Bruguiera hainesii, a critically endangered mangrove species, is a hybrid between B. cylindrica and B. gymnorhiza (Rhizophoraceae)
Abstract
Bruguiera hainesii (Rhizophoraceae) is one of the two Critically Endangered mangrove species listed in the IUCN Red List of Threatened Species. Although the species is vulnerable to extinction, its genetic diversity and the evolutionary relationships with other Bruguiera species are not well understood. Also, intermediate morphological characters imply that the species might be of hybrid origin. To clarify the genetic relationship between B. hainesii and other Bruguiera species, we conducted molecular analyses including all six Bruguiera species using DNA sequences of two nuclear genes (CesA and UNK) and three chloroplast regions (intergenic spacer regions of trnL-trnF, trnS-trnG and atpB-rbcL). For nuclear DNA markers, all nine B. hainesii samples from five populations were heterozygous at both loci, with one allele was shared with B. cylindrica, and the other with B. gymnorhiza. For chloroplast DNA markers, the two haplotypes found in B. hainesii were shared only by B. cylindrica. These results suggested that B. hainesii is a hybrid between B. cylindrica as the maternal parent and B. gymnorhiza as the paternal one. Furthermore, chloroplast DNA haplotypes found in B. hainesii suggest that hybridization has occurred independently in regions where the distribution ranges of the parental species meet. As the IUCN Red List of Threatened Species currently excludes hybrids (except for apomictic plant hybrids), the conservation status of B. hainesii should be reconsidered.
Keywords
Mangrove Hybridization Endangered species GeneticsNotes
Acknowledgments
The authors thank Drs. Myint Aung, Ian Cowie, Sanjay Deshmukh, Norman Duke, Kyaw Kyaw Khaung, Jurgenne Primavera, Ms. Latifah Zainal Abidin, Mr. Vando Márcio da Silva, Ms. Norhaslinda Malekal, Ms. Hoho Takayama, Mr. Masaru Bamba, Sabah Forestry Department (SFD), and Department of Environment and Natural Resources, Region VI for field work to collect materials. This work was supported by JSPS KAKENHI 22405005 and 25290080 to TK, JSPS JENESYS Programme 2009 and 2011 to the Graduate School of Science of Chiba University (coordinated by TK), Singapore Ministry of Education (Grant Number R154-000-440-112) to EW, Fujiwara Natural History Foundation to KT and the Research Assistant Program 2013 of Chiba University to JO. This study is a part of PhD study of JO.
Supplementary material
References
- Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349CrossRefGoogle Scholar
- Birky CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. PNAS 92:11331–11338CrossRefPubMedPubMedCentralGoogle Scholar
- Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:167–1660CrossRefGoogle Scholar
- Cronn RC, Small RL, Wendel JF (1999) Duplicated genes evolve independently after polyploid formation in cotton. PNAS 96:14406–14411CrossRefPubMedPubMedCentralGoogle Scholar
- Dahdouh-Guebas F, Jayatissa LP, Di Nitto D, Bosire JO, Lo Seen D, Koedam N (2005) How effective were mangroves as a defence against the recent tsunami? Curr Biol 15:443–447CrossRefGoogle Scholar
- Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
- Duke NC (1984) A mangrove hybrid, Sonneratia × gulngai (Sonneratiaceae) from north-eastern Australia. Austrobaileya 2:103–105Google Scholar
- Duke NC (2010) Overlap of eastern and western mangrove in the south-western Pacific: hybridization of all three Rhizophora (Rhizophoraceae) combinations in New Caledonia. Blumea 55:171–188CrossRefGoogle Scholar
- Duke NC, Ge XJ (2011) Bruguiera (Rhizophoraceae) in the Indo-West Pacific: a morphometric assessment of hybridization within single-flowered taxa. Blumea 56:36–48CrossRefGoogle Scholar
