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Abstract The symbiosis between clownfish and giant tropical sea anemones (Order Actiniaria) is one of the most iconic on the planet. Distributed on tropical reefs, 28 species of clownfishes form obligate mutualistic relationships with 10 nominal species of venomous sea anemones. Our understanding of the symbiosis is limited by the fact that most research has been focused on the clownfishes. Chromosome scale reference genomes are available for all clownfish species, yet there are no published reference genomes for the host sea anemones. Recent studies have shown that the clownfish-hosting sea anemones belong to three distinct clades of sea anemones that have evolved symbiosis with clownfishes independently. Here we present the first high quality long read assemblies for three species of clownfish hosting sea anemones belonging to each of these clades:Entacmaea quadricolor, Stichodactyla haddoni, Radianthus doreensis. PacBio HiFi sequencing yielded 1,597,562, 3,101,773, and 1,918,148 million reads forE. quadricolor, S. haddoni, andR. doreensis, respectively. All three assemblies were highly contiguous and complete with N50 values above 4Mb and BUSCO completeness above 95% on the Metazoa dataset. Genome structural annotation with BRAKER3 predicted 20,454, 18,948 and 17,056 protein coding genes inE. quadricolor, S. haddoniandR. doreeensisgenome, respectively. These new resources will form the basis of comparative genomic analyses that will allow us to deepen our understanding of this mutualism from the host perspective. SignificanceChromosome-scale genomes are available for all 28 clownfish species yet there are no high-quality reference genomes published for the clownfish-hosting sea anemones. The lack of genomic resources impedes our ability to understand evolution of this iconic symbiosis from the host perspective. The clownfish-hosting sea anemones belong to three clades of sea anemones that have evolved mutualism with clownfish independently. Here we assembled the first high-quality long-read genomes for three species of host sea anemones each belonging to a different host clade:Entacmaea quadricolor, Stichodactyla haddoni, Radianthus doreensis. These resources will enable in depth comparative genomics of clownfish-hosting sea anemones providing a critical perspective for understanding how the symbiosis has evolved. Finally, these reference genomes present a significant increase in the number of high-quality long-read genome assemblies for sea anemones (11 currently published) and double the number of high-quality reference genomes for the sea anemone superfamily Actinoidea. 

Abstract The symbiosis between clownfishes (or anemonefishes) and their host sea anemones ranks among the most recognizable animal interactions on the planet. Found on coral reef habitats across the Indian and Pacific Oceans, 28 recognized species of clownfishes adaptively radiated from a common ancestor to live obligately with only 10 nominal species of host sea anemones. Are the host sea anemones truly less diverse than clownfishes? Did the symbiosis with clownfishes trigger a reciprocal adaptive radiation in sea anemones, or minimally, a co-evolutionary response to the mutualism? To address these questions, we combined fine- and broad-scale biogeographic sampling with multiple independent genomic datasets for the bubble-tip sea anemone,Entacmaea quadricolor—the most common clownfish host anemone throughout the Indo-West Pacific. Fine-scale sampling and restriction site associated DNA sequencing (RADseq) throughout the Japanese Archipelago revealed three highly divergent cryptic species: two of which co-occur throughout the Ryukyu Islands and can be differentiated by the clownfish species they host. Remarkably, broader biogeographic sampling and bait-capture sequencing reveals that this pattern is not simply the result of local ecological processes unique to Japan, but part of a deeper evolutionary signal where some species ofE. quadricolorserve as host to the generalist clownfish speciesAmphiprion clarkiiand others serve as host to the specialist clownfishA. frenatus. In total, we delimit at least five cryptic species inE. quadricolorthat have diversified within the last five million years. The rapid diversification ofE. quadricolorcombined with functional ecological and phenotypic differentiation supports the hypothesis that this may represent an adaptive radiation in response to mutualism with clownfishes. Our data indicate that clownfishes are not merely settling in locally available hosts but recruiting to specialized host lineages with which they have co-evolved. These findings have important implications for understanding how the clownfish-sea anemone symbiosis has evolved and will shape future research agendas on this iconic model system.