Ron Sinclair

Invasive species can't cover their tracks : using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia

Invasive species are known to cause environmental and economic damage, requiring management by control agencies worldwide. These species often become well established in new environments long before their detection, resulting in a lack of knowledge regarding their history and dynamics. When new invasions are discovered, information regarding the source and pathway of the invasion, and the degree of connectivity with other populations can greatly benefit management strategies. Here we use invasive common starling (Sturnus vulgaris) populations from Australia to demonstrate that genetic techniques can provide this information to aid management, even when applied to highly vagile species over continental scales. Analysis of data from 11 microsatellites in 662 individuals sampled at 17 localities across their introduced range in Australia revealed four populations. One population consisted of all sampling sites from the expansion front in Western Australia, where control efforts are focused. Despite evidence of genetic exchange over both contemporary and historical timescales, gene flow is low between this population and all three more easterly populations. This suggests that localized control of starlings on the expansion front may be an achievable goal and the long‐standing practice of targeting select proximal eastern source populations may be ineffective on its own. However, even with low levels of gene flow, successful control of starlings on the expansion front will require vigilance, and genetic monitoring of this population can provide essential information to managers. The techniques used here are broadly applicable to invasive populations worldwide.

Mitochondrial DNA offers unique insights into invasion history of the common starling.

Mitochondrial DNA (mtDNA) can be a powerful genetic marker for tracing origins and history of invasive populations. Here, we use mtDNA to address questions relevant to the understanding of invasion pathways of common starlings (Sturnus vulgaris) into Western Australia (WA) and discuss the utility of this marker to provide information useful to invasive species management. Mitochondrial sequence data indicate two geographically restricted genetic groups within Australia. Evidence of dispersal from genetically distinct sources outside the sampled range of starlings in Australia suggests increased vigilance by management agencies may be required to prevent further incursions from widely separated localities. Overall, genetic diversity in Australia was lower than in samples from the native range. Within Australia, genetic diversity was lowest in the most recently colonized area in the west, indicating that demographic bottlenecks have occurred in this area. Evidence of restricted dispersal between localities on the edge of the range expansion (ERE) in WA and other Australian sampling localities suggests that localized control within the ERE may be effective in preventing further range expansion. Signatures of spatial and demographic expansion are present in mismatch analyses from sampling localities located at the ERE, but neutrality indices did not support this finding, suggesting that the former may be more sensitive to recent expansion. Additionally, mismatch analyses support the presence of admixture, which is likely to have occurred pre‐introduction. We compare our findings with those from a microsatellite study of the same samples and discuss how the mtDNA analyses used here offer valuable and unique insights into the invasion history of introduced species.

Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics

Infectious diseases can exert a strong influence on the dynamics of host populations, but it remains unclear why such disease-mediated control only occurs under particular environmental conditions. We used 16 years of detailed field data on invasive European rabbits (Oryctolagus cuniculus) in Australia, linked to individual-based stochastic models and Bayesian approximations, to test whether (i) mortality associated with rabbit haemorrhagic disease (RHD) is driven primarily by seasonal matches/mismatches between demographic rates and epidemiological dynamics and (ii) delayed infection (arising from insusceptibility and maternal antibodies in juveniles) are important factors in determining disease severity and local population persistence of rabbits. We found that both the timing of reproduction and exposure to viruses drove recurrent seasonal epidemics of RHD. Protection conferred by insusceptibility and maternal antibodies controlled seasonal disease outbreaks by delaying infection; this could have also allowed escape from disease. The persistence of local populations was a stochastic outcome of recovery rates from both RHD and myxomatosis. If susceptibility to RHD is delayed, myxomatosis will have a pronounced effect on population extirpation when the two viruses coexist. This has important implications for wildlife management, because it is likely that such seasonal interplay and disease dynamics has a strong effect on long-term population viability for many species.

Does a benign calicivirus reduce the effectiveness of rabbit haemorrhagic disease virus (RHDV) in Australia? Experimental evidence from field releases of RHDV on bait

Context. European rabbits are serious environmental and agricultural pests throughout their range in Australia. Rabbit haemorrhagic disease virus (RHDV) greatly reduced rabbit numbers in arid central Australia but had less impact in cooler, higher-rainfall areas. RHDV-like benign caliciviruses (bCVs) have been implicated in limiting the impact of RHDV in the higher-rainfall regions of Australia and also in Europe. Aims. Experimental releases of RHDV on bait were tested as a means of initiating disease outbreaks. Serological evidence of antibodies to bCVs was examined to determine whether they reduce mortality rates and/or spread of the released RHDV, and how that might influence the effectiveness of future RHDV releases for rabbit management. Methods. Four experimental releases were conducted in high-rainfall and coastal regions of southern Australia. Virus activity was implied from recapture rates and serological changes in marked rabbits, and genetic sequencing of virus recovered from dead rabbits. Changes in rabbit abundance were estimated from spotlight transect counts. Key results. Release of RHDV on bait produced disease outbreaks that challenged almost all animals within the general release area and spread up to 4 km beyond the release sites. Recapture rates were high in marked rabbits that possessed antibodies from previous exposure to RHDV and extremely low amongst rabbits that lacked any detectable antibodies. Rabbits carrying antibodies classified as being due to previous infection with bCVs had recapture rates that were dependent on circulating antibody titre and were ~55% of recapture rates in rabbits with clear antibodies to RHDV. Conclusions. This is the first quantified evidence that antibodies produced against bCVs provide significant protection against RHD outbreaks in field populations of rabbits. Implications. bCVs can greatly reduce the impact of RHDV on wild-rabbit populations in Australia and presumably elsewhere. RHDV can be effectively released on bait although further releases are likely to be of minor or inconsistent benefit for controlling rabbit numbers where bCVs are common.

