Contrasting demographic patterns of Ceriops tagal (Rhizophoraceae) populations in the South China Sea
Pei-Chun Liao A , Shih-Ying Hwang B , Shong Huang B , Yu-Chung Chiang C D and Jenn-Che Wang B DA Department of Biological Science and Technology, National Pingtung University of Science and Technology, 1 Shuehfu Road, Neipu, Pingtung 91201, Taiwan.
B Department of Life Science, National Taiwan Normal University, 88 Ting-Chow Road, Sect. 4, Taipei 11676, Taiwan.
C Department of Biological Sciences, National Sun Yat-sen University, 70 Lien-Hai Road, Kaohsiung 80424, Taiwan.
D Corresponding authors. Email: yuchung@mail.nsysu.edu.tw; biofv017@ntnu.edu.tw
Australian Journal of Botany 59(6) 523-532 https://doi.org/10.1071/BT10290
Submitted: 26 October 2010 Accepted: 27 July 2011 Published: 5 October 2011
Abstract
Demographic history and dispersal ability are significant factors in determining the genetic composition of a population. In this study, we examined the phylogeographic patterns of Ceriops tagal from the Hainan Island and the Gulf of Thailand in the South China Sea, where there are abundant mangrove species. Nucleotide variations in two chloroplast DNA spacers were compared with trace Ceriops propagule dispersal routes and demographic history. An analysis of Templeton, Crandall and Sing’s (TCS) parsimonious networks and population demographics suggests that the Ceriops population gradually expanded from the northern parts of the South China Sea to the south-western populations in the Gulf of Thailand. Such phylogeographic inferences reflect a postglacial southward shift in the mangrove genetic diversity centre and a connection between the demographic dynamics and the coastal range expansion caused by the sea-level rise in the Pleistocene. Therefore, the phylogeographic pattern and historical demography of mangrove species were affected by glaciations during the Pleistocene such as temperate biota.
References
Allen JA, Krauss KW (2006) Influence of propagule flotation longevity and light availability on establishment of introduced mangrove species in Hawai’i. Pacific Science 60, 367–376.| Influence of propagule flotation longevity and light availability on establishment of introduced mangrove species in Hawai’i.Crossref | GoogleScholarGoogle Scholar |
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=114470b3f5ef46c4c6e633d3ff4b7ae7CAS |
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311, 522–527.
| Scaling of connectivity in marine populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVymtg%3D%3D&md5=0d533f2c7caf9de2f8e0c32d3dc7701dCAS |
Dodd RS, Afzal-Rafii Z (2002) Evolutionary genetics of mangroves: continental drift to recent climate change. Trees-Structure and Function 16, 80–86.
Duke NC, Lo EYY, Sun M (2002) Global distribution and genetic discontinuities of mangroves – emerging patterns in the evolution of Rhizophora. Trees-Structure and Function 16, 65–79.
Ellison AM, Farnsworth EJ, Merkt RE (1999) Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global Ecology and Biogeography 8, 95–115.
Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10, 315–319.
| Testing significance of incongruence.Crossref | GoogleScholarGoogle Scholar |
Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5, 164–166.
Fulford GR, Roberts MG, Heesterbeek JA (2002) The metapopulation dynamics of an infectious disease: tuberculosis in possums. Theoretical Population Biology 61, 15–29.
| The metapopulation dynamics of an infectious disease: tuberculosis in possums.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387msVGktg%3D%3D&md5=5fac8a54e521dcbe3f4be3fa903d76a2CAS |
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the Sunda Shelf: a late-glacial sea-level record. Science 288, 1033–1035.
| Rapid flooding of the Sunda Shelf: a late-glacial sea-level record.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsVShsbc%3D&md5=1e03c51638ae9ec1c092dd848bb5d0ccCAS |
Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST (1998) Genetic traces of ancient demography. Proceedings of the National Academy of Sciences of the United States of America 95, 1961–1967.
