Quantifying intraspecific variation in host resistance and tolerance to a lethal pathogen

Testing for intraspecific variation for host tolerance or resistance in
wild populations is important for informing conservation decisions about
captive breeding, translocation, and disease treatment. Here, we test the
importance of tolerance and resistance in multiple populations of boreal
toads (Anaxyrus boreas boreas) against Batrachochytrium dendrobatidis
(Bd), the amphibian fungal pathogen responsible for the greatest host
biodiversity loss due to disease. Boreal toads have severely declined in
Colorado (CO) due to Bd, but toad populations challenged with Bd in
western Wyoming (WY) appear to be less affected. We used a common garden
infection experiment to expose post-metamorphic toads sourced from four
populations (2 in CO and 2 in WY) to Bd and monitored changes in mass,
pathogen burden, and survival for eight weeks. We used a multi-state
modeling approach to estimate weekly survival and transition probabilities
between infected and cleared states, reflecting a dynamic infection
process that traditional approaches fail to capture. We found that WY
boreal toads are more tolerant to Bd infection with higher survival
probabilities than those in CO when infected with identical pathogen
burdens. WY toads also appeared more resistant to Bd with a higher
probability of infection clearance and an average of five days longer to
reach peak infection burdens. Our results demonstrate strong intraspecific
differences in tolerance and resistance that likely contribute to why
population declines vary regionally across this species. Our multi-state
framework allowed us to gain inference on typically hidden disease
processes when testing for host tolerance or resistance. Our findings
demonstrate that describing an entire host species as ‘tolerant’ or
‘resistant’ (or lack thereof) is unwise without testing for intraspecific
variation.

检测野生种群中宿主耐受与抗性的种内变异，可为人工繁育、易地保护及疾病防治等保育决策提供科学依据。本研究以北方蟾蜍（Anaxyrus boreas boreas）的多个种群为对象，探究其对蛙壶菌（Batrachochytrium dendrobatidis, Bd）的耐受与抗性作用——该病原菌是引发全球两栖动物生物多样性大规模丧失的主要真菌病原体。受Bd感染影响，科罗拉多州（CO）的北方蟾蜍种群已严重衰退，而怀俄明州西部（WY）的受感染蟾蜍种群受影响程度相对较轻。本研究采用同质园感染实验，将采自4个种群（科罗拉多州2个、怀俄明州西部2个）的变态后蟾蜍暴露于Bd环境中，并连续8周监测其体重、病原体负荷及存活情况的变化。我们采用多状态建模方法，估算了每周存活率以及感染与清除感染状态间的转移概率，以此反映传统方法无法捕捉的动态感染过程。研究发现，当病原体负荷相同时，怀俄明州西部的北方蟾蜍对Bd感染的耐受能力更强，存活率显著高于科罗拉多州的种群。此外，怀俄明州西部的蟾蜍对Bd的抗性也更强，其感染清除概率更高，且达到感染负荷峰值的平均时间比科罗拉多州种群晚5天。本研究结果表明，北方蟾蜍的耐受与抗性存在显著的种内差异，这或许是该物种种群衰退程度存在区域差异的关键原因。我们所采用的多状态分析框架，可在检测宿主耐受与抗性的过程中，揭示以往难以观测的疾病动态过程。本研究结果表明，若未检测种内变异就将整个宿主物种笼统定义为"tolerant"或"resistant"（或无此特性），并非科学严谨的做法。