Spatio-temporal genetic structure and the effects of long-term fishing in two partially sympatric offshore demersal fishes

Environmental gradients have been shown to disrupt gene flow in marine species, yet their influence in structuring populations at depth remains poorly understood. The Cape hakes (Merluccius paradoxus and M. capensis) are demersal species co-occurring in the Benguela Current system, where decades of intense fishing resulted in severely depleted stocks in the past. Previous studies identified conflicting mtDNA genetic substructuring patterns and thus contrasting evolutionary trajectories for both species. Using 10 microsatellite loci, the control region of mtDNA and employing a seascape genetics approach, we investigated genetic connectivity and the impact of prolonged exploitation in the two species, which are characterized by different patterns of fishing pressure. Three consecutive years were sampled covering the entire distribution (N = 2100 fishes). Despite large estimated population sizes, both species exhibited low levels of contemporary genetic diversity (0.581 < HE < 0.692), implying that fishing has had a significant impact on their genetic composition and evolutionary trajectories. Further, for M. paradoxus, significant temporal, but not spatial, divergence points to the presence of genetic chaotic patchiness. In contrast, M. capensis exhibited a clear latitudinal cline in genetic differentiation between Namibia and South Africa (FST = 0.063, P < 0.05), with low (0.2% per generation) estimates of contemporary gene flow. Seascape analyses reveal an association with bathymetry and upwelling events, suggesting that adaptation to local environmental conditions may drive genetic differentiation in M. capensis. Importantly, our results highlight the need for temporal sampling in disentangling the complex factors that impact population divergence in marine fishes.

已有研究证实，环境梯度可干扰海洋物种的基因流，但目前学界对其在深海水域种群结构塑造中的作用仍不甚明晰。开普无须鳕（Cape hakes）包含悖论无须鳕（Merluccius paradoxus）与南非无须鳕（M. capensis），二者均为底栖性物种，共同栖息于本格拉洋流系统；该海域历经数十年高强度捕捞，曾导致其渔业种群严重枯竭。既往针对这两个物种的研究得出了相互矛盾的线粒体DNA（mtDNA）遗传亚结构模式，进而提出了截然不同的进化轨迹假说。本研究借助10个微卫星位点、线粒体DNA控制区序列，并采用海洋景观遗传学（seascape genetics）分析方法，针对这两个受不同捕捞压力特征影响的物种，探究了其遗传连通性以及长期捕捞活动的种群影响。研究连续三年覆盖两个物种的全部分布范围，共计采集2100尾样本（N=2100）。尽管预估种群规模庞大，但两个物种的当代遗传多样性水平均较低（期望杂合度HE介于0.581至0.692之间），这表明捕捞活动已对其遗传组成与进化轨迹造成了显著影响。进一步分析显示，悖论无须鳕仅存在显著的时间分化而非空间分化，提示其存在遗传混沌斑块结构。与之形成鲜明对比的是，南非无须鳕在纳米比亚与南非之间呈现出清晰的遗传分化纬度梯度（固定指数FST=0.063，P<0.05），其当代基因流估计值较低，仅为每世代0.2%。海洋景观遗传学分析结果表明，其遗传分化与海底地形及上升流事件存在关联，提示对局部环境条件的适应性进化可能推动了南非无须鳕的遗传分化。值得注意的是，本研究结果强调了开展时间维度采样的必要性，以厘清影响海洋鱼类种群分化的各类复杂因素。