Evolution of Bluetongue Virus Serotype 1 in Northern Australia over 30 Years

Abstract

Bluetongue virus serotype 1 (BTV 1) was first isolated in Australia from cattle blood collected in 1979 at Beatrice Hill Farm (BHF), Northern Territory (NT). From long-term surveillance programs (1977 to 2011), 2,487 isolations of 10 BTV serotypes were made. The most frequently isolated serotype was BTV 1 (41%, 1,019) followed by BTV 16 (17.5%, 436) and BTV 20 (14%, 348). In 3 years, no BTVs were isolated, and in 12 years, no BTV 1 was isolated. Seventeen BTV 1 isolates were sequenced and analyzed in comparison with 10 Australian prototype serotypes. BTV 1 showed an episodic pattern of evolutionary change characterized by four distinct periods. Each period consisted primarily of slow genetic drift which was punctuated from time to time by genetic shifts generated by segment reassortment and the introduction of new genome segments. Evidence was found for coevolution of BTV genome segments. Evolutionary dynamics and selection pressure estimates showed strong temporal and clocklike molecular evolutionary dynamics of six Australian BTV genome segments. Bayesian coalescent estimates of mean substitution rates clustered in the range of 3.5 ؋ 10 ؊4 to 5.3 ؋ 10 ؊4 substitutions per site per year. All BTV genome segments evolved under strong purifying (negative) selection, with only three sites identified as under pervasive diversifying (positive) selection. The obligate replication in alternate hosts (insect vector and vertebrate hosts) imposed strong evolutionary constraints. The dominant mechanism generating genetic diversity of BTV 1 at BHF was through the introduction of new viruses and reassortment of genome segments with existing viruses. IMPORTANCE Bluetongue virus (BTV) is the causative agent of bluetongue disease in ruminants.It is a disease of concern globally and is transmitted by biting midges (Culicoides species). Analysis of the evolutionary and selection pressures on BTV 1 at a single surveillance site in northern Australia showed strong temporal and clock-like dynamics. Obligate replication in alternate hosts of insect and vertebrate imposed strong evolutionary constraints, with all BTV genome segments evolving under strong purifying (negative) selection. Generation of genetic diversity of BTV 1 in northern Australia is through genome segment reassortment and the introduction of new serotypes.

Isolation and evolutionary analysis of Australasian topotype of bluetongue virus serotype 4 from India

“…South African reference virus, MLV vaccine strains and some of the European isolates similar to MLV were not included for this analysis. The estimated nucleotide substitution rate was 2.0 × 10 −4 /nucleotide/year (Table ), similar to those estimated for different genomic segments of BTV earlier (Boyle et al., ).…”

Identification and genomic characterization of the first isolate of bluetongue virus serotype 5 detected in Australia

“…From the mid ‐1990s more extensive vector and host screening programs were established globally which drove an exponential growth in virus isolations and the publication of whole genome data for a diverse range of bluetongue viruses (Boyle et al . , ; Maan et al . ; Nomikou et al .…”

“…The collective BTV-5 and BTV-9 sequence data presented in this study and the earlier work of others (Maan et al 2009Rao et al 2012b) have further highlighted the apparent discrepancies between the current internationally recognized serological tests for BTV serotype designation (Huismans & Erasmus 1981;Erasmus 1990) and the range of percentage nucleotide identities that have subsequently been found to exist between the Seg-2 genes of different isolates of the same serotypes. From the mid -1990s more extensive vector and host screening programs were established globally which drove an exponential growth in virus isolations and the publication of whole genome data for a diverse range of bluetongue viruses (Boyle et al 2012(Boyle et al , 2014Maan et al 2015;Nomikou et al 2015). Subsequent thorough interrogation of these data has, in hindsight, suggested analysis by serology alone has potentially interpreted intra-serotype variants isolated between distant geographic regions as 'new' serotypes (Della-Porta et al 1981;Groocock et al 1982) while also potentially failing to detect truly novel BTV strains.…”

“…These studies, alongside more recent evidence, have clearly demonstrated that BTV continually enters northern Australia via infected Culicoides (of varying species) transported on seasonally occurring, prevailing winds from specific island sites within Southeast Asia (Eagles et al 2012(Eagles et al , 2013Bellis et al 2015). However a clear attribution of geographic origin to individual virus isolates can be problematic due to a very high level of gene segment reassortment resulting from mixed infections in both vector and host (Carpi et al 2010;Boyle et al 2012Boyle et al , 2014Nomikou et al 2015). Hence a new serotype incursion may rapidly reassort with genes from an endemic and or another recently introduced exotic strain or even vaccine strains (Br eard et al 2003;Batten et al 2008;Maan et al 2010).…”

Animal Disease Surveillance in the 21st Century: Applications and Robustness of Phylodynamic Methods in Recent U.S. Human-Like H3 Swine Influenza Outbreaks

“…Hence, when analyzing novel sequence datasets, it is critical to combine them with genetically related lineages published in the scientific literature or publicly available databases to reduce the impact of sampling bias as well as improve the reliability and accuracy of posterior evolutionary inferences. Unfortunately, several examples published in the scientific literature used phylodynamic methods on novel sequence datasets while ignoring their published relatives (127)(128)(129). This led to inferring MCC trees with unaccounted phylogenetic relationships such as nodes, branches, and roots.…”