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1. The prevention and management of transmissible diseases hinges upon understanding host dispersal because it influences distribution of wildlife, affects the rate of disease transmission, and alters the spatial distribution of infection. The relationship between host dispersal and chronic wasting disease (CWD) in cervids is of interest because potential interspecies transmission of fatal prion diseases creates serious risks for wildlife, domestic species, and humans.
2. We used molecular techniques to examine dispersal in a population of Illinois white-tailed deer Odocoileus virginianus. Sampled individuals inhabited areas with confirmed cases of CWD, a transmissible prion disease of cervids, with additional sampling in uninfected locations. We genotyped 1410 deer harvested through CWD surveillance using 10 microsatellites and measured gene flow, determined population structure and quantified gender-specific differences in dispersal. Additionally we used spatial autocorrelation and parentage assignments to examine individual movements.
3. Female deer demonstrated philopatry as evidenced by higher levels of genetic structure, positive spatial autocorrelation and maternity assignments within one home range.
4. Male deer were less genetically structured and frequently exchanged genes across >100 km.
5. Synthesis and applications. Dispersal contributes to the spread of wildlife diseases. Therefore, knowledge of wildlife movement patterns can enhance the efficacy of disease control programmes. Our findings show that samples collected for disease surveillance are useful for measuring gene flow and inferring dispersal in white-tailed deer. High genetic admixture indicates males disperse regardless of landscape features. In contrast, distinct clustering of females demonstrates localized dispersal and philopatry. Taken together, results suggest that CWD surveillance and culling of males should be broadly expanded after an outbreak. Furthermore, surveillance of hunter-harvested deer can be used to identify locales in which CWD occurs, and this information should be used to focus culling efforts on females within genetically defined clusters (‘matriarchal groups’). Removal of matriarchal groups at those locations will reduce horizontal transmission more than widely distributed population reductions.
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- Materials and methods
Dispersal has long been considered the foundation of ecology (Andrewartha & Birch 1954) and is equally important to epidemiology as it determines interconnectivity among animals, humans, and zoonotic pathogens. As wildlife hosts and vectors move through the landscape they influence the rate of disease spread, spatial extent of infection and likelihood of new outbreaks (Cullingham et al. 2008). Because it impacts spatial and temporal disease dynamics, dispersal must be carefully considered when implementing disease control strategies as it will influence the effectiveness of management programmes. Interconnections between disease and dispersal can make wildlife management difficult particularly when interspecies contacts are frequent in landscapes where urbanization, agriculture, and wildlife habitats overlap (Bennett, Radford & Haslem 2006).
An understanding of dispersal in white-tailed deer Odocoileus virginianus (Zimmermann, 1780) is critical for the management of chronic wasting disease (CWD), a prion disease of cervids. Chronic wasting disease in North America has caused economic losses associated with reduced hunting, depopulation of farmed cervids and loss of international markets (Arnot et al. 2009). Outbreaks of CWD in the U.S. have occurred near cities and agricultural farms which can create opportunities for zoonotic prion disease transmission (Macdonald & Laurenson 2006). While CWD associated prion disease has not been documented in humans, transmission of bovine spongiform encephalopathy (BSE) as variant Creutzfeldt–Jakob disease (vCJD) and experimental infection of cattle with CWD suggest that species barriers for prion diseases are limited (Belay et al. 2004). Chronic wasting disease management is therefore essential to protect wildlife resources and minimize risks to humans and livestock. As a result several states have implemented disease surveillance and management plans in captive and wild cervids. Wildlife managers need information on deer movement to determine the risk of prion spread among habitats and into urban and agricultural landscapes in order to implement the most effective strategies for disease control.
Radiotelemetry studies have suggested that dispersal is male-biased with fawns and females demonstrating philopatry (Marchinton & Hirth 1984). Dispersal distances for radiocollared deer in Illinois ranged from 28–44 km and most deer did not disperse >50 km (Nixon et al. 2007). Unfortunately, telemetry studies are labour intense and limited by sample size, study area, and the difficulties of trapping a random sample (Koenig, Van Vuren & Hooge 1996). Recently, genetic measures of dispersal have gained popularity because population-level movements can be examined across entire landscapes to provide essential information for ecosystem-based management plans. Habitat connectivity can be assessed by quantifying gene flow among populations (Berry, Tocher & Sarre 2004). Furthermore, Bayesian assignment tests (Pritchard, Stephens & Donnelly 2000) and parentage analyses (Kalinowski, Taper & Marshall 2007) can assign individuals to demes, and quantify geographic distances between parent-offspring pairs.
We applied genetic methods to assess movements of white-tailed deer, a species that has been intensely managed and hunted for decades (Calhoun & Loomis 1974). In this study we utilized tissues from deer harvested through CWD surveillance and management programmes aimed at reducing further CWD transmission. Our goals were to:
Examine population-level movements and test for male-biased dispersal by quantifying gene flow among populations.
Identify genetic clusters and determine admixture with individual-based Bayesian assignment tests.
Examine dispersal using spatial autocorrelation and parentage assignment.
