The return of the frogs: The importance of habitat refugia in maintaining diversity during a disease outbreak.

ABSTRACT

Recent decades have seen the emergence and spread of numerous infectious diseases, often with severe negative consequences for wildlife populations. Nevertheless, many populations survive the initial outbreaks, and even undergo recoveries. Unfortunately, the long-term effects of these outbreaks on host population genetics are poorly understood; to increase this understanding, we examined the population genetics of two species of rainforest frogs (Litoria nannotis and Litoria serrata) that have largely recovered from a chytridiomycosis outbreak at two national parks in the Wet Tropics of northern Australia. At the wetter, northern park there was little evidence of decreased genetic diversity in either species, and all of the sampled sites had high minor allele frequencies (mean MAF = 0.230-0.235), high heterozygosity (0.318-0.325), and few monomorphic markers (1.4%-4.0%); however, some recovered L. nannotis populations had low Ne values (59.3-683.8) compared to populations that did not decline during the outbreak (1,537.4-1,756.5). At the drier, southern park, both species exhibited lower diversity (mean MAF = 0.084-0.180; heterozygosity = 0.126-0.257; monomorphic markers = 3.7%-43.5%; Ne  = 18.4-676.1). The diversity patterns in this park matched habitat patterns, with both species having higher diversity levels and fewer closely related individuals at sites with higher quality habitat. These patterns were more pronounced for L. nannotis, which has lower dispersal rates than L. serrata. These results suggest that refugia with high quality habitat are important for retaining genetic diversity during disease outbreaks, and that gene flow following disease outbreaks is important for re-establishing diversity in populations where it was reduced.