Evolutionary trajectory of white spot syndrome virus (WSSV) genome shrinkage during spread in Asia.

Mark P Zwart,Anthony R Fooks,Just M Vlak,Bui Thi Minh Dieu,Lia Hemerik

doi:10.1371/journal.pone.0013400

Abstract

BackgroundWhite spot syndrome virus (WSSV) is the sole member of the novel Nimaviridae family, and the source of major economic problems in shrimp aquaculture. WSSV appears to have rapidly spread worldwide after the first reported outbreak in the early 1990s. Genomic deletions of various sizes occur at two loci in the WSSV genome, the ORF14/15 and ORF23/24 variable regions, and these have been used as molecular markers to study patterns of viral spread over space and time. We describe the dynamics underlying the process of WSSV genome shrinkage using empirical data and a simple mathematical model.Methodology/Principal FindingsWe genotyped new WSSV isolates from five Asian countries, and analyzed this information together with published data. Genome size appears to stabilize over time, and deletion size in the ORF23/24 variable region was significantly related to the time of the first WSSV outbreak in a particular country. Parameter estimates derived from fitting a simple mathematical model of genome shrinkage to the data support a geometric progression (k<1) of the genomic deletions, with k = 0.371±0.150.Conclusions/SignificanceThe data suggest that the rate of genome shrinkage decreases over time before attenuating. Bioassay data provided support for a link between genome size and WSSV fitness in an aquaculture setting. Differences in genomic deletions between geographic WSSV isolates suggest that WSSV spread did not follow a smooth pattern of geographic radiation, suggesting spread of WSSV over long distances by commercial activities. We discuss two hypotheses for genome shrinkage, an adaptive and a neutral one. We argue in favor of the adaptive hypothesis, given that there is support for a link between WSSV genome size and fitness.

Highlights

White spot syndrome virus (WSSV) was first reported in shrimp aquaculture in Taiwan in the early 1990s [1]
Description of WSSV isolates WSSV isolates originating from a single host were collected from ponds distributed over five different Asian countries (Fig. 1, Table 1)
Model of WSSV genome shrinkage We develop a simple mathematical model to describe the dynamics of WSSV genome shrinkage, and in particular to identify whether the rate of genome shrinkage is constant over time

Summary

Introduction

White spot syndrome virus (WSSV) was first reported in shrimp aquaculture in Taiwan in the early 1990s [1]. The most significant genotypic changes during WSSV spread in Asia appear to be two genomic deletions, in the ORF14/15 and ORF23/24 variable regions [8,9,10,11,12]. White spot syndrome virus (WSSV) is the sole member of the novel Nimaviridae family, and the source of major economic problems in shrimp aquaculture. Genomic deletions of various sizes occur at two loci in the WSSV genome, the ORF14/15 and ORF23/24 variable regions, and these have been used as molecular markers to study patterns of viral spread over space and time. We describe the dynamics underlying the process of WSSV genome shrinkage using empirical data and a simple mathematical model

Methods

Results

Conclusion