Evaluate the feasibility of indirectly measuring dispersal using samples collected through wildlife management programmes.
Our study provides a rare opportunity to assess indirect measures of movement in the context of wildlife disease management. Our genetic evaluation of behaviour also allows comparison to previous studies of deer dispersal employing direct measures, thus broadening our understanding of deer ecology and contributing to adaptive management of wildlife diseases.
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Predicting the spread of wildlife disease and identifying areas at high risk for infection hinges upon quantification of animal dispersal (Castillo-Chavez & Yakubu 2001). Many ecological and epidemiological studies have focused on cervids because their elevated mobility can rapidly spread disease to new locations (Conner et al. 2008; Blanchong et al. 2008). Furthermore, cervids frequently cohabitate with livestock and also reside in urban areas, thus providing opportunities for zoonotic disease transmission (Dazak, Cunningham & Hyatt 2000). Utilizing genetic samples obtained through disease surveillance programmes, we quantified deer movements in areas infected with CWD. Admixture proportions calculated from assignment tests suggest that long-distance dispersal (≤300 km) occurs and that CWD could spread across the landscape through occasional long-distance movements. These findings implicate long-distance dispersers as potential carriers of disease, and are consistent with the current distribution of CWD in Illinois where isolated cases are detected >100 km from the outbreak focus near Rockford (Illinois Department of Natural Resources 2008; Fig. 1).
Our genetic analyses suggest that males have potential to spread disease because of their extensive local dispersal (<100 km). More importantly, the genetic structure of males suggests that a substantial proportion of the population disperse >100 km, which in turn, implicates them as vehicles for long-distance transmission. Dispersing males often form bachelor groups, and infectious prions could be transmitted through saliva during male grooming behaviours (Marchinton & Hirth 1984; Mathiason et al. 2006). Alternatively, sick animals can shed prions into the environment and contaminate the areas they traverse (Williams & Miller 2002). During the rut, male deer often scrape the ground and then urinate, or rub branches with their antlers to mark territories (Marchinton & Hirth 1984). Urine (Gonzalez-Romero et al. 2008) and antler velvet (Angers et al. 2009) can contain infectious prions. These behaviors could be facilitating environmental transmission of CWD because multiple deer visit rubs and scrapes within a season (Marchinton & Hirth 1984).
In contrast to males, spatial autocorrelation and parentage assignments indicate that females are philopatric, suggesting that they are more likely to spread diseases locally within their cohort. Thus Grear et al. (2010) reached a similar conclusion for female deer in Wisconsin. Although, these authors were unable to observe spatial autocorrelation at more than 3·2 km, possibly because of Hardy–Weinburg disequilibrium or low sampling density. Nonetheless, similar outcomes from geographically different areas strengthen this conclusion. Social contact among female relatives in close proximity is associated with elevated risk of CWD, because of increased horizontal transmission or increased environmental exposure to CWD within shared natal ranges (Grear et al. 2010).
Sites near agricultural habitats (such as those to the north-east of the city) were generally highly admixed for both male and female deer and corresponded to the areas of initial CWD outbreak and early rapid spread of disease. Furthermore, admixture between deer from northern Illinois and RAP was higher than admixture between northern Illinois and GTA. Although the distance to RAP is greater, the intervening landscape to the south is more intensively agricultural, in contrast to the intervening landscape to GTA which is more heavily forested. Genetic exchange is elevated to the south consistent with the tendency for southerly spread of CWD. Though preliminary, disease spread appears to parallel gene flow, and our results support the concept of CWD transmission following dispersal of infected animals.
Uninfected deer populations experiencing high genetic admixture with infected locations represent areas at high risk for future infection unless dispersal is unidirectional away from uninfected locations. Such locations, for example DuP in this study, are of particular interest for further research, both to monitor for future infection and to understand processes that have enabled them to remain uninfected despite high admixture with infected areas.
Our data show that genetic structure in deer is shaped by differences in gender-specific dispersal with male-biased dispersal evident in FST values and spatial autocorrelation patterns. Overall males were genetically homogeneous locally (<100 km) and slightly admixed regionally (<300 km), which in turn demonstrates their enhanced dispersal capabilities. In contrast, females were genetically structured locally (<48 km) according to spatial autocorrelation and contingency tests, indicating reduced connectivity among philopatric subpopulations. Collectively, female philopatry is responsible for genetic structuring at distances <100 km whereas male dispersal is primarily responsible for connectivity among habitats separated by ≤300 km.
Our results also indicate that males and females respond differently to habitat fragmentation induced by urbanization, suggesting disease spread into urbanized areas may be gender-based. We detected barriers for female dispersal between geographically proximate study sites using FST and contingency tests. Female structure corresponded to habitat isolation induced by an interstate freeway (I-39: a 4 lane, divided and fence roadway with limited vehicle access) built in the 1980s. However, males reflected homogeneity of allele frequencies at these same study sites (Fig. 3) suggesting the freeway does not limit connectivity for males at this location. Furthermore, the panmictic population quantified in northern Illinois implies that males disperse freely within this 6900 km2 area, apparently undeterred by Rockford, the third largest city in Illinois. Females, on the other hand, were inhibited by Rockford, as female gene flow was reduced and separate populations were detected on each side of this urbanized area.
