Gaboriau Théo, Marcionetti Anna, Garcia-Jimenez Alberto, Schmid Sarah, Fitzgerald Lucy M, Micheli Baptiste, Titus Benjamin, Salamin Nicolas
Department of Computational Biology, Université de Lausanne, Lausanne 1015, Switzerland.
Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487.
Proc Natl Acad Sci U S A. 2025 Apr 29;122(17):e2419716122. doi: 10.1073/pnas.2419716122. Epub 2025 Apr 25.
Clownfishes (Amphiprioninae) are a fascinating example of a marine radiation. From a central Pacific ancestor, they quickly colonized the coral reefs of the Indo-Pacific and diversified independently on each side of the Indo-Australian Archipelago. Their association with sea anemones has been proposed to be a key innovation that enabled the clownfish radiation. However, this intuition has little empirical or theoretical support given our current knowledge of the group. To date, no ecological variable has been identified to explain clownfish niche partitioning, phenotypic evolution, species co-occurrence, and thus, the adaptive aspect of the group's radiation. Our study solves this long-standing mystery by testing the influence of sea anemone host use on phenotypic divergence. We provide a major revision of the known clownfish-sea anemone host associations, accounting for the biologically relevant aspects of host associations. We gathered whole-genome data for all 28 clownfish species and reconstructed a fully supported species tree for the Amphiprioninae. Integrating this data into comparative genomic approaches, we demonstrate that the host sea anemones are the drivers of convergent evolution in clownfish color pattern and morphology. During the diversification of this group, clownfishes in different regions that associate with the same hosts have evolved similar phenotypes. Comparative genomics also reveals several genes under convergent positive selection linked to host specialization events. Our findings reveal that the sea anemone host plays a crucial role in driving clownfish diversification. This highlights how a strong mutualistic interaction can promote the diversification of entire clades by influencing their phenotypes, defining their geographic distribution, and ultimately contributing to their evolutionary and ecological success.
小丑鱼（双锯鱼亚科）是海洋物种辐射演化的一个引人入胜的例子。从太平洋中部的一个祖先开始，它们迅速在印度-太平洋的珊瑚礁中定殖，并在印度-澳大利亚群岛两侧独立分化。它们与海葵的共生关系被认为是使小丑鱼辐射演化的关键创新。然而，根据我们目前对该类群的了解，这种直觉几乎没有实证或理论支持。迄今为止，尚未发现任何生态变量能够解释小丑鱼的生态位划分、表型进化、物种共存，以及该类群辐射演化的适应性方面。我们的研究通过测试海葵宿主利用对表型分化的影响，解开了这个长期存在的谜团。我们对已知的小丑鱼-海葵宿主共生关系进行了重大修订，考虑了宿主共生关系的生物学相关方面。我们收集了所有28种小丑鱼的全基因组数据，并重建了一个得到充分支持的双锯鱼亚科物种树。将这些数据整合到比较基因组学方法中，我们证明宿主海葵是小丑鱼颜色模式和形态趋同进化的驱动力。在这个类群的分化过程中，不同地区与相同宿主共生的小丑鱼进化出了相似的表型。比较基因组学还揭示了几个与宿主特化事件相关的处于趋同正选择下的基因。我们的研究结果表明，海葵宿主在推动小丑鱼多样化方面起着至关重要的作用。这凸显了一种强烈的互利共生相互作用如何通过影响其表型、定义其地理分布，并最终促成其进化和生态成功，来促进整个进化枝的多样化。
