Skip to main content

Advertisement

Log in

Chloroplast DNA phylogeography of the Holly mangrove Acanthus ilicifolius in the Indo-West Pacific

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Acanthus ilicifolius is a widespread mangrove species in the Indo-West Pacific (IWP) with high ecological value. In this study, we analyzed the patterns of genetic variation in the species across its distribution range and assessed factors that may have influenced its genetic structure across the IWP using data from four chloroplast DNA fragments. Our results demonstrated high genetic diversity at the species level with little variation within populations, indicating restricted gene flow among A. ilicifolius populations. Strong genetic divergence was found between populations in the Indian Ocean and populations in the Pacific Ocean, likely due to the land barrier effect of the Malay Peninsula (or in the past, the Sundaland). Ecological niche modeling revealed no significant niche differentiation between the two groups, suggesting that ecological divergence was less responsible for the divergence of A. ilicifolius. Despite the ability for long-distance dispersal, genetic barriers identified within the Pacific Ocean suggested ocean currents to be a cryptic barrier for gene flow in this region. This study provides new insights into the historical population dynamics of mangrove species in the IWP region and is valuable for the long-term conservation of A. ilicifolius.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alfaro, M. E., D. R. Karns, H. K. Voris, E. Abernathy & S. L. Sellins, 2004. Phylogeny of Cerberus (Serpentes: Homalopsinae) and phylogeography of Cerberus rynchops: diversification of a coastal marine snake in Southeast Asia. Journal of Biogeography 31: 1277–1292.

    Google Scholar 

  • Antoro, S., U. Na-Nakorn & W. Koedprang, 2006. Study of genetic diversity of orange-spotted grouper, Epinephelus coioides, from Thailand and Indonesia using microsatellite markers. Marine Biotechnology 8: 17–26.

    CAS  PubMed  Google Scholar 

  • Avise, J. C., 2000. Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Ayre, D. J. & S. Dufty, 1994. Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia’s Great Barrier Reef. Evolution 48: 1183–1201.

    PubMed  Google Scholar 

  • Babu, B. H., B. S. Shylesh & J. Padikkala, 2002. Tumour reducing and anticarcinogenic activity of Acanthus ilicifolius in mice. Journal of Ethnopharmacology 79: 27–33.

    CAS  PubMed  Google Scholar 

  • Bandelt, H.-J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    CAS  PubMed  Google Scholar 

  • Barber, P. H., S. R. Palumbi, M. V. Erdmann & M. K. Moosa, 2000. A marine Wallace’s line? Nature 406: 692–693.

    CAS  PubMed  Google Scholar 

  • Barbier, E. B., S. D. Hacker, C. Kennedy, E. W. Kock, A. C. Stier & B. R. Sillman, 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81: 169–193.

  • Benzie, J. A., 1999. Major genetic differences between crown-of-thorns starfish (Acanthaster planci) populations in the Indian and Pacific Oceans. Evolution 53: 1782–1795.

    CAS  PubMed  Google Scholar 

  • Cannon, C. H., R. J. Morley & A. B. G. Bush, 2009. The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proceedings of the National Academy of Sciences, USA 106: 11188.

    CAS  Google Scholar 

  • Cheng, Y. P., S. Y. Hwang & T. P. Lin, 2005. Potential refugia in Taiwan revealed by the phylogeographical study of Castanopsis carlesii Hayata (Fagaceae). Molecular Ecology 14: 2075–2085.

    CAS  PubMed  Google Scholar 

  • Clarke, P. J., R. A. Kerrigan & C. J. Westphal, 2001. Dispersal potential and early growth in 14 tropical mangroves: do early life history traits correlate with patterns of adult distribution? Journal of Ecology 89: 648–659.

    Google Scholar 

  • Dodd, R., Z. Afzal-Rafii, N. Kashani & J. Budrick, 2002. Land barriers and open oceans: effects on gene diversity and population structure in Avicennia germinans L. (Avicenniaceae). Molecular Ecology 11: 1327–1338.

    CAS  PubMed  Google Scholar 

  • Doyle, J. J. & J. L. Doyle, 1990. A rapid total DNA preparation procedure for fresh plant tissue. Focus 12: 13–15.

    Google Scholar 

  • Drexler, J. Z., 2001. Maximum longevities of Rhizophora apiculata and R. mucronata propagules. Pacific Science 55: 17–22.

