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Ten described species of sea anemones (Anthozoa: Hexacorallia: Actiniaria) serve as hosts to charismatic clownfishes (or anemonefishes) on coral reefs throughout the tropical Indo-West Pacific. Although not diverse in number, the clownfish-hosting sea anemones have large biogeographic ranges, exhibit extensive intraspecific phenotypic appearances, and have been surrounded by a great deal of historical and contemporary taxonomic and nomenclatural confusion. We believe these factors have created challenges for field scientists making real-time species-level identifications of host sea anemones. Subsequently, a surprising amount of peer-reviewed clownfish literature never accounts for the host sea anemone, omitting critical data for understanding the symbiosis ecologically and evolutionarily. Here, we leverage the revolution that has taken place in the realm of digital underwater photography over the past 30 years to provide an updated, practical field guide for the clownfish-hosting sea anemones. First however, we review and revise the nomenclature for each species to better reflect valid changes that were made in the historical literature but never broadly adopted. Next, we demonstrate that machine learning algorithms may be of limited use for automating sea anemone species IDs from digital photographs alone—highlighting the importance of organismal expertise for identifying these animals. Finally, we present high-resolution digital photographs that encompass much of the intraspecific phenotypic variation encountered underwater, discuss important characteristics useful for field IDs, and provide updated range maps for each species to better reflect the known biogeographic range of each host anemone. We hope the increased confidence in field identification provided by this guide will result in more papers incorporating the sea anemone host data into research frameworks and subsequent publications.  

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. 

Abstract The mutualism between clownfishes (or anemonefishes) and their giant host sea anemones are among the most immediately recognizable animal interactions on the planet and have attracted a great deal of popular and scientific attention [1-5]. However, our evolutionary understanding of this iconic symbiosis comes almost entirely from studies on clownfishes— a charismatic group of 28 described species in the genusAmphiprion[2]. Adaptation to venomous sea anemones (Anthozoa: Actiniaria) provided clownfishes with novel habitat space, ultimately triggering the adaptive radiation of the group [2]. Clownfishes diverged from their free-living ancestors 25-30 MYA with their adaptive radiation to sea anemones dating to 13.2 MYA [2, 3]. Far from being mere habitat space, the host sea anemones also receive substantial benefits from hosting clownfishes, making the mutualistic and co-dependent nature of the symbiosis well established [4, 5]. Yet the evolutionary consequences of mutualism with clownfishes have remained a mystery from the host perspective. Here we use bait-capture sequencing to fully resolve the evolutionary relationships among the 10 nominal species of clownfish-hosting sea anemones for the first time (Figure 1). Using time-calibrated divergence dating analyses we calculate divergence times of less than 25 MYA for each host species, with 9 of 10 host species having divergence times within the last 13 MYA (Figure 1). The clownfish-hosting sea anemones thus diversified coincidently with clownfishes, potentially facilitating the clownfish adaptive radiation, and providing the first strong evidence for co-evolutionary patterns in this iconic partnership.