Abstract
A central question in evolutionary biology is how interactions between organisms and the environment shape genetic differentiation. The pathogen Batrachochytrium dendrobatidis (Bd) has caused variable population declines in the lowland leopard frog (Lithobates yavapaiensis); thus, disease has potentially shaped, or been shaped by, host genetic diversity. Environmental factors can also influence both amphibian immunity and Bd virulence, confounding our ability to assess the genetic effects on disease dynamics. Here, we used genetics, pathogen dynamics, and environmental data to characterize L. yavapaiensis populations, estimate migration, and determine relative contributions of genetic and environmental factors in predicting Bd dynamics. We found that the two uninfected populations belonged to a single genetic deme, whereas each infected population was genetically unique. We detected an outlier locus that deviated from neutral expectations and was significantly correlated with mortality within populations. Across populations, only environmental variables predicted infection intensity, whereas environment and genetics predicted infection prevalence, and genetic diversity alone predicted mortality. At one locality with geothermally elevated water temperatures, migration estimates revealed source–sink dynamics that have likely prevented local adaptation. We conclude that integrating genetic and environmental variation among populations provides a better understanding of Bd spatial epidemiology, generating more effective conservation management strategies for mitigating amphibian declines.
Highlights
Infectious diseases are potent agents of natural selection (Darwin 1871) that impact population demography and population genetic variation, even at ecological timescales (Tishkoff and Verrelli 2003; Campbell et al 2010)
Studies of wildlife populations commonly find a positive correlation between host genetic diversity and disease resistance (Meagher 1999; Pearman and Garner 2005), a pattern attributed to higher adaptive potential in genetically diverse populations or species (Frankham 2005)
Our analyses provide insight into past and present interactions of host population genetics with pathogen dynamics and environmental variation in a declining amphibian species, with implications for management and conservation strategies for this and other species affected by Batrachochytrium dendrobatidis (Bd)
Summary
Infectious diseases are potent agents of natural selection (Darwin 1871) that impact population demography and population genetic variation, even at ecological timescales (Tishkoff and Verrelli 2003; Campbell et al 2010). Other studies of host–pathogen systems detect no relationship between genetic variability of the host and prevalence of the pathogen (Ortego et al 2007; Hawley et al 2010). A simple relationship between host population genetics and pathogen dynamics may be unlikely, given the multitude of environmental factors that can influence disease in natural populations (Osnas and Lively 2004). Epidemiological researchers highlight the need for studies integrating genetic, spatial, and environmental processes influencing pathogen dynamics and host population genetics (Balkenhol et al 2009; Biek and Real 2010)
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