Genetic Diversity of the Habitat-forming Red Alga Gracilaria vermiculophylla along Chinese Coasts

Ruoyu Liu ¹^,² Zhongmin Sun ¹^,³ Jianting Yao ¹^,⁴ Zimin Hu ¹^,⁴ Delin Duan ¹^,⁴

(1.Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong 266071)
(2.University of Chinese Academy of Sciences, Beijing 100049)
(3.Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong 266071)
(4.Qingdao National Laboratory for Marine Science and Technology, Qingdao, Shandong 266237)

【Knowledge Link】benthos; gene flow; polymorphism; gametophyte; Pleistocene

【Abstract】As a habitat-forming species, the red alga Gracilaria vermiculophylla has been noted to play an essential role in shaping coastal marine communities and maintaining intertidal ecosystems along Chinese coasts. However, few studies have been conducted that analyzed the genetic structure of the population and the distribution patterns of genetic variation. In this study, we compiled partial mitochondrial DNA cytochrome c oxidase subunit I gene (cox1) of 19 G. vermiculophylla populations (461 individuals) and performed phylogenetic analysis and population genetic surveys. A total of 461 mt-DNA cox1 sequences were obtained and edited into 641 bp, which contained 21 polymorphic sites and yielded 15 haplotypes. Phylogenetic inferences, haplotype networking, and principal component analysis consistently indicated that G. vermiculophylla populations diverged into two groups: the north group is comprised of specimens from the Yellow-Bohai Sea and the Shengsi Islands, while the south group is comprised of specimens from six locations south to Xiamen, Fujian Province. Analysis of the molecular variation and Nei's genetic distances indicated low genetic differentiation between populations in each group while group-level genetic divergence is comparable to the degree of subspecies differentiation.

【Keywords】 Gracilaria vermiculophylla; mitochondrial cox1; phylogenetics; genetic diversity; population genetic differentiation;

【DOI】

【Funds】 National Natural Science Foundation of China (31370264)

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References

Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.

Bellorin AM, Olivera MC, Olivera EC (2004) Gracilaria vermiculophylla: a western Pacific species of Gracilariaceae (Rhodophyta) first recorded from the eastern Pacific. Phycological Research, 52, 69-79.

Boo GH, Kim KM, Nelson WA, Rafael RR, Yoon KJ, Boo SM (2014) Taxonomy and distribution of selected species of the agarophyte genus Gelidium (Gelidiales, Rhodophyta) . Journal of Applied Phycology, 26, 1243-1251.

Cheang CC, Chu KH, Put AO (2010) Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae Heterokontophyta) in northwestern Pacific. Molecular Ecology, 19, 2933-2948.

Chen Z, Zhang J, Fu HF, Xu ZZ, Deng KZ, Zhang JY (2012) On the validity of the species Phenacoccus solenopsis based on morphological and mitochondrial COI data, with the description of a new body color variety. Biodiversity Science20, 443-450. (in Chinese with English abstract)

Chu D, Liu GX, Fu HB, Xu W (2009) Phylogenetic analysis of mt-COI reveals the cryptic lineages in Phenacoccus solenopsis complex (Hemiptera: Pseudococcidae) . Acta Entomologica Sinica, 52, 1261-1265.

Geraldino PJL, Yang EC, Kim MS, Boo SM (2009) Systematics of Hypnea asiatica sp. nov. (Hypneaceae, Rhodophyta) based on morphology and nr DNA SSU, plastid rbc L, and mitochondrial cox1. Taxon, 58, 606-616.

Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JAValero M (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilenesis: how farming practices favor asexual reproduction and heterozygosity. Evolution, 62, 1500-1519.

Guiry MD, Guiry GM (2016) Algae Base. World-wide electronic publication, National University of Ireland, Galway http: //www. algaebase. org. (accessed on 2016-04-12) .

Gulbransen DJ, Mc Glathery KJ, Marklund M, Norris JNGurgel CFD (2012) Gracilaria vermiculophylla (Rhodophyta, Gracilariales) in the Virginia coastal bays, USA: cox1analysis reveals high genetic richness of an introduced macroalga. Journal of Phycology, 48, 1278-1283.

Hall TA (1999) Bio Edit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.

Hebert PD, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270, 313-321.

