Submitted to: Virology
Publication Type: Peer reviewed journal
Publication Acceptance Date: 8/1/2010
Publication Date: 8/23/2010
Publication URL: dx.doi.org/10.1016/j.virol.2010.08.002
Citation: Stenger, D.C., Sisterson, M.S., French, R.C. 2010. Population genetics of Homalodisca vitripennis reovirus validates timing and limited introduction to California of its invasive insect host, the glassy-winged sharpshooter. Virology. 407:53-59. Interpretive Summary: Factors contributing to establishment and subsequent expansion of an invasive species population in a new ecosystem are complex and only partially understood. Age, structure, and source(s) of populations are critical parameters for describing and understanding invasive species ecology. Most molecular-based data sets for invasive species populations have utilized variation in protein or genome microsatellite markers. Application of nucleotide sequence polymorphism to distinguish populations of invasive species has been applied with limited success because the rate of evolutionary change for multi-cellular organisms is too slow for accrual of a sufficient number of taxonomically informative characters between populations of the same species within the time frame in which modern human activities have led to introduction of invasive species. In contrast to cellular organisms, RNA viruses evolve at a rate which is many log units greater as generation time is brief and replication is error-prone. Therefore, it was hypothesized that genetic diversity within a virus endogenous to an invasive species could serve as a surrogate marker to 1) differentiate recently separated populations, 2) assess population structure for evidence of a genetic bottleneck in an introduced population, 3) assess gene flow between native and introduced populations and, 4) potentially identify source(s) of the introduced population. Recently, a phytoreovirus (Homalodisca vitripennis reovirus, HoVRV) was shown to be present in glassy-winged sharpshooter(GWSS) populations in California and in the native range of the insect. Analysis of HoVRV nucleotide sequence polymorphism revealed a genetic bottleneck in the Californian population and estimates of population age were consistent with the timing of GWSS introduction to California. The results also indicated a lack of gene flow (secondary introductions) among new and old GWSS populations and suggested that source of the California GWSS population could be identified based on HoVRV genotype. Collectively, the data support the contention that nucleotide sequence polymorphism of an endogenous virus can be used as a high resolution surrogate genetic marker system. Application of this new approach will improve basic understanding of invasive species and provide new tools for tracking and management of invasive species.
Technical Abstract: The glassy-winged sharpshooter (GWSS; Homalodisca vitripennis Germar) is an invasive insect introduced to California circa 1989. Native to the southeastern U.S. and northeastern Mexico, GWSS is of economic concern as a vector of the Pierce’s disease bacterium Xylella fastidiosa. Recently, a novel phytoreovirus species (Homalodisca vitripennis reovirus, HoVRV) infecting GWSS was characterized. As viral genomes evolve at a rate many log units greater than their hosts, it was postulated that HoVRV polymorphism may serve as a surrogate marker to discriminate GWSS populations. Complete genome sequences of five Californian and four southeastern HoVRV isolates were evaluated for polymorphism. Pairwise nucleotide sequence diversity was ~10-fold less for HoVRV in California (<0.1%) compared to the southeastern U. S. (~1%). Phylogenetic analysis of each dsRNA segment indicated that the Californian isolates grouped as a monophyletic lineage. In contrast, relative placement of southeastern U. S. isolates varied among dsRNA segments. To sample diversity at single locations, dsRNA segment 11 was sequenced for nine additional isolates each from Riverside, CA and Johnston Co., NC. Whereas 9 of 10 Riverside isolates were identical (the 10th varied at one position), diversity among Johnston Co. isolates approached that of the four completely sequenced southeastern U. S. isolates from locations separated by up to 650 km. Coalescent analyses estimated median time to most recent common ancestor of the Californian population at 11.9 to 26.3 years, depending upon the demographic model employed. Estimates of median molecular clock rate for the Californian population were 1.662 X 10-5 to 5.502 X 10-5 nt substitutions/site/year. Collectively, the results indicate that HoVRV diversity in the native range of GWSS was high relative to a newly established population, and that the Californian population of HoVRV was subjected to a bottleneck coinciding with introduction of GWSS. By proxy, the results suggest that GWSS establishment in California resulted from a limited introduction of a small founding population and that HoVRV genotype could serve to identify source of the Californian GWSS population.