Polymorphic adaptations in metazoans to establish ...

Biol. Rev. (2018), pp. 000–000. doi: 10.1111/brv.12430

1

Polymorphic adaptations in metazoans to establish and maintain photosymbioses Jenny Melo Clavijo1 , Alexander Donath1 , João Serôdio2 and Gregor Christa1,2∗ 1 Center 2

for Molecular Biodiversity Research (zmb), Zoological Research Museum Alexander Koenig, Adenauerallee 160, Bonn, 53113, Germany Department of Biology and Center for Environmental and Marine Studies, University of Aveiro, Campus Santiago, Aveiro, 3810-192, Portugal

ABSTRACT Mutualistic symbioses are common throughout the animal kingdom. Rather unusual is a form of symbiosis, photosymbiosis, where animals are symbiotic with photoautotrophic organisms. Photosymbiosis is found among sponges, cnidarians, flatworms, molluscs, ascidians and even some amphibians. Generally the animal host harbours a phototrophic partner, usually a cyanobacteria or a unicellular alga. An exception to this rule is found in some sea slugs, which only retain the chloroplasts of the algal food source and maintain them photosynthetically active in their own cytosol – a phenomenon called ‘functional kleptoplasty’. Research has focused largely on the biodiversity of photosymbiotic species across a range of taxa. However, many questions with regard to the evolution of the ability to establish and maintain a photosymbiosis are still unanswered. To date, attempts to understand genome adaptations which could potentially lead to the evolution of photosymbioses have only been performed in cnidarians. This knowledge gap for other systems is mainly due to a lack of genetic information, both for non-symbiotic and symbiotic species. Considering non-photosymbiotic species is, however, important to understand the factors that make symbiotic species so unique. Herein we provide an overview of the diversity of photosymbioses across the animal kingdom and discuss potential scenarios for the evolution of this association in different lineages. We stress that the evolution of photosymbiosis is probably based on genome adaptations, which (i) lead to recognition of the symbiont to establish the symbiosis, and (ii) are needed to maintain the symbiosis. We hope to stimulate research involving sequencing the genomes of various key taxa to increase the genomic resources needed to understand the most fundamental question: how have animals evolved the ability to establish and maintain a photosymbiosis? Key words: evolutionary genomics, biodiversity, photosynthesis, photosymbiosis, kleptoplasty. CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 II. Biodiversity of photosymbiosis in animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 (1) Photosymbioses in Porifera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 (2) Photosymbioses in Cnidaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 (3) Photosymbioses in basal bilaterians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 (4) Photosymbioses in molluscs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 (5) Photosymbioses in chordates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 (6) Photosymbioses is also widely distributed in protists . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 III. Evolution of photosymbioses in animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 IV. Evolutionary genomics of photosymbioses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 (1) Onset and maintenance of photosymbioses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 (2) Maintenance of the symbiont includes phagosome arrest and ROS tolerance . . . . . . . . . . . . . . . . . . . . . . . . 8 (3) Most lineages lack genomic information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 (4) Implications of the mode of symbiont transmission on the evolution of the host genome . . . . . . . . . . . . . 9 (5) Additional genomes of non-model organisms are needed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

* Address for correspondence (Tel: +351 234 370 968; E-mail: [email protected]) Biological Reviews (2018) 000–000 © 2018 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Jenny Melo Clavijo and others

2

V. VI. VII. VIII.

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I. INTRODUCTION In 1878, Heinrich Anton de Bary defined symbiosis as a long-term relationship between organisms from different species (de Bary, 1878). It is found among all domains of life and classified as either mutualistic (both partners benefit), commensalistic (just one partner benefits, but without harming the other), or parasitic (one partner is negatively affected by the other) (Decelle, Colin & Foster, 2015). A particular form of symbiosis is endosymbiosis, in which one symbiotic partner lives within the other (Sagan, 1967; Kutschera & Niklas, 2005). A special form of mutualistic symbiosis is photosymbiosis (Cowen, 1988). This term is used when a heterotrophic organism acquires the benefits of photosynthesis by establishing an extra- or intracellular mutualistic symbiosis with a phototrophic organism (Buchner, 1921; Yonge, 1934; Cowen, 1988). Perhaps surprisingly, photosymbioses in animals are widespread across multiple phyla including sponges, cnidarians, acoelomorphs, platyhelminths, molluscs, ascidians, and even some vertebrates (Yonge, 1934; Venn, Loram & Douglas, 2008; Rumpho, Summer & Manhart, 2000). The vast majority of photosymbiotic animals inhabit marine environments, with the notable exception of few freshwater species (see online Supporting Information, Table S1) (e.g. Jensen & Pedersen, 1994; Huss, 1999; McCoy & Balzer, 2001). Generally, the phototrophic symbionts are either oxygenic photosynthetic bacteria, cyanobacteria, or unicellular algae (Trench, 1987; Venn et al., 2008; Kirk & Weis, 2016). A functionally unique system of acquiring the benefits of photosynthesis in animals is found among members of sacoglossan sea slugs. These marine gastropods are able to ‘steal’ and retain only the chloroplasts of their food algae: these are referred to as kleptoplasts (‘stolen plastids’) (Rumpho et al., 2011). In some species, the kleptoplasts remain photosynthetically active even during times of starvation (Wägele et al., 2011; Rumpho et al., 2011; Christa et al., 2015). This is referred to as functional kleptoplasty (Waugh & Clark, 1986), for which the term photosymbiosis is not entirely accurate, because the endosymbiosis only involves a non-reproducing organelle. However, the kleptoplasts may (perhaps transiently) benefit from their intracellular presence in the animal host due to enriched availability of carbon dioxide (Serôdio et al., 2014). In metazoans, functional kleptoplasty is taxonomically restricted to Sacoglossa, but it is also found in some protists, including Ciliates and Foraminifera (Pillet, de Vargas & Pawlowski, 2011; Pillet & Pawlowski, 2012; Not et al., 2016). The mechanisms involved in the recognition and incorporation of a symbiont by the animal host are now

10 10 10 15

under intensive investigation. The symbionts are either taken up from the environment (horizontal transmission) or they are passed from parent to offspring (vertical transmission) during reproduction (Muller-Parker, D’elia & Cook, 2015). Inside the animal host, the symbionts may enter a ‘vegetative cyst’ phase where the cell cycle is arrested and the symbionts are potentially under host control. For example, the dinoflagellate Symbiodinium is only found in non-motile forms inside hosts (Koike et al., 2004; Stambler, 2011) in which they are surrounded by a membrane, called a symbiosome in corals (Stambler, 2011) or perialgal vacuole in Hydra (McNeil, 1981). These symbiont compartments are important to guarantee the regulation of molecular exchanges and of the symbiont environment (Blackall, Wilson & Oppen, 2015). Whether kleptoplasts reside in such a membrane is still under debate (Rumpho, Summer & Manhart, 2000; Muniain, Marin & Penchaszadeh, 2001; Hirose, 2005; Martin, Walther & Tomaschko, 2013, 2015). The host shelters the symbiont or the kleptoplasts against predators and environmental fluctuations, and supplies sufficient inorganic compounds, such as CO2 , for photosynthesis (Pearse & Muscatine, 1971; Stat, Carter & Hoegh-Guldberg, 2006; Yellowlees, Rees & Leggat, 2008), although CO2 limitation in the host can occur (Rädecker et al., 2017). In turn, the host receives photosynthates, mainly in the form of fixed carbon, which can meet at least 50% of their overall nutritional requirements (Fitt, Fisher & Trench, 1986; Klumpp & Griffiths, 1994; Stat et al., 2006; Hernawan, 2008; Stanley & Lipps, 2011). In comparison, kleptoplasts are probably only able to supply their host slugs with between 1% (Rauch et al., 2017) and 60% (Raven et al., 2001) of their nutritional requirements. The discrepancy between the latter two values presumably arises from methodological differences, emphasising the need for further studies to unravel the true extent of nutritional support provided by kleptoplasts. Extensive studies have been carried out on the biodiversity and physiology of symbionts and their hosts. However, the evolution of photosymbiosis is comparatively less well understood. Recent advances in next-generation-sequencing techniques now allow us to analyse these symbionts and hosts from an evolutionary genomics perspective. While many recent studies have focused on the transcriptomic and genomic properties of the symbiont, only a few have begun to examine the host. Comparative analyses involving multiple photosymbiotic and non-photosymbiotic animal lineages are important to answer the most fundamental question: what genomic adaptations have enabled the evolution of photosymbiosis in animals?

Biological Reviews (2018) 000–000 © 2018 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Evolution of photosymbiosis II. BIODIVERSITY OF PHOTOSYMBIOSIS IN ANIMALS (1) Photosymbioses in Porifera The photosymbiotic relationship of marine sponges is regarded as a driving force for the establishment of reefs over a wide geological timescale (Lipps & Stanley, 2016a). Sponges are probably the most diverse group in terms of number of photosymbiotic species and the variety of symbionts (Fig. 1). For example, in some temperate and tropical regions more than 60% of sponge species were found to harbour photosymbionts from multiple different lineages (Steindler, Beer & Ilan, 2002; Lemloh et al., 2009). Photosymbiosis is found in four Porifera classes: Demospongiae, Hexactinellida, Homoscleromorpha, and Calcarea (Díaz & Ward, 1999; Díaz et al., 2007; Fromont et al., 2016). While most species generally establish photosymbiosis with cyanobacteria (Fig. 1; Usher, 2008; Adams, Duggan & Jackson, 2012; Thacker & Freeman, 2012), demospongian sponges might also harbour green non-sulfur bacteria of the genus Chloroflexi (Schmitt et al., 2011; Webster & Taylor, 2012), members of the Clionaidae are symbiotic with the dinoflagellate Symbiodinium (Fig. 1; Granados et al., 2008; Hill et al., 2011), chlorophyte algae such as Chlorella are found in Spongilla (Fig. 1; Reisser, 1984), and even rhodophytes like Ceratodictyon spongiosum are symbiotic with Sigmadocia symbiotica (Tan et al., 2000). Antarctic sponges harbour diatoms, which are, however, reported to become parasitic and use the host tissue as an energy source when photosynthesis is limited (Bavestrello et al., 2000; Cerrano et al., 2000). (2) Photosymbioses in Cnidaria Together with sponges, corals are the main contributors in establishing reefs (Stanley & Lipps, 2011; Lipps & Stanley, 2016b) and the diversity of species that harbour photosymbionts is comparable between these two taxa. Yet, cnidarians are either photosymbiotic with chlorophytes (Kovacevic, 2012) or dinoflagellates (Muller-Parker et al., 2015); in rare cases even with both (Fig. 1; Verde & McCloskey, 1996). Their photosymbiosis with Symbiodinium is thought to underlie the ability of corals to form massive reefs: more than 95% of the energy required is provided by the symbiont’s photosynthetic activity (Muscatine, Pool & Trench, 1975; Stat et al., 2006; Harii, Yamamoto & Hoegh-Guldberg, 2010; Stanley & Lipps, 2011). This energetic boost provides the energy needed for light-enhanced calcification (Goreau, 1959; Muscatine et al., 1975; Roth, 2014). In particular tropical and temperate members of Anthozoa, Hexacorallia and Octocorallia harbour photosymbionts, while the sister group to Hexacorallia, the Ceriantharia, are photosymbiont-free (Rodríguez et al., 2014; Stampar, Morandini & Da Silveira, 2014). Sister to Anthozoa is the clade Medusozoa which includes Hydrozoa, Scyphozoa, Staurozoa and Cubozoa. While the latter two taxa are not reported to be symbiotic,