| Genetic traces of ancient demography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1ajsLk%3D&md5=4c39450e366e0eedd2384e3fff850516CAS |
Heatwole H, Busack S, Cogger H (2005) Geographic variation in sea kraits of the Laticauda colubrina complex (Serpentes: Elapidae: Hydrophiinae: Laticaudini). Herpetological Monograph 19, 1–136.
| Geographic variation in sea kraits of the Laticauda colubrina complex (Serpentes: Elapidae: Hydrophiinae: Laticaudini).Crossref | GoogleScholarGoogle Scholar |
Horton BP, Gibbard PL, Milne GM, Morley RJ, Purintavaragul C, Stargardt JM (2005) Holocene sea levels and palaeoenvironments, Malay-Thai Peninsula, southeast Asia. The Holocene 15, 1199–1213.
| Holocene sea levels and palaeoenvironments, Malay-Thai Peninsula, southeast Asia.Crossref | GoogleScholarGoogle Scholar |
Huang YL, Tan FX, Su GH, Deng SL, He HH, Shi SH (2008) Population genetic structure of three tree species in the mangrove genus Ceriops (Rhizophoraceae) from the Indo West Pacific. Genetica 133, 47–56.
| Population genetic structure of three tree species in the mangrove genus Ceriops (Rhizophoraceae) from the Indo West Pacific.Crossref | GoogleScholarGoogle Scholar |
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53, 1898–1914.
| Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability.Crossref | GoogleScholarGoogle Scholar |
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6, 13
| Isolation by distance, web service.Crossref | GoogleScholarGoogle Scholar |
Jian SG, Tang T, Zhong Y, Shi SB (2004) Variation in inter-simple sequence repeat (ISSR) in mangrove and non-mangrove populations of Heritiera littoralis (Sterculiaceae) from China and Australia. Aquatic Botany 79, 75–86.
| Variation in inter-simple sequence repeat (ISSR) in mangrove and non-mangrove populations of Heritiera littoralis (Sterculiaceae) from China and Australia.Crossref | GoogleScholarGoogle Scholar |
Karns DR, O’Bannon A, Voris HK, Weigt LA (2000) Biogeographical implications of mitochondrial DNA variation in the bockadam snake (Cerberus rynchops, Serpentes: Homalopsinae) in Southeast Asia. Journal of Biogeography 27, 391–402.
| Biogeographical implications of mitochondrial DNA variation in the bockadam snake (Cerberus rynchops, Serpentes: Homalopsinae) in Southeast Asia.Crossref | GoogleScholarGoogle Scholar |
Kim JH, Dupont L, Behling H, Versteegh GJM (2005) Impacts of rapid sea-level rise on mangrove deposit erosion: application of taraxerol and Rhizophora records. Journal of Quaternary Science 20, 221–225.
| Impacts of rapid sea-level rise on mangrove deposit erosion: application of taraxerol and Rhizophora records.Crossref | GoogleScholarGoogle Scholar |
Kittlein MJ, Gaggiotti OE (2008) Interactions between environmental factors can hide isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay. Proceedings. Biological Sciences 275, 2633–2638.
| Interactions between environmental factors can hide isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay.Crossref | GoogleScholarGoogle Scholar |
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=1896007d0c49398fc5b629f745276fcaCAS |
Kumaran KPN, Shindikar M, Limaye RB (2004) Mangrove associated lignite beds of Malvan, Konkan: evidence for higher sea-level during the Late Tertiary (Neogene) along the west coast of India. Current Science 86, 335–340.
Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55, 955–975.
| Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltFelu7c%3D&md5=d74062322a6dc29956e7cd4a65cf3512CAS |
Liao PC, Havanond S, Huang S (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.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1aq&md5=593b9a774a44ac29968ff91a4e50b8d9CAS |
Liao PC, Chiang YC, Huang S, Wang JC (2009) Gene flow of Ceriops tagal (Rhizophoraceae) across the Kra Isthmus in the Thai Malay Peninsula. Botanical Studies (Taipei, Taiwan) 50, 193–204.
