Ecological and biogeographic features shaped the complex evolutionary history of an iconic apex predator (Galeocerdo cuvier).

Pierre Lesturgie, Hugo Lainé, Arnaud Suwalski, Pascaline Chifflet-Belle, Pierpaolo Maisano Delser, Eric Clua, Sébastien Jaquemet, Hélène Magalon, Stefano Mona
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Abstract

Background: The tiger shark (Galeocerdo cuvier) is a large iconic marine predator inhabiting worldwide tropical and subtropical waters. So far, only mitochondrial markers and microsatellites studies have investigated its worldwide historical demography with inconclusive outcomes. Here, we assessed for the first time the genomic variability of tiger shark based on RAD-seq data for 50 individuals from five sampling sites in the Indo-Pacific (IP) and one in the Atlantic Ocean (AO) to decipher the extent of the species' global connectivity and its demographic history.

Results: Clustering algorithms (PCA and NMF), FST and an approximate Bayesian computation framework revealed the presence of two clusters corresponding to the two oceanic basins. By modelling the two-dimensional site frequency spectrum, we tested alternative isolation/migration scenarios between these two identified populations. We found the highest support for a divergence time between the two ocean basins of ~ 193,000 years before present (B.P) and an ongoing but limited asymmetric migration ~ 176 times larger from the IP to the AO (Nm ~ 3.9) than vice versa (Nm ~ 0.02).

Conclusions: The two oceanic regions are isolated by a strong barrier to dispersal more permeable from the IP to the AO through the Agulhas leakage. We finally emphasized contrasting recent demographic histories for the two regions, with the IP characterized by a recent bottleneck around 2000 years B.P. and the AO by an expansion starting 6000 years B.P. The large differentiation between the two oceanic regions and the absence of population structure within each ocean basin highlight the need for two large management units and call for future conservation programs at the oceanic rather than local scale, particularly in the Indo-Pacific where the population is declining.

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生态和生物地理特征塑造了一种标志性的顶端捕食者(Galeocerdo cuvier)的复杂进化历史。
背景:虎鲨(Galeocerdo cuvier)是栖息在世界各地热带和亚热带水域的大型标志性海洋捕食者。到目前为止,只有线粒体标记和微卫星研究对其全球历史人口统计进行了调查,结果不确定。在这里,我们首次基于来自印度洋-太平洋(IP)和大西洋(AO)五个采样点的50个个体的RAD-seq数据评估了虎鲨的基因组变异性,以破译该物种的全球连接程度及其人口统计学历史。结果:聚类算法(PCA和NMF)、FST和近似贝叶斯计算框架揭示了两个海洋盆地对应的两个聚类。通过对二维站点频谱进行建模,我们测试了这两个已确定种群之间的隔离/迁移方案。我们发现两个洋盆之间的分岔时间在距今约193,000年之前(b.p.),并且从IP到AO的持续但有限的不对称迁移(Nm ~ 3.9)比反之(Nm ~ 0.02)大176倍。结论:这两个海洋区域被一个强大的屏障隔离,通过阿古拉斯渗漏更容易从IP扩散到AO。我们最后强调了两个地区最近的人口历史对比,其中IP的特征是在公元前2000年左右出现瓶颈,而AO的特征是在公元前6000年开始扩张。两个海洋区域之间的巨大差异和每个海洋盆地内人口结构的缺失突出了两个大型管理单位的需求,并呼吁未来在海洋而不是局部尺度上进行保护计划。特别是在印度-太平洋地区,那里的人口正在减少。
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