Genetic diversity and structure lag the effects of contemporary environmental changes in a platypus meta-population

The platypus is an evolutionary unique mammal found on the east coast of mainland Australia and throughout Tasmania. The species is dependent on freshwater ecosystems and is declining throughout its range, and is listed as Vulnerable in the state of Victoria, and Near Threatened on the IUCN Red List. This relatively long-lived species is cryptic and nocturnal making it difficult to study in natural populations. Relatively little is known about its demographic history or the forces that shape genetic variation. We use a unique genomic dataset comprising 2,715 single nucleotide polymorphisms from 545 individual platypuses sampled from five catchments across Melbourne, Victoria. This dataset enabled us to describe the genetic variation across the catchments and test hypotheses relating to migration, effective population size, and potential negative effects of anthropogenic barriers. We found relatively consistent levels of genetic diversity in platypuses across Melbourne’s catchments, moderate levels of within catchment migration, and genetic differentiation both between and within catchments. This genetic structure is explained by several factors including isolation-by-river-distance, isolation-by-environment and within-catchment sex biased dispersal at short distances. These patterns are likely explained by a temporal lag between indirect and direct anthropogenic changes to the environmental and genetic variation, and that these contemporary analyses likely reflect historical demographic patterns. In addition, we find that anthropogenic barriers such as dams have not measurably affected migration in these catchments. Our study highlights future evolutionary challenges that exist for platypuses in Melbourne’s catchments, which could be representative of their entire range along the east coast of Australia.

鸭嘴兽是一种演化上独具特色的哺乳动物，分布于澳大利亚大陆东海岸及塔斯马尼亚全境。该物种依赖淡水生态系统，其种群在整个分布范围内呈下降趋势，在维多利亚州被列为易危物种，在IUCN红色名录（IUCN Red List）中被列为近危物种。该物种寿命相对较长，生性隐蔽且夜行性，使得野外种群的研究难度较大。目前学界对其种群历史与塑造遗传变异的驱动力仍知之甚少。本研究使用了一套独特的基因组数据集，包含来自澳大利亚维多利亚州墨尔本地区5个集水区的545只鸭嘴兽个体的2715个单核苷酸多态性（single nucleotide polymorphisms）位点。该数据集帮助我们刻画了各集水区内的遗传变异情况，并检验了与迁移、有效种群大小（effective population size）以及人为障碍潜在负面影响相关的假说。研究发现，墨尔本各集水区内鸭嘴兽的遗传多样性水平相对一致，集水区内部的迁移程度中等，且集水区之间与集水区内部均存在遗传分化。这种遗传结构可由多种因素解释，包括依河流距离的隔离效应、环境隔离效应，以及集水区内部短距离的性别偏向扩散现象。上述模式可能源于环境与遗传变异所受的间接、直接人为干扰之间存在时间滞后效应，且本次当代分析大概率反映了历史种群动态模式。此外，本研究发现，大坝等人为障碍并未对这些集水区内的鸭嘴兽迁移造成可检测的影响。本研究揭示了墨尔本集水区内鸭嘴兽所面临的未来演化挑战，这一情况或可代表澳大利亚东海岸全境鸭嘴兽种群的普遍处境。