DOI QR코드

DOI QR Code

A unique genetic lineage at the southern coast of China in the agar-producing Gracilaria vermiculophylla (Gracilariales, Florideophyceae)

  • Hu, Zi-Min (Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences) ;
  • Liu, Ruo-Yu (Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences) ;
  • Zhang, Jie (Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences) ;
  • Duan, De-Lin (Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences) ;
  • Wang, Gao-Ge (College of Marine Life Science, Ocean University of China) ;
  • Li, Wen-Hong (College of Animal Science and Technology, Guangxi University)
  • Received : 2018.06.15
  • Accepted : 2018.08.30
  • Published : 2018.09.15

Abstract

Ocean warming can have significant negative impacts on population genetic diversity, local endemism and geographical distribution of a wide range of marine organisms. Thus, the identification of conservation units with high risk of extinction becomes an imperative task to assess, monitor, and manage marine biodiversity for policy-makers. Here, we surveyed population structure and genetic variation of the red seaweed Gracilaria vermiculophylla along the coast of China using genome-based amplified fragment length polymorphism (AFLP) scanning. Regardless of analysis methods used, AFLP consistently revealed a south to north genetic isolation. Populations at the southern coast of China showed unique genetic variation and much greater allelic richness, heterozygosity, and average genetic diversity than the northern. In particular, we identified a geographical barrier that may hinder genetic exchange between the two lineages. Consequently, the characterized genetic lineage at the southern coast of China likely resulted from the interplay of post-glacial persistence of ancestral diversity, geographical isolation and local adaptation. In particular, the southern populations are indispensable components to explore evolutionary genetics and historical biogeography of G. vermiculophylla in the northwestern Pacific, and the unique diversity also has important conservation value in terms of projected climate warming.

Acknowledgement

Supported by : National Natural Science Foundation of China, Guangxi Natural Science Foundation