    Google Scholar 

  • Duke, N. C., 1995. Genetic diversity, distributional barriers and rafting continents? More thoughts on the evolution of mangroves. Hydrobiologia 295: 167–181.

    Google Scholar 

  • Duke, N. C., 2013. World mangrove ID: expert information at your fingertips. MangroveWatch Publications, Brisbane.

    Google Scholar 

  • Duke, N. C., E. Lo & M. Sun, 2002. Global distribution and genetic discontinuities of mangroves–emerging patterns in the evolution of Rhizophora. Trees 16: 65–79.

    Google Scholar 

  • Duke, N. C., J. O. Meynecke, S. Dittmann, A. M. Ellison, K. Anger, U. Berger, S. Cannicci, K. Diele, K. C. Ewel, C. D. Field, N. Koedam, S. Y. Lee, C. Marchand, I. Nordhaus & F. Dahdouh-Guebas, 2007. A world without mangroves? Science 317: 41–43.

    CAS  PubMed  Google Scholar 

  • Dupanloup, I., S. Schneider & L. Excoffier, 2002. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11: 2571–2581.

    CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    PubMed  Google Scholar 

  • Fan, D. M., J. P. Yue, Z. L. Nie, Z. M. Li, H. P. Comes & H. Sun, 2013. Phylogeography of Sophora davidii (Leguminosae) across the ‘Tanaka-Kaiyong Line’, an important phytogeographic boundary in Southwest China. Molecular Ecology 22: 4270–4288.

    CAS  PubMed  Google Scholar 

  • Fang G., G. Wang, Y. Fang & W. Fang, 2012. A review on the South China Sea western boundary current. Acta Oceanologica Sinica 31: 1–10.

  • Flenley, J. R., 1998. Tropical forests under the climates of the last 30,000 years. In Markham, A. (ed.), Potential impacts of climate change on tropical forest ecosystems. Springer, Netherlands, Dordrecht: 37–57.

    Google Scholar 

  • Fu, Y.-X. & W.-H. Li, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.

  • Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaither, M. R., B. W. Bowen, T.-R. Bordenave, L. A. Rocha, S. J. Newman, J. A. Gomez, L. van Herwerden & M. T. Craig, 2011. Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle. BMC Evolutionary Biology 11: 189.

    PubMed  PubMed Central  Google Scholar 

  • Galindo, H. M., D. B. Olson & S. R. Palumbi, 2006. Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology 16: 1622–1626.

    CAS  PubMed  Google Scholar 

  • Gallaher, T., M. W. Callmander, S. Buerki, S. Setsuko & S. C. Keeley, 2017. Navigating the ‘broad freeway’: ocean currents and inland isolation drive diversification in the Pandanus tectorius complex (Pandanaceae). Journal of Biogeography 44: 1598–1611.

    Google Scholar 

  • Gómez, A. & D. H. Lunt, 2007. Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In Weiss, S. & N. Ferrand (eds), Phylogeography of Southern European Refugia. Springer, Dordrecht: 155–188.

    Google Scholar 

  • Guo, Z., Y. Huang, Y. Chen, N. C. Duke, C. Zhong & S. Shi, 2016. Genetic discontinuities in a dominant mangrove Rhizophora apiculata (Rhizophoraceae) in the Indo-Malesian region. Journal of Biogeography 43: 1856–1868.

    Google Scholar 

  • Guo, W., W. L. Ng, H. Wu, W. Li, L. Zhang, S. Qiao, X. Yang, X. Shi & Y. Huang, 2018a. Chloroplast phylogeography of a widely distributed mangrove species, Excoecaria agallocha, in the Indo-West Pacific region. Hydrobiologia 807: 333–347.

    CAS  Google Scholar 

  • Guo, Z., W. Guo, H. Wu, X. Fang, W. L. Ng, X. Shi, Y. Liu, Z. Huang, W. Li & L. Gan, 2018b. Differing phylogeographic patterns within the Indo-West Pacific mangrove genus Xylocarpus (Meliaceae). Journal of Biogeography 45: 676–689.

    Google Scholar 

  • Hamilton, M. B., 1999. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology 8: 521–523.

    CAS  PubMed  Google Scholar 

  • Harpending, H. C., 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66: 591–600.

    CAS  PubMed  Google Scholar 

  • Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.

