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

Abstract

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.

Selection outweighs drift at a fine scale: Lack of MHC differentiation within a family living lizard across geographically close but disconnected rocky outcrops

“…Genetic differentiation of E. stokesii at microsatellites but not the MHC is consistent with patterns found for wolverines (Rico et al., ), house sparrows (Bichet et al., ), black grouse (Strand et al., ) and a molly (Tobler et al., ). On the other hand, our results contrast with cases where MHC differentiation has been stronger compared to microsatellites (Ekblom et al., ; Kyle et al., ; Loiseau et al., ; Miller, Kaukinen, Beacham, & Withler, ) and cases where both the MHC and microsatellites exhibited similar patterns of differentiation (Boyce et al., ; Zeisset & Beebee, ). However, all the aforementioned comparative studies of MHC and microsatellite differentiation sampled multiple populations across broad spatial scales.…”

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

“…These genes are affected by pathogen-mediated selection in a wide range of vertebrate species (Wegner et al 2003;Piertney and Oliver 2006;Savage and Zamudio 2011), and spatial patterns of variation in the MHC can serve as an immunogenetic proxy for the potential of a declining population to adapt to shifting selection by pathogens (Hawley and Fleischer 2012;Kyle et al 2014). The MHC has been studied in several bats, including a suite of Neotropical phyllostomid species (Schad et al 2012b;Real-Monroy et al 2014;Salmier et al 2016), the sac-winged bat (Saccopteryx bilineata; Mayer and Brunner 2007), and two North American Myotis species (M. velifer, M. velesi;Richman et al 2010).…”

Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white‐nose syndrome

“…For infectious diseases of conservation significance, this process of local adaptation can result in evolutionary rescue of a population, where disease‐resistant animals survive a strong selective sweep from disease and pass their resistance to their offspring (Carlson, Cunningham, & Westley, ; Maslo & Fefferman, ). Spatial patterns of local adaptation to strong selective sweeps may be linked to particular gene variants favored in local interactions (Hansen, Olivieri, Waller, & Nielsen, ; Kyle et al., ; Rico, Morris‐Pocock, Zigouris, Nocera, & Kyle, ; Schoville et al., ). Determining how these variants are spread or localized among populations is essential to understanding and managing the emergence of new selective pressures, such as emerging infectious diseases (Eizaguirre, Lenz, Kalbe, & Milinski, ; Kyle et al., ).…”