Rabbit haemorrhagic disease: virus persistence and adaptation in Australia

Abstract

In Australia, the rabbit haemorrhagic disease virus (RHDV) has been used since 1996 to reduce numbers of introduced European rabbits (Oryctolagus cuniculus) which have a devastating impact on the native Australian environment. RHDV causes regular, short disease outbreaks, but little is known about how the virus persists and survives between epidemics. We examined the initial spread of RHDV to show that even upon its initial spread, the virus circulated continuously on a regional scale rather than persisting at a local population level and that Australian rabbit populations are highly interconnected by virus-carrying flying vectors. Sequencing data obtained from a single rabbit population showed that the viruses that caused an epidemic each year seldom bore close genetic resemblance to those present in previous years. Together, these data suggest that RHDV survives in the Australian environment through its ability to spread amongst rabbit subpopulations. This is consistent with modelling results that indicated that in a large interconnected rabbit meta-population, RHDV should maintain high virulence, cause short, strong disease outbreaks but show low persistence in any given subpopulation. This new epidemiological framework is important for understanding virus-host co-evolution and future disease management options of pest species to secure Australia's remaining natural biodiversity.

Keywords: Oryctolagus cuniculus; adaptation; calicivirus; rabbit haemorrhagic disease virus epidemiology.

Figure 1

Map of the locations and estimated day of virus arrival after the escape of rabbit haemorrhagic disease virus (RHDV) from Wardang Island and during its spread through South Australia in 1995.

Figure 2

The counts of new rabbit haemorrhagic disease (RHD) outbreaks in South Australia in 1995/96. An outbreak was confirmed through the presence RHD viral RNA in recovered rabbit carcasses (see Kovaliski 1998). It shows that RHD was always active somewhere on a regional scale. The first record is the appearance of a dead rabbit outside the quarantine area on Wardang Island in September 1995.

Figure 3

Map of presently known Southern Australian rabbit populations. Combined data from Rabbit Scan and databases on the first years of spread of rabbit haemorrhagic disease virus (RHDV). Each black dot represents a recorded rabbit population.

Figure 4

ML tree of rabbit haemorrhagic disease virus (RHDV) sequences (GenBank accession numbers) obtained from rabbits found dead at the Turretfield site (South Australia) between 1999 and 2011. Most variants cluster according to the year. The tree was rooted with the Australian RHDV inoculums strain that was manufactured from Czech CAPM-V351. It has been used since 1996 for biocontrol purpose and was in the same year deliberately released in the Turretfield population. Later, blood analyses showed, however, that the Turretfield population had already experienced a previous virus contact (most likely in 1995 when the virus escaped from an experimental site on Wardang Island, South Australia). Numbers at nodes represent bootstrap support (1000 iterations).