    CAS  PubMed  Google Scholar 

  • Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones & A. Jarvis, 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology: A Journal of the Royal Meteorological Society 25: 1965–1978.

    Google Scholar 

  • Huang, Y., F. Tan, G. Su, S. Deng, H. He & S. Shi, 2008. Population genetic structure of three tree species in the mangrove genus Ceriops (Rhizophoraceae) from the Indo West Pacific. Genetica 133: 47–56.

    PubMed  Google Scholar 

  • Hudson, R. R., 1990. Gene genealogies and the coalescent process. Oxford surveys in evolutionary biology 7: 44.

    Google Scholar 

  • Inomata, N., X.-R. Wang, S. Changtragoon & A. E. Szmidt, 2009. Levels and patterns of DNA variation in two sympatric mangrove species, Rhizophora apiculata and R. mucronata from Thailand. Genes & Genetic Systems 84: 277–286.

    CAS  Google Scholar 

  • Kennedy, J. P., M. W. Pil, C. E. Proffitt, W. A. Boeger, A. M. Stanford & D. J. Devlin, 2016. Postglacial expansion pathways of red mangrove, Rhizophora mangle, in the Caribbean Basin and Florida. American Journal of Botany 103: 260–726.

    PubMed  Google Scholar 

  • Lakshmi, M., S. Rajalakshmi, M. Parani, C. S. Anuratha & A. Parida, 1997. Molecular phylogeny of mangroves I. Use of molecular markers in assessing the intraspecific genetic variability in the mangrove species Acanthus ilicifolius Linn. (Acanthaceae). Theoretical and Applied Genetics 94: 1121–1127.

    CAS  Google Scholar 

  • Lee, T.-Y. & L. A. Lawver, 1995. Cenozoic plate reconstruction of Southeast Asia. Tectonophysics 251: 85–138.

    Google Scholar 

  • Lessios, H. A., 2008. The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology, Evolution, Systematics 39: 63–91.

    Google Scholar 

  • Li, J., Y. Yang, Q. Chen, L. Fang, Z. He, W. Guo, S. Qiao, Z. Wang, M. Guo, C. Zhong, R. Zhou & S. Shi, 2016. Pronounced genetic differentiation and recent secondary contact in the mangrove tree Lumnitzera racemosa revealed by population genomic analyses. Scientific Reports 6: 29486.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liao, B. W., 2009. Studies on Dongzhai harbor mangrove wetland ecosystem on Hainan island in China. China Ocean University Press, Qingdao.

    Google Scholar 

  • Liao, P.-C., S. Havanond & S. Huang, 2007. Phylogeography of Ceriops tagal (Rhizophoraceae) in Southeast Asia: the land barrier of the Malay Peninsula has caused population differentiation between the Indian Ocean and South China Sea. Conservation Genetics 8: 89–98.

    CAS  Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    CAS  PubMed  Google Scholar 

  • Maguire, T. L., P. Saenger, P. Baverstock & R. Henry, 2000. Microsatellite analysis of genetic structure in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Molecular Ecology 9: 1853–1862.

    CAS  PubMed  Google Scholar 

  • Manni, F., E. Guerard & E. Heyer, 2004. Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Human Biology 76: 173–190.

    PubMed  Google Scholar 

  • McDade, L. A., T. F. Daniel, C. A. Kiel & K. Vollesen, 2005. Phylogenetic relationships among Acantheae (Acanthaceae): major lineages present contrasting patterns of molecular evolution and morphological differentiation. Systematic Botany 30: 834–862.

    Google Scholar 

  • Meirmans, P. G., 2012. The trouble with isolation by distance. Molecular Ecology 21: 2839–2846.

    PubMed  Google Scholar 

  • Minobe, S., S. Fukui, R. Saiki, T. Kajita, S. Changtragoon, N.A. Ab Shukor, A. Latiff, B. R. Ramesh, O. Koizumi & T. Yamazaki, 2010. Highly differentiated population structure of a Mangrove species, Bruguiera gymnorhiza (Rhizophoraceae) revealed by one nuclear GapCp and one chloroplast intergenic spacer trnF-trnL. Conservation Genetics 11: 301–310.

  • Mori, G. M., M. I. Zucchi & A. P. Souza, 2015. Multiple-geographic-scale genetic structure of two mangrove tree species: the roles of mating system, hybridization, limited dispersal and extrinsic factors. PLoS One 10: e0118710.

