Micheli, B. | bioRxiv Science

bioRxiv2024

Host-use Drives Convergent Evolution in Clownfish and Disentangles the Mystery of an Iconic Adaptive Radiation

Clownfishes (Amphiprioninae) are a fascinating example of 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 venomous sea anemones is often thought to be the key innovation that enabled the clownfish radiation. However, this intuition has little empirical or theoretical support given our current knowledge of the clade. To date, no ecological variable has been identified that can explain clownfish niche partitioning, phenotypic evolution, species co-occurrence, and thus, the adaptive radiation of the group. Our synthetic work solves this long-standing mystery by testing the influence of sea anemone host use on phenotypic divergence. We provide the first major revision to the known clownfish-sea anemone host associations in over 30 years, accounting for host associations in a biologically relevant way. We gathered whole-genome data for all 28 clownfish species and reconstructed a fully supported species tree for the Amphiprioninae. Integrating this new data into comparative phylogenomic approaches, we demonstrate for the first time, that the host sea anemones are the drivers of convergent evolution in clownfish color pattern and morphology. During the adaptive radiation of this group, clownfishes in different regions that associate with the same hosts have evolved the same phenotypes. Comparative genomics also reveals several genes under convergent positive selection linked to host specialisation events. Our results identify the sea anemone host as the key ecological variable that disentangles the entire adaptive radiation. As one of the most recognizable animals on the planet and an emerging model organism in the biological sciences, our findings bear on the interpretation of dozens of prior studies on clownfishes and will radically reshape research agendas for these iconic organisms.

evolutionary biology↗

bioRxiv2022

Extensive hybridisation throughout clownfishes evolutionary history

The contribution of hybridisation in the generation of global species diversity has long been controversial among evolutionary biologists. However, it is now increasingly accepted that hybridisation has many impacts on the process of speciation. Notably, it is an important mechanism fostering adaptive radiation since it can generate new phenotypic combinations enabling the occupancy of new niches. Here, we focused on clownfish (Pomacentridae), a clade of 28 coral reef fishes displaying a mutualistic interaction with sea anemones. This behaviour is the key innovation that triggered adaptive radiation of clownfishes, as each species is able to occupy a different combination of host anemone species and habitat. Previous work suggested that hybridisation might be responsible for the extant diversity of clownfish species. To test this hypothesis, we analysed whole-genome datasets for each clownfish species. First, we reconstructed the phylogeny of the clade based on topology weighting methods, which enables the visualisation of the relationships between taxa across the genome. Then, we highlighted possible ancient hybridisation events based on a comparative genomic framework for detecting introgression in genomes. The resulting phylogeny is consistent with previous works based on a few mitochondrial and nuclear genes, and shallow nodes are now well supported in contrast to past studies. Furthermore, we detected multiple past hybridisation events throughout the evolutionary history of clownfishes, corroborating the potential role of hybridisation in the clownfish adaptive radiation. This study adds to the growing number of studies investigating the genomic mechanisms behind species diversification, drawing us closer to understanding how Earth biodiversity is generated.

evolutionary biology↗