References

  1. Abreu, M. H., Pereira, R., Yarish, C., Buschmann, A. H. & Sousa-Pinto, I. 2011. IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77-87. https://doi.org/10.1016/j.aquaculture.2010.12.036
  2. Bonin, A., Bellemain, E., Bronken Eidesen, P., Pompanon, F., Brochmann, C. & Taberlet, P. 2004. How to track and assess genotyping errors in population genetic studies. Mol. Ecol. 13:3261-3273. https://doi.org/10.1111/j.1365-294X.2004.02346.x
  3. Castric, V. & Bernatchez, L. 2003. The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163:983-996.
  4. Chao, A. & Shen, T. J. 2003. Program SPADE (Species Prediction and Diversity Estimation). Available from: http://chao.stat.nthu.edu.tw. Accessed Apr 20, 2018.
  5. Cheang, C. C., Chu, K. H. & Ang, P. O. 2010. Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae, Heterokontophyta) in northwestern Pacific. Mol. Ecol. 19:2933-2948. https://doi.org/10.1111/j.1365-294X.2010.04685.x
  6. Diekmann, O. E. & Serrao, E. A. 2012. Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina. Mol. Ecol. 21:1647-1657. https://doi.org/10.1111/j.1365-294X.2012.05500.x
  7. Doney, S. C., Ruckelshaus, M., Duffy, J. E., Barry, J. P., Chan, F., English, C. A., Galindo, H. M., Grebmeier, J. M., Hollowed, A. B., Knowlton, N., Polovina, J., Rabalais, N. N., Sydeman, W. J. & Talley, L. D. 2012. Climate change impacts on marine ecosystems. Ann. Rev. Mar. Sci. 4:11-37. https://doi.org/10.1146/annurev-marine-041911-111611
  8. Eckert, C. G., Samis, K. E. & Lougheed, S. C. 2008. Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond. Mol. Ecol. 17:1170-1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x
  9. Emerson, B. C., Paradis, E. & Thebaud, C. 2001. Revealing the demographic histories of species using DNA sequences. Trends Ecol. Evol. 16:707-716. https://doi.org/10.1016/S0169-5347(01)02305-9
  10. Excoffier, L. & Lischer, H. E. L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
  11. Gibson, S. Y., van der Marel, R. C. & Starzomski, B. M. 2009. Climate change and conservation of leading-edge peripheral populations. Conserv. Biol. 23:1369-1373. https://doi.org/10.1111/j.1523-1739.2009.01375.x
  12. Gorman, L., Kraemer, G. P., Yarish, C., Boo, S. M. & Kim, J. K. 2017. The effects of temperature on the growth rate and nitrogen content of invasive Gracilaria vermiculophylla and native Gracilaria tikvahiae from Long Island Sound, USA. Algae 32:57-66. https://doi.org/10.4490/algae.2017.32.1.30
  13. Hampe, A. & Petit, R. J. 2005. Conserving biodiversity under climate change: the rear edge matters. Ecol. Lett. 8:461-467. https://doi.org/10.1111/j.1461-0248.2005.00739.x
  14. He, L., Zhang, A., Weese, D., Zhu, C., Jiang, C. & Qiao, Z. 2010. Late Pleistocene population expansion of Scylla paramamosain along the coast of China: a population dynamic response to the last interglacial sea level high stand. J. Exp. Mar. Biol. Ecol. 385:20-28. https://doi.org/10.1016/j.jembe.2010.01.019
  15. Hu, Z. -M. & Juan, L. -B. 2014. Adaptation mechanisms and ecological consequences of seaweed invasions: a review case of agarophyte Gracilaria vermiculophylla. Biol. Invasions 16:967-976. https://doi.org/10.1007/s10530-013-0558-0
  16. Hu, Z. -M., Kantachumpoo, A., Liu, R. -Y., Sun, Z. -M., Yao, J. -T., Komatsu, T., Uwai, S. & Duan, D. -L. 2018. A late Pleistocene marine glacial refugium in the south-west of Hainan Island, China: phylogeographical insights from the brown alga Sargassum polycystum. J. Biogeogr. 45:355-366. https://doi.org/10.1111/jbi.13130
  17. Hu, Z. -M., Li, J. -J., Sun, Z. -M., Gao, X., Yao, J. -T., Choi, H. -G., Endo, H. & Duan, D. -L. 2017. Hidden diversity and phylogeographic history provide conservation insights for the edible seaweed Sargassum fusiforme in the Northwest Pacific. Evol. Appl. 10:366-378. https://doi.org/10.1111/eva.12455
  18. Hu, Z. -M., Li, J. -J., Sun, Z. -M., Oak, J. -H., Zhang, J., Fresia, P., Grant, S. & Duan, D. -L. 2015. Phylogeographic structure and deep lineage diversification of the red alga Chondrus ocellatus Holmes in the Northwest Pacific. Mol. Ecol. 24:5020-5033. https://doi.org/10.1111/mec.13367
  19. Hu, Z. -M., Uwai, S., Yu, S. -H., Komatsu, T., Ajisaka, T. & Duan, D. -L. 2011. Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol. Ecol. 20:3894-3909. https://doi.org/10.1111/j.1365-294X.2011.05220.x
  20. Jakobsson, M. & Rosenberg, N. A. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806. https://doi.org/10.1093/bioinformatics/btm233
  21. Kim, S. Y., Weinberger, F. & Boo, S. M. 2010. Genetic data hint at a common donor region for invasive Atlantic and Pacific populations of Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J. Phycol. 46:1346-1349. https://doi.org/10.1111/j.1529-8817.2010.00905.x
  22. Krueger-Hadfield, S. A., Kollars, N. M., Strand, A. E., Byers, J. E., Shainker, S. J., Terada, R., Greig, T. W., Hammann, M., Murray, D. C., Weinberger, F. & Sotka, E. E. 2017. Genetic identification of source and likely vector of a widespread marine invader. Ecol. Evol. 7:4432-4447. https://doi.org/10.1002/ece3.3001
  23. Krueger-Hadfield, S. A., Roze, D., Mauger, S. & Valero, M. 2013. Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Mol. Ecol. 22:3242-3260. https://doi.org/10.1111/mec.12191
  24. Li, J. -J., Hu, Z. -M., Sun, Z. -M., Yao, J. -T., Liu, F. -L., Fresia, P. & Duan, D. -L. 2017. Historical isolation and contemporary gene flow drive population diversity of the brown alga Sargassum thunbergii along the coast of China. BMC Evol. Biol. 17:246. https://doi.org/10.1186/s12862-017-1089-6