3 some members of the Scyphozoa, the upside-down jellyfish of the genus Cassiopea, harbour Symbiodinium (Thornhill et al., 2006; Lampert, 2016). In Hydrozoa, the situation is more complex: the H. viridissima group (also referred to as green Hydra), the H. vulgaris group and the H. oligactis group are symbiotic with chlorophyte algae of the genus Chlorella or Chlorococcum (Matthias, Frederike & Thomas, 2003; Bosch, 2012; Kawaida et al., 2013), but only in H. viridissima is the symbiosis stable (Kawaida et al., 2013; Ishikawa et al., 2016). The H. braueri group, however, is completely symbiont-free (Kovacevic, 2012). (3) Photosymbioses in basal bilaterians Acoelomorphs are particularly abundant in marine and brackish water habitats but are rather poorly investigated with regard to photosymbiosis (McCoy & Balzer, 2001). All photosymbiotic members belong to the Convolutidae of the ‘Acoelomorpha’ (Paps, Baguña` & Riutort, 2009). The ‘Acoelomorpha’ were previously assigned to Platyhelminthes but recent phylogenetic studies indicate a paraphyletic nature, and place the Acoela as the sister group to all bilaterians (Hejnol et al., 2009; Mwinyi et al., 2010; Philippe et al., 2011). The nature of the symbionts of Acoela is poorly understood. In some taxonomic reports the symbiont is simply described as zoochlorella or zooxanthella (Fig. 1; Ax, 1970; Shannon & Achatz, 2007). This uncertainty arises because of issues with culturing and the lack of proper morphological identification of the algae. The convolutids Symsagittifera roscoffensis and Convolutriloba longifissura harbour the chlorophyte Tetraselmis convolutae (Bartolomaeus & Balzer, 1997; Serôdio et al., 2011), while Amphiscolops sp., A. langerhansi, Waminoa litus, and W. brickneri can harbour the dinoflagellates Symbiodinium and/or Amphidinium klebsii (Taylor, 1971; Lopes & Silveira, 1994; Barneah et al., 2007; Hikosaka-Katayama et al., 2012). Convoluta convoluta harbours the diatom Licomorpha sp. (Fig. 1; Ax & Apelt, 1965; Apelt, 1969). Photosymbiosis is also found in freshwater platyhelminths belonging to the Rhabdocoela, but this is probably the least-understood system. Here, particular members of the Provorticidae, Dalyeliidae, and Typhloplanidae are symbiotic. Members of the genus Pogaina of the Provorticidae, e.g. Pogaina kinnei, feed on diatoms and presumably retain them as symbionts (Ax, 1970). Dalyellia viridis (Dalyelliidae), Typhloplana viridata and Phaenocora typhlops (both Typhloplanidae) live symbiotically with the chlorophyte Chlorella sp. (Eaton & Young, 1975; Douglas, 1987). Various other members are photosymbiotic with as yet undescribed algae (Ax, 1970; Armonies, 1989; McCoy & Balzer, 2001). (4) Photosymbioses in molluscs In Mollusca, photosymbiosis is taxonomically restricted to some bivalves and gastropods. Tropical marine bivalves from the family Cardiidae host the dinoflagellate Symbiodinium (Ohno, Katoh & Yamasu, 1995; Maruyama et al., 1998; Hernawan, 2008). This bivalve family encompasses large


4


Fig. 1. Sankey diagram of animal taxa that are photosymbiotic and their respective symbiotic partner. Most animal lineages establish a symbiosis with dinoflagellates or with chlorophytes, but may also with cyanobacteria or even, in rare cases, diatoms. Diatoms are, however, reported to be parasitic in arctic sponges. Some members of Porifera might also be symbiotic with green-sulfur bacteria or red algae, but as this is only known from a few taxa, they are not included in the figure. Some members of the sacoglossan sea slugs only incorporate chloroplasts, which are then referred to as kleptoplasts.

species that can reach up to 1 m in diameter, like Tridacna, and are occasionally referred to as giant clams (Vermeij, 2013). Their exceptionally large sizes are thought to result from the establishment of symbioses (Griffiths & Klumpp, 1996) often with several clades of Symbiodinium (Baillie, Belda-Baillie & Maruyama, 2000; DeBoer et al., 2012; Ikeda et al., 2017). The major characteristic of cardiids is an enlarged and colourful mantle, in which Symbiodinium is hosted in extracellular spaces (Hernawan, 2008). This is different from other photosymbiotic systems, in which the symbiont resides intracellularly (Wakefield & Kempf, 2001). Besides Tridacninae (Hirose, 2005), photosymbiosis in the Cardiidae is also found in members of the Fraginae (Farmer, Fitt & Trench, 2001), but is lacking in the Laevicardiinae and Trachycardiinae (Maruyama et al., 1998). The only known photosymbiotic freshwater bivalve belongs to the genus Anodonta and hosts the chlorophyte Chlorella (Goetsch & Scheuring, 1926; Pardy, 1980). In contrast to the photosymbiotic Cardiidae, the symbionts in Anodonta reside in the gills and mantle (Pardy, 1980). In gastropods photosymbiosis is found in various genera. The ceanogastropod Strombus gigas hosts Symbiodinium (Banaszak, Ramos & Goulet, 2013). The snails acquire the symbiont during the larval stage (Garcia-Ramos &

Banaszak, 2007) and the symbiosis only appears to be mutualistic at this stage. In adults it takes a parasitic form: the snails provide nutrition to their symbiont because the presence of a shell reduces the possibility of photosynthesis (Banaszak et al., 2013). This is the only known member of the Caenogastropoda reported to be photosymbiotic (Garcia-Ramos & Banaszak, 2007). Among heterobranch sea slugs (Gastropoda) two very different systems of photosynthetic symbiosis have been described. (i) Some members of the Nudibranchia acquire symbionts by feeding on photosymbiotic cnidarians and subsequently embed the symbiotic algae (Symbiodinium) in their own cytosol (Burghardt et al., 2005; Burghardt, Stemmer & Wägele, 2008). Several different taxa are able to carry Symbiodinium: Melibe engeli (Dendronotida) harbours a dinoflagellate acquired from an unknown source (Burghardt et al., 2008); members of the Aeolidida, e.g. Berghia stephanieae and Spurilla neapolitana, ingest Symbiodinium after feeding on Anthozoa (Carroll & Kempf, 1990; Schlesinger et al., 2009; Dionísio et al., 2013); and the feacellinidean Phyllodesmium briareum obtains its symbionts from feeding on the soft coral Briareum violaceum (Burghardt et al., 2008). (ii) Members of the Sacoglossa remove the cell contents of their macroalgal food and specifically sequester the chloroplasts, which are then


Evolution of photosymbiosis called kleptoplasts (Fig. 1), in cells of their digestive system (Händeler et al., 2009). However, the basal-branching shelled Oxynoacea, e.g. Cylindrobulla schuppi or Oxynoe antillarum, and most Limapontioidea (e.g. Placida dendritica), are not able to ingest the kleptoplasts in a functional state and instead digest them rather quickly (Christa et al., 2015). By contrast, some members of the Costasiellidae, such as Costasiella ocellifera or C. kuroshimae and most Plakobranchaceae, e.g. Elysia timida or Plakobranchus ocellatus, are able to retain photosynthetic activity in the kleptoplasts, even during starvation (Christa et al., 2014, 2015; de Vries, Christa & Gould, 2014; Wägele & Martin, 2014). (5) Photosymbioses in chordates A few chordates are known to be able to establish photosymbiosis. Knowledge about the diversity and physiology of this phenomenon is, however, scarce. A lifelong and obligate relationship in chordates is found only in tropical colonial ascidians from the family Didemnidae. These ascidians are mainly associated extracellularly with cyanobacteria from the genus Prochloron (Hirose, 2015) or in a few cases with the cyanobacterium Synechocystis trididemni (Fig. 1; Hirose et al., 2009). The ascidian Lissoclinum punctatum is known to incorporate Prochloron intracellularly in phycocyte cells (Hirose et al., 1996). A total of 30 species from four genera of Didemnidae (Didemnum, Trididemnum, Diplosoma and Lissoclinum) have been reported to establish photosymbiosis (Hirose et al., 2009; Hirose, 2015). In higher Chordata, embryos of the spotted salamander Ambystoma maculatum share a symbiosis-like association with the green alga Oophila amblystomatis (Fig. 1; Gilbert, 1942, 1944). Unlike the symbioses discussed above, the symbiont is located in the egg capsules of the salamander, mainly around the embryo blastopore (Kerney, 2011). The eggs are covered by jelly and appear to be green due to the dense accumulation of algae, which invades the embryonic tissues (somatic cells and endodermal cells around the alimentary canal) during development (Kerney, 2011). Once in the eggs, the algae enter a coccoid stage and may be either in direct contact with the host cytoplasm or surrounded by an outer envelope. This envelope is not the distinct symbiosomal membrane seen in corals, rather resembling an algal encystment process (Kerney, 2011). Other amphibian species also establish symbiosis in embryonic stages with Oophila algae: the north-western salamander A. gracile, the Jefferson salamander A. jeffersonium and the tiger salamander A. trigrinum, the japanese black salamander Hynobius nigrescens (Muto et al., 2017), the wood frog Lithobates sylvaticus and the red-legged frog L. aurora (Kerney et al., 2011). (6) Photosymbioses is also widely distributed in protists Photosymbiosis has evolved multiple times in the protist phyla Ciliophora, Foraminifera, Radiolaria, Dinoflagellata and diatoms (Decelle et al., 2015). Among these, Foraminifera and Radiolaria are skeleton-building protists who establish

5 photosymbiosis as primary producers of open ocean planktonic communities (Decelle et al., 2015). Photosymbiotic Foraminifera play a major ecological role contributing to the global carbon cycle and to 25% of carbonate calcium deposits (Langer, Silk & Lipps, 1997; Erez, 2003; Lipps & Stanley, 2016b). Foraminifera acquire their symbionts either vertically or horizontally (Fay, Weber & Lipps, 2009). They associate with a variety of symbionts including dinoflagellates, diatoms, rhodophytes, chlorophytes and cyanophytes (Hansen & Buchardt, 1977; Hansen & Dalberg, 1979; Smith, 1991; Lee, 2006; Lipps & Stanley, 2016b), a range that covers all known symbionts from animal lineages. Of the 150 foraminiferan families, 10% are hosts of algal symbionts (Lee & Anderson, 1991). Benthic foraminiferans either establish symbioses with Symbiodinium (Schmidt, Kucera & Uthicke, 2014) or, as in Sacoglossa, retain only the chloroplasts from their algal prey (Bernhard & Bowser, 1999; Pillet et al., 2011; Pillet & Pawlowski, 2012). Planktonic foraminiferans, however, mainly associate with the dinoflagellate Pelagodinium, a sister taxon of Symbiodinium (Decelle et al., 2015). The symbiotic relationship between photosynthetic partners and Foraminifera is sensitive to environmental stressors that can cause a massive release of symbionts known as bleaching (Hallock, Forward & Hansen, 1986; Hallock et al., 2003, 2006). In this sense, Foraminifera have been used as indicators of water quality and temperature of the reef ecosystem (Reymond, Uthicke & Pandolfi, 2012).

III. EVOLUTION OF PHOTOSYMBIOSES IN ANIMALS Although there are many records showing the biodiversity of photosymbioses in animals, we lack information on the evolution of these symbioses across most lineages. Figure 2 provides a brief overview of the phylogenetic relationships among non-photosymbiotic or photosymbiotic taxa. Given the tremendous diversity of photosymbiotic species, this figure contains only hypothetical origins or losses of photosymbiosis in the respective clades. Sponges are probably the sister taxon to all other metazoans (Philippe et al., 2009; Jékely, Paps & Nielsen, 2015; Pisani et al., 2015; Whelan, Kocot & Halanych, 2015). Surprisingly, no studies of the great diversity of photosymbiosis in sponges have been carried out. On the basis of current evolutionary hypotheses (Wörheide et al., 2012; Simion et al., 2017) and the fact that photosymbiotic species exist in all sponge classes, it is possible that the ability to incorporate symbionts either evolved in the last common ancestor (LCA) of all sponges with subsequent multiple losses in different lineages or that several independent acquisitions occurred (Fig. 2). In cnidarians, several analyses on single taxa have been performed to clarify the evolution of photosymbiosis (Kawaida et al., 2013; Schwentner & Bosch, 2015; Ishikawa et al., 2016). Phylogenetic analyses in Hydra (Kawaida et al., 2013; Schwentner & Bosch, 2015) suggest the evolution of


6


Fig. 2. Legend on next page. Biological Reviews (2018) 000–000 © 2018 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Evolution of photosymbiosis non-stable symbiosis in the LCA of the Hydra group, while stable symbiosis originated in the LCA of the H. viridissima group (Fig. 2). Under this scenario, non-stable symbiosis has been secondarily lost in the LCA of the H. braueri group (Fig. 2). Thus, symbiosis in Hydra was established first followed later by mechanisms allowing a long and stable symbiosis (e.g. oxidative stress tolerance) (Ishikawa et al., 2016). Among cnidarians four distinct taxa evolved photosymbiosis, i.e. Hexacorallia, Octocorallia, Scyphozoa, and Hydrozoa (Fig. 2; Kayal et al., 2013; Stampar et al., 2014; Zapata et al., 2015). Yet, whether this reflects independent acquisitions of symbiotic taxa or multiple losses is unclear (Fig. 2). Phylogenetic analyses in Acoela are mainly focused on their taxonomic position within bilaterians (Paps et al., 2009) or on the evolution of selected morphological characters (Jondelius et al., 2011). Based on published, unresolved phylogenies, photosymbiosis evolved in the LCA of the Convolutidae clade of the Acoela (Fig. 2; Jondelius et al., 2011). The phylogeny of Platyhelminthes is also under intense investigation. The photosymbiotic Dalyellia viridis and Typhloplana viridata are distantly related to photosymbiotic members of the Provorticidae, such as Pogaina kinnei (Fig. 2; Jondelius & Thollesson, 1993; Littlewood et al., 1999; Zamparo et al., 2001; Van Steenkiste et al., 2013). Thus, photosymbioses may have evolved at least twice independently in the platyhelminthes (Fig. 2), or was lost in the Dugesiidae, such as Schmidtea meditteranea (Fig. 2). Recent phylogenetic analyses in molluscs (Giribet & Wheeler, 2002) suggest that photosymbioses evolved at least twice in bivalves, once in Anodonta sp. (Pardy, 1980) and once in the Cardiidae. For the latter, two scenarios for the evolution of photosymbiosis are feasible, based on their phylogenetic position (Maruyama et al., 1998): either photosymbiosis evolved in the LCA of Cardiidae and was subsequently lost in the sister taxa Laevicardiinae (e.g. Fulvia) and Trachycardiinae (e.g. Vasticardium) (Fig. 2) or two independent acquisitions occurred, once in the LCA of Fraginae (e.g. Corculum) (Kirkendale, 2009) and once in the LCA of Tridacnidae (e.g. Fragum) (Fig. 2; Maruyama et al., 1998). In Nudibranchs, photosymbioses evolved at least twice, once in the LCA of Melibe and once in Aeolidida (Fig. 2).

