The Many Faced Symbiotic Snakelocks Anemone (Anemonia Viridis, Anthozoa): Host and Symbiont Genetic Differentiation Among Colour Morphs

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The Many Faced Symbiotic Snakelocks Anemone (Anemonia Viridis, Anthozoa): Host and Symbiont Genetic Differentiation Among Colour Morphs Heredity (2020) 124:351–366 https://doi.org/10.1038/s41437-019-0266-3 ARTICLE The many faced symbiotic snakelocks anemone (Anemonia viridis, Anthozoa): host and symbiont genetic differentiation among colour morphs 1,2 1 3 4 1,5 1 Barbara Porro ● Cédric Mallien ● Benjamin C. C. Hume ● Alexis Pey ● Emilie Aubin ● Richard Christen ● 3,6 1,2 1,2 Christian R. Voolstra ● Paola Furla ● Didier Forcioli Received: 24 December 2018 / Revised: 30 July 2019 / Accepted: 15 August 2019 / Published online: 16 September 2019 © The Author(s), under exclusive licence to The Genetics Society 2019 Abstract How can we explain morphological variations in a holobiont? The genetic determinism of phenotypes is not always obvious and could be circumstantial in complex organisms. In symbiotic cnidarians, it is known that morphology or colour can misrepresent a complex genetic and symbiotic diversity. Anemonia viridis is a symbiotic sea anemone from temperate seas. This species displays different colour morphs based on pigment content and lives in a wide geographical range. Here, we investigated whether colour morph differentiation correlated with host genetic diversity or associated symbiotic genetic 1234567890();,: 1234567890();,: diversity by using RAD sequencing and symbiotic dinoflagellate typing of 140 sea anemones from the English Channel and the Mediterranean Sea. We did not observe genetic differentiation among colour morphs of A. viridis at the animal host or symbiont level, rejecting the hypothesis that A. viridis colour morphs correspond to species level differences. Interestingly, we however identified at least four independent animal host genetic lineages in A. viridis that differed in their associated symbiont populations. In conclusion, although the functional role of the different morphotypes of A. viridis remains to be determined, our approach provides new insights on the existence of cryptic species within A. viridis. Introduction the applicability of this. Indeed, in several cases, different species have no distinguishing phenotypic features, leading The most straightforward way to recognize a species is from to the concept of cryptic species (see for review Struck et al. its morphological description. However, there are limits to 2018;Fišer et al. 2018). Many studies have shown that cryptic species are quite common in most of the animal phyla (Pfenninger and Schwenk 2007; Pérez-Ponce de León and Poulin 2016). In the marine realm, the number of These authors contributed equally: Barbara Porro, Cédric Mallien described cryptic species has increased in the last years, These authors contributed equally: Paola Furla, Didier Forcioli thanks to new and diversified molecular approaches (see for Supplementary information The online version of this article (https:// review Pante Puillandre et al. 2015), but Appeltans et al. doi.org/10.1038/s41437-019-0266-3) contains supplementary (2012) estimated that many species remain to be discovered. material, which is available to authorized users. * Barbara Porro 3 Red Sea Research Center, Division of Biological and [email protected] Environmental Science and Engineering, King Abdullah * Didier Forcioli University of Science and Technology (KAUST), Thuwal 23955- [email protected] 6900, Saudi Arabia 4 THALASSA Marine research & Environmental awareness, 17 rue 1 UPMC Univ Paris 06, Univ Antilles, Univ Nice Sophia Antipolis, Gutenberg, 06000 Nice, France CNRS, Symbiose Marine, Evolution Paris Seine—Institut de 5 Laboratoire Génome et Développement des Plantes—UMR Biologie Paris Seine (EPS—IBPS), Sorbonne Universités, 75005 CNRS/UPVD 5096, Université de Perpignan, 66860 Paris, France Perpignan, France 2 Institute for Research on Cancer and Aging, Nice (IRCAN), 6 Department of Biology, University of Konstanz, 78457 Université Côte d’Azur, CNRS, INSERM, 06107 Nice, France Konstanz, Germany 352 B. Porro et al. The forces explaining the existence of cryptic species in coding for fluorescent and non-fluorescent proteins (FPs): some groups are not clear, but could be the result of low the three most frequent of these morphs are var. rustica (no standing genetic variation or environmental/developmental detectable fluorescence and no pink tentacle apex), var. constraints (see for review Struck et al. 2018). smaragdina (green FPs expression and pink tentacle apices) On the other hand, morphological polymorphisms could and var. rufescens (green and red–orange FPs expression be due to phenotypic plasticity and response to a given and pink tentacle apices) (Wiedenmann et al. 1999; environment (Price et al. 2003). Many species transplant Wiedenmann et al. 2000). The taxonomic