Population genetic structure and disease in montane boreal toads: more heterozygous individuals are more likely to be infected with amphibian chytrid

Abstract

Amphibians are more threatened than any other vertebrate group, with 41 % of species classified as threatened. The causes of most declines are not well understood, though many declines have been linked to disease. Additionally, amphibians are physiologically constrained to moist habitats and considered poor dispersers; thus, they may suffer genetic consequences of population isolation. To understand threats to the persistence of boreal toads (Bufo boreas) in Glacier National Park, USA, we genotyped 551 individuals at 11 microsatellite loci and used Bayesian clustering methods to describe population genetic structure and identify barriers to gene flow. We found evidence of two primary genetic groups that differed substantially in elevation and two secondary groups within the high elevation group. There was also evidence of further substructure within the southern high elevation group, suggesting mountain ridges are barriers to gene flow at local scales. Overall, genetic variation was high, but allelic richness declined with increasing elevation, reflecting greater isolation or smaller effective population sizes of high altitude populations. We tested for Batrachochytrium dendrobatidis (Bd), the fungal pathogen which causes chytridiomycosis, and we found that 35 of 199 toads were positive for Bd. Unexpectedly, more heterozygous individuals were more likely to be infected. This suggests that dispersal facilitates the spread of disease because heterozygosity may be highest where dispersal and gene flow are greatest.

Host–pathogen metapopulation dynamics suggest high elevation refugia for boreal toads

“…The global impacts of chytridiomycosis (Skerratt et al 2007) coupled with local extirpations and differential susceptibility of amphibian populations (Schloegel et al 2006, Murphy et al 2009), make identifying the factors that lead to extinction a conservation priority (Wilber et al 2017). Geographic isolation of populations, host species community richness, variation in climate, and habitat differences across sites have all been suggested to influence amphibian-Bd dynamics (Searle et al 2011, Heard et al 2013, Addis et al 2015, Clare et al 2016. Assessing the relative contributions of these factors to host-pathogen dynamics will improve our ability to successfully manage landscapes, species, and populations challenged by chytridiomycosis (Venesky et al 2014b, Garner et al 2016.…”

Pathogens in space: Advancing understanding of pathogen dynamics and disease ecology through landscape genetics

“…Landscape genetic clustering and assignment methods have largely built upon classical methods from population genetics (e.g., principal components analysis, STRUCTURE, Pritchard, Stephens, & Donnelly, ) by incorporating spatial information (e.g., GENELAND, Guillot, Mortier, & Estoup, ; sPCA, Jombart, Devillard, Dufour, & Pontier, ) and environmental heterogeneity (e.g., constrained ordination, Anderson & Willis, ; POPS, Jay, ) into estimates of population structure and providing quantitative estimates of ancestry for each individual (François & Waits, ). Clustering methods have been relatively popular in studying pathogens and implemented for the inference of landscape barriers affecting both host (Addis, Lowe, Hossack, & Allendorf, ; Cote, Garant, Robert, Mainguy, & Pelletier, ; Cullingham, Kyle, Pond, Rees, & White, ; Frantz, Cellina, Krier, Schley, & Burke, ) and microparasite (Brar et al., ; Rieux et al., ) spatial genetic variation. Edge detection methods, such as Monmonier's maximum difference algorithm, (Monmonier, ) have also been used to detect landscape barriers to transmission in pathogen studies (Carrel et al., ; Joannon et al., ).…”

Chytrid fungus infection in alpine tree frogs is associated with individual heterozygosity and population isolation but not population-genetic diversity

“…Our study capitalised on a unique opportunity for contrasting such populations, but we acknowledge that the number of unexposed sites is very low (only two such populations are known for this species), and the environmental factors that have kept them isolated from Bd exposure (low connectivity) may also influence levels of genetic diversity in those populations, as in a previous study of corroboree frogs (Pseudophryne corroboree, Pseudophryne pengilleyi) and boreal toads (Anaxyrus boreas) (Addis et al 2015, Morgan et al 2008. Indeed, the two populations where Bd was absent at the time of sampling were the only populations with no evidence of any admixture with other sampled populations (Figure 3).…”

“…The few studies that have investigated the genetic impacts of chytridiomycosis on amphibian populations have yielded diverse and sometimes contrasting results for genetic diversity at the individual and population levels (Addis et al 2015, Luquet et al 2012, Savage and Zamudio 2011, Wagner et al 2017. For example, in lowland leopard frogs (Lithobates yavapaiensis) higher heterozygosity is associated with lower risk of Bd-associated mortality (Savage et al 2015).…”

“…For example, in lowland leopard frogs (Lithobates yavapaiensis) higher heterozygosity is associated with lower risk of Bd-associated mortality (Savage et al 2015). In contrast, in boreal toads (Bufo boreas) more heterozygous individuals had increased risk of Bd infection (Addis et al 2015). Variable species responses likely reflect that chytridiomycosis influences the demography and ecology of amphibian species in diverse ways, potentially leading to different genetic impacts, and different opportunities for evolutionary responses.…”