7 In Aoelidida several gains or losses of photosymbioses are conceivable, as most genera include photosymbiotic and non-photosymbiotic members (Fig. 2). No analyses have yet been conducted with regard to the most likely evolutionary scenarios and the phylogenetic reconstructions in this group are still ongoing. In sacoglossans, functional kleptoplasty was acquired at least twice, once in the LCA of Costasiellidae and once in the LCA of the Plakobranchacea (Fig. 2; Christa et al., 2015). There is little information on the evolution of photosymbioses in chordates. In Ascidia, more than 30 species from four genera of the Didemnidae are photosymbiotic, but their congeners are mostly non-symbiotic (Fig. 2). This suggests multiple origins of this symbiosis (at least once in each genus) in the ascidians (Fig. 2; Yokobori et al., 2006), but further work is needed. In amphibians, the photosymbiotic salamanders of the genus Ambystoma and Hynobius and frogs of the genus Lithobathes are only distantly related. Thus, again photosymbiosis is likely to have evolved several times independently (Fig. 2).

IV. EVOLUTIONARY GENOMICS OF PHOTOSYMBIOSES In addition to the uncertainties in scenarios of how photosymbioses evolved, the underlying molecular mechanisms needed to establish and maintain photosymbioses also remain largely unknown. (1) Onset and maintenance of photosymbioses In corals, detailed work unravelling the genomic adaptations that enable photosymbiosis has increased our understanding of the onset and maintenance of this symbiosis significantly (Baumgarten et al., 2015; Neubauer et al., 2016, 2017; van der Burg et al., 2016). Discrimination by the coral host among symbionts, pathogens, and food particles is key to symbiosis establishment and depends most likely on features of the host innate immune system (Davy, Allemand & Weis, 2012). It involves the recognition of specific microbial-associated molecular patterns (MAMPs) of the symbiont or pathogen by pattern-recognition receptors (PRRs) (Davy et al., 2012). In symbiotic cnidarians a set of PRRs has been identified

Fig. 2. Metazoan lineages in which photosymbioses occurs. Several animal lineages from different habitats (column 1: marine, cyan circles; freshwater, blue circles; terrestrial, green circles) have a symbiotic relationship with a phototrophic partner. For almost all metazoan lineages, evolutionary scenarios of how photosymbioses evolved are not available. For Sacoglossa, two studies investigated the most likely evolution of functional kleptoplasty (blue circles in the tree). Based on studies on photosymbiotic and non-photosymbiotic taxa (column 2: green and white circles, respectively), different hypothesis of evolving (red circles in the tree) or losing (white circles in the tree) photosymbioses are feasible. Unfortunately, for the vast majority of taxa neither genome (column 3) nor transcriptome (column 4) data exist (black circles, present; white circles, absent). Tree assembled from published studies (Maruyama et al., 1998; Zamparo et al., 2001; Yokobori et al., 2006; Kirkendale, 2009; Jondelius et al., 2011; Pyron & Wiens, 2011; Wörheide et al., 2012; Carmona et al., 2013; Kawaida et al., 2013; Kayal et al., 2013; Van Steenkiste et al., 2013; Rodríguez et al., 2014; Christa et al., 2015; Schwentner & Bosch, 2015; Zapata et al., 2015). Photograph credits: Heike Wägele (Didemnum, Costasiella, Phyllodesmium, Tridacna, Briareum, Haliclona), João Serôdio (Symsagittifera) and Jenny Melo (Ambystoma). Biological Reviews (2018) 000–000 © 2018 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

8 that is absent in non-symbiotic species: a repertoire of thrombospondin-type-1 repeat protein (TSR) (Neubauer et al., 2017) and a set of expanded scavenger receptors (SRs), including a unique c-type lectin domain (LOX1), several scavenger receptor cystein-rich (SRCR) receptors, and a specific set of Class B scavenger receptors (CD36) (Neubauer et al., 2016). Experimental studies on SRs and TSRs support their role in symbiont recognition (Rodriguez-Lanetty, Phillips & Weis, 2006; Lehnert et al., 2014; Neubauer et al., 2016, 2017). Additionally, cnidarian ficolin-like (CniFL) proteins are found in symbiotic and non-symbiotic cnidarians, but their role in symbiont recognition is still debated (Baumgarten et al., 2015; van der Burg et al., 2016). Recently, a study in a functional kleptoplast bearing sea slug showed that similar factors as in corals might be involved in plastid recognition (Chan et al., 2018). (2) Maintenance of the symbiont includes phagosome arrest and ROS tolerance Stable and long-lasting photosymbiosis is thought to be dependent on cellular response mechanisms coping with elevated levels of reactive oxygen species (ROS) (Kawano et al., 2004; Johnson, 2011; Ishikawa et al., 2016). In Hydra vulgaris and H. viridissima, the host first establishes the symbiosis and later develops tolerance to oxidative stress. Gene expression studies showed that H. vulgaris is less tolerant to ROS in an aposymbiotic state than in symbioses (Ishikawa et al., 2016). Under stress conditions, such as excessive light or high temperature, corals suffer from ROS stress generated by their symbionts (although the host itself is also stressed by high temperature). The symbiosis is then disrupted and the symbionts are expelled by various cellular mechanisms (Weis, 2008). In Sacoglossa, ROS tolerance was recently hypothesized to play a role in enduring long periods of starvation (de Vries et al., 2015). Although not studied in detail, it seems that coping with elevated ROS levels, potentially produced by the symbiont, is a common mechanism in different animal lineages to maintain the symbiosis. Besides ROS tolerance, stopping or delaying digestion allows stable integration and maintenance of the symbioses (Rodriguez-Lanetty et al., 2006; Dunn, Schnitzler & Weis, 2007; Voolstra et al., 2009). The mechanism behind such digestion control is unknown. For corals, the ‘arrested phagosome’ hypothesis attempts to provide one explanation (Hill & Hill, 2012), although experimental verification and analyses of genomic regulation that would enable this are still missing. This is of particular interest as selective forces could act on genomic adaptations to allow the evolution of photosymbiosis. For instance, nutritional support provided by the symbiont might lead to (i) better survival in oligotrophic waters, (ii) reduced predation through an associated increase in body size, or (iii) the ability to endure periods of starvation (especially in gastropods). Such ecological benefits could also explain why photosymbiosis apparently evolved multiple times independently within various taxa. However, nutritional support may not be the only factor. Often non-photosymbiotic species are sympatric

Jenny Melo Clavijo and others within the same habitat and in the case of gastropods, non-photosymbiotic species often have the same survival during periods of starvation as photosymbiotic species. It remains important to identify potential evolutionary forces leading to genome adaptations to identify the relevant genome adaptions. (3) Most lineages lack genomic information Unfortunately, analyses focusing on genomic adaptations that allow the establishment and maintenance of photosymbiosis in most symbiotic species other than corals are absent. This is partly due to the lack of available genome sequences, especially of photosymbiotic species. In sponges, analyses of genomic and transcriptomic data have focused on carbon and nitrogen metabolism, vitamin biosynthesis, and proteins that act as symbiont factors (Hentschel et al., 2012). However, data for candidate sponge species to understand the evolutionary genomics involved in photosymbioses are still lacking (Pita, Fraune & Hentschel, 2016). The genomes of the anthozoans Acropora digitifera, Aiptasia pallida and Nematostella vectensis, several transcriptomes of other anthozoan species, the genome of the hydrozoan Hydra vulgaris (Chapman et al., 2010) and the transcriptome of H. viridissima (Ishikawa et al., 2016) have been published (see online Supporting Information, Table S1). The Hydra genome is highly complex and exhibits dramatic changes in genome size. The smallest genome is estimated for H. viridissima (380 Mbp) based on microphotometry of Feulgen-stained nuclei of epithelial and interstitial cells (Zacharias et al., 2004; Chapman et al., 2010; Bosch, 2012). According to Bosch (2012) this small genome size could be related to the small cell size of H. viridissima and contributions of the symbiont to the host’s metabolism. Likewise, the highly reduced genome of strepsiterian insects is hypothesized to be a result of their parasitic lifestyle (Niehuis et al., 2012). Because stable symbioses only evolved in the H. viridissima group, comparative analyses of genomes of the other three Hydra groups could shed light on adaptations needed to maintain photosymbiosis. Unfortunately, no genomic or transcriptomic data are accessible for any photosymbiotic member of the Acoela or Platyhelminthes (Fig. 2). Only the genome of the free-living freshwater planarian Schmidtea mediterranea has been sequenced to date, a non-photosymbiotic species frequently used in regeneration, tissue homeostasis, and stem-cell research (Robb et al., 2015). Few studies using genomic resources have been performed among molluscs. Among bivalves only the genome of the pacific oyster Crassostrea gigas has been sequenced (Zhang et al., 2012). For the photosymbiotic Tridacna maxima, Mies et al. (2017b) showed that four specific genes are expressed during the onset of the symbiosis: a clam-specific actin, a symbiont-specific Ribulose-1,5bisphosphate-carboxylase/-oxygenase (RuBisCO) gene, a symbiosis-specific H+ -ATPase gene and an aldo-keto oxidoreductase gene. The H+ -ATPase gene is considered


Evolution of photosymbiosis a symbiosis indicator, since it is expressed in symbiotic cells of Symbiodinium and not in free-living or aposymbiotic cells (Bertucci et al., 2009). By contrast, Symbiodinium expresses aldo-keto oxidoreductase only in the presence of light, both in free-living and in symbiotic forms (Mies et al., 2017b). This protein is necessary for glycerol synthesis (Jez et al., 1997), which might be continuously translocated to Tridacna (Mies et al., 2017b). Yet, no genomic sequences of these bivalve hosts are available to facilitate the search for further genetic factors that might underpin the establishment or maintenance of symbiosis. In sea slugs, only the draft genome of Aplysia californica is currently available (https://www.broadinstitute.org/ aplysia/aplysia-genome-project, last updated in 2013). For the kleptoplastic sacoglossan Elysia chlorotica a non-assembled short-read draft genome exists (Bhattacharya et al., 2013). Transcriptomic data sets have been generated for 13 nudibranch species (Goodheart et al., 2015) and five sacoglossans (Schwartz, Curtis & Pierce, 2010; Wägele et al., 2010; Han et al., 2015; de Vries et al., 2015): in Nudibranchia only one out of the 13 sequenced species is symbiotic, in Sacoglossa four. In Sacoglossa one study compared the transcriptomic response of two species that differed in longevity of plastid retention (de Vries et al., 2015). Yet, we still do not understand what sets functional kleptoplasty species apart from non-kleptoplastic sister taxa. Among Ascidia the genome of the carpet sea squirt, Didemnum vexillum (Didemnidae), has been sequenced (Velandia-Huerto et al., 2016). This non-symbiotic species (Lin et al., 2016) is currently considered a highly successful invasive taxon (Bullard et al., 2007; Lengyel, Collie & Valentine, 2009; Locke & Carman, 2009; Stefaniak et al., 2012). In addition, the genomes of seven non-photosymbiotic species, i.e. Ciona intestinalis (Dehal et al., 2002), Ciona savignyi (Small et al., 2007), Botryllus schlosseri (Voskoboynik et al., 2013), Oikopleura dioca (Seo et al., 2001), and three species of Molgula (Stolfi et al., 2014), have been sequenced (see online Supporting Information, Table S1). No genetic and transcriptomic data regarding the unique association between didemnidaen ascidians and Prochloron are available. No studies have reported genomic information from amphibian–algae symbioses. The closest species to photosymbiotic salamanders with a sequenced genome and available transcriptome is the non-symbiotic Mexican axolotl Ambystoma mexicanum, well known for its ability to regenerate amputated limbs and for its neotenic form with external gills and caudal fin (Wu et al., 2013; Keinath et al., 2015). Recently, thorough comparative transcriptomic analysis of the expression of cells of photosymbiotic Ambystoma maculatum bearing Oophila algae, alga-free cells, and eggs with extracellular algae have been performed (Burns et al., 2017). Interestingly, algae in host cells show stress responses and a shift in energy acquisition compared to algae inside the egg capsule. Under low light conditions and low oxygen levels, intracellular algae obtain phosphates and glutamine from their host, but rely on fermentation instead of photosynthesis (Burns et al., 2017). Salamander cells with intracellular algae