    PubMed  PubMed Central  Google Scholar 

  • Moritz, C., 1994. Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution 9: 373–375.

    CAS  Google Scholar 

  • Nettel, A. & R. S. Dodd, 2007. Drifting propagules and receding swamps: genetic footprints of mangrove recolonization and dispersal along tropical coasts. Evolution 61: 958–971.

    CAS  PubMed  Google Scholar 

  • Ngeve, M. N., T. Van der Stocken, D. Menemenlis, N. Koedam & L. Triest, 2016. Contrasting effects of historical sea level rise and contemporary ocean currents on regional gene flow of Rhizophora racemosa in eastern Atlantic mangroves. PLoS One 11: e0150950.

    PubMed  PubMed Central  Google Scholar 

  • Otto-Bliesner, B. L., S. J. Marsha, J. T. Overpeck, G. H. Miller, A. X. Hu & C. L. I. P. Mem, 2006. Simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science 311: 1751–1753.

    CAS  PubMed  Google Scholar 

  • Parks, D. H., M. Porter, S. Churcher, S. Wang, C. Blouin, J. Whalley, S. Brooks & R. G. Beiko, 2009. GenGIS: a geospatial information system for genomic data. Genome Research 19: 1896–1904.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peakall, R. & P. E. Smouse, 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28: 2537–2539.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips, S. J. & M. Dudík, 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31: 161–175.

    Google Scholar 

  • Phillips, S. J., R. P. Anderson & R. E. Schapire, 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231–259.

    Google Scholar 

  • Pil, M. W., M. R. Boeger, V. C. Muschner, M. R. Pie, A. Ostrensky & W. A. Boeger, 2011. Postglacial north-south expansion of populations of Rhizophora mangle (Rhizophoraceae) along the Brazilian coast revealed by microsatellite analysis. American Journal of Botany 98: 1031–1039.

    PubMed  Google Scholar 

  • Pons, O. & R. J. Petit, 1996. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144: 1237–1245.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qu, T., Y. T. Song & T. Yamagata, 2009. An introduction to the South China Sea throughflow: its dynamics, variability, and application for climate. Dynamics of Atmospheres and Oceans 47: 3–14.

    Google Scholar 

  • Ragavan, P., A. Saxena, P. M. Mohan, R. S. Jayaraj & K. Ravichandran, 2015. Taxonomy and distribution of species of the genus Acanthus (Acanthaceae) in mangroves of the Andaman and Nicobar Islands, India. Biodiversitas 16: 225–237.

    Google Scholar 

  • Richardson, J. E., R. T. Pennington, T. D. Pennington & P. M. Hollingsworth, 2001. Rapid diversification of a species-rich genus of Neotropical rain forest trees. Science 293: 2242–2245.

    CAS  PubMed  Google Scholar 

  • Rogers, A. R. & H. Harpending, 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552–569.

    CAS  PubMed  Google Scholar 

  • Saenger, P. & M. F. Bellan, 1995. The mangrove vegetation of the Atlantic coast of Africa: a review. Université de Toulouse, Toulouse.

    Google Scholar 

  • Scotese, C. R., 2003. Paleogeographic maps, PALEOMAP project: www.scotese.com.

  • Su, G., Y. Huang, F. Tan, X. Ni, T. Tang & S. Shi, 2007. Conservation genetics of Lumnitzera littorea (Combretaceae), an endangered mangrove, from the Indo-West Pacific. Marine Biology 150: 321–328.

    Google Scholar 

  • Taberlet, P., L. Gielly, G. Pautou & J. Bouvet, 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105–1109.

    CAS  PubMed  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thiel, M. & L. Gutow, 2005. The ecology of rafting in the marine environment. II. The rafting organisms and community Oceanography and Marine Biology. CRC Press, 289-428.

  • Tomlinson, P. B., 2016. The botany of mangroves. Cambridge University Press, Cambridge.

    Google Scholar 

  • Triest, L., 2008. Molecular ecology and biogeography of mangrove trees towards conceptual insights on gene flow and barriers: a review. Aquatic Botany 89: 138–154.