Hu ZM, Zhang J, Lopez-Bautista J, Duan DL (2013) Asymmetric genetic exchange in the brown seaweed Sargassum fusiforme (Phaeophyceae) driven by oceanic currents. Marine Biology, 160, 1407-1414.

Hu ZM, Juan LB (2014) Adaptation mechanisms and ecological consequences of seaweed invasions: a review case of agarophyte Gracilaria vermiculophylla. Biological Invasions, 16, 967-976.

Kim SY, Weinberger F, Boo SM (2010) Genetic data hint at a common donor region for invasive Atlantic and Pacific populations of Gracilaria vermiculophylla (Gracilariales Rhodophyta) . Journal of Phycology, 46, 1346-1349.

Librado P, Roas J (2009) DNAsp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformations, 25, 1451-1452.

Li JJ, Zhang J, Hu ZM, Duan DL (2013) Population genetics and demographic history of red seaweed, Palmaria palmata from the Canada-northwest Atlantic. Biodiversity Science21, 306-314. (in Chinese with English abstract)

Peakall R, Smouse PE (2012) Gen Al Ex 6. 5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28, 2537-2539.

Peason EA, Murray SN (1997) Patterns of reproduction, genetic diversity and genetic differentiation in California populations of the geniculate coralline alga Lithothrix aspergillum (Rhodophyta) . Journal of Phycology, 33, 753-763.

Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817-818.

Riosmena RR, Talavera SA, Acosta VB, Gardner SC (2009) Heavy metals dynamics in seaweeds and seagrasses in Bahía Magdalena, BCS, México. Journal of Applied Phycology22, 283-291.

Robba L, Russell SJ, Barker GL, Brodie J (2006) Assessing the use of the mitochondrial Cox1 marker for use in DNA barcoding of red algae (Rhodophyta) . American Journal of Botany, 93, 1101-1108.

Rueness J (2005) Life history and molecular sequences of Gracilaria vermiculophylla (Gracilariales, Rhodophyta), a new introduction to European waters. Phycologia, 44120-128.

Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 3601879-1888.

Saunders GW (2009) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Molecular Ecology Resources, 9 (Suppl. 1), 140-150.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version6. 0. Molecular Biology and Evolution, 30, 2725-2729.

Terada R, Yamamoto H (2002) Review of Gracilaria vermiculophylla and other species in Japan and Asia. Taxonomy of Economic Seaweeds, 8, 215-224.

Thomsen MS, Stæhr PA, Nejrup L, Schiel DR (2013) Effects of the invasive macroalgae Gracilaria vermiculophylla on two co-occurring foundation species and associated invertebrates. Aquatic Invasions, 8, 133-145.

Tseng CK, Chen JF (1959) Reproductive of Gracilaria vermiculophylla and cultivation seedings inlaboratory. 90, 202-203. (in Chinese)

Tseng CK (2008) 中国黄渤海海藻. Science Press, Beijing. (in Chinese)

Wang PX (1999) Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology, 156, 5-39.

Xia BM, Chang CF (1999) 中国海藻志第二卷红藻门 (第五分册): 伊谷藻目, 杉藻目, 红皮藻目. Science Press, Beijing. (in Chinese)

Yang EC, Kim MS, Geraldino PJL, Sahoo D, Shin JA, Boo SM (2008) Mitochondrial cox1 and plastid rbc L genes of Gracilaria vermiculophylla (Gracilariaceae, Rhodophyta) . Journal of Applied Phycology, 20, 161-168.

Zhao XB, Pang SJ, Shan TF, Liu F (2013) Applications of three DNA barcodes in assorting intertidal red macroalgal flora in Qingdao, China. Journal of Ocean University of China, 12, 139-145.

Zheng WJ, Zhu SH, Shen XQ, Liu BQ, Pan ZC, Ye YF (2009) Genetic differentiation of Tegillarca granosa based on mitochondrial COI gene sequences. Zoological Research, 30, 17-23. (in Chinese with English abstract)

Zhong CH, Huang RF, Lin Q, Zheng YY, Li LB, Liu B (2014) Molecular identification of a green type of Gracilaria vermiculophylla. Journal of Applied Oceanography, 33, 183-189. (in Chinese with English abstract)

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