9 show inhibition of immune responses to tolerate the symbiont (Burns et al., 2017). To what degree this process might also occur in other photosymbiotic clades is not known. (4) Implications of the mode of symbiont transmission on the evolution of the host genome In order to understand the genome adaptations that are needed to evolve photosymbiosis, the mode of symbiont transmission should also be considered. Acquiring symbionts horizontally always includes an aposymbiotic life stage present in all photosymbiotic animal lineages, which is usually the larval phase before metamorphosis into juveniles (e.g. Belda-Baillie et al., 1999; Weis et al., 2001; Harrison, 2011; Pelletreau et al., 2014; Mies et al., 2017a). Juveniles then successfully take up the symbiont from their environment, but there seems to be little co-evolution of species with horizontal transmission and their symbiont partners (van Oppen et al., 2001; Bright & Bulgheresi, 2010). The identification of symbionts in adult stages may mask potentially non-specific symbiont uptake during the juvenile stages. For example, in corals it has been shown that juveniles have a rather unspecific symbiont uptake and symbiont selection is based on intracellular sorting and adaptive bleaching (Buddemeier & Fautin, 1993) in adults (Little, van Oppen & Willis, 2004). This might also apply to Foraminifera (Fay et al., 2009). On what this sorting is based, i.e. if certain genome adaptations are needed or there is interspecific competition among symbionts or selection based on ecological factors, is unknown. Alternatively, the whole community of algal symbionts can be altered during re-colonization following a bleaching event (Jones et al., 2008). Thus, analyses of symbionts only at a distinct adult stage will provide only restricted information about the potential diversity of the recognition mechanisms involved. Nevertheless, it seems reasonable to assume that acquiring a broad diversity of symbionts via horizontal transmission could represent a high level of diversity in symbiont-recognition mechanisms. In this scenario, species that are only able to incorporate symbionts from a distinct lineage may have a reduced set of recognition mechanisms. Vertical transmission is found among sponges (Usher et al., 2001; Oren, Steindler & Ilan, 2005), corals (Baird, Guest & Willis, 2009; Padilla-Gaminño et al., 2012), acoelomorphs (Barneah et al., 2007; Hikosaka-Katayama et al., 2012) and ascidians (Hirose, Oka & Akahori, 2004). For this mode of transmission the symbionts need to be translocated into the reproductive system, requiring a rather complicated mechanism in ascidia, for example (Hirose, 2000). In contrast to horizontal transmission, vertical transmission might well lead to genomic adaptations and co-evolution of symbionts and hosts is likely (Barneah et al., 2004). Further, because the symbionts are not necessarily acquired from the water column, genomic adaptations for symbiont recognition could be lost during evolution. As a result, the plasticity of the recognition system might become reduced. This could provide an explanation of higher specificity of endosymbiotic algae in corals with vertical transmission



10 (Stat et al., 2008). Vertical transmission might also favour the successful colonization of environments in which the horizontally transmitted symbiont is not found (Oren et al., 2005). In species with both modes of transmission (Bright & Bulgheresi, 2010) genomic adaptation might even be more complex.

(4) Comparative analyses of photosymbiotic and non-photosymbiotic species are key to understanding what makes photosymbiotic species so special.

(5) Additional genomes of non-model organisms are needed

The authors would like to thank Heike Wägele and Matthew Nitschke for critically assessing the manuscript and for providing photographs. Funding through the Fundaça˜ o para a Ciência e a Tecnologia (FCT) to G.C. (SFRH/BPD/109892/2015), the Alexander-Koenig-Gesellschaft (AKG) to G.C., and the German Research Foundation (DFG) to A.D. (DO 1781/1-1) is gratefully acknowledged. For financial support, thanks are due to the CESAM - Centre for Environmental and Marine Studies (UID/AMB/50017), FCT/Ministry of Science and Education through national funds, and co-funding by the European Fund For Regional Development, within the PT2020 Partnership Agreement and Compete 2020.

Analyses of already sequenced transcriptomes and genomes of various photosymbiotic and non-photosymbiotic taxa will certainly help to understand the genomic adaptations needed to establish and maintain photosymbiosis. Broad taxon sampling will uncover whether these mechanisms are evolutionarily ancient or whether they are the result of convergence. In this regard it will be of particular interest to investigate Foraminifera, because they share many features of photosymbiosis with animals. To obtain the necessary information more genome data sets are needed and are preferred over transcriptomic data sets. The absence of a transcript in a sequenced transcriptome does not translate into the absence of the gene or gene product and is thus only of limited use. Nevertheless, initial studies relying on a mixture of transcriptomic and genomic resources are a first step towards understanding the adaptations necessary to evolve photosymbiosis in animals. In the near future, techniques such as single-cell RNA sequencing (scRNA-seq) and long-read sequencing, will allow more accurate determination of the transcriptional state of an organism and the identification of stage- and tissue-specific expressed and alternatively spliced genes (Shapiro, Biezuner & Linnarsson, 2013; Kolodziejczyk et al., 2015; Garalde et al., 2018).

V. CONCLUSIONS (1) The phenomenon of photosymbiosis in the animal kingdom is remarkably widespread. Many studies have increased our understanding of the biodiversity of the animal hosts and algal symbionts. However, in most lineages the evolution of photosymbiosis is still poorly known, especially with regard to selective forces leading to genome adaptations that enable the evolution of symbiont recognition and stable integration. (2) Studies in corals should inspire future analyses: specific receptors of the host innate immune system have evolved in symbiotic corals that are most likely involved in the recognition of Symbiodinium. Similar analyses for other photosymbiotic animals are absent but will be fundamental to advancing our understanding of how photosymbioses evolved, whether there are common genomic adaptations in different lineages, and how the mode of transmission might influence the genome evolution. (3) Such analyses will help to understand why some species harbour multiple symbionts of different lineages, while others are restricted to single species.

VI. ACKNOWLEDGEMENTS

VII. REFERENCES Adams, D. G., Duggan, P. S. & Jackson, O. (2012). Cyanobacterial symbioses. In Ecology of Cyanobacteria II (ed. B. A. Whitton), pp. 593–647. Springer, Dordrecht, Netherlands. *Albertin, C. B., Simakov, O., Mitros, T., Wang, Z. Y., Pungor, J. R., Edsinger-Gonzales, E., Brenner, S., Ragsdale, C. W. & Rokhsar, D. S. (2015). The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524, 220–224. *Alié, A., Hayashi, T., Sugimura, I., Manuel, M., Sugano, W., Mano, A., Satoh, N., Agata, K. & Funayama, N. (2015). The ancestral gene repertoire of animal stem cells. Proceedings of the National Academy of Sciences of the United States of America 112, E7093–E7100. *Anderson, D. A., Walz, M. E., Weil, E., Tonellato, P. & Smith, M. C. (2016). RNA-Seq of the Caribbean reef-building coral Orbicella faveolata (Scleractinia-Merulinidae) under bleaching and disease stress expands models of coral innate immunity. PeerJ 4, e1616. Apelt, G. (1969). Die Symbiose zwischen dem acoelen turbellar Convoluta convoluta und Diatomeen der Gattung Licmophora. Marine Biology 3, 165–187. Armonies, W. (1989). Semiplanktonic plathelminthes in the Wadden Sea. Marine Biology 101, 521–527. Ax, P. (1970). Neue Pogaina-Arten (Turbellaria, Dalyellioda) mit Zooxanthellen aus dem Mesopsammal der Nordsee-und Mittelmeerküste. Marine Biology 5, 337–340. Ax, P. & Apelt, G. (1965). Die ‘‘Zooxanthellen’’ von Convoluta convoluta (Turbellaria Acoela) entstehen aus Diatomeen. Naturwissenschaften 52, 444–446. Baillie, B. K., Belda-Baillie, C. A. & Maruyama, T. (2000). Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. Journal of Phycology 36, 1153–1161. Baird, A. H., Guest, J. R. & Willis, B. L. (2009). Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annual Review of Ecology, Evolution, and Systematics 40, 551–571. Banaszak, A. T., Ramos, M. G. & Goulet, T. L. (2013). The symbiosis between the gastropod Strombus gigas and the dinoflagellate Symbiodinium: an ontogenic journey from mutualism to parasitism. Journal of Experimental Marine Biology and Ecology 449, 358–365. Barneah, O., Brickner, I., Hooge, M., Weis, V. M. & Benayahu, Y. (2007). First evidence of maternal transmission of algal endosymbionts at an oocyte stage in a triploblastic host, with observations on reproduction in Waminoa brickneri (Acoelomorpha). Invertebrate Biology 126, 113–119. Barneah, O., Weis, V. M., Perez, S. & Benayahu, Y. (2004). Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Marine Ecology Progress Series 275, 89–95. *Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor-Knowles, N. & Palumbi, S. R. (2013). Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences of the United States of America 110, 1387–1392.