Manni F, Guerard E, Herey E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Human Biology 76, 173–190.
| Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm.Crossref | GoogleScholarGoogle Scholar |
McCoy ED, Heck KL (1976) Biogeography of corals, seagrasses, and mangroves: an alternative to the center of origin concept. Systematic Zoology 25, 201–210.
| Biogeography of corals, seagrasses, and mangroves: an alternative to the center of origin concept.Crossref | GoogleScholarGoogle Scholar |
Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geographical Analysis 5, 245–261.
| Maximum-difference barriers: an alternative numerical regionalization method.Crossref | GoogleScholarGoogle Scholar |
Nei M (1987) ‘Molecular evolutionary genetics.’ (Columbia University Press: New York)
Plaziat JC, Cavagnetto C, Koeniguer JC, Baltzer F (2001) History and biogeography of the mangrove ecosystem, based on a critical reassessment of the paleontological record. Wetlands Ecology and Management 9, 161–180.
| History and biogeography of the mangrove ecosystem, based on a critical reassessment of the paleontological record.Crossref | GoogleScholarGoogle Scholar |
Ricklefs RE, Latham RE (1993) Global patterns of diversity in mangrove floras. In ‘Species diversity in ecological communities’. (Eds RE Ricklefs, D Schluter) pp. 215–229. (University of Chicago Press: Chicago)
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics (Oxford, England) 19, 2496–2497.
| DnaSP, DNA polymorphism analyses by the coalescent and other methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSisLo%3D&md5=fd62df257f3219b452ae38109852704bCAS |
Sathiamurthy E, Voris HK (2006) Maps of Holocene sea level transgression and submerged lakes on the Sunda Shelf. Natural History Journal of Chulalongkorn University 2, 1–43.
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152, 1079–1089.
Shi SH, Zhong Y, Huang YL, Du YQ, Qiu XZ, Chang HT (2002) Phylogenetic relationships of the Rhizophoraceae in China based on sequences of the chloroplast gene matK and the internal transcribed spacer regions of nuclear ribosomal DNA and combined data set. Biochemical Systematics and Ecology 30, 309–319.
| Phylogenetic relationships of the Rhizophoraceae in China based on sequences of the chloroplast gene matK and the internal transcribed spacer regions of nuclear ribosomal DNA and combined data set.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFWitro%3D&md5=558786d83bff7b7be6e9f19bcd2adafeCAS |
Slatkin M, Wade MJ (1978) Group selection on a quantitative character. Proceedings of the National Academy of Sciences of the United States of America 75, 3531–3534.
| Group selection on a quantitative character.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cngslOksg%3D%3D&md5=3c5ac49bb7915cb6f72050c515a82e3fCAS |
Solomon Raju AJ, Karyamsetty HJ (2008) Reproductive ecology of mangrove trees Ceriops decandra (Griff.) Ding Hou and Ceriops tagal (Perr.) C.B. Robinson (Rhizophoraceae). Acta Botanica Croatica 67, 201–208.
Steinke TD, Ward CJ (2003) Use of plastic drift cards as indicators of possible dispersal of propagules of the mangrove Avicennia marina by ocean currents. African Journal of Marine Science 25, 169–176.
| Use of plastic drift cards as indicators of possible dispersal of propagules of the mangrove Avicennia marina by ocean currents.Crossref | GoogleScholarGoogle Scholar |
Su GH, Huang YL, Tan FX, Ni XW, Tang T, Shi SH (2006) Genetic variation in Lumnitzera racemosa, a mangrove species from the Indo-West Pacific. Aquatic Botany 84, 341–346.
| Genetic variation in Lumnitzera racemosa, a mangrove species from the Indo-West Pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVGkurs%3D&md5=4ea4d05644344c1609c7a4d664c892d6CAS |
Swofford DL (2002) ‘PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0b8.’ (Sinauer Associates: Sunderland, MA)
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of 3 noncoding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhslel&md5=881be45efb56742ff78711a8a4bdb4cfCAS |
Tan FX, Huang YL, Ge XJ, Su GH, Ni XW, Shi SH (2005) Population genetic structure and conservation implications of Ceriops decandra in Malay Peninsula and North Australia. Aquatic Botany 81, 175–188.
