Phenotypic Divergence along Geographic Gradients Reveals Potential for Rapid Adaptation of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans, in North America

Abstract

White-nose syndrome (WNS) is an ongoing epizootic affecting multiple species of North American bats, caused by epidermal infections of the psychrophilic filamentous fungus Since its introduction from Europe, WNS has spread rapidly across eastern North America and resulted in high mortality rates in bats. At present, the mechanisms behind its spread and the extent of its adaptation to different geographic and ecological niches remain unknown. The objective of this study was to examine the geographic patterns of phenotypic variation and the potential evidence for adaptation among strains representing broad geographic locations in eastern North America. The morphological features of these strains were evaluated on artificial medium, and the viability of asexual arthroconidia of representative strains was investigated after storage at high (23°C), moderate (14°C), and low (4°C) temperatures at different lengths of time. Our analyses identified evidence for a geographic pattern of colony morphology changes among the clonal descendants of the fungus, with trait values correlated with increased distance from the epicenter of WNS. Our genomic comparisons of three representative isolates revealed novel genetic polymorphisms and suggested potential candidate mutations that might be related to some of the phenotypic changes. These results show that even though this pathogen arrived in North America only recently and reproduces asexually, there has been substantial evolution and phenotypic diversification during its rapid clonal expansion. The causal agent of white-nose syndrome in bats is , a filamentous fungus recently introduced from its native range in Europe. Infections caused by have progressed across the eastern parts of Canada and the United States over the last 10 years. It is not clear how the disease is spread, as the pathogen is unable to grow above 23°C and ambient temperature can act as a barrier when hosts disperse. Here, we explore the patterns of phenotypic diversity and the germination of the fungal asexual spores, arthroconidia, from strains across a sizeable area of the epizootic range. Our analyses revealed evidence of adaptation along geographic gradients during its expansion. The results have implications for understanding the diversification of and the limits of WNS spread in North America. Given the rapidly expanding distribution of WNS, a detailed understanding of the genetic bases for phenotypic variations in growth, reproduction, and dispersal of is urgently needed to help control this disease.

Multiscale model of regional population decline in little brown bats due to white‐nose syndrome

“…Multiple empirical studies indicate that microclimate strongly influences Pd growth, with warmer and more humid sites increasing fungal load and mortality (Langwig et al, ; Wilder, Frick, Langwig, & Kunz, ). While some of these differences may be confounded by species differences (Moore et al, ; Wilder et al, ; Willis, Menzies, Boyles, & Wojciechowski, ), models and laboratory studies suggest that effects of temperature on Pd and bat energetics could strongly influence mortality (Boyles & Willis, ; Forsythe et al, ; Hallam & Federico, ; Marroquin, Lavine, & Windstam, ). Therefore, natural differences among hibernacula, coupled with metapopulation dynamics, could substantially slow spread and/or population decline.…”

“…We also conducted an experiment examining the impact of potential variation in fungal growth rates between hibernacula. Cave microclimate is known to influence Pd growth (Forsythe et al, 2018;Martínková et al, 2018;Verant et al, 2012) and survival of infected bats (Langwig et al, 2012). Thus, we constructed a scenario in which the rate of disease progression to moderately infected (γ 1 ) varies among hibernacula.…”

“…In addition to these mechanisms, metapopulation dynamics (e.g., rescue effects from uncontaminated hibernacula) could be important for sustaining populations infected by Pd (Grenfell & Harwood, 1997), but few studies have considered the role of interhibernacula dispersal in driving population persistence for the WNS system. Further, variability in environmental conditions among hibernacula could produce differences in WNS-driven mortality, even without resistance or tolerance as an explanatory mechanism (Forsythe, Giglio, Asa, & Xu, 2018;Gargas, Trest, Christensen, Volk, & Blehert, 2009;Langwig et al, 2012). For instance, the growth rate of Pd on bats increases with temperature up 12-15°C (Verant, Boyles, Waldrep, Wibbelt, & Blehert, 2012)), leading to reduced survival in warmer portions of hibernacula (Langwig et al, 2012).…”

Geology of the Trout Rock caves (Hamilton Cave, Trout Cave, New Trout Cave) in Pendleton County, West Virginia (USA), and implications regarding the origin of maze caves

“…After this field trip, participants are advised to wash their clothes and gear in hot water and to avoid taking the clothing and gear used on this trip into other karst regions. The WNS-causing fungus came to North America from Europe; it first appeared in North America in New York during 2006, and since then it has been spreading across North America and killing millions of bats (Gargas et al, 2009;Lorch et al, 2011;Garrity, 2011a, 2011b;Minnis and Lindner, 2013;Reeder and Moore, 2013;Forsythe et al, 2018;Verant et al, 2018). White-nose syndrome was first detected in Pendleton County during January 2009 at both Hamilton Cave and Trout Cave (U.S. Geological Survey National Wildlife Health Center, 2009;Anonymous, 2010aAnonymous, , 2010bDasher, 2009;Hoke, 2009aHoke, , 2009bStihler, 2009;Turner et al, 2011).…”

Comparative eco-physiology revealed extensive enzymatic curtailment, lipases production and strong conidial resilience of the bat pathogenic fungus Pseudogymnoascus destructans

“…Its psychrophilic nature enables bats to clear any visible infection during summer, when ambient temperatures exceed the upper limit for P. destructans growth. Nevertheless, we have only sparse information about its conidial resilience 13,38,39 . It therefore remains unknown whether P. destructans conidia can disseminate on the body surface of bats during the active flight season to new hibernacula and participate in the spreading of the disease.…”