Host use drives convergent evolution in clownfish.

Abstract

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.