, and involved the 539 emergence of only one MD type (mG110M) instead of the three (types mG111M, 540 mG110M, and mG139M) observed in coastal Washington. These three types first 541 emerged in the Columbia basin, and of the three, type mG110M was the most widely and 542 frequently detected (Breyta et al 2013;Breyta et al 2016a). The detection of only type 543 mG110M in coastal Oregon waters might imply that only the most prominent MD type 544 was able to emerge there, or it may be due to regional differences in surveillance, or 545 mechanism(s) that make the fish of Washington and Oregon coasts different, such as 546 different marine migration patterns.…”

Transmission routes maintaining a viral pathogen of steelhead trout within a complex multi‐host assemblage

“…Prevalence of IHNV in juvenile steelhead was greater than 30% across hatchery sites for the majority of the study period, especially after 2002 (Figure ). The dramatic rise from 0% to a peak at 35% in 2002 in juvenile steelhead coincided with the emergence of a specific genotype within the M genogroup, which was shown to be more virulent in steelhead relative to earlier viral forms (Breyta, McKenney, Tesfaye, Ono, & Kurath, ; Breyta, Samson, Blair, Black, & Kurath, ). Juvenile Chinook prevalence has been both lower and more variable, ranging between 0 and a peak at 16% during the study period.…”

“…The IHNV pathogen–host system has a complex disease ecology that involves multiple host species, each with differing susceptibilities and genetically distinct subpopulations, and a rapidly evolving virus covering a wide range of virulence profiles (Breyta et al., ; Breyta, McKenney, et al., ; Brieuc, Purcell, Palmer, & Naish, ; Garver, Conway, & Kurath, ; LaPatra, Fryer, & Rohovec, ; Peñaranda et al., , ; Purcell et al., ). Wild‐ and semi‐cultured hatchery populations are often conspecific within species, and sympatric among species, but their pathogen transmission routes are largely uncharacterized.…”

“…The IHNV pathogen-host system has a complex disease ecology that involves multiple host species, each with differing susceptibilities and genetically distinct subpopulations, and a rapidly evolving virus covering a wide range of virulence profiles (Breyta et al, 2014;Breyta, McKenney, et al, 2016;Brieuc, Purcell, Palmer, & Naish, 2015;Garver, Conway, & Kurath, 2006;LaPatra, Fryer, & Rohovec, 1993;Peñaranda et al, 2009Peñaranda et al, , 2011Purcell et al, 2009) in disease outbreaks can be urgent and thus, analysis and interpretation must be performed despite these caveats (Wasserberg, Osnas, Rolley, & Samuel, 2009). The dataset presented here is comprehensive in its scope, including all regional agencies operating within the study area, and it is unique in analyzing both positive/negative and genetic surveillance records of an aquatic pathogen.…”

“…in juvenile steelhead coincided with the emergence of a specific genotype within the M genogroup, which was shown to be more virulent in steelhead relative to earlier viral forms (Breyta, McKenney, Tesfaye, Ono, & Kurath, 2016;Breyta, Samson, Blair, Black, & Kurath, 2016).…”