Spatio-temporal analyses reveal infectious disease-driven selection in a free-ranging ungulate

Abstract

Infectious diseases play an important role in wildlife population dynamics by altering individual fitness, but detecting disease-driven natural selection in free-ranging populations is difficult due to complex disease–host relationships. Chronic wasting disease (CWD) is a fatal infectious prion disease in cervids for which mutations in a single gene have been mechanistically linked to disease outcomes, providing a rare opportunity to study disease-driven selection in wildlife. In Wyoming, USA, CWD has gradually spread across mule deer ( Odocoileus hemionus ) populations, producing natural variation in disease history to evaluate selection pressure. We used spatial variation and a novel temporal comparison to investigate the relationship between CWD and a mutation at codon 225 of the mule deer prion protein gene that slows disease progression. We found that individuals with the ‘slow’ 225F allele were less likely to test positive for CWD, and the 225F allele was more common in herds exposed to CWD longer. We also found that in the past 2 decades, the 225F allele frequency increased more in herds with higher CWD prevalence. This study expanded on previous research by analysing spatio-temporal patterns of individual and herd-based disease data to present multiple lines of evidence for disease-driven selection in free-ranging wildlife.

Pathogen‐mediated selection and management implications for white‐tailed deer exposed to chronic wasting disease

“…We are not aware of any study evaluating differential harvest of deer with different PRNP genotypes; however, a number of deer studies evaluating genotypic differences in CWD status have also assumed harvest was not based on PRNP genotype (see Ketz, Johnson, et al., 2019; Robinson, Samuel, Johnson, et al., 2012). PRNP genotype distributions have consistently demonstrated that the frequency of least susceptible PRNP alleles are uncommon (LaCava et al., 2021; Monello et al., 2017; Robinson, Samuel, O’Rourke, et al., 2012). These findings have led to the hypotheses that the low frequency of least susceptible PRNP genotypes is a result of non‐random mating or reduced fitness in the absence of CWD (Robinson, Samuel, Johnson, et al., 2012; Robinson, Samuel, O’Rourke, et al., 2012; Wolfe et al., 2012).…”

“…When pathogens affect individual fitness, there is an added potential for natural selection of less susceptible genotypes. However, documenting pathogen‐driven genetic selection in wildlife populations is difficult due to potentially complex host–pathogen interactions (LaCava et al., 2021). Moreover, development of strategies to manage disease‐affected wildlife populations can be challenging because of the potentially complex interaction between harvest, host demographics, disease dynamics and genetic selection.…”

“…We are not aware of any study evaluating differential harvest of deer with different PRNP genotypes; however, a number of deer studies evaluating genotypic differences in CWD status have also assumed harvest was not based on PRNP genotype (see Ketz, Johnson, et al, 2019;. PRNP genotype distributions have consistently demonstrated that the frequency of least susceptible PRNP alleles are uncommon (LaCava et al, 2021;Monello et al, 2017;Robinson, Samuel, O'Rourke, et al, 2012).…”

“…Existing and emerging pathogens can drive population dynamics (Anderson & May, 1978; Daszak et al., 2000), determine host geographical distributions (Chafin et al., 2020; LaPointe et al., 2012) and potentially drive host natural selection (Goldmann, 2008; LaCava et al., 2021; Monello et al., 2017; Van Blerkom, 2003). It is often difficult to identify which host genetic components are directly impacted by pathogen selection and to quantify the potential rate of population adaptation to pathogen pressures (Dwyer et al., 1990; McKnight et al., 2017).…”

“…LaCava et al. (2021) found that less susceptible mule deer Odocoileus hemionus were less likely to be positive for CWD and the less susceptible allele was more common in populations exposed to CWD for longer. However, emerging strains of infectious PrP CWD suggest that both transmission dynamics and clinical signs may be altered in the future (Herbst et al., 2017).…”