nature of these experiments have shown that the same genotype could morphs has been debated for a long time and the functional generate different phenotypes depending on the environ- role of the fluorescence is not elucidated in A. viridis yet. mental conditions (Merilä and Hendry 2013). Those mor- Recently, De Brauwer et al. (2018) suggested to use the phological variations among individuals could even be due fluorescence properties of coral reef fishes as a survey tool to environmentally stabilized allelic polymorphisms, as in for cryptic marine species. Therefore, the hypothesis of the the well-known example of the peppered moth Biston existence of a correlation between genetic differentiation betularia (Creed et al. 1980), rather than to a loss of and fluorescence among A. viridis morphs could be rele- interfecundity among morphs. vant. In the past, based on allozyme differentiation and In cnidarians, morphological variation is often a poor presumed different reproduction strategies, some authors indicator of species divergence. Corals are especially well already raised the non-fluorescent var. rustica to species known to demonstrate extraordinary variation in ecomor- level, (Bulnheim and Sauer 1984; Sauer 1986; Sauer et al. phology that may or may not correspond well with the 1986). Furthermore, Wiedenmann et al. (1999) highlighted underlying genetic diversity (Veron and Pichon 1976; Flot a differential bathymetric distribution of the var. rustica and et al. 2011; Schmidt-Roach et al. 2013). In addition, var. smaragdina in the first 2 meters of depth, raising the Schmidt-Roach et al. (2013) showed that depending on the question of the adaptive nature of the morphs. In our pre- molecular marker used, the ecomorphs could be either vious work (Mallien et al. 2017), using exon-primed intron- grouped together or sub-divided. In sea anemones also, crossing (EPIC) polymorphism analysis with relatively few morphological traits are poor predictors of species delimi- EPIC loci (n = 5) for a relatively low number of individuals tation (Rodríguez et al. 2014). In the species Actinia equina (n = 34), we did not detect any clear phylogenetic split (Douek et al. 2002; Pereira et al. 2014) and Phymanthus among the morphs. However, our conclusions may have crucifer (González-Muñoz et al. 2015), phenotypic diversity lacked the resolution needed to detect incompletely sepa- was not strictly linked to genetic differences. Moreover, in rated lineages. This last scenario will correspond to what De the genus Anthothoe, Spano et al. (2018) recently identified Queiroz (2007)defined as the “grey zone of speciation”, the existence of several cryptic species not revealed by the where the level of population interconnectivity is decreasing characters used in morphological classification. In addition, leading to the build-up of independent genetic pools. This many species of cnidarians live in symbiosis with intra- scenario could not be a priori excluded for the A. viridis cellular photosynthetic dinoflagellates belonging to the colour morphs, but to evaluate such an ongoing split family Symbiodiniaceae (LaJeunesse et al. 2018) that play between emergent morph lineages, it is necessary to use an important trophic role (Muscatine et al. 1991) and could more powerful molecular investigations than the ones we also influence the cnidarian phenotype. Indeed, it has been used previously. Consequently, here we have used a RAD shown that in the coral Madracis pharensis, a correlation sequencing (RADseq) approach in order to generate several between the symbiont Breviolum sp. (formerly clade B) tens of thousands of genetic markers in a larger collection of present in the host cells and the colour morph of the host individuals, a sampling scheme fit to uncover population exists (Frade et al. 2008). The authors suggested that this level diversity patterns, species delimitation, and their diversity in colour could be a functional response to light, phylogenetic relationships (Emerson et al. 2010; Pante et al. thus demonstrating the existence of putative strong links 2015; Ree and Hipp 2015). Moreover, previous studies between host phenotype and symbiont population. investigating the nature of A. viridis morphs did not sys- The sea anemone Anemonia viridis (Forskål 1775) is a tematically consider A. viridis as a holobiont. A. viridis’ conspicuous member of benthic communities throughout gastrodermal tissue harbours millions of dinoflagellate cells the Mediterranean Sea and from the Azores to the North (Muscatine et al. 1998; Suggett et al. 2012; Zamoum and Sea. It is among the largest sea anemones in the region and Furla 2012; Ventura et al. 2016) belonging to the family can form extensive aggregations of clonemates that can Symbiodiniaceae (LaJeunesse et al. 2018) that live in a carpet the benthos. It thus plays an important role in shaping close trophic relationship (Davy et al. 1996)
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