Species Diversity and Distribution of the Genus Colpomenia (Scytosiphonaceae, Phaeophyceae) Along the Coast of China
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Research Article Algae 2019, 34(3): 217-228 https://doi.org/10.4490/algae.2019.34.7.22 Open Access Species diversity and distribution of the genus Colpomenia (Scytosiphonaceae, Phaeophyceae) along the coast of China Xiao-Han Song1,2,3, Zi-Min Hu1,2,*, Zhong-Min Sun4, Stefano G. A. Draisma5, Pablo Fresia6 and De-Lin Duan1,2 1Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Acad- emy of Sciences, Qingdao 266071, China 2Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China 3University of Chinese Academy Sciences, Beijing 100094, China 4Laboratory of Marine Organism Taxonomy & Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China 5Excellence Center for Biodiversity of Peninsular Thailand, Faculty of Science, Prince of Songkla University, 15 Karnjana- vit Road, 90112, Hat Yai, Songkhla, Thailand 6Unidad de Bioinformatica, Institut Pasteur de Montevideo, Mataojo, 2020 Montevideo, Uruguay The marine brown algal genus Colpomenia has a worldwide distribution, with five species reported in Korea and Ja- pan. However, no studies to date attempted to identify the number of species and geographical distribution of Colpome- nia along Chinese coast. To fill the biodiversity knowledge gap, we analyzed 63 mitochondrial cox3 and 62 mitochondrial atp6 sequences of Colpomenia specimens collected from 30 localities along the Chinese coast. Maximum likelihood and Bayesian inference trees suggest the presence of at least three Colpomenia species (i.e., C. peregrina, C. claytoniae, and C. sinuosa) in China. C. peregrina and C. claytoniae are documented for the first time. C. sinuosa was only found in the South China Sea and its distribution didn’t overlap with that of C. peregrina which was found in the Yellow-Bohai Sea and the East China Sea. C. claytoniae appears to be confined to three isolated islands in the East and the South China Sea, where it occurs in sympatry with, respectively, C. peregrina and C. sinuosa. Future study can focus on comparing eco- physiological differences of Colpomenia species in response to environmental variables and exploring possible genetic hybridization / introgression at inter-specific contact zones. Key Words: distribution range; genetic variation; new record species; phylogenetic diversity INTRODUCTION Colpomenia (Endlicher) Derbès et Solier (Scytosi- or lower intertidal zone. Due to developmental varia- phonaceae, Phaeophyceae) is a cosmopolitan brown al- tion, Colpomenia has been traditionally divided into two gal genus frequently found attached to rock with gentle morphological groups: (1) globular species producing slopes or attached to other marine macroalgae at middle plurilocular and unilocular zoidangia on crustose spo- This is an Open Access article distributed under the Received January 12, 2019, Accepted July 22, 2019 terms of the Creative Commons Attribution Non-Com- Corresponding Author mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which * permits unrestricted non-commercial use, distribution, and reproduction E-mail: [email protected] in any medium, provided the original work is properly cited. Tel: +86-532-8289-8783, Fax: +86-532-8289-8556 Copyright © 2019 The Korean Society of Phycology 217 http://e-algae.org pISSN: 1226-2617 eISSN: 2093-0860 Algae 2019, 34(3): 217-228 rophytes, and (2) species with elongate or tubular thalli multiple introductions might occur among Australasia, producing only unilocular zoidangia on sporophytes Europe, and America. (Kogame et al. 1999, Boo et al. 2011, Lee et al. 2012). Chinese coast, in particular the Yellow-Bohai Sea However, Santiañez et al. (2018) recently removed the tu- (YBS), geographically adjoins and shares homologous bular species [i.e., Colpomenia bullosa (D. A. Saunders) coastal marine environments with the Korean Peninsula Yamada, Colpomenia durvillei (Bory) M. E. Ramírez, and and the Japanese Archipelago (Tyberghein et al. 2012). Colpomenia wynnei K. M. Lee, R. Riosmena-Rodriguez, Similar coastal configurations in those neighboring areas K. Kogame et S. M. Boo] from Colpomenia and proposed during the LGM (Wang 1999), produced seaweed floras them as a new genus Dactylosiphon Santiañez, K. M. Lee, that are closely related taxonomically (Tseng 1983, Yoshi- S. M. Boo et Kogame based on combined mitochondrial da et al. 2015). In addition, the Kuroshio Current can con- and chloroplast phylogenies. nect populations of marine species, including seaweeds, The globular Colpomenia species usually contain oxy- along the coasts of East Asia (Barkley 1970, Hu et al. 2013, gen generated by photosynthesis, making them buoyant. Li et al. 2017). The coastal currents in China (e.g., the Bo- When oysters are the substrate, they can become buoy- hai Sea coastal current, the Yellow Sea coastal current and ant and drift with the current, earning members of the the East China Sea coastal current) in different seasons globular species the moniker “oyster thieves” (Black- can also contribute to multiple dispersal to a great ex- ler 1967, Vandermeulen 1984). Adding to such mischief tent. Taken together, these historical climate change and caused by the globular species, floating thalli can travel oceanic currents can interplay and ultimately affect the long distances and spread Colpomenia species in oyster richness, diversity and distribution patterns of present- mariculture (Lee et al. 2014a). Therefore, the behavior day seaweeds in China, Korea, and Japan (e.g., Chondrus and mobility of globular Colpomenia species make them ocellatus Holmes, Hu et al. 2015, Sargassum fusiforme ideal for studying how maritime transportation affects (Harvey) Setchel, Hu et al. 2017). biodiversity trends, population genetic structure and Colpomenia species have broad latitudinal distribu- biogeographical patterns of seaweeds. tions in the West Pacific (Guiry and Guiry 2019). For ex- Ten Colpomenia species have been recognized (Guiry ample, C. peregrina appears in coastal temperate waters and Guiry 2019). Five species have been recorded from in the northern hemisphere of Japan, Korea, and Rus- the coasts of Korea and Japan, i.e., C. claytoniae S. M. sia (e.g., Perestenko 1980, Lee et al. 2014a, Yoshida et al. Boo, K. M. Lee, G. Y. Cho et W. Nelson (Boo et al. 2011), C. 2015) and in the southern hemisphere of southern Aus- ecuticulata M. J. Parsons (Lee and Kang 2001), C. expansa tralia and New Zealand (e.g., Harper et al. 2012, Nelson (D. A. Saunders) Y. -P. Lee (Lee 2008, Lee et al. 2012), C. 2013, Scott 2017), respectively. Similar patterns have peregrina Sauvageau (Kogame et al. 1999, Boo 2010), and been reported for C. claytoniae (e.g., Boo and Ko 2012, C. sinuosa (Mertens ex Roth) Derbès et Solier (Boo 2010, Nelson 2013). China, which stretches over some 18,000 Yoshida et al. 2015). These studies indicate that Colpo- kilometers of coastlines and has considerable environ- menia species diversity in the northwest Pacific is rich. mental shifts (e.g., the significantly different sea surface C. sinuosa is common in Korea, Japan, and China (e.g., temperature, annual precipitation and solar radiation Okamura 1936, Tseng 1983, Kogame 1997, Cho et al. 2005, between northern and southern coast) (Ma et al. 2017), Lee et al. 2013). Cho et al. (2009) presented a first glimpse is the main component of the China Sea Coastal Province at genetic diversity of C. sinuosa on a global scale. They (Longhurst 2007) and geographically located near Japan analyzed nuclear internal transcribed spacers of the ri- and Korea. However, for the genus Colpomenia, only C. bosomal cistron (ITS) and chloroplast encoded large sinuosa has been reported in the past few decades (Tseng subunit of the ribulose-1,5-bisphosphate carboxylase 1983, 2008, Liu 2008), and there has been no study of gene (rbcL) and found that the unique tandem repeats the quantity and distribution of Colpomenia species. We in the ITS region correspond to the geographical distri- thus speculate that previous studies (Tseng 1983) may bution of C. sinuosa. Lee et al. (2013) observed three ge- have underestimated the number of Colpomenia species netic lineages within C. sinuosa around the world using along the coast of mainland China. Furthermore, climate mitochondrial cytochrome c oxidase subunit III (cox3) change induced a northward shift of temperature zones and chloroplast rbcL. They suggested that C. sinuosa had in China, together with ocean acidification and coastal broad and complicated biogeographical patterns in the erosion, have exerted the necessary obligation of pro- Indo-Pacific Ocean region where the Red Sea was likely tecting seaweed species diversity (Zheng et al. 2018). The a refugium before the Last Glacial Maximum (LGM), and present study focuses on Colpomenia specimens collect- https://doi.org/10.4490/algae.2019.34.7.22 218 Song et al. Colpomenia Diversity in China nomic DNA were checked by OD260 / OD280 ratios and 1% agarose gel electrophoresis. Polymerase chain reaction amplification and DNA sequencing Based on a recent molecular study of Colpomenia (Lee et al. 2014a), mitochondrial cox3 and atp6 were selected as gene markers. Primer sets F49 / R20 and F25P / R754P (Lee et al. 2014a) were used to amplify, respectively, cox3 and atp6 fragments from 63 specimens. Polymerase chain reaction (PCR) amplification was performed in 50 μL volumes, each containing 25 μL 2× Es Taq Master Mix (+dye) (CWBIO, Beijing, China), 10 pmol of each primer and 6 ng of template DNA. For the cox3 gene, PCR reac- tions consisted of an initial denaturation at 95°C for 4 min, followed by 35 amplification cycles (denaturation at 94°C for 45 s, annealing at 53°C for 1 min, extension at 72°C for 1 min) with a final extension at 72°C for 10 min. Sampling sites and distribution of Colpomenia along the Fig. 1. For the atp6 gene, PCR reactions consisted of an initial coast of China. denaturation at 95°C for 4 min, followed by 35 amplifi- cation cycles (denaturation at 94°C for 30 s, annealing at ed from the entire Chinese coast.