Temporal Genetic Variance and Propagule-Driven Genetic Structure Characterize Naturalized Rainbow Trout (<i>Oncorhynchus mykiss</i>) from a Patagonian Lake Impacted by Trout Farming

Knowledge about the genetic underpinnings of invasions—a theme addressed by invasion genetics as a discipline—is still scarce amid well documented ecological impacts of non-native species on ecosystems of Patagonia in South America. One of the most invasive species in Patagonia’s freshwater systems and elsewhere is rainbow trout (Oncorhynchus mykiss). This species was introduced to Chile during the early twentieth century for stocking and promoting recreational fishing; during the late twentieth century was reintroduced for farming purposes and is now naturalized. We used population- and individual-based inference from single nucleotide polymorphisms (SNPs) to illuminate three objectives related to the establishment and naturalization of Rainbow Trout in Lake Llanquihue. This lake has been intensively used for trout farming during the last three decades. Our results emanate from samples collected from five inlet streams over two seasons, winter and spring. First, we found that significant intra- population (temporal) genetic variance was greater than inter-population (spatial) genetic variance, downplaying the importance of spatial divergence during the process of naturalization. Allele frequency differences between cohorts, consistent with variation in fish length between spring and winter collections, might explain temporal genetic differences. Second, individual-based Bayesian clustering suggested that genetic structure within Lake Llanquihue was largely driven by putative farm propagules found at one single stream during spring, but not in winter. This suggests that farm broodstock might migrate upstream to breed during spring at that particular stream. It is unclear whether interbreeding has occurred between “pure” naturalized and farm trout in this and other streams. Third, estimates of the annual number of breeders (Nb) were below 73 in half of the collections, suggestive of genetically small and recently founded populations that might experience substantial genetic drift. Our results reinforce the notion that naturalized trout originated recently from a small yet genetically diverse source and that farm propagules might have played a significant role in the invasion of Rainbow Trout within a single lake with intensive trout farming. Our results also argue for proficient mitigation measures that include management of escapes and strategies to minimize unintentional releases from farm facilities.关于生物入侵的遗传基础这一研究主题，作为入侵遗传学（invasion genetics）这一学科的核心范畴，目前相关认知仍较为匮乏，尽管南美巴塔哥尼亚地区外来物种对当地生态系统造成的生态影响已有充分记录。虹鳟（Oncorhynchus mykiss）是巴塔哥尼亚淡水生态系统及其他区域入侵性最强的物种之一。该物种于20世纪早期被引入智利，用于人工增殖种群并推动休闲渔业发展；20世纪晚期又因养殖目的再次引入，目前已成功归化。我们借助单核苷酸多态性（single nucleotide polymorphisms, SNPs）的种群与个体水平推断分析方法，针对兰基胡湖（Lake Llanquihue）内虹鳟的定殖与归化过程阐明三项研究目标。兰基胡湖在过去三十年中被广泛用于高密度虹鳟养殖。本研究的样本采集自5条入湖溪流，涵盖冬季与春季两个采样季节。其一，我们发现种群内（时间维度）的显著遗传变异高于种群间（空间维度）的遗传变异，这表明在归化过程中空间分化的重要性被低估。同龄组间的等位基因频率差异，与春季和冬季采样中鱼类体长的变异特征相符，或可解释时间维度上的遗传差异。其二，基于个体的贝叶斯聚类（Bayesian clustering）分析显示，兰基胡湖内的遗传结构主要由春季单一条溪流中检出的疑似养殖繁殖体驱动，冬季采样则未发现该现象。这表明养殖亲鱼可能于春季在该特定溪流上游洄游产卵。目前尚不清楚该溪流及其他溪流中，纯归化虹鳟与养殖虹鳟之间是否发生了杂交。其三，半数采样点的年度有效繁殖个体数（Nb）估计值低于73，提示存在遗传规模较小且近期建立的种群，这类种群可能经历了显著的遗传漂变（genetic drift）。本研究结果进一步证实，归化虹鳟近期起源于一个规模较小但遗传多样性丰富的源种群，且养殖繁殖体可能在该高密度养殖湖泊内的虹鳟入侵过程中发挥了重要作用。本研究结果同时呼吁制定行之有效的防控措施，包括养殖个体逃逸管理及降低养殖设施意外放生的相关策略。