Revealing the drivers of parasite community assembly: using avian haemosporidians to model global dynamics of parasite species turnover

Why do some regions share more or fewer species than others? Community assembly relies on the ability of individuals to disperse, colonize, and thrive in new regions. Therefore, many distinct factors, such as geographic distance and environmental features, can determine the odds of a species colonizing a new environment. For parasites, host community composition (i.e., resources) also plays a key role in their ability to colonize a new environment as they rely on their hosts to complete their life cycle. Thus, variation in host community composition and environmental conditions should determine parasite turnover among regions. Here, we explored the global drivers of parasite turnover using avian malaria and malaria-like (haemosporidian) parasites. We compiled global databases on avian haemosporidian lineages distributions, environmental conditions, avian species distributions and functional traits and ran generalized dissimilarity models to uncover the main drivers of parasite turnover. We demonstrated that haemosporidian parasite turnover is mainly driven by geographic distance followed by host functional traits, environmental conditions, and host distributions. The main host functional traits associated with high parasite turnover were the predominance of resident (i.e., non-migratory) species and strong territoriality while the most important climatic drivers of haemosporidian turnover were mean temperature and temperature seasonality. Overall, we establish the importance of geographic distance as a key predictor of ecological dissimilarity and show that host resources influence parasite turnover more strongly than environmental conditions. We also evidenced that parasite turnover is most pronounced among tropical and less interconnected regions (i.e., regions with mostly territorial and non-migratory hosts). Our findings provide a robust foundation for the prediction of avian pathogen spread and the emergence of infectious diseases.

为何不同区域间的物种共享程度存在差异？群落构建过程依赖于个体在新区域的扩散、定殖与存活能力。因此，多种不同驱动因子，如地理距离与环境特征，均可决定物种定殖新环境的概率。
对于寄生虫而言，宿主群落组成（即其可利用的资源）在其定殖新环境的能力中同样发挥关键作用——寄生虫依赖宿主完成自身生活史。因此，宿主群落组成与环境条件的变异，理应决定区域间的寄生虫周转格局。
本研究以鸟类疟原虫及类疟原虫（haemosporidian，血孢子虫）为研究对象，探究全球尺度下寄生虫周转的核心驱动因子。我们整合了全球鸟类血孢子虫支系分布、环境条件、鸟类物种分布及功能性状的数据库，并运用广义差异模型（generalized dissimilarity models）解析寄生虫周转的主要驱动因子。
研究结果表明，血孢子虫的物种周转主要由地理距离驱动，其次依次为宿主功能性状、环境条件与宿主分布。与高寄生虫周转相关的主要宿主功能性状为居留型（即非迁徙）物种占优以及强领域性；而影响血孢子虫周转的关键气候因子为年均温与温度季节性波动。
总体而言，本研究明确了地理距离作为生态非相似性核心预测因子的重要性，并证实宿主资源对寄生虫周转的调控作用强于环境条件。我们还发现，寄生虫周转在热带区域及连通性较弱的区域（即主要以领域性、非迁徙宿主为主的区域）最为显著。本研究结果为预测鸟类病原体传播及传染病暴发提供了坚实的理论基础。