- Duke N, Kathiresan K, Salmo III SG, Fernando ES, Peras JR, Sukardjo S, Miyagi T, Ellison J, Koedam NE, Wang Y, Primavera J, Jin Eong O, Wan-Hong Yong J, Ngoc Nam V (2010) Bruguiera hainesii. The IUCN Red List of Threatened SpeciesGoogle Scholar
- FAO (Food and Agriculture Organization) (2007) The world’s mangroves 1980–2005, FAO Forestry Paper 153. FAO, RomeGoogle Scholar
- Field CD (1998) Rehabilitation of mangrove ecosystems: an overview. Mar Pollut Bull 37:383–392CrossRefGoogle Scholar
- Fosberg FR (1971) Mangroves versus tidal waves. Biol Conserv 4:38–39CrossRefGoogle Scholar
- Ge XJ (2001) Reproductive biology and conservation genetics of mangroves in South China and Hong Kong. Ph. D. thesis, the University of Hong KongGoogle Scholar
- Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:513–525CrossRefGoogle Scholar
- Hou D (1957) A conspectus of the genus Bruguiera (Rhizophoraceae). Nova Guinea (ns) 8:163–171Google Scholar
- Hou D (1958) Rhizophoraceae. In: van Steenis CGGJ (ed) Flora malesiana, vol 1. Noordhoff- Kolff, Djakarta, pp 429–493Google Scholar
- Imai N, Takyu M, Nakamura Y, Nakamura T (2006) Gap formation and regeneration of tropical mangrove forests in Ranong, Thailand. Plant Ecol 186:37–46CrossRefGoogle Scholar
- IUCN (2015) The IUCN Red List of Threatened Species. Version 2. www.iucnredlist.org
- Jaruwattanaphan T, Matsumoto S, Watano Y (2013) Reconstructing hybrid speciation events in the Pteris cretica group (Pteridaceae) in Japan and adjacent regions. Syst Bot 38:15–27CrossRefGoogle Scholar
- Kathiresan K (1995) Rhizophora × annamalayana: a new species of mangroves. Environ Ecol 13:240–241Google Scholar
- Kathiresan K (1999) Rhizophora × annamalayana Kathir (Rhizophoraceae), a new nothospecies from Pichavaram mangrove forest in southeastern peninsular India. Environ Ecol 17:500–501Google Scholar
- Kochummen KM (1989) Rhizophoraceae. In: Ng FSP (ed) Tree flora of Malaya. A manual for foresters. Longman, Malaysia, pp 302–323Google Scholar
- Kondo K, Tsuruda T, Saito K, Yaguchi Y (1987) Pollination in Bruguiera gymnorrhiza and Rhizophora mucronata (Rhizophoraceae) in Ishigaki island, the Ryukyu islands, Japan. Biotropica 19:377–380CrossRefGoogle Scholar
- Kondo K, Nakamura T, Piyakarnchana T, Mechvichai W (1991) Pollination in Bruguiera gymnorrhiza (Rhizophoraceae) in Miyara River, Ishigaki Island, Japan, and Phangnga, Thailand. Plant Species Biol 6:105–109CrossRefGoogle Scholar
- Miryeganeh M, Takayama K, Tateishi Y, Kajita T (2014) Long-distance dispersal by sea-drifted seeds has maintained the global distribution of Ipomoea pes-caprae subsp. brasiliensis (Convolvulaceae). PLoS One 9(4):e91836. doi: 10.1371/journal.pone.0091836 CrossRefPubMedPubMedCentralGoogle Scholar
- Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404CrossRefGoogle Scholar
- Noske RA (1993) Bruguiera hainesii: another bird-pollinated mangrove? Biotropica 25:481–483CrossRefGoogle Scholar
- Ong JE (1993) Mangroves—a carbon source and sink. Chemosphere 27:1097–1107CrossRefGoogle Scholar
- Polidoro BA, Carpenter KE, Collins L, Duke NC, Ellison AM, Ellison JC, Farnsworth EJ, Fernando ES, Kathiresan K, Koedam NE, Livingstone SR, Miyagi T, Moore GE, Nam VN, Ong JE, Primavera JH, Salmo SG III, Sanciangco JC, Sukardjo S, Wang Y, Yong JWH (2010) The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS One 5:e10095CrossRefPubMedPubMedCentralGoogle Scholar
- Primavera JH (1998) Mangroves as nurseries: shrimp populations in mangrove and non-mangrove habitats. Estuar Coast Shelf S 46:457–464CrossRefGoogle Scholar
- Putz FE, Chan HT (1986) Tree growth, dynamics, and productivity in a mature mangrove forest in Malaysia. For Ecol Manag 17:211–230CrossRefGoogle Scholar
- Robertson AI, Duke NC (1987) Mangroves as nursery sites: comparisons of the abundance and species composition of fish and crustaceans in mangroves and other nearshore habitats