| Population genetic structure and conservation implications of Ceriops decandra in Malay Peninsula and North Australia.Crossref | GoogleScholarGoogle Scholar |
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=3509e71f7587a578b592f0b15ffdfe10CAS |
Tomlinson PB (1986) ‘The botany of mangroves.’ (Cambridge of University Press: Cambridge)
Torrescano N, Islebe GA (2006) Tropical forest and mangrove history from southeastern Mexico: a 5000 year pollen record and implications for sea level rise. Vegetation History and Archaeobotany 15, 191–195.
| Tropical forest and mangrove history from southeastern Mexico: a 5000 year pollen record and implications for sea level rise.Crossref | GoogleScholarGoogle 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.
| Molecular ecology and biogeography of mangrove trees towards conceptual insights on gene flow and barriers: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1Siu7w%3D&md5=c49eb3a10aad46b6672f2a113138c135CAS |
Vedel V, Behling H, Cohen M, Lara R (2006) Holocene mangrove dynamics and sea-level changes in northern Brazil, inferences from the Taperebal core in northeastern Para State. Vegetation History and Archaeobotany 15, 115–123.
| Holocene mangrove dynamics and sea-level changes in northern Brazil, inferences from the Taperebal core in northeastern Para State.Crossref | GoogleScholarGoogle Scholar |
Wade MJ, McCauley DE (1988) Extinction and recolonization – their effects on the genetic differentiation of local populations. Evolution 42, 995–1005.
| Extinction and recolonization – their effects on the genetic differentiation of local populations.Crossref | GoogleScholarGoogle Scholar |
Wang PX (1999) Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology 156, 5–39.
| Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features.Crossref | GoogleScholarGoogle Scholar |
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7, 256–276.
| On the number of segregating sites in genetical models without recombination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7pvFSquw%3D%3D&md5=82b2b150b1584e94d277cb34f6e5371eCAS |
Wright S (1949) The genetical structure of populations. Annals of Eugenics 15, 323–354.
| The genetical structure of populations.Crossref | GoogleScholarGoogle Scholar |
Xu JW, Chan TY, Tsang LM, Chu KH (2009) Phylogeography of the mitten crab Eriocheir sensu stricto in East Asia: Pleistocene isolation, population expansion and secondary contact. Molecular Phylogenetics and Evolution 52, 45–56.
| Phylogeography of the mitten crab Eriocheir sensu stricto in East Asia: Pleistocene isolation, population expansion and secondary contact.Crossref | GoogleScholarGoogle Scholar |
Yulianto E, Sukapti WS, Rahardjo A, Noeradi D, Siregar DA, Suparan P, Hirakawa K (2004) Mangrove shoreline responses to holocene environmental change, Makassar strait, Indonesia. Review of Palaeobotany and Palynology 131, 251–268.
| Mangrove shoreline responses to holocene environmental change, Makassar strait, Indonesia.Crossref | GoogleScholarGoogle Scholar |
Yulianto E, Rahardjo AT, Noeradi D, Siregar DA, Hirakawa K (2005) A Holocene pollen record of vegetation and coastal environmental changes in the coastal swamp forest at Batulicin, South Kalimantan, Indonesia. Journal of Asian Earth Sciences 25, 1–8.
| A Holocene pollen record of vegetation and coastal environmental changes in the coastal swamp forest at Batulicin, South Kalimantan, Indonesia.Crossref | GoogleScholarGoogle Scholar |
Zhong Y, Shi SH, Tang XH, Huang YL, Tan FX, Zhang XY (2000) Testing relative evolutionary rates and estimating divergence times among six genera of Rhizophoraceae using cpDNA and nrDNA sequences. Chinese Science Bulletin 45, 1011–1015.
| Testing relative evolutionary rates and estimating divergence times among six genera of Rhizophoraceae using cpDNA and nrDNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFCnsbc%3D&md5=c98625c10235ecf3e6c99035e22993ccCAS |