Our results for females contradict those from a deer study in Wisconsin (Blanchong et al. 2008) where female dispersal was not deterred by roads. However, the road was a highway (US18/151: a divided 4-lane road, but with high vehicle access) which presents less of a physical barrier than an interstate freeway. Our findings are consistent with Epps et al. (2005) who showed that gene flow in big horn sheep Ovis canadensis was truncated by interstate highways while Pérez-Espona et al. (2008) found that red deer movement was deterred by high traffic roads. These anthropogenic alterations of wildlife habitats promoted genetic structuring over a period of 20–40 years (Epps et al. 2005).
Dispersal, as quantified in our study through gene flow, did not always agree with direct estimates of dispersal for Illinois deer. We did not detect positive autocorrelation in female yearlings, suggesting that they had dispersed at the time of sampling. This is in contrast to other studies of female deer reporting philopatry (Hawkins & Klimstra 1970). However, in our study only 69 yearling females were sampled, and this number is low compared to other studies (Hawkins & Klimstra 1970; N = 79). Additionally, STRUCTURE results showed that ongoing genetic exchange occurs at distances >200 km (Fig. 3), even though long-distance dispersals (c. 200 km) are rarely documented in ecological studies of deer (Brinkman et al. 2005; Oyer, Matthews & Skuld 2007). Further, while male-biased dispersal was detected with our genetic data, telemetry data suggests that both sexes disperse in Illinois (Nixon et al. 1991; Hansen, Nixon & Beringer 1997; Nixon et al. 2007). In agricultural habitats of Midwestern North America similar proportions of radiocollared deer dispersed from their natal ranges in RAP (57% of males and 49% of females), and in DeKalb County (68% of males and 45% of females) (Nixon et al. 2007). Goudet, Perrin & Waser (2002) argued that sex-biased dispersal must be stronger than that documented (for example) by Nixon et al. (2007) before it can be detected using genetic data. Nevertheless, our study was performed at the population-level and included >1400 deer sampled across the northern half of Illinois. Given this, we were able to detect long-distance dispersals and subpopulation processes that are often overlooked in short-term ecological investigations.
Discretion must be used when gene flow estimates are employed as a surrogate for dispersal in mobile organisms, especially with samples obtained from disease surveillance. In Illinois, surveillance is concentrated in areas with CWD, therefore, our geographic distribution of samples is limited. Given the high genetic admixture observed, the spatial scale examined may not capture the potential for gene flow across the region. Sampling at a larger spatial scale or across a wider array of habitats would have allowed us to more accurately quantify long-distance dispersals and landscape barriers to deer movement across the Midwest. Also, because we sampled to detect disease, rather than continuously across the landscape, uneven sampling may have affected the likelihood of detecting mother-offspring pairs and spatial autocorrelation. Hence, while parentage analysis allowed us to identify mother-offspring pairs within a single home range, our sampling distribution probably prevented identification of pairs at larger distances. Nevertheless, we applied conservative criteria to detect parentage in that simulated error rates were five times lower than observed. In addition, when performing spatial autocorrelation and parentage, we carefully subsampled the data and omitted deer from GTA and RAP so as to prevent bias due to clustered sampling.
The practice of culling CWD-positive herds to minimize the risk of spreading the disease has raised some concerns about negative impacts on population viability. However, we did not detect population bottlenecks, and allelic diversity was equal to (or greater than) that documented in other regional studies (Anderson et al. 2002; Blanchong 2003), suggesting that reductions in deer abundance did not result in an observable loss of genetic diversity within the time frame examined. More importantly, as predicted by theoretical studies (Lloyd-Smith et al. 2005) and modelling scenarios (Wasserberg et al. 2009) to date, culling as a management strategy has lowered prevalence in CWD-positive areas in Illinois and minimized its spread to other areas (H.Y. Weng, unpublished data). These are optimistic results in an otherwise rather bleak prognosis on containment and potential eradication of CWD.
Our findings have shown that in heterogeneous landscapes such as Illinois, white-tailed deer populations are maintained by long-distance male dispersal and female philopatry. Profound differences in males and female genetic structure underscore the importance of utilizing several statistical approaches to quantify gene flow at varying spatial scales. With this comparative approach, we were able to make meaningful conclusions about the genders despite vast differences in their movement behaviours. This work contributes to an overall understanding of deer population genetics and wildlife disease while providing a larger context for the comparison of demography, behaviour and genetic tendencies of deer in Midwestern North America. Furthermore, our study has shown that with careful analysis indirect estimates of movement can be obtained from samples collected through disease surveillance, a finding that offers great potential for future studies examining the interplay between disease and dispersal. To limit spatial expansion of infectious disease outbreaks in cervids, males should be targeted for harvest and surveillance across a broad geographic range as they are readily capable of spreading disease across >100 km. Additionally, we agree with Grear et al. (2010) in that harvesting matriarchal groups would help prevent the establishment of disease foci by decreasing the risk for horizontal transmission among philopatric females.