    CAS  Google Scholar 

  • Umali, R., P. Zamora, R. Gatera, R. Jara, A. CAMA-CHO & M. Vannucci, 1987. Mangroves of Asia and the Pacific: Status and management. Technical Report of the UNDP/UNESCO Research and Training Pilot Programme on mangrove ecosystems in Asia and the Pacific.

  • Urashi, C., K. M. Teshima, S. Minobe, O. Koizumi & N. Inomata, 2013. Inferences of evolutionary history of a widely distributed mangrove species, Bruguiera gymnorrhiza, in the Indo-West Pacific region. Ecology and Evolution 3: 2251–2261.

    PubMed  PubMed Central  Google Scholar 

  • Warren, D. L., R. E. Glor & M. Turelli, 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33: 607–611.

    Google Scholar 

  • Waters, J. M., 2008. Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Diversity and Distributions 14: 692–700.

    Google Scholar 

  • Wee, A. K., K. Takayama, T. Asakawa, B. Thompson, S. Sungkaew, N. X. Tung, M. Nazre, K. K. Soe, H. T. Tan & Y. Watano, 2014. Oceanic currents, not land masses, maintain the genetic structure of the mangrove Rhizophora mucronata Lam. (Rhizophoraceae) in Southeast Asia. Journal of biogeography 41: 954–964.

    Google Scholar 

  • Wee, A. K., K. Takayama, J. L. Chua, T. Asakawa, S. H. Meenakshisundaram, Onrizal, B. Adjie, E. R. Ardli, S. Sungkaew, N. B. Malekal, N. X. Tung, S. G. Salmo, 3rd, O. B. Yllano, M. N. Saleh, K. K. Soe, Y. Tateishi, Y. Watano, S. Baba, E. L. Webb & T. Kajita, 2015. Genetic differentiation and phylogeography of partially sympatric species complex Rhizophora mucronata Lam. and R. stylosa Griff. using SSR markers. BMC Evolutionary Biology 15:57

  • Wolfe, K. H., W. H. Li & P. M. Sharp, 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences, USA 84: 9054–9058

  • Wolfe, K. H., W. H. Li & P. M. Sharp, 2003. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences, USA 84: 9054–9058.

    Google Scholar 

  • Wu, J., S. Zhang, Q. Xiao, Q. Li, J. Huang, L. Long & L. Huang, 2003. Phenylethanoid and aliphatic alcohol glycosides from Acanthus ilicifolius. Phytochemistry 63: 491–495.

    CAS  PubMed  Google Scholar 

  • Yang, Y., N. C. Duke, F. Peng, J. Li, S. Yang, C. Zhong, R. Zhou & S. Shi, 2016. Ancient geographical barriers drive differentiation among Sonneratia caseolaris populations and recent divergence from S. lanceolata. Frontiers in Plant Science 7:1618.

  • Zhou, W., Y. Wen, J. Fu, Y. Xu, J. Jin, L. Ding, M. Min, J. Che & Y. Zhang, 2012. Speciation in the Rana chensinensis species complex and its relationship to the uplift of the Qinghai-Tibetan Plateau. Molecular Ecology 21: 960–973.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study is supported by grants from the National Natural Science Foundation of China (Grant No. 31700178 and 41776166), the Natural Science Foundation of Guangdong Province (Grant No. 2017A030313159), Guangdong Basic and Applied Basic Research Foundation (Grant No. 2019A15150122211), and Chang Hungta Science Foundation of Sun Yat-sen University. The authors wish to thank Drs. Suhua Shi, Ying Liu, Renchao Zhou, and Tian Tang (Sun Yat-sen University, China), Dr. Sonjai Havanond (Department of National Parks, Wildlife and Plant Conservation, Thailand), Mr. Chanop Jaengjai (Department of Marine and Coastal Resources, Thailand), and Dr. Albert Williams (Department of Environmental Protection and Conservation, Vanuatu) for assistance in collecting and providing plant material. We would especially like to thank the Associate Editor and the reviewer for their thoughtful and constructive comments towards improving the quality of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yelin Huang.

Additional information

Handling editor: Emily M. Dangremond

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, W., Banerjee, A.K., Ng, W.L. et al. Chloroplast DNA phylogeography of the Holly mangrove Acanthus ilicifolius in the Indo-West Pacific. Hydrobiologia 847, 3591–3608 (2020). https://doi.org/10.1007/s10750-020-04372-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04372-1

Keywords

Navigation