Evolution of photosymbiosis Bartolomaeus, T. & Balzer, I. (1997). Convolutriloba longifissura nov. spec.(Acoela)-the first case of longitudinal fission in Plathelminthes. Microfauna Marina 11, 7–18. ¨ de Bary, A. (1878). Vortrag: Uber Symbiose. In Tagblatt der 51. Versammlung Deutscher ¨ Naturforscher und Aerzte in Cassel (ed K. F. Trubner), pp. 121–126. Baier & Lewalter, Kassel. Baumgarten, S., Simakov, O., Esherick, L. Y., Liew, Y. J., Lehnert, E. M., Michell, C. T., Li, Y., Hambleton, E. A., Guse, A., Oates, M. E., Gough, J., Weis, V. M., Aranda, M., Pringle, J. R., Vollstra, C. R., et al. (2015). The genome of Aiptasia, a sea anemone model for coral symbiosis. Proceedings of the National Academy of Sciences of the United States of America 112, 11893–11898. Bavestrello, G., Arillo, A., Calcinai, B., Cattaneo-Vietti, R., Cerrano, C., Gaino, E., Penna, A. & Sara, M. (2000). Parasitic diatoms inside Antarctic sponges. Biological Bulletin 198, 29–33. Belda-Baillie, C. A., Sison, M., Silvestre, V., Villamor, K., Monje, V., Gomez, E. D. & Baillie, B. K. (1999). Evidence for changing symbiotic algae in juvenile tridacnids. Journal of Experimental Marine Biology and Ecology 241, 207–221. Bernhard, J. M. & Bowser, S. S. (1999). Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth-Science Reviews 46, 149–165. https://doi.org/10.1016/S0012-8252(99)00017-3. ´ Tambutté, S., Allemand, D. & Zoccola, D. Bertucci, A., Tambutté, E., (2009). Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+ -ATPase gene. Proceedings of the Royal Society of London B: Biological Sciences 277, 87–95. Bhattacharya, D., Pelletreau, K. N., Price, D. C., Sarver, K. E. & Rumpho, M. E. (2013). Genome analysis of Elysia chlorotica egg DNA provides no evidence for horizontal gene transfer into the germ line of this kleptoplastic mollusc. Molecular Biology and Evolution 30, 1843–1852. Blackall, L. L., Wilson, B. & Oppen, M. J. (2015). Coral—the world’s most diverse symbiotic ecosystem. Molecular Ecology 24, 5330–5347. Bosch, T. C. (2012). What Hydra has to say about the role and origin of symbiotic interactions. Biological Bulletin 223, 78–84. Bright, M. & Bulgheresi, S. (2010). A complex journey: transmission of microbial symbionts. Nature Reviews Microbiology 8, 218–230. Buchner, P. (1921). Tier und Pflanze in intrazellularer Symbiose. Gebrüder Borntraeger. Buddemeier, R. W. & Fautin, D. G. (1993). Coral bleaching as an adaptive mechanism. Bioscience 43, 320–326. Bullard, S. G., Lambert, G., Carman, M. R., Byrnes, J., Whitlatch, R. B., Ruiz, G., Miller, R., Harris, L., Valentine, P. C., Collie, J. S., Pederson, J., McNaught, D. C., Cohen, A. N., Asch, R. G., Dijkstra, J. & Heinonen, K. (2007). The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. Journal of Experimental Marine Biology and Ecology 342, 99–108. van der Burg, C. A., Prentis, P. J., Surm, J. M. & Pavasovic, A. (2016). Insights into the innate immunome of actiniarians using a comparative genomic approach. BMC Genomics 17, 850. Berlin, Germany. Burghardt, I., Evertsen, J., Johnsen, G. & Wägele, H. (2005). Solar powered seaslugs- mutualistic symbiosis of Aeolid Nudibranchia (Mollusca, Gastropoda, Opisthobranchia) with Symbiodinium. Symbiosis 38, 227–250. Burghardt, I., Stemmer, K. & Wägele, H. (2008). Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention. Organisms Diversity & Evolution 8, 66–76. Burns, J. A., Zhang, H., Hill, E., Kim, E. & Kerney, R. (2017). Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis. eLife 6, e22054. Carmona, L., Pola, M., Gosliner, T. M. & Cervera, J. L. (2013). A tale that morphology fails to tell: a molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS One 8, e63000. Carroll, D. J. & Kempf, S. C. (1990). Laboratory culture of the aeolid nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia): some aspects of its development and life history. Biological Bulletin 179, 243–253. Cerrano, C., Arillo, A., Bavestrello, G., Calcinai, B., Cattaneo-Vietti, R., Penna, A., Sarà, M. & Totti, C. (2000). Diatom invasion in the Antarctic hexactinellid sponge Scolymastra joubini. Polar Biology 23, 441–444. Chan, C. X., Vaysberg, P., Price, D. C., Pelletreau, K. N., Rumpho, M. E. & Bhattacharya, D. (2018). Active host response to algal symbionts in the sea slug Elysia chlorotica. Molecular Biology and Evolution msy061, https://doi.org/10.1093/ molbev/msy061 Chapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D., Disbennett, K., Pfannkoch, C., Sumin, N., Sutton, G. G., Viswanathan, L. D., et al. (2010). The dynamic genome of Hydra. Nature 464, 592–596. Christa, G., Gould, S. B., Franken, J., Vleugels, M., Karmeinski, D., Händeler, K., Martin, W. F. & Wägele, H. (2014). Functional kleptoplasty in a limapontioidean genus: phylogeny, food preferences and photosynthesis in Costasiella, with a focus on C. ocellifera (Gastropoda: Sacoglossa). Journal of Molluscan Studies 80, 499–507. ¨ Christa, G., Händeler, K., Kuck, P., Vleugels, M., Franken, J., Karmeinski, D. & Wägele, H. (2015). Phylogenetic evidence for multiple independent origins

11 of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda). Organisms Diversity & Evolution 15, 23–36. Cowen, R. (1988). The role of algal symbiosis in reefs through time. PALAIOS 3, 221–227. Davy, S. K., Allemand, D. & Weis, V. M. (2012). Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews 76, 229–261. DeBoer, T. S., Baker, A. C., Erdmann, M. V., Ambariyanto, Jones, P. R. & Barber, P. H. (2012). Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Marine Ecology Progress Series 444, 117–132. Decelle, J., Colin, S. & Foster, R. A. (2015). Photosymbiosis in marine planktonic protists. In Marine Protists (eds S. Ohtsuka, T. Suzaki, T. Horiguchi, N. Suzuki and F. Not), pp. 465–500. Springer, Tokyo, Japan. Dehal, P., Satou, Y., Campbell, R. K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., Goodstein, D. M., Harafuji, N., Hastings, K. E. M., Ho, I., Hotta, K., Huang, W., et al. (2002). The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298, 2157–2167. *Denoeud, F., Henriet, S., Mungpakdee, S., Aury, J. M., Da Silva, C., Brinkmann, H., Mikhaleva, L., Olsen, L. O., Jubin, C., Ca˜ nestro, C., Bouquet, J. M., Danks, B., Poulain, J., Campsteijn, C., Adamski, M., Cross, I., et al. (2010). Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330, 1381–1385. ¨ Díaz, M. C., Thacker, R. W., Rutzler, K. & Piantoni Dietrich, C. (2007). Two new haplosclerid sponges from Caribbean Panama with symbiotic filamentous cyanobacteria, and an overview of sponge-cyanobacteria associations. ´ In Porifera Research: Biodiversity, Innovation and Sustainability (eds M. R. Custodio, G. Lˆ obo-Hajdu, E. Hajdu and G. Muricy), pp. 31–39. National Museum, Rio de Janeiro, Brazil. Díaz, M. C. & Ward, B. B. (1999). Perspectives on sponge-cyanobacterial symbioses. Memoirs of the Queensland Museum 44, 154. Dionísio, G., Rosa, R., Leal, M. C., Cruz, S., Brandão, C., Calado, G., Serˆ odio, J. & Calado, R. (2013). Beauties and beasts: a portrait of sea slugs aquaculture. Aquaculture 408, 1–14. Douglas, A. E. (1987). Experimental studies on symbiotic Chlorella in the neorhabdocoel turbellaria Dalyellia viridis and Typhloplana viridata. British Phycological Journal 22, 157–161. Dunn, S. R., Schnitzler, C. E. & Weis, V. M. (2007). Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proceedings of the Royal Society of London B: Biological Sciences 274, 3079–3085. Eaton, J. & Young, J. (1975). Studies on the symbiosis of Phaenocora typhlops (Vejovsky) (Turbellaria; Neorhabdocoela) and Chlorella vulgaris var. vulgaris, Fott & Novakova (Chlorococcales). Archiv für Hydrobiologie 75, 50–75. Erez, J. (2003). The source of ions for biomineralization in Foraminifera and their implications for paleoceanographic proxies. Reviews in Mineralogy and Geochemistry 54, 115–149. Farmer, M. A., Fitt, W. K. & Trench, R. K. (2001). Morphology of the symbiosis between Corculum cardissa (Mollusca: Bivalvia) and Symbiodinium corculorum (Dinophyceae). Biological Bulletin 200, 336–343. Fay, S. A., Weber, M. X. & Lipps, J. H. (2009). The distribution of Symbiodinium diversity within individual host foraminifera. Coral Reefs 28, 717–726. *Fernandez-Valverde, S. L., Calcino, A. D. & Degnan, B. M. (2015). Deep developmental transcriptome sequencing uncovers numerous new genes and enhances gene annotation in the sponge Amphimedon queenslandica. BMC Genomics 16, 387. *Fiore, C. L., Labrie, M., Jarett, J. K. & Lesser, M. P. (2015). Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: molecular evidence for metabolic interchange. Frontiers in Microbiology 6, 364. Fitt, W. K., Fisher, C. R. & Trench, R. K. (1986). Contribution of the symbiotic dinoflagellate Symbiodinium microadriaticum to the nutrition, growth and survival of larval and juvenile tridacnid clams. Aquaculture 55, 5–22. *Fortunato, S. A., Adamski, M., Ramos, O. M., Leininger, S., Liu, J., Ferrier, D. E. & Adamska, M. (2014). Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514, 620–623. ¨ Fromont, J., Huggett, M. J., Lengger, S. K., Grice, K. & Schonberg, C. H. (2016). Characterization of Leucetta prolifera, a calcarean cyanosponge from South-Western Australia, and its symbionts. Journal of the Marine Biological Association of the United Kingdom 96, 541–552. Garalde, D. R., Snell, E. A., Jachimowicz, D., Sipos, B., Lloyd, J. H., Bruce, M., Pantic, N., Admassu, T., James, P., Warland, A., Jordan, M., Ciccone, J., Serra, S., Keenan, J., Martin, S., et al. (2018). Highly parallel direct RNA sequencing on an array of nanopores. Nature Methods 15, 201–206. Garcia-Ramos, M. & Banaszak, A. T. (2007). The distribution of the dinoflagellate Symbiodinium in the conch Strombus gigas. Gulf and Caribbean Fisheries Institute 58, 403–406.


12 Gilbert, P. W. (1942). Observations on the eggs of Ambystoma maculatum with especial reference to the green algae found within the egg envelopes. Ecology 23, 215–227. Gilbert, P. W. (1944). The alga-egg relationship in Ambystoma maculatum, a case of symbiosis. Ecology 25, 366–369. Giribet, G. & Wheeler, W. (2002). On bivalve phylogeny: a high level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebrate Biology 121, 271–324. Goetsch, W. & Scheuring, L. (1926). Parasitismus und symbiose der algengattung Chlorella. Zoomorphology 7, 220–253. Goodheart, J. A., Bazinet, A. L., Collins, A. G. & Cummings, M. P. (2015). Relationships within Cladobranchia (Gastropoda: Nudibranchia) based on RNA-Seq data: an initial investigation. Royal Society Open Science 2, 150196. Goreau, T. F. (1959). The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biological Bulletin 116, 59–75. Granados, C., Camargo, C., Zea, S. & Sánchez, J. (2008). Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Molecular Phylogenetics and Evolution 49, 554–560. Griffiths, C. & Klumpp, D. (1996). Relationships between size, mantle area and zooxanthellae numbers in five species of giant clam (Tridacnidae). Marine Ecology Progress Series 137, 139–147. Hallock, P., Forward, L. B. & Hansen, H. J. (1986). Environmental influence of test shape in Amphistegina. Journal of Foraminiferal Research 16, 224–231. Hallock, P., Lidz, B. H., Cockey-Burkhard, E. M. & Donnelly, K. B. (2003). Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM Index. Environmental Monitoring and Assessment 81, 221–238. Hallock, P., Williams, D. E., Toler, S. K., Fisher, E. M. & Talge H. K. (2006). Bleaching in reef dwelling foraminifers: implications for reef decline. In Proceedings, 10th International Coral Reef Symposium, Volume 1, pp. 729–737. Okinawa, 28 June–02 July 2004. Han, J. H., Klochkova, T. A., Han, J. W., Shim, J. & Kim, G. H. (2015). Transcriptome analysis of the short-term photosynthetic sea slug Placida dendritica. Algae 30, 303–312. Händeler, K., Grzymbowski, Y. P., Krug, P. J. & Wägele, H. (2009). Functional chloroplasts in metazoan cells-a unique evolutionary strategy in animal life. Frontiers in Zoology 6, 28. Hansen, H. J. & Buchardt, B. (1977). Depth distribution of Amphistegina in the Gulf of Elat, Israel. Utrecht Micropaleontological Bulletins 15, 205–239. Hansen, H. J. & Dalberg, P. (1979). Symbiotic algae in milioline foraminifera: CO2 uptake and shell adaptations. Bulletin of the Geological Society of Denmark 28, 47–55. Harii, S., Yamamoto, M. & Hoegh-Guldberg, O. (2010). The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Marine Biology 157, 1215–1224. Harrison, P. L. (2011). Sexual reproduction of scleractinian corals. In Coral Reefs: An Ecosystem in Transition (eds Z. Dubinsky and N. Stambler), pp. 59–85. Springer, Dordrecht, Netherlands. Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., Martinez, P., Bagu˜ na` , J., Bailly, X., Jondelius, U., Wiens, M., ¨ Muller, W. E. G., Seaver, E., Wheeler, W. C., Martindale, M. Q., et al. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society of London B: Biological Sciences 276, 4261–4270. Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. (2012). Genomic insights into the marine sponge microbiome. Nature Reviews Microbiology 10, 641–654. Hernawan, U. E. (2008). Symbiosis between the giant clams (Bivalvia: Cardiidae) and zooxanthellae (Dinophyceae). Biodiversitas 9, 53–58. *Heyland, A., Vue, Z., Voolstra, C. R., Medina, M. & Moroz, L. L. (2011). Developmental transcriptome of Aplysia californica. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 316, 113–134. Hikosaka-Katayama, T., Koike, K., Yamashita, H., Hikosaka, A. & Koike, K. (2012). Mechanisms of maternal inheritance of dinoflagellate symbionts in the acoelomorph worm Waminoa litus. Zoological Science 29, 559–567. ¨ Hill, M., Allenby, A., Ramsby, B., Schonberg, C. & Hill, A. (2011). Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Molecular Phylogenetics and Evolution 59, 81–88. Hill, M. & Hill, A. (2012). The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biological Reviews 87, 804–821. Hirose, E. (2000). Plant Rake and algal pouch of the larvae in the tropical ascidian Diplosoma similis: an adaptation for vertical transmission of photosynthetic symbionts Prochloron sp. Zoological Science 17, 233–240. Hirose, E. (2005). Digestive system of the sacoglossan Plakobranchus ocellatus (Gastropoda: Opisthobranchia): light-and electron-microscopic observations with remarks on chloroplast retention. Zoological Science 22, 905–916. Hirose, E. (2015). Ascidian photosymbiosis: diversity of cyanobacterial transmission during embryogenesis. Genesis 53, 121–131.

