Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors such as disease. The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a nearly 100% fatal, transmissible cancer, devil facial tumor disease (DFTD). Devils persist in regions of long-term infection despite epidemiological model predictions of species’ extinction, suggesting possible adaptation to DFTD. Here, we test the extent to which spatial variation and genetic diversity are associated with the abiotic environment and/or DFTD. We employ genetic-environment association analyses using a RAD-capture panel including 6,886 SNPs from 3,286 individuals sampled pre- and post-disease arrival. Pre-disease, we find significant correlations of allele frequencies with environmental variables, including 365 unique loci linked to 71 genes, suggesting local adaptation to abiotic environment. The majority of candidate loci detected pre-DFTD were not detected post disease arrival. Several post-DFTD candidate loci were associated with disease prevalence and were in linkage disequilibrium with genes involved in tumor suppression and immune response. Loss of apparent signal of abiotic local adaptation post-disease suggests swamping by the strong selection resulting from the rapid onset of DFTD.

景观基因组学（Landscape genomics）研究主要聚焦于通过非生物环境变量的空间变异来识别受选择的候选基因，却极少关注病害等生物因子介导的选择作用。袋獾（Sarcophilus harrisii）仅分布于环境异质性较强的塔斯马尼亚岛，目前正面临一种致死率近乎100%的可传播性癌症——袋獾面部肿瘤病（Devil Facial Tumor Disease，简称DFTD）的灭绝威胁。尽管流行病学模型预测该物种会走向灭绝，但袋獾仍能在长期受病害侵染的区域存活，这提示它们可能已对DFTD产生适应性演化。本研究旨在探究空间变异与遗传多样性分别与非生物环境及/或DFTD的关联程度。我们采用遗传-环境关联分析方法，使用RAD捕获测序（RAD-capture）面板，该面板涵盖了从3286个采集于病害传入前后的个体中检测得到的6886个单核苷酸多态性位点（Single Nucleotide Polymorphisms，简称SNPs）。在病害传入前的群体中，我们发现等位基因频率与环境变量存在显著关联，其中365个独特位点与71个基因相关联，这表明袋獾已对非生物环境产生了本地适应。绝大多数在DFTD传入前检测到的候选位点在病害传入后未被再次检出。部分在DFTD传入后检出的候选位点与病害流行率相关，且与参与肿瘤抑制及免疫应答的基因存在连锁不平衡。病害传入后，非生物环境本地适应的显著信号消失，这表明DFTD快速暴发所带来的强烈选择压已掩盖了此类信号。