bioRxiv Science⌕ Search

Biology subjects

Chiodo, T.

Publications and source records attributed to Chiodo, T..

4 recordsLinked to original sources

The ecology and adaptive function of clownfish color patterns

Anti-predator coloration strategies vary widely from conspicuous to cryptic, and everything between. Coloration serves multiple functions, and determining the selective pressures that drive this diversity is a long-standing mystery. Clownfishes display enormous inter- and intra-specific variation in coloration without the influence of sexual selection, providing an excellent system in which to explore these drivers in closely related and sympatric species. Across clownfishes, three color-pattern phenotypes have evolved convergently with host anemone use, implying adaptive functions linked to the hosts physical and chemical properties. Here we conducted a comprehensive study to infer the ultimate functions of clownfish color patterns. By integrating multiple levels of biological organization, including behavior, visual ecology, dietary niche, and microbiome, our data overwhelmingly indicate that specialist and generalist clownfish color patterns have different underlying ecologies and adaptive functions. Specialist clownfishes background match their anemones, remain near hosts, and have specialized diets and microbiomes. Generalists are highly contrasting with their anemones, remain far from hosts, and have variable diets and microbiomes. Taken together, specialist color patterns align with functional expectations of camouflage while generalists align with aposematic or disruptive coloration. Our study provides novel insights into how ecological conditions shape the evolution of multiple anti-predator coloration strategies.

ecology↗

Nemo knows: clownfishes differentiate cryptic host species across fine and broad geographic scales and reveal a potential adaptive radiation in the clownfish-hosting sea anemones.

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 of E. quadricolor serve as host to the generalist clownfish species Amphiprion clarkii and others serve as host to the specialist clownfish A. frenatus. In total, we delimit at least five cryptic species in E. quadricolor that have diversified within the last five million years. The rapid diversification of E. quadricolor combined 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.

evolutionary biology↗

Phylogenomics reveals coincident divergence between giant host sea anemones and the clownfish adaptive radiation.

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 genus Amphiprion [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. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=187 SRC="FIGDIR/small/576469v1_fig1.gif" ALT="Figure 1"> View larger version (58K): org.highwire.dtl.DTLVardef@7053b4org.highwire.dtl.DTLVardef@876c65org.highwire.dtl.DTLVardef@dd6d9forg.highwire.dtl.DTLVardef@147fddd_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFigure 1.C_FLOATNO Diversification of the clownfish-hosting sea anemones was coincident with the clownfish adaptive radiation. A) Time-calibrated maximum likelihood cladogram of Order Actiniaria based on 328 ultra-conserved element and exon loci (75% data occupancy matrix). The three clades containing the clownfish hosting sea anemones are highlighted reflecting the multiple evolutionary origins of symbiosis with clownfishes within superfamily Actinioidea. B-D) Detailed time-calibrated maximum likelihood cladograms of Entacmaea quadricolor, Clade Stichodactylina, and Clade Heteractina, respectively. In all panels, the orange line denotes the beginning of the clownfish adaptive radiation 13 MYA. Sea anemone superfamilies Actinostoloidea, Metridioidea, Actiniernoidea, and Edwardsioidea are collapsed for clarity. C_FIG

evolutionary biology↗

Phylogenetic relationships among the clownfish-hosting sea anemones

The clownfish-sea anemone symbiosis has been a model system for understanding fundamental evolutionary and ecological processes. However, our evolutionary understanding of this symbiosis comes entirely from studies of clownfishes. A holistic understanding of a model mutualism requires systematic, biogeographic, and phylogenetic insight into both partners. Here, we conduct the largest phylogenetic analysis of sea anemones (Order Actiniaria) to date, with a focus on expanding the biogeographic and taxonomic sampling of the 10 nominal clownfish-hosting species. Using a combination of mtDNA and nuDNA loci we test 1) the monophyly of each clownfish-hosting family and genus, 2) the current anemone taxonomy that suggests symbioses with clownfishes evolved multiple times within Actiniaria, and 3) whether, like the clownfishes, there is evidence that host anemones have a Coral Triangle biogeographic origin. Our phylogenetic reconstruction demonstrates widespread poly-and para-phyly at the family and genus level, particularly within the family Stichodactylidae and genus Sticodactyla, and suggests that symbioses with clownfishes evolved minimally three times within sea anemones. We further recover evidence for a Tethyan biogeographic origin for some clades. Our data provide the first evidence that clownfish and some sea anemone hosts have different biogeographic origins, and that there may be cryptic species of host anemones. Finally, our findings reflect the need for a major taxonomic revision of the clownfish-hosting sea anemones.

evolutionary biology↗