Jenny Melo Clavijo and others Hirose, E., Maruyama, T., Cheng, L. & Lewin, R. A. (1996). Intracellular symbiosis of a photosynthetic prokaryote, Prochloron sp., in a colonial ascidian. Invertebrate Biology 115, 343–348. Hirose, E., Neilan, B. A., Schmidt, E. W. & Murakami, A. (2009). Enigmatic life and evolution of Prochloron and related cyanobacteria inhabiting colonial ascidians. In Handbook on Cyanobacteria (eds P. M. Gault and H. J. Marler), pp. 161–189. CRC Press, Boca Raton, USA. Hirose, E., Oka, A. T. & Akahori, M. (2004). Sexual reproduction of the photosymbiotic ascidian Diplosoma virens in the Ryukyu Archipelago, Japan: vertical transmission, seasonal change, and possible impact of parasitic copepods. Marine Biology 146, 677–682. Huss, V. (1999). Freshwater algal symbioses in protozoa and invertebrates. In Enigmatic Microorganisms and Life in Extreme Environments (ed. J. Seckbach), pp. 641–650. Springer, Dordrecht, Netherlands. Ikeda, S., Yamashita, H., Kondo, S.-n., Inoue, K., Morishima, S.-y. & Koike, K. (2017). Zooxanthellal genetic varieties in giant clams are partially determined by species-intrinsic and growth-related characteristics. PLoS One 12, e0172285. Ishikawa, M., Yuyama, I., Shimizu, H., Nozawa, M., Ikeo, K. & Gojobori, T. (2016). Different endosymbiotic interactions in two hydra species reflect the evolutionary history of endosymbiosis. Genome Biology and Evolution 8, 2155–2163. Jékely, G., Paps, J. & Nielsen, C. (2015). The phylogenetic position of ctenophores and the origin(s) of nervous systems. EvoDevo 6:1. Jensen, K. S. & Pedersen, M. F. (1994). Photosynthesis by symbiotic algae in the freshwater sponge, Spongilla lacustris. Limnology and Oceanography 39, 551–561. Jez, J. M., Bennett, M. J., Schlegel, B. P., Lewis, M., Trevor, M. & Penning, T. M. (1997). Comparative anatomy of the aldo-keto reductase superfamily. Biochemical Journal 326, 625–636. Johnson, M. D. (2011). Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. Journal of Eukaryotic Microbiology 58, 185–195. Jondelius, U. & Thollesson, M. (1993). Phylogeny of the Rhabdocoela (Platyhelminthes): a working hypothesis. Canadian Journal of Zoology 71, 298–308. Jondelius, U., Wallberg, A., Hooge, M. & Raikova, O. I. (2011). How the worm got its pharynx: phylogeny, classification and Bayesian assessment of character evolution in Acoela. Systematic Biology 60, 845–871. Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. (2008). A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society of London B: Biological Sciences 275, 1359–1365. Kawaida, H., Ohba, K., Koutake, Y., Shimizu, H., Tachida, H. & Kobayakawa, Y. (2013). Symbiosis between Hydra and Chlorella: molecular phylogenetic analysis and experimental study provide insight into its origin and evolution. Molecular Phylogenetics and Evolution 66, 906–914. Kawano, T., Kadono, T., Kosaka, T. & Hosoya, H. (2004). Green paramecia as an evolutionary winner of oxidative symbiosis: a hypothesis and supportive data. Zeitschrift für Naturforschung C 59, 538–542. Kayal, E., Roure, B., Philippe, H., Collins, A. G. & Lavrov, D. V. (2013). Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evolutionary Biology 13, 5. Keinath, M. C., Timoshevskiy, V. A., Timoshevskaya, N. Y., Tsonis, P. A., Voss, S. R. & Smith, J. J. (2015). Initial characterization of the large genome of the salamander Ambystoma mexicanum using shotgun and laser capture chromosome sequencing. Scientific Reports 5, 16413. Kerney, R. (2011). Symbioses between salamander embryos and green algae. Symbiosis 54, 107–117. Kerney, R., Kim, E., Hangarter, R. P., Heiss, A. A., Bishop, C. D. & Hall, B. K. (2011). Intracellular invasion of green algae in a salamander host. Proceedings of the National Academy of Sciences of the United States of America 108, 6497–6502. Kirk, N. L. & Weis, V. M. (2016). Animal-Symbiodinium symbioses: foundations of coral reef ecosystems. In The Mechanistic Benefits of Microbial Symbionts (ed. C. J. Hurst), pp. 269–294. Springer, Cham, Switzerland. Kirkendale, L. (2009). Their Day in the sun: molecular phylogenetics and origin of photosymbiosis in the ‘other’ group of photosymbiotic marine bivalves (Cardiidae: Fraginae). Biological Journal of the Linnean Society 97, 448–465. *Kitchen, S. A., Crowder, C. M., Poole, A. Z., Weis, V. M. & Meyer, E. (2015). De novo assembly and characterization of four anthozoan (Phylum Cnidaria) transcriptomes. G3: Genes, Genomes, Genetics 5, 2441–2452. Klumpp, D. & Griffiths, C. (1994). Contributions of phototrophic and heterotrophic nutrition to the metabolic and growth requirements of four species of giant clam (Tridacnidae). Marine Ecology Progress Series 115, 103–115. Koike, K., Jimbo, M., Sakai, R., Kaeriyama, M., Muramoto, K., Ogata, T., Maruyama, T. & Kamiya, H. (2004). Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biological Bulletin 207, 80–86. Kolodziejczyk, A. A., Kim, J. K., Svensson, V., Marioni, J. C. & Teichmann, S. A. (2015). The technology and biology of single-cell RNA sequencing. Molecular Cell 58, 610–620. Kovacevic, G. (2012). Value of the Hydra model system for studying symbiosis. International Journal of Developmental Biology 56, 627–635.


Evolution of photosymbiosis Kutschera, U. & Niklas, K. J. (2005). Endosymbiosis, cell evolution, and speciation. Theory in Biosciences 124, 1–24. Lampert, K. P. (2016). Cassiopea and its zooxanthellae. In The Cnidaria, Past, Present and Future (eds S. Goffredo and Z. Dubinsky), pp. 415–423. Springer, Cham, Switzerland. Langer, M. R., Silk, M. T. & Lipps, J. H. (1997). Global ocean carbonate and carbon dioxide production; the role of reef Foraminifera. The Journal of Foraminiferal Research 27, 271–277. Lee, J. J. (2006). Algal symbiosis in larger foraminifera. Symbiosis 42, 63–75. Lee, J. J. & Anderson, O. R. (1991). Symbiosis in Foraminifera. In Biology of Foraminifera (eds J. J. Lee and O. R. Anderson), pp. 157–220. Academic Press, London. *Lehnert, E. M., Burriesci, M. S. & Pringle, J. R. (2012). Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida. BMC Genomics 13, 271. Lehnert, E. M., Mouchka, M. E., Burriesci, M. S., Gallo, N. D., Schwarz, J. A. & Pringle, J. R. (2014). Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3: Genes, Genomes, Genetics 4, 277–295. ¨ Lemloh, M.-L., Fromont, J., Brummer, F. & Usher, K. M. (2009). Diversity and abundance of photosynthetic sponges in temperate Western Australia. BMC Ecology 9, 4. Lengyel, N. L., Collie, J. S. & Valentine, P. C. (2009). The invasive colonial ascidian Didemnum vexillum on Georges Bank - ecological effects and genetic identification. Aquatic Invasions 4, 143–152. Lin, Z., Torres, J. P., Tianero, M. D., Kwan, J. C. & Schmidt, E. W. (2016). Origin of chemical diversity in Prochloron-tunicate symbiosis. Applied and Environmental Microbiology 82, 3450–3460. Lipps, J. H. & Stanley, G. D. Jr. (2016a). Photosymbiosis in past and present reefs. In Coral Reefs at the Crossroads (eds D. K. Hubbard, C. S. Rogers, J. H. Lipps and G. D. Stanley Jr.), pp. 47–68. Springer, Dordrecht, Netherlands. Lipps, J. H. & Stanley, G. D. Jr. (2016b). Reefs through time: an evolutionary view. In Coral Reefs at the Crossroads (eds D. K. Hubbard, C. S. Rogers, J. H. Lipps and G. D. Stanley Jr.), pp. 175–196. Springer, Dordrecht, Netherlands. Little, A. F., van Oppen, M. J. H. & Willis, B. L. (2004). Flexibility in the algal endosymbioses shapes growth in reef corals. Science 304, 1492–1494. Littlewood, D. T. J., Rohde, K., Bray, R. A. & Herniou, E. A. (1999). Phylogeny of the Platyhelminthes and the evolution of parasitism. Biological Journal of the Linnean Society 68, 257–287. Locke, A. & Carman, M. (2009). Adventures of a sea squirt sleuth: unraveling the identity of Didemnum vexillum, a global ascidian invader. Aquatic Invasions 4, 5–28. Lopes, R. M. & Silveira, M. (1994). Symbiosis between a pelagic flatworm and a dinoflagellate from a tropical area: structural observations. Hydrobiologia 287, 277–284. Martin, R., Walther, P. & Tomaschko, K.-H. (2013). Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa). Zoomorphology 132, 253–259. Martin, R., Walther, P. & Tomaschko, K.-H. (2015). Variable retention of kleptoplast membranes in cells of sacoglossan sea slugs: plastids with extended, shortened and non-retained durations. Zoomorphology 134, 523–529. Maruyama, T., Ishikura, M., Yamazaki, S. & Kanai, S. (1998). Molecular phylogeny of zooxanthellate bivalves. Biological Bulletin 195, 70–77. *Matsuoka, T., Ikeda, T., Fujimaki, K. & Satou, Y. (2013). Transcriptome dynamics in early embryos of the ascidian, Ciona intestinalis. Developmental Biology 384, 375–385. Matthias, H., Frederike, A. & Thomas, C. (2003). The Hydra viridis / Chlorella symbiosis. Growth and sexual differentiation in polyps without symbionts. Zoology 106, 101–108. McCoy, M. A. & Balzer, I. (2001). Algal symbiosis in flatworms. In Symbiosis Mechanisms and Model Systems (ed. J. Seckbach), pp. 559–574. Springer, Dordrecht, Netherlands. McNeil, P. L. (1981). Mechanisms of nutritive endocytosis. I. Phagocytic versatility and cellular recognition in Chlorohydra digestive cells, a scanning electron microscope study. Journal of Cell Science 49, 311–339. *Mehr, S. F. P., DeSalle, R., Kao, H. T., Narechania, A., Han, Z., Tchernov, D., Pieribone, V. & Gruber, D. F. (2013). Transcriptome deep-sequencing and clustering of expressed isoforms from Favia corals. BMC Genomics 14, 546. Mies, M., Sumida, P. Y., Rädecker, N. & Voolstra, C. R. (2017a). Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Frontiers in Ecology and Evolution 5, 56. Mies, M., Van Sluys, M., Metcalfe, C. & Sumida, P. (2017b). Molecular evidence of symbiotic activity between Symbiodinium and Tridacna maxima larvae. Symbiosis 72, 13–22. *Mohamed, A. R., Cumbo, V., Harii, S., Shinzato, C., Chan, C. X., Ragan, M. A., Bourne, D. G., Willis, B. L., Ball, E. E., Satoh, N. & Miller, D. J. (2016). The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome. Molecular Ecology 25, 3127–3141.

