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

Sam C Banks,Ceridwen I Fraser,Amy Macris,Cameron Jack,David Hunter,Ben C Scheele

doi:10.21425/f5fbg43875

Abstract

Chytridiomycosis, a disease caused by the emerging fungus Batrachochytrium dendrobatidis (Bd), has been implicated in the decline of over 500 amphibian species. Population declines could have important genetic consequences, including reduced genetic diversity. We contrasted genetic diversity among both long-Bd-exposed and unexposed populations of the south-east Australian alpine tree frog (Litoria verreauxii alpina) across its range. At the population level, we found no significant differences in genetic diversity between Bd-exposed and unexposed populations. Encouragingly, even Bd-infected remnant populations that are now highly isolated maintain genetic diversity comparable to populations in which Bd is absent. Spatial genetic structure among populations followed an isolation-by-distance pattern, suggesting restricted movement among remnant populations. At the individual level, greater heterozygosity was associated with reduced probability of infection. Loss of genetic diversity in remnant populations that survived chytridiomycosis epidemics does not appear to be a threat to L. v. alpina. We suggest several factors underpinning maintenance of genetic diversity: (1) remnant populations have remained large enough to avoid losses of genetic diversity; (2) many individuals in the population are able to breed once before succumbing to disease; and (3) juveniles in the terrestrial environment have low exposure to Bd, providing an annual ‘reservoir’ of genetic diversity. The association between individual heterozygosity and infection status suggests that, while other work has shown all breeding adults are typically killed by Bd, males with greater heterozygosity may survive longer and obtain fitness benefits through extended breeding opportunities. Our results highlight the critical role of life history in mitigating the impacts of Bd infection for some amphibian species, but we infer that increased isolation as a result of disease-induced population extirpations will enhance population differentiation and thus biogeographic structure.

Highlights

In recent decades amphibians have been declining faster than any other vertebrate taxon, both in terms of numbers of individuals and numbers of species, and at least one third of all species are threatened with extinction (Stuart et al 2004)
We investigated whether infected frog populations contained lower genetic diversity than uninfected populations and whether heterozygosity-fitness correlations might be associated with Batrachochytrium dendrobatidis (Bd)-infection status among individuals
This may be due to the presence of historical biogeographic structure in the alpine region of southern New South Wales indicated by the strong genetic clustering of a group of sites from west-flowing catchments in the northern region of the Snowy Mountains (GM, KI, 3M, Ogilvies Creek (OG)), which clustered separately from a group comprising the remaining sites except BF (Figure 2)

Summary

Introduction

In recent decades amphibians have been declining faster than any other vertebrate taxon, both in terms of numbers of individuals and numbers of species, and at least one third of all species are threatened with extinction (Stuart et al 2004). While chytridiomycosis has already caused the extinction of many species (Scheele et al 2019), a major conservation challenge lies in preventing further extinctions in species that have suffered declines from Bd, but persist in remnant populations (Scheele et al 2014, Scheele et al 2016, Scheele et al 2017b) This challenge is evident across the world, in species such as the boreal toad (Anaxyrus boreas) (Muths et al 2011) and yellow-legged frog (Rana muscosa) in North America (Vredenburg et al 2010), the midwife toad (Alytes obstetricans) in Europe (Rosa et al 2013), and tropical rainforest frogs in Australia, including the armoured mist frog (Litoria lorica) (Puschendorf et al 2011)

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