  25. Liu, R. Y., Sun, Z. M., Yao, J. T., Hu, Z. M. & Duan, D. L. 2016. Genetic diversity of the habitat-forming red alga Gracilaria vermiculophylla along the Chinese coasts. Biodivers. Sci. 24:781-790 (in Chinese with English abstract). https://doi.org/10.17520/biods.2016038
  26. Manni, F., Guerard, E. & Heyer, E. 2004. Goegraphic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier's algorithm. Hum. Biol. 76:173-190. https://doi.org/10.1353/hub.2004.0034
  27. Neiva, J., Assis, J., Coelho, N. C., Fernandes, F., Pearson, G. A. & Serrao, E. A. 2015. Genes left behind: climate change threatens cryptic genetic diversity in the canopy-forming seaweed Bifurcaria bifurcata. PLoS ONE 10:e0131530. https://doi.org/10.1371/journal.pone.0131530
  28. Neiva, J., Pearson, G. A., Valero, M. & Serrao, E. A. 2012. Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoides. J. Biogeogr. 39:1167-1178. https://doi.org/10.1111/j.1365-2699.2011.02670.x
  29. Nicastro, K. R., Zardi, G. I. & McQuaid, C. D. 2010. Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments. Biol. Invasions 12:2165-2177. https://doi.org/10.1007/s10530-009-9619-9
  30. Olsen, J. L., Stam, W. T., Coyer, J. A., Reusch, T. B. H., Billingham, M., Bostrom, C., Calvert, E., Christie, H., Granger, S., La Lumiere, R., Milchakova, N., Oudot-Le Secq, M.-P., Procaccini, G., Sanjabi, B., Serrao, E., Veldsink, J., Widdicombe, S. & Wyllie-Echeverria, S. 2004. North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol. Ecol. 13:1923-1941. https://doi.org/10.1111/j.1365-294X.2004.02205.x
  31. Pauls, S. U., Nowak, C., Balint, M. & Pfenninger, M. 2013. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22:925-946. https://doi.org/10.1111/mec.12152
  32. Peakall, R. & Smouse, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28:2537-2539. https://doi.org/10.1093/bioinformatics/bts460
  33. Pritchard, J. K., Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
  34. Provan, J. & Maggs, C. A. 2012. Unique genetic variation at a species' rear edge is under threat from global climate change. Proc. R. Soc. B Biol. Sci. 279:39-47. https://doi.org/10.1098/rspb.2011.0536
  35. Ramirez, F., Afán, I., Davis, L. S. & Chiaradia, A. 2017. Climate impacts on global hot spots of marine biodiversity. Sci. Adv. 3:e1601198. https://doi.org/10.1126/sciadv.1601198
  36. Ramus, A. P., Silliman, B. R., Thomsen, M. S. & Long, Z. T. 2017. An invasive foundation species enhances multifunctionality in a coastal ecosystem. Proc. Natl. Acad. Sci. U. S. A. 114:8580-8585. https://doi.org/10.1073/pnas.1700353114
  37. Rosenberg, N. A. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 4:137-138.
  38. Sotka, E. E., Baumgardner, A. W., Bippus, P. M., Destombe, C., Duermit, E. A., Endo, H., Flanagan, B. A., Kamiya, M., Lees, L. E., Murren, C. J., Nakaoka, M., Shainker, S. J., Strand, A. E., Terada, R., Valero, M., Weinberger, F. & Krueger-Hadfield, S. A. 2018. Combining niche shift and population genetic analyses predicts rapid phenotypic evolution during invasion. Evol. Appl. 11:781-793. https://doi.org/10.1111/eva.12592
  39. Terada, R. & Yamamoto, H. 2002. Review of Gracilaria vermiculophylla and other species in Japan and Asia. In Abbott, I. A. & Mcdermid, K. J. (Eds.) Taxonomy of Economic Seaweeds with Reference to Some Pacific Species, Vol. 8. California Sea Grant College Program, University of California, La Jolla, CA, pp. 215-224.
  40. Tseng, C. K. & Chen, S. F. 1959. Reproductive biology and seeding development of Gracilaria asiatica in laboratory. Chin. Sci. Bull. 202-203.
  41. Tseng, C. K. & Xia, B. -M. 1999. On the Gracilaria in the western Pacific and southeastern Asia region. Bot. Mar. 42:209-218.
  42. Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T., Hornes, M., Friters, A., Pot, J., Paleman, J., Kuiper, M. & Zabeau, M. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acid Res. 23:4407-4414. https://doi.org/10.1093/nar/23.21.4407
  43. Wang, B. -D., Wang, X. -L. & Zhan, R. 2003. Nutrient conditions in the Yellow Sea and the East China Sea. Estuar. Coast. Shelf Sci. 58:127-136.
  44. Wang, P. -X. 1999. Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar. Geol. 156:5-39. https://doi.org/10.1016/S0025-3227(98)00172-8
  45. Wernberg, T., Smale, D. A., Tuya, F., Thomsen, M. S., Langlois, T. J., de Bettignies, T., Bennett, S. & Rousseaux, C. S. 2013. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3:78-82. https://doi.org/10.1038/nclimate1627
  46. Whitlock, R., Hipperson, H., Mannarelli, M., Butlin, R. K. & Burke, T. 2008. An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Mol. Ecol. Resour. 8:725-735. https://doi.org/10.1111/j.1755-0998.2007.02073.x
  47. Xu, S. N., Wen, S. S., Wu, W. X. & He, P. M. 2008. Bioremediation of caged fish aquaculture by the red alga Gracilaria verrucosa in an integrated multitrophic aquaculture system. Acta Ecol. Sin. 28:1466-1475 (in Chinese with English abstract).
  48. Zardi, G. I., Nicastro, K. R., Costa, J. F., Serrao, E. A. & Pearson, G. A. 2013. Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure. Estuar. Coast. Shelf Sci. 131:140-148. https://doi.org/10.1016/j.ecss.2013.08.016
  49. Zardi, G. I., Nicastro, K. R., Serrao, E. A., Jacinto, R., Monteiro, C. A. & Pearson, G. A. 2015. Closer to the rear edge: ecological and genetic diversity down the core-edge gradient of a marine macroalga. Ecosphere 6:1-25.