13 *Moya, A., Huisman, L., Ball, E. E., Hayward, D. C., Grasso, L. C., Chua, C. M., Woo, H. N., Gattuso, J.-P., Forêt, S. & Miller, D. J. (2012). Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2 driven acidification during the initiation of calcification. Molecular Ecology 21, 2440–2454. Muller-Parker, G., D’elia, C. F. & Cook, C. B. (2015). Interactions between corals and their symbiotic algae. In Coral Reefs in the Anthropocene (ed. C. Birkeland), pp. 99–116. Springer, Dordrecht, Ntherlands. Muniain, C., Marin, A. & Penchaszadeh, P. (2001). Ultrastructure of the digestive gland of larval and adult stages of the sacoglossan Elysia patagonica. Marine Biology 139, 687–695. Muscatine, L., Pool, R. & Trench, R. (1975). Symbiosis of algae and invertebrates: aspects of the symbiont surface and the host-symbiont interface. Transactions of the American Microscopical Society 94, 450–469. Muto, K., Nishikawa, K., Kamikawa, R. & Miyashita, H. (2017). Symbiotic green algae in eggs of Hynobius nigrescens, an amphibian endemic to Japan. Phycological Research 65, 171–174. Mwinyi, A., Bailly, X., Bourlat, S. J., Jondelius, U., Littlewood, D. T. J. & Podsiadlowski, L. (2010). The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evolutionary Biology 10, 309. Neubauer, E. F., Poole, A. Z., Detournay, O., Weis, V. M. & Davy, S. K. (2016). The scavenger receptor repertoire in six cnidarian species and its putative role in cnidarian-dinoflagellate symbiosis. PeerJ 4, e2692 /correction-1. Neubauer, E.-F., Poole, A. Z., Neubauer, P., Detournay, O., Tan, K., Davy, S. K. & Weis, V. M. (2017). A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis. eLife 6, e24494. *Nichols, S. A., Roberts, B. W., Richter, D. J., Fairclough, S. R. & King, N. (2012). Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β -catenin complex. Proceedings of the National Academy of Sciences of the United States of America 109, 13046–13051. Niehuis, O., Hartig, G., Grath, S., Pohl, H., Lehmann, J., Tafer, H., Donath, A., Krauss, V., Eisenhardt, C., Hertel, J., Petersen, M., Mayer, C., Meusemann, K., Peters, R. S., Stadler, P. F., et al. (2012). Genomic and morphological evidence converge to resolve the enigma of Strepsiptera. Current Biology 22, 1309–1313. Not, F., Probert, I., Gerikas Ribeiro, C., Crenn, K., Guillou, L., Jenathon, C. & Vaulot, D. (2016). Photosymbiosis in marine pelagic environments. In The Marine Microbiome (eds L. J. Stahl and M. Silvia Cretoiu), pp. 305–322. Springer, Cham, Switzerland. Ohno, T., Katoh, T. & Yamasu, T. (1995). The origin of algal-bivalve photo-symbiosis. Palaeontology 38, 1–22. van Oppen, M. J. H., Palstra, F. P., Piquet, A. M.-T. & Miller, D. J. (2001). Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proceedings of the Royal Society of London B: Biological Sciences 268, 1759–1767. Oren, M., Steindler, L. & Ilan, M. (2005). Transmission, plasticity and the molecular identification of cyanobacterial symbionts in the Red Sea sponge Diacarnus erythraenous. Marine Biology 148, 35–41. Padilla-Gamin˜ no, J. L., Pochon, X., Bird, C., Concepcion, G. T. & Gates, R. D. (2012). From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the Reef Building Coral Montipora capitata. PLoS One 7, 38440. Paps, J., Bagu˜ na` , J. & Riutort, M. (2009). Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal Acoelomorpha. Molecular Biology and Evolution 26, 2397–2406. Pardy, R. (1980). Symbiotic algae and 14 C incorporation in the freshwater clam, Anodonta. Biological Bulletin 158, 349–355. Pearse, V. B. & Muscatine, L. (1971). Role of symbiotic algae (zooxanthellae) in coral calcification. Biological Bulletin 141, 350–363. Pelletreau, K. N., Weber, A. P., Weber, K. L. & Rumpho, M. E. (2014). Lipid accumulation during the establishment of kleptoplasty in Elysia chlorotica. PLoS One 9, e97477. Philippe, H., Brinkmann, H., Copley, R. R., Moroz, L. L., Nakano, H., Poustka, A. J., Wallberg, A., Peterson, K. J. & Telford, M. J. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255–258. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., Da Silva, C., Wincker, P., Le Guyader, H., Leys, S., Jackson, D. J., et al. (2009). Phylogenomics revives traditional views on deep animal relationships. Current Biology 19, 706–712. Pillet, L., de Vargas, C. & Pawlowski, J. (2011). Molecular identification of sequestered diatom chloroplasts and kleptoplastidy in foraminifera. Protist 162, 394–404.


14 Pillet, L. & Pawlowski, J. (2012). Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy. Molecular Biology and Evolution 30, 66–69. Pisani, D., Pett, W., Dohrmann, M., Feuda, R., Rota-Stabelli, O., Philippe, ¨ H., Lartillot, N. & Worheide, G. (2015). Genomic data do not support comb jellies as the sister group to all other animals. Proceedings of the National Academy of Sciences of the United States of America 112, 15402–15407. Pita, L., Fraune, S. & Hentschel, U. (2016). Emerging sponge models of animal-microbe symbioses. Frontiers in Microbiology 7, 2102. *Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., Jurka, J., Genikhovich, G., Grigoriev, I. V., Lucas, S. M., Steele, R. E., et al. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94. Pyron, R. A. & Wiens, J. J. (2011). A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61, 543–583. Rädecker, N., Pogoreutz, C., Wild, C. & Voolstra, C. R. (2017). Stimulated respiration and net photosynthesis in Cassiopeia sp. during glucose enrichment suggests in hospite CO2 limitation of algal endosymbionts. Frontiers in Marine Science 4, 267. Rauch, C., Jahns, P., Tielens, A. G., Gould, S. B. & Martin, W. F. (2017). On being the right size as an animal with plastids. Frontiers in Plant Science 8, 1402. Raven, J. A., Walker, D. I., Jensen, K. R., Handley, L. L., Scrimgeour, C. M. & McInroy, S. G. (2001). What fraction of the organic carbon in sacoglossans is obtained from photosynthesis by kleptoplastids? An investigation using the natural abundance of stable carbon isotopes. Marine Biology 138, 537–545. Reisser, W. (1984). The taxonomy of green algae endosymbiotic in ciliates and a sponge. British Phycological Journal 19, 309–318. Reymond, C. E., Uthicke, S. & Pandolfi, J. M. (2012). Tropical Foraminifera as indicators of water quality and temperature. In Proceedings of the 12th International Coral Reef Symposium, pp. 9–13. Cairns, Australia. *Riesgo, A., Andrade, S. C., Sharma, P. P., Novo, M., Pérez-Porro, A. R., Vahtera, V., González, V. L., Kawauchi, G. Y. & Giribet, G. (2012). Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Frontiers in Zoology 9, 33. *Riesgo, A., Peterson, K., Richardson, C., Heist, T., Strehlow, B., McCauley, M., Cotman, C., Hill, M. & Hill, A. (2014a). Transcriptomic analysis of differential host gene expression upon uptake of symbionts: a case study with Symbiodinium and the major bioeroding sponge Cliona varians. BMC Genomics 15, 376. *Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G. & Leys, S. P. (2014b). The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Molecular Biology and Evolution 31, 1102–1120. Robb, S. M., Gotting, K., Ross, E. & Sánchez Alvarado, A. (2015). SmedGD 2.0: the Schmidtea mediterranea genome database. Genesis 53, 535–546. *Robb, S. M., Ross, E. & Alvarado, A. S. (2007). SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Research 36, D599–D606. Rodríguez, E., Barbeitos, M. S., Brugler, M. R., Crowley, L. M., Grajales, A., Gusmão, L., Häussermann, V., Reft, A. & Daly, M. (2014). Hidden among sea anemones: the first comprehensive phylogenetic reconstruction of the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of hexacorals. PLoS One 9, e96998. Rodriguez-Lanetty, M., Phillips, W. S. & Weis, V. M. (2006). Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7, 23. Roth, M. S. (2014). The engine of the reef: photobiology of the coral-algal symbiosis. Frontiers in Microbiology 5, 422. Rumpho, M. E., Pelletreau, K. N., Moustafa, A. & Bhattacharya, D. (2011). The making of a photosynthetic animal. Journal of Experimental Biology 214, 303–311. Rumpho, M. E., Summer, E. J. & Manhart, J. R. (2000). Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiology 123, 29–38. *Ryu, T., Seridi, L., Moitinho-Silva, L., Oates, M., Liew, Y. J., Mavromatis, C., Wang, X., Haywood, A., Lafi, F. L., Kupresanin, M., Sougrat, R., Alzahrani, M. A., Giles, E., Ghosheh, Y., Schunter, C., et al. (2016). Hologenome analysis of two marine sponges with different microbiomes. BMC Genomics 17, 158. Sagan, L. (1967). On the origin of mitosing cells. Journal of Theoretical Biology 14, 225IN1–274IN6. Schlesinger, A., Goldshmid, R., Hadfield, M. G., Kramarsky-Winter, E. & Loya, Y. (2009). Laboratory culture of the aeolid nudibranch Spurilla neapolitana (Mollusca, Opisthobranchia): life history aspects. Marine Biology 156, 753–761. Schmidt, C., Kucera, M. & Uthicke, S. (2014). Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa. Coral Reefs 33, 805–818.

Jenny Melo Clavijo and others Schmitt, S., Deines, P., Behnam, F., Wagner, M. & Taylor, M. W. (2011). Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. FEMS Microbiology Ecology 78, 497–510. Schwartz, J. A., Curtis, N. E. & Pierce, S. K. (2010). Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evolutionary Biology 37, 29–37. *Schwarz, J. A., Brokstein, P. B., Voolstra, C., Terry, A. Y., Miller, D. J., Szmant, A. M., Coffroth, M. A. & Medina, M. (2008). Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9, 97. Schwentner, M. & Bosch, T. C. (2015). Revisiting the age, evolutionary history and species level diversity of the genus Hydra (Cnidaria: Hydrozoa). Molecular Phylogenetics and Evolution 91, 41–55. Seo, H.-C., Kube, M., Edvardsen, R. B., Jensen, M. F., Beck, A., Spriet, E., Gorsky, G., Thompson, E. M., Lehrach, H., Reinhardt, R. & Chourrout, D. (2001). Miniature genome in the marine chordate Oikopleura dioica. Science 294, 2506–2506. Serˆ odio, J., Cruz, S., Cartaxana, P. & Calado, R. (2014). Photophysiology of kleptoplasts: photosynthetic use of light by chloroplasts living in animal cells. Philosophical Transactions of the Royal Society B: Biological Sciences 369, 20130242. Serˆ odio, J., Silva, R., Ezequiel, J. & Calado, R. (2011). Photobiology of the symbiotic acoel flatworm Symsagittifera roscoffensis: algal symbiont photoacclimation and host photobehaviour. Journal of the Marine Biological Association of the United Kingdom 91, 163–171. Shannon, T. & Achatz, J. G. (2007). Convolutriloba macropyga sp. nov., an uncommonly fecund acoel (Acoelomorpha) discovered in tropical aquaria. Zootaxa 1525, 1–17. Shapiro, E., Biezuner, T. & Linnarsson, S. (2013). Single-cell sequencing-based technologies will revolutionize whole-organism science. Nature Reviews Genetics 14, 618–630. *Shinzato, C., Inoue, M. & Kusakabe, M. (2014). A snapshot of a coral ‘‘holobiont’’: a transcriptome assembly of the scleractinian coral, Porites, captures a wide variety of genes from both the host and symbiotic zooxanthellae. PLoS One 9, e85182. *Shinzato, C., Shoguchi, E., Kawashima, T., Hamada, M., Hisata, K., Tanaka, M., Manube, F., Fujiwara, M., Koyanagi, R., Ikuta, T., Fujiyama, A., Miller, D. J. & Satoh, N. (2011). Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476, 320–323. *Simakov, O., Marletaz, F., Cho, S. J., Edsinger-Gonzales, E., Havlak, P., Hellsten, U., Kuo, D.-H., Larsson, T., Lv, J., Arendt, D., Savage, R., Osoegawa, K., de Jong, P., Grimwood, J., Chapman, J. A., Shapiro, H., et al. (2013). Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526–531. Simion, P., Philippe, H., Baurain, D., Jager, M., Richter, D. J., Di Franco, ´ Ereskovsky, A., Lapébie, P., Corre, A., Roure, B., Satoh, N., Quéinnec, E., ¨ E., Delsuc, F., King, N., Worheide, G. & Manuel, M. (2017). A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Current Biology 27, 958–967. Small, K. S., Brudno, M., Hill, M. M. & Sidow, A. (2007). A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biology 8, R41–R41. Smith, D. C. (1991). Why do so few animals form endosymbiotic associations with photosynthetic microbes? Philosophical Transactions of the Royal Society B: Biological Sciences 333, 225–230. *Speiser, D. I., Pankey, M. S., Zaharoff, A. K., Battelle, B. A., Bracken-Grissom, H. D., Breinholt, J. W., Bybee, S. M., Cronin, T. W., Garm, A., Lindgren, A. R., Patel, N. H., Porter, M. L., Protas, M. E., Rivera, A. S., Serb, J. M., et al. (2014). Using phylogenetically-informed annotation (PIA) to search for light-interacting genes in transcriptomes from non-model organisms. BMC Bioinformatics 15, 350. *Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., Larroux, C., Putnam, N. H., Stanke, M., Adamska, M., Darling, A., et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720–726. Stambler, N. (2011). Zooxanthellae: the yellow symbionts inside animals. In Coral Reefs: An Ecosystem in Transition (eds Z. Dubinsky and N. Stambler), pp. 87–106. Springer, Dordrecht, Netherlands. Stampar, S. N., Morandini, A. C. & Da Silveira, F. L. (2014). A new species of Pachycerianthus (Cnidaria, Anthozoa, Ceriantharia) from tropical southwestern Atlantic. Zootaxa 3827, 343–354. Stanley, G. D. Jr. & Lipps, J. H. (2011). Photosymbiosis: the driving force for reef success and failure. Paleontological Society Papers 17, 33–60. Stat, M., Carter, D. A. & Hoegh-Guldberg, O. (2006). The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology, Evolution and Systematics 8, 23–43. Stat, M., Loh, W. K. W., Hoegh-Guldberg, O. & Carter, D. A. (2008). Symbiont acquisition strategy drives host–symbiont associations in the southern Great Barrier Reef. Coral Reefs 27, 763–772.


