Eco-evolutionary rescue promotes host-pathogen coexistence

Emerging infectious pathogens are responsible for some of the most severe host mass-mortality events in wild populations. Yet, effective pathogen control strategies are notoriously difficult to identify, in part because quantifying and forecasting pathogen spread and disease dynamics is challenging. Following an outbreak, hosts must cope with the presence of the pathogen, leading to host-pathogen coexistence or extirpation. Despite decades of research, little is known about host-pathogen coexistence post-outbreak when low host abundances and cryptic species make these interactions difficult to study. Using a novel disease-structured N-mixture model, we evaluate empirical support for three host-pathogen coexistence hypotheses (source-sink, eco-evolutionary rescue, and spatial variation in pathogen transmission) in a Neotropical amphibian community decimated by Batrachochytrium dendrobatidis (Bd) in 2004. During 2010 – 2014, we surveyed amphibians in Parque Nacional G. D. Omar Torríjos Herrera, Coclé Province, El Copé, Panama. We found that the primary driver of host-pathogen coexistence was eco-evolutionary rescue, as evidenced by similar amphibian survival and recruitment rates between infected and uninfected hosts. Average apparent monthly survival rates of uninfected and infected hosts were both close to 96%, and the expected number of uninfected and infected hosts recruited (via immigration/reproduction) was less than one host per disease state per 20 m site. The secondary driver of host-pathogen coexistence was spatial variation in pathogen transmission as we found that transmission was highest in areas of low abundance but there was no support for the source-sink hypothesis. Our results indicate that changes in the host community (i.e., through genetic or species composition) can reduce the impacts of emerging infectious disease post-outbreak. Our disease-structured N-mixture model represents a valuable advancement for conservation managers trying to understand underlying host-pathogen interactions and provides new opportunities to study disease dynamics in remnant host populations decimated by virulent pathogens.

新兴传染性病原体是引发野生种群中若干最严重宿主大规模死亡事件的元凶。然而，有效的病原体防控策略向来难以确定，部分原因在于量化与预测病原体传播及疾病动态极具挑战性。疫情暴发后，宿主需应对病原体的持续存在，最终走向宿主-病原体共存或宿主灭绝的结局。尽管已有数十年研究，但当宿主丰度偏低、隐秘物种众多导致宿主-病原体互作难以开展研究时，学界对暴发后宿主-病原体共存机制的认知仍极为有限。本研究依托一款新型疾病结构化N混合模型（N-mixture model），针对2004年被蛙壶菌（Batrachochytrium dendrobatidis, Bd）重创的新热带两栖动物群落，评估了三项宿主-病原体共存假说（源汇假说、生态进化拯救假说及病原体传播空间变异假说）的实证支持度。2010年至2014年间，我们在巴拿马科克莱省埃尔科佩的G·D·奥马尔·托里霍斯·埃雷拉国家公园开展了两栖动物调查。研究结果显示，宿主-病原体共存的主要驱动因素为生态进化拯救，受感染与未受感染两栖动物的存活率及补充率（通过迁入/繁殖实现）相近，即为该结论的佐证。未受感染与受感染宿主的平均表观月存活率均接近96%，且每个20平方米样地内，各疾病状态下预期新增宿主（通过迁入或繁殖产生）的数量均不足1只。宿主-病原体共存的次要驱动因素为病原体传播的空间变异：我们发现传播率在宿主丰度较低的区域最高，但未找到支持源汇假说的证据。本研究结果表明，宿主群落的改变（即通过遗传或物种组成调整）可减轻暴发后新兴传染性疾病带来的影响。我们所搭建的疾病结构化N混合模型，可为试图解析宿主-病原体互作机制的保护管理者提供极具价值的研究工具，同时为探究受强毒性病原体重创的残存宿主种群中的疾病动态开辟了新的研究路径。