Rabbit haemorrhagic disease: virus persistence and adaptation in Australia.

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 Australias remaining natural biodiversity.

Efficacy of zinc phosphide, strychnine and chlorpyrifos as rodenticides for the control of house mice in South Australian cereal crops

Replicated field trials were conducted to compare the efficacy of zinc phosphide, strychnine and chlorpyrifos for the control of house mice (Mus domesticus) infesting recently sown wheat crops in South Australia. Bait was prepared using whole-wheat grain or grain-based pellets and broadcast into the crops at 1 kg ha–1. Treatment with zinc phosphide reduced mouse numbers by 98%. Two treatments with strychnine baits, applied 11 days apart, also reduced mouse numbers by 98% with no evidence of bait aversion in mice that survived the initial treatment. On the basis of these and other published results, zinc phosphide is considered an effective alternative to strychnine for control of house mice in cereal crops. Chlorpyrifos baits reduced mouse numbers by less than 10%. The trial began too late in the growing season to prevent substantial mouse damage to seed grain and seedlings. The number of seedlings established at treatment time one month after sowing explained 84% of variation in crop yield. Mouse damage is estimated to have reduced yield by more than 0.5 t ha–1 or 15% of potential yield and cost the grower more than

Selection on Mitochondrial Variants Occurs between and within Individuals in an Expanding Invasion

30 000 in lost production from the 300-ha study area.

Longevity record for a wild European rabbit (Oryctolagus cuniculus) from South Australia

Mitochondria are critical for life, yet their underlying evolutionary biology is poorly understood. In particular, little is known about interaction between two levels of evolution: between individuals and within individuals (competition between cells, mitochondria or mitochondrial DNA molecules). Rapid evolution is suspected to occur frequently in mitochondrial DNA, whose maternal inheritance predisposes advantageous mutations to sweep rapidly though populations. Rapid evolution is also predicted in response to changed selection regimes after species invasion or removal of pathogens or competitors. Here, using empirical and simulated data from a model invasive bird species, we provide the first demonstration of rapid selection on the mitochondrial genome within individuals in the wild. Further, we show differences in mitochondrial DNA copy number associated with competing genetic variants, which may provide a mechanism for selection. We provide evidence for three rarely documented phenomena: selection associated with mitochondrial DNA abundance, selection on the mitochondrial control region, and contemporary selection during invasion.

High adaptive variability and virus-driven selection on major histocompatibility complex (MHC) genes in invasive wild rabbits in Australia

A population of European rabbits (Oryctolagus cuniculus) has been monitored since November 1996 through mark–recapture as part of a longitudinal epidemiological study into two Australian rabbit biocontrol agents, rabbit haemorrhagic disease (RHD) and myxomatosis. A female rabbit, first captured as a subadult in late November 1999, was recaptured 18 times before its final capture at the end of February 2007. The longevity of this rabbit, being from its calculated birth date to the date it was last captured, was 7.6 years. A review of the literature indicates this to be the longest lifespan recorded for a European rabbit in the wild.

RHDV2 overcoming RHDV immunity in wild rabbits (Oryctolagus cuniculus) in Australia

The rabbit haemorrhagic disease virus (RHDV) was imported into Australia in 1995 as a biocontrol agent to manage one of the most successful and devastating invasive species, the European rabbit (Oryctolagus cuniculus cuniculus). During the first disease outbreaks, RHDV caused mortality rates of up to 97% and reduced Australian rabbit numbers to very low levels. However, recently increased genetic resistance to RHDV and strong population growth has been reported. Major histocompatibility complex (MHC) class I immune genes are important for immune responses against viruses, and a high MHC variability is thought to be crucial in adaptive processes under pathogen-driven selection. We asked whether strong population bottlenecks and presumed genetic drift would have led to low MHC variability in wild Australian rabbits, and if the retained MHC variability was enough to explain the increased resistance against RHD. Despite the past bottlenecks we found a relatively high number of MHC class I sequences distributed over 2–4 loci. We identified positive selection on putative antigen-binding sites of the MHC. We detected evidence for RHDV-driven selection as one MHC supertype was negatively associated with RHD survival, fitting expectations of frequency-dependent selection. Gene duplication and pathogen-driven selection are possible (and likely) mechanisms that maintained the adaptive potential of MHC genes in Australian rabbits. Our findings not only contribute to a better understanding of the evolution of invasive species, they are also important in the light of planned future rabbit biocontrol in Australia.