Evolution of photosymbiosis Stefaniak, L., Zhang, H., Gittenberger, A., Smith, K., Holsinger, K., Lin, S. & Whitlatch, R. B. (2012). Determining the native region of the putatively invasive ascidian Didemnum vexillum Kott, 2002. Journal of Experimental Marine Biology and Ecology 422, 64–71. Steindler, L., Beer, S. & Ilan, M. (2002). Photosymbiosis in intertidal and subtidal tropical sponges. Symbiosis 33, 263–274. Stolfi, A., Lowe, E. K., Racioppi, C., Ristoratore, F., Brown, C. T., Swalla, B. J. & Christiaen, L. (2014). Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians. eLife 3, e03728. *Sun, J., Chen, Q., Lun, J. C., Xu, J. & Qiu, J. W. (2013). PcarnBase: development of a transcriptomic database for the brain coral Platygyra carnosus. Marine Biotechnology 15, 244–251. Tan, L. T., Williamson, R. T., Gerwick, W. H., Watts, K. S., McGough, K. & Jacobs, R. (2000). Cis, cis-and trans, trans-ceratospongamide, new bioactive cyclic heptapeptides from the Indonesian red alga Ceratodictyon spongiosum and symbiotic sponge Sigmadocia symbiotica. The Journal of Organic Chemistry 65, 419–425. Taylor, D. (1971). On the symbiosis between Amphidinium klebsii [Dinophyceae] and Amphiscolops langerhansi [Turbellaria: Acoela] 1. Journal of the Marine Biological Association of the United Kingdom 51, 301–313. Thacker, R. W. & Freeman, C. J. (2012). Sponge-microbe symbioses: recent advances and new directions. Advances in Marine Biology 62, 57. Thornhill, D. J., Daniel, M. W., LaJeunesse, T. C., Schmidt, G. W. & Fitt, W. K. (2006). Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology 338, 50–56. *Traylor-Knowles, N., Granger, B. R., Lubinski, T. J., Parikh, J. R., Garamszegi, S., Xia, Y., Marto, J. A., Kaufmann, L. & Finnerty, J. R. (2011). Production of a reference transcriptome and transcriptomic database (PocilloporaBase) for the cauliflower coral, Pocillopora damicornis. BMC Genomics 12, 585. Trench, R. K. (1987). Dinoflagellates in non parasitic symbioses. In The Biology of Dinoflagellates (ed. F. J. R. Taylor), pp. 531–570. Blackwell Scientific Publications, Boston, USA. *Tulin, S., Aguiar, D., Istrail, S. & Smith, J. (2013). A quantitative reference transcriptome for Nematostella vectensis earlyembryonic development: a pipeline for de novo assembly in emergingmodel systems. EvoDevo 4, 16. Usher, K. M. (2008). The ecology and phylogeny of cyanobacterial symbionts in sponges. Marine Ecology 29, 178–192. Usher, K. M., Kou, J., Fromont, J. & Sutton, D. C. (2001). Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461, 15–23. Van Steenkiste, N., Tessens, B., Willems, W., Backeljau, T., Jondelius, U. & Artois, T. (2013). A comprehensive molecular phylogeny of Dalytyphloplanida (Platyhelminthes: Rhabdocoela) reveals multiple escapes from the marine environment and origins of symbiotic relationships. PLoS One 8, e59917. Velandia-Huerto, C. A., Gittenberger, A. A., Brown, F. D., Stadler, P. F. ´ & Bermudez-Santana, C. I. (2016). Automated detection of ncRNAs in the draft genome sequence of a colonial tunicate: the carpet sea squirt Didemnum vexillum. BMC Genomics 17, 691. Venn, A., Loram, J. & Douglas, A. (2008). Photosynthetic symbioses in animals. Journal of Experimental Botany 59, 1069–1080. Verde, E. A. & McCloskey, L. (1996). Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). Journal of Experimental Marine Biology and Ecology 195, 187–202. Vermeij, G. J. (2013). The evolution of molluscan photosymbioses: a critical appraisal. Biological Journal of the Linnean Society 109, 497–511. Voolstra, C. R., Schwarz, J. A., Schnetzer, J., Sunagawa, S., Desalvo, M. K., Szmant, A. M., Coffroth, M. A. & Medina, M. (2009). The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Molecular Ecology 18, 1823–1833. Voskoboynik, A., Neff, N. F., Sahoo, D., Newman, A. M., Pushkarev, D., Koh, W., Passarelli, B., Fan, H. C., Mantalas, G. L., Palmeri, K. J., Ishizuka, K. J., Gissi, C., Griggio, F., Ben-Shlomo, R., Corey, D. M., et al. (2013). The genome sequence of the colonial chordate, Botryllus schlosseri. eLife 2, e00569. de Vries, J., Christa, G. & Gould, S. B. (2014). Plastid survival in the cytosol of animal cells. Trends in Plant Science 19, 347–350. de Vries, J., Woehle, C., Christa, G., Wägele, H., Tielens, A. G., Jahns, P. & Gould, S. B. (2015). Comparison of sister species identifies factors underpinning

15 plastid compatibility in green sea slugs. Proceedings of the Royal Society of London B: Biological Sciences 282, 20142519. *Wägele, H., Deusch, O., Händeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S. B., Dagan, T., Klussmann-Kolb, A. & Martin, W. (2011). Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Molecular Biology and Evolution 28, 699–706. Wägele, H. & Martin, W. F. (2014). Endosymbioses in sacoglossan seaslugs: plastid-bearing animals that keep photosynthetic organelles without borrowing ¨ genes. In Endosymbiosis (ed. W. Loffelhardt), pp. 291–324. Springer, Vienna, Austria. Wakefield, T. S. & Kempf, S. C. (2001). Development of host-and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biological Bulletin 200, 127–143. Waugh, G. & Clark, K. (1986). Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Marine Biology 92, 483–487. Webster, N. S. & Taylor, M. W. (2012). Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology 14, 335–346. Weis, V. M. (2008). Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Journal of Experimental Biology 211, 3059–3066. Weis, V. M., Reynolds, W. S., DeBoer, M. D. & Krupp, D. A. (2001). Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20, 301–308. *Wenger, Y. & Galliot, B. (2013). RNAseq versus genome-predicted transcriptomes: a large population of novel transcripts identified in an Illumina-454 Hydra transcriptome. BMC Genomics 14, 204. Whelan, N. V., Kocot, K. M. & Halanych, K. M. (2015). Employing phylogenomics to resolve the relationships among cnidarians, ctenophores, sponges, placozoans, and bilaterians. Integrative and Comparative Biology 55, 1084–1095. ¨ Worheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C. & Lavrov, D. V. (2012). Deep phylogeny and evolution of sponges (Phylum Porifera). Advances in Marine Biology 61, 1–78. Wu, C.-H., Tsai, M.-H., Ho, C.-C., Chen, C.-Y. & Lee, H.-S. (2013). De novo transcriptome sequencing of axolotl blastema for identification of differentially expressed genes during limb regeneration. BMC Genomics 14, 434. Yellowlees, D., Rees, T. A. V. & Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell & Environment 31, 679–694. Yokobori, S. I., Kurabayashi, A., Neilan, B. A., Maruyama, T. & Hirose, E. (2006). Multiple origins of the ascidian-Prochloron symbiosis: molecular phylogeny of photosymbiotic and non-symbiotic colonial ascidians inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 40, 8–19. Yonge, C. (1934). Origin and nature of the association between invertebrates and unicellular algae. Nature 134, 12–15. Zacharias, H., Anokhin, B., Khalturin, K. & Bosch, T. C. (2004). Genome sizes and chromosomes in the basal metazoan Hydra. Zoology 107, 219–227. Zamparo, D., Brooks, D. R., Hoberg, E. P. & McLennan, D. A. (2001). Phylogenetic analysis of the Rhabdocoela (Platyhelminthes) with emphasis on the Neodermata and relatives. Zoologica Scripta 30, 59–77. Zapata, F., Goetz, F. E., Smith, S. A., Howison, M., Siebert, S., Church, S. H., Sanders, S. M., Ames, C. L., McFadden, C. S., France, S. C., Daly, M., Collins, A. G., Haddock, S. H. D., Dunn, C. W. & Cartwright, P. (2015). Phylogenomic analyses support traditional relationships within Cnidaria. PLoS One 10, e0139068. Zhang, G., Fang, X., Guo, X., Li, L., Luo, R., Xu, F., Yang, P., Zhang, L., Wang, X., Qi, H., Xiong, Z., Que, H., Xie, Y., Holland, P. W. H., Paps, J., et al. (2012). The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490, 49–54.

VIII. SUPPORTING INFORMATION Additional supporting information may be found online in the Supporting Information section at the end of the article. Table S1. Genomes and transcriptomes of photosymbiotic animals and their close relatives.

(Received 13 December 2017; revised 30 April 2018; accepted 2 May 2018 )


Polymorphic adaptations in metazoans to establish ...

Polymorphic adaptations in metazoans to establish ...

Suggest Documents

Metazoans in Extreme Environments: Adaptations of ... - CiteSeerX

Substrate adaptations of sessile benthic metazoans ...

Morphological Complexity Increase in Metazoans

Immunological Adaptations to Pregnancy in

Neuromuscular Adaptations to Training

Attempting to Establish Standards in Ethics ...

regulatory elements in metazoans cis Deep ...

Collaborative Study to Establish Human

Psychological adaptations to performing in extreme ... - Core

Adaptations to Postural Perturbations in Patients

Aging in Basal Metazoans : A Biodemographic ...

Adaptations to chronic rapamycin in mice

Adaptations To Training In Endurance Cyclists

Adaptations in Muscle Activity to Induced, Short

Postural adaptations to workbench modifications in ...

Adaptations to ocean acidification in mesozooplankton

adaptations to cold environments: globins in ...

How to establish operational recommendations to ...

Training Intraverbal Naming to Establish Matching-to

Cardiovascular Adaptations to Resistance Training in ...

Adaptations to Submarine Hydrothermal ... - WordPress.com

The Adaptations to Strength Training

JOINT COORDINATION ADAPTATIONS TO AN

Plant Adaptations to Herbivory