A comparative study of gene expression in wild and domesticated Atlantic salmon (Salmo salar L.). Farmed vs Wild Salmon (mtRAD)

Atlantic salmon (Salmo salar L.) has been domesticated since the 1960s and has undergone over 10 generations of artificial selection for economically important traits. As a result, domesticated salmon have diverged with respect to a number of phenotypic, genotypic and behavioural traits from their wild counterparts. Since the selection pressures that are present in the wild differ greatly from the ones that shape salmon under culture conditions, domesticated salmon stocks are considered to be maladapted to natural conditions. Despite strict regulations, insoluble issues pertaining to large-scale cage rearing of farmed fish mean that there is a continuous presence of farm escapees in the wild. Gene flow from escapees has been perceived as a factor in the decline of wild populations, suggested to occur through disruption of local adaptation. This study aims to improve understanding of the genetic differences between wild and domesticated stocks by comparing the transcriptomes of Figgjo (wild) and Mowi (domesticated) strains. A series of common garden experiments have been performed, utilizing pure and reciprocal hybrid crosses of the wild and domesticated stocks, reared under two different conditions and sampled at four time points and three distinct life stages (embryo, sac-fry and feeding fry). Microarray interrogations were performed employing a 44K custom microarray design to identify genes and gene pathways that are differentially expressed between the stocks. KEGG-based functional analyses have been implemented using different gene set enrichment packages, and dominance and additive parameters were calculated from normalized expression values to predict the mode of heritability of the genes identified as differentially expressed between stocks. Most biological functions represented in wild and domesticated crosses were consistent across life stages and environments. The transcriptomic differences detected between stocks in multiple developmental stages likely reflected adaptations to selection pressures differing between natural and aquaculture environments. Down-regulated environmental information processing and immune and nervous system functions in domesticated vs. wild fish may be due to local adaptation to captivity. These included reduced information acquisition and processing systems, altered stress responsiveness and changes in feeding behaviour. In line with the resource allocation theory of production trait animals, reduced immune function was coupled with increased expression of growth and development related pathways in domesticated salmon, compared to wild counterparts. Although there is support for this trade-off in all life-stages, resource allocation showed a shift over time; possibly reflecting variation in the utilization of energy sources during the transition from endogenous to exogenous feeding. Differences in cell communication and signalling pathways between wild and domesticated stocks, associated with organogenesis during the embryo stage, reflect sampling time and are indicative of altered organ development in response to domestication. Stress responses common across stocks included the down-regulation of cellular processes, including cell cycle and meiosis, and genetic information processing, such as replication and repair, transcription and translation pathways, probably reflecting the reallocation of energy resources away from growth and towards the restoration of homeostasis. Moreover, the mobilization of energy to cover the increased demands of maintaining homeostasis was indicated by the up-regulation of some metabolic pathways, mostly involved in energy, lipid and carbohydrate metabolism in response to stress. The analysis also revealed cross-specific stress responses, including indicators of a non-additive stress response in hybrid crosses. Most differentially expressed transcripts exhibited additive (31-59%) or maternal dominant (19-33%) inheritance patterns, although maternal over-dominance (23-26%) was also significant in the embryo stage. The mode of heritability of some immune transcripts was suggestive of maternal environmental influence having been affected by aquaculture. This study has demonstrated that biological functions affected by domestication include those associated with allocation of resources, involve reduction of information acquisition and processing systems and may lead to loss of local adaptation to wild conditions. Since such changes may affect key systems, such as immunity and responsiveness to stress, they can potentially have serious negative consequences under natural conditions. Transcriptomic differences observed between wild and domesticated stocks primarily exhibited additive and maternal dominant inheritance modes. Since gene-flow from farmed fish can be frequent and primarily concerns farmed females, this suggests that introgression due to repeated large scale escape events has the capacity to significantly erode local adaptation. [Beatrix Bicskei, PhD These: https://hdl.handle.net/1893/22932]

大西洋鲑（Salmo salar L.）自20世纪60年代起便已实现驯化，且针对经济重要性状经历了超过10代的人工选育。由此，驯化鲑在诸多表型、基因型与行为性状上均与其野生种群产生了分化。由于野外环境与养殖环境下的选择压力差异悬殊，驯化鲑种群被认为对自然环境存在适应不良的问题。尽管有严格的监管规定，但规模化网箱养殖水产动物所带来的棘手难题始终存在，即养殖逃逸个体持续出现在野生环境中。人们认为逃逸个体带来的基因流是野生种群数量下降的诱因之一，推测其通过破坏局部适应过程实现。本研究旨在通过对比Figgjo（野生）与Mowi（驯化）品系的转录组（transcriptome），加深对野生与驯化种群遗传差异的理解。研究开展了一系列共同花园实验，利用野生与驯化种群的纯系及正反交杂交组合，在两种不同环境下进行饲养，并在四个时间点采集三个不同生活史阶段的样本：胚胎期、卵黄囊稚鱼与摄食稚鱼。本研究采用44K定制基因芯片（microarray）进行杂交检测，以鉴定种群间差异表达的基因及基因通路。基于京都基因与基因组百科全书（KEGG）的功能分析通过多款基因集富集分析工具完成，同时从标准化表达值中计算显性与加性参数，以预测在种群间鉴定出的差异表达基因的遗传模式。野生与驯化杂交组合所涉及的多数生物学功能在不同生活史阶段与环境中均保持一致。在多个发育阶段中检测到的种群间转录组差异，大概率反映了对自然与养殖环境中不同选择压力的适应。相较于野生鱼类，驯化个体中环境信息加工、免疫与神经系统功能的下调，可能源于对圈养环境的局部适应，具体表现为信息获取与加工系统的弱化、应激响应的改变以及摄食行为的变化。根据生产性状动物的资源分配理论，与野生种群相比，驯化鲑的免疫功能下调的同时，与生长发育相关的通路表达量上升。尽管在所有生活史阶段均存在这种权衡关系，但资源分配模式随时间发生了变化，这可能反映了从内源性营养到外源性营养转变过程中能源利用的差异。野生与驯化种群间在细胞通信与信号通路方面的差异，与胚胎期的器官发生相关，这体现了采样时间的影响，同时也表明驯化过程中器官发育发生了改变。各种群共有的应激响应包括细胞过程（如细胞周期与减数分裂）以及遗传信息加工（如复制与修复、转录与翻译通路）的下调，这大概率反映了能源资源从生长转向维持稳态的重新分配。此外，部分代谢通路（主要参与能量、脂质与碳水化合物代谢）的上调表明，机体动员能量以满足维持稳态增加的需求，以响应应激。本分析还揭示了跨特异性应激响应，包括杂交组合中非加性应激响应的相关指标。多数差异表达转录本表现为加性（31%~59%）或母本显性（19%~33%）遗传模式，尽管在胚胎期母本超显性（23%~26%）同样具有统计学显著性。部分免疫相关转录本的遗传模式表明，养殖环境影响了母本环境效应。本研究证实，驯化所影响的生物学功能包括与资源分配相关的过程，涉及信息获取与加工系统的弱化，且可能导致对野生环境局部适应能力的丧失。由于这类变化可能影响免疫与应激响应等关键系统，因此在自然环境下可能带来严重的负面影响。野生与驯化种群间观测到的转录组差异主要表现为加性与母本显性遗传模式。由于养殖鱼类的基因流频发且主要涉及养殖雌性个体，这表明反复发生的大规模逃逸事件所导致的基因渐渗，有可能显著削弱局部适应能力。[比阿特丽克斯·比克斯凯（Beatrix Bicskei），博士] 链接：https://hdl.handle.net/1893/22932