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CORE Arrigoni Et Al Millepora.Docx Click Here To An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea Item Type Article Authors Arrigoni, Roberto; Maggioni, Davide; Montano, Simone; Hoeksema, Bert W.; Seveso, Davide; Shlesinger, Tom; Terraneo, Tullia Isotta; Tietbohl, Matthew; Berumen, Michael L. Citation Arrigoni R, Maggioni D, Montano S, Hoeksema BW, Seveso D, et al. (2018) An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea. Coral Reefs. Available: http://dx.doi.org/10.1007/s00338-018-01739-8. Eprint version Post-print DOI 10.1007/s00338-018-01739-8 Publisher Springer Nature Journal Coral Reefs Rights Archived with thanks to Coral Reefs Download date 05/10/2021 19:48:14 Link to Item http://hdl.handle.net/10754/629424 Manuscript Click here to access/download;Manuscript;CORE Arrigoni et al Millepora.docx Click here to view linked References 1 2 3 4 1 An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea 5 6 2 7 8 3 Roberto Arrigoni1, Davide Maggioni2,3, Simone Montano2,3, Bert W. Hoeksema4, Davide Seveso2,3, Tom Shlesinger5, 9 10 4 Tullia Isotta Terraneo1,6, Matthew D. Tietbohl1, Michael L. Berumen1 11 12 5 13 14 6 Corresponding author: Roberto Arrigoni, [email protected] 15 16 7 1Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah 17 18 8 University of Science and Technology, Thuwal 23955-6900, Saudi Arabia 19 20 9 2Dipartimento di Scienze dell’Ambiente e del Territorio (DISAT), Università degli Studi di Milano-Bicocca, Piazza 21 22 10 della Scienza 1, Milano 20126, Italy 23 24 11 3Marine Research and High Education (MaRHE) Center, Faafu Magoodhoo 12030, Republic of the Maldives 25 26 12 4Taxonomy and Systematics Group, Naturalis Biodiversity Center, P.O. Box 9517, 2300, RA Leiden, the Netherlands 27 28 5School of Zoology, The George S. Wise Faculty of Life Sciences, Tel-Aviv University, Tel-Aviv 69978, Israel 29 13 30 6College of Marine and Environmental Science, James Cook University, Townsville, QLD 4811, Australia 31 14 32 33 15 34 35 16 Keywords Fire corals ∙ Phylogeny ∙ Pore ∙ Nematocyst ∙ Eumedusoid 36 37 17 38 39 18 Abstract Fire corals of the hydrocoral genus Millepora provide an important ecological role as framework 40 41 19 builders of coral reefs in the Indo-Pacific and the Atlantic. Recent works have demonstrated the incongruence between 42 43 20 molecular data and the traditional taxonomy of Millepora spp. based on overall skeleton growth form and pores. In an 44 45 21 attempt to establish a reliable and standardized approach for defining species boundaries in Millepora, we focused on 46 47 22 those from the Red Sea. In this region, three species are currently recognized the fan-shaped branching M. dichotoma, 48 49 23 the blade-like M. platyphylla, and the massive/encrusting M. exaesa. A total of 412 colonies were collected from six 50 51 24 localities. Two mitochondrial marker genes (COI and 16S rDNA) were sequenced to obtain phylogeny reconstructions 52 53 25 and haplotype networks. Eight morphological traits of pores and the nematocysts of both polyp and eumedusoid stages 54 55 26 were measured to determine if significant morphological differences occur among the three species. Both markers 56 57 27 clearly resolved M. dichotoma, M. platyphylla, and M. exaesa as distinct, monophyletic lineages in the Red Sea. 58 59 28 Nevertheless, they also revealed deep genetic breaks with Southwestern Indian Ocean populations of the three species. 60 61 62 1 63 64 65 1 2 3 4 29 In the Red Sea, the three species were further distinguished based on their pore and nematocyst features. A 5 6 30 discriminant analyses revealed dactylopore density, number of dactylopores per gastropore, dactylopore distance, and 7 8 31 gastropore diameter as the most informative discriminative characters. The heteronemes, the large and small stenoteles 9 10 32 of polyps, and the distribution of mastigophores of eumedusoids also showed significantly interspecific differences. 11 12 33 An integrated morpho-molecular approach proved to be decisive in defining species boundaries of Millepora 13 14 34 supported by a combination of pore and nematocyst characters which may be phylogenetically informative. 15 16 35 17 18 36 Introduction 19 20 37 Species of the hydrocoral genus Millepora are popularly known as fire corals (Pourtales 1877). They are 21 22 38 colonial organisms building persistent calcareous skeletons and as such playing an important ecological role as 23 24 39 framework builders of coral reefs (Lewis 2006). These hydrocorals are among the most relevant reef builders in 25 26 40 shallow-water tropical seas, second only to scleractinians (Lewis 1989; Edmunds 1999; Smith et al. 2014). Millepora 27 28 occurs in tropical and sub-tropical coral reefs of both the Atlantic and the Indo-Pacific and its depth distribution is 29 41 30 restricted from less than 1 m to about 50 m deep because of the obligate symbiosis with zooxanthellae of the genus 31 42 32 33 43 Symbiodinium (Boschma 1948, 1956; Cairns et al. 1999). 34 35 44 Despite the wide geographical distribution and the relevant ecological role, Millepora has scarcely been 36 37 45 investigated in coral reef studies and, in particular, its taxonomy and systematics are controversial and much debated 38 39 46 (Hickson 1898, 1899; Crossland 1948; Boschma 1948a, 1966; Moshchenko 1992, 1997; Razak and Hoeksema 2003; 40 41 47 de Souza et al. 2017). Fire corals have been historically identified based on morphological features such as colony 42 43 48 growth form, skeletal pores, and ampullae (Klunzinger 1879; Quelch 1884; Hickson 1898; Boschma 1948b, 1949, 44 45 49 1956). Nevertheless, all these morphological characters are intraspecifically variable and even in a single specimen as 46 47 50 a result of ecophenotypic variation (de Weerdt et al. 1981, 1984; Boschma 1948a; Moshchenko 1994, 1995a, 1996a; 48 49 51 Amaral et al. 1997; Dubé et al. 2017a, b). Although growth form has been traditionally used as the main diagnostic 50 51 52 character for species identification (Forskål 1775; Ehrenberg 1834; Duchassaing and Michelotti 1860; Klunzinger 52 53 53 1879; Hickson 1898; Crossland 1941; Boschma 1948a, b), this feature has been shown to be highly variable. For 54 55 54 example, Millepora platyphylla Hemprich and Ehrenberg, 1834 in Vietnam displayed distinct morphotypes associated 56 57 55 to different reef zones and the occurrence of different colony growth forms was hypothesized to be related to factors 58 59 56 such as radiation availability, water movement, and settling suspended matter (Moshchenko 1995a). A complicating 60 61 62 2 63 64 65 1 2 3 4 57 factor herein is that juvenile Millepora corals usually start with an encrusting growth form (see e.g. Fig. 2g, Hoeksema 5 6 58 et al. 201: Fig. 1), which makes it difficult to distinguish species at early stage. Similarly, pore characters are known 7 8 59 to noticeably vary in response to the rapidity of growth and the amount of light on the skeleton surface and some 9 10 60 taxonomists have suggested to discard their use in Millepora taxonomy (Hickson 1898, 1899; Boschma 1948a, b). 11 12 61 However, Moshchenko (1994, 1995b, 1996b) proposed a quantitative approach for the analysis of pore structures and 13 14 62 was able to tell M. platyphylla apart from the branching Millepora species of the Indian Ocean. As a consequence of 15 16 63 this morphological variation, traditional morphology-based species identification since the first valid description of a 17 18 64 fire coral by Linnaeus (1758) generated more than 50 nominal species of Millepora, nine of which are now considered 19 20 65 valid in the Indo-Pacific and six in the Atlantic (Razak and Hoeksema 2003; Amaral et al. 2008; de Souza et al. 2017). 21 22 66 Recent outcomes of molecular phylogenetic analyses and DNA taxonomy have provided advantages for the 23 24 67 understanding of Millepora systematics and connectivity (López et al. 2015; Hoeksema et al. 2014; de Souza et al. 25 26 68 2017; Dubé et al. 2017c). The use of genetics has elucidated the identification and the geographic origin of fire corals 27 28 in some isolated and remote islands of the central and eastern Atlantic Ocean, including for example the Canaries, 29 69 30 Cape Verde Islands, and Ascension Island (López et al. 2015; Hoeksema et al. 2017). Moreover, the three endemic 31 70 32 33 71 species of the Brazilian province, i.e. Millepora braziliensis Veriill, 1868, Millepora nitida Veriill, 1868, and 34 35 72 Millepora laboreli Amaral, 2008, were successfully resolved based on molecular data although the traditional 36 37 73 morphological characters of pores were not sufficient to discriminate these taxa (de Souza et al. 2017). Nevertheless, 38 39 74 other studies have shown discordances between morphology-based taxonomy and genetics suggesting the need to 40 41 75 combine new molecular and morphological data for the definition of species boundaries (Meroz-Fine et al. 2003; 42 43 76 Ruiz-Ramos et al. 2014; Takama et al. 2018). For example, Ruiz-Ramos et al. (2014) genetically characterized four 44 45 77 Caribbean Millepora representatives, i.e. Millepora alcicornis Linnaeus, 1758, Millepora complanata Lamarck, 1816, 46 47 78 Millepora squarrosa Lamarck, 1816, and Millepora striata Duchassaing and Michelotti, 1864, and recovered the latter 48 49 79 two species as distinct molecular lineages while the otherss form an unresolved species complex. Furthermore, a recent 50 51 80 study from Japan demonstrated that the three branching species Millepora dichotoma Forskål, 1775, Millepora 52 53 81 intricata Milne Edwards, 1860, and Millepora tenera Boschma, 1949 were receovered in a single molecular clade 54 55 82 while a previously unknown lineage of an encrusting Millepora form was discovered, which overgrows living 56 57 83 scleractinian corals (Takama et al.
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