Spatial patterns of neutral and functional genetic variations reveal patterns of local adaptation in raccoon (Procyon lotor) populations exposed to raccoon rabies.

Local adaptation is necessary for population survival and depends on the interplay between responses to selective forces and demographic processes that introduce or retain adaptive and maladaptive attributes. Host-parasite systems are dynamic, varying in space and time, where both host and parasites must adapt to their ever-changing environment in order to survive. We investigated patterns of local adaptation in raccoon populations with varying temporal exposure to the raccoon rabies virus (RRV). RRV infects approximately 85% of the population when epizootic and has been presumed to be completely lethal once contracted; however, disease challenge experiments and varying spatial patterns of RRV spread suggest some level of immunity may exist. We first assessed patterns of local adaptation in raccoon populations along the eastern seaboard of North America by contrasting spatial patterns of neutral (microsatellite loci) and functional, major histocompatibility complex (MHC) genetic diversity and structure. We explored variation of MHC allele frequencies in the light of temporal population exposure to RRV (0-60 years) and specific RRV strains in infected raccoons. Our results revealed high levels of MHC variation (66 DRB exon 2 alleles) and pronounced genetic structure relative to neutral microsatellite loci, indicative of local adaptation. We found a positive association linking MHC genetic diversity and temporal RRV exposure, but no association with susceptibility and resistance to RRV strains. These results have implications for landscape epidemiology studies seeking to predict the spread of RRV and present an example of how population demographics influence the degree to which populations adapt to local selective pressures.

Understanding effects of barriers on the spread and control of rabies.

This chapter reviews the evidence for the impact of natural and anthropogenic barriers on the spread of rabies using evidence mainly drawn from the epidemics of fox and raccoon variant rabies virus over the past 60 years in North America. Those barriers have both directed and inhibited the spread of rabies and, at a regional scale, have been integrated with rabies control efforts in North America. Few studies have been done, however, to examine how the texture (grain) and configuration of the habitat at finer scales affect rabies control, particularly the massive oral vaccination campaigns in operation along the Atlantic coast and southeastern Canada (Ontario, Québec, New Brunswick). To explore these questions, the authors used stochastic simulation. The model of choice was the Ontario Rabies Model (ORM) adapted for use on the high performance computing resources network in Québec (RQCHP-Réseau québécois de calcul de haute performance; http://rqchp.qc.ca). The combination of the ORM and RQCHP allowed us to run many thousands of experiments to explore interactions between nine landscape grain/configuration combinations and vaccination barriers with varying widths and immunity levels. Our results show that breaches of vaccine barriers increase as the grain size of the landscape increases and as the landscape becomes more structured. We caution that mid levels of vaccination can be counterproductive resulting in rabies persistence rather than control. We also note that our model/computing system has the flexibility and capacity to explore a wide range of questions pertinent to improving the efficacy of rabies control.

Landscape modelling spatial bottlenecks: implications for raccoon rabies disease spread.

A landscape genetic simulation modelling approach is used to understand factors affecting raccoon rabies disease spread in southern Ontario, Canada. Using the Ontario Rabies Model, we test the hypothesis that landscape configuration (shape of available habitat) affects dispersal, as indicated by genetic structuring. We simulated range expansions of raccoons from New York into vacant landscapes in Ontario, in two areas that differed by the presence or absence of a landscape constriction. Our results provide theoretical evidence that landscape constriction acts as a vicariant bottleneck. We discuss implications for raccoon rabies spread.

Differential permeability of rivers to raccoon gene flow corresponds to rabies incidence in Ontario, Canada.

The correlation of landscape features with genetic discontinuities reveals barriers to dispersal that can contribute to understanding present and future spread of wildlife diseases. This knowledge can then be used for targeting control efforts. The impact of natural barriers on raccoon dispersal was assessed through genetic analysis of samples from two regions, Niagara (N = 666) and St. Lawrence (N = 802). These areas are transected by major rivers and are at the northern front of a raccoon rabies epizootic. Genetic clusters were identified in each region using Bayesian clustering algorithms. In the Niagara region, two clusters were identified corresponding to either side of the Niagara River. For the St. Lawrence region, spatially congruent clusters were not identified, despite the presence of the intervening St. Lawrence River. These genetic data are consistent with raccoon rabies incidence data where rabies has been detected across the St. Lawrence River in Ontario while no cases have been detected in Ontario across the Niagara River. This is despite expectations of rabies incidence in Niagara before the St. Lawrence based on the progression of rabies from New York. The results from the two regions suggest different permeabilities to raccoons between New York and Ontario that may be attributed to the rivers. However, other factors have also been explored that could contribute to this difference between these study sites including the shape of the landscape and resource distribution.

Assessing a landscape barrier using genetic simulation modelling: implications for raccoon rabies management.

Landscape barriers influence movement patterns of animals, which in turn, affect spatio-temporal spread of infectious wildlife disease. We compare genetic data from computer simulations to those acquired from field samples to measure the effect of a landscape barrier on raccoon (Procyon lotor) movement, enabling risk assessment of raccoon rabies disease spread across the Niagara River from New York State into Ontario, an area currently uninfected by rabies. An individual-based spatially explicit model is used to simulate the expansion of a raccoon population to cross the Niagara River, for different permeabilities of the river to raccoon crossings. Since the model records individual raccoon genetics, the genetic population structure of neutral mitochondrial DNA haplotypes are characterised in the expanding population, every 25 years, using a genetic distance measure, phi ST, Mantel tests and a gene diversity measure. The river barrier effect is assessed by comparing genetic measures computed from model outputs to those calculated from 166 raccoons recently sampled from the same landscape. The "best fit" between modelled scenarios and field data indicate the river prevents 50% of attempts to cross the river. Founder effects dominated the colonizing genetic population structure, and, as the river barrier effect increased, its genetic diversity decreased. Using gene flow to calibrate the effect of the river as a barrier to movement provides an estimate of the effect of a river in reducing the likelihood of cross-river infection. Including individual genetic markers in simulation modelling benefits investigations of disease spread and control.

Fishers, farms, and forests in eastern North America.

The fisher (Martes pennanti) has recently recovered from historic extirpations across much of its geographic range. There are at least five explanations for the recovery of the fisher, including changes in the amount of habitat, the suitability of habitat, trapping pressure, societal attitudes toward predators, and climate. We evaluated a recovering fisher population in Ontario to test two conditions we viewed as necessary to support the hypothesis that fisher populations have increased due to an increase in the amount of forested land. First, we tested whether the amount of forested land has increased. Second, we tested whether contemporary fisher abundance (and therefore habitat quality) was related to the amount of forest. Topographic maps showed that the proportion of forested land in the study area had increased by 1.9% per decade since 1934 and 3.3% per decade since 1959, likely as a result of land conversion from agricultural uses. Overall the proportion of the study area that was forested increased from 29% to 40% during 1934 to 1995. Census data from the region indicated that there had been a decline in the amount of land area being farmed during the last 50 years. Recent livetrapping data showed that fisher abundance was positively related to the proportion of landscapes that were forested. Based on our results, we could not reject the hypothesis that an increase in the amount of forested land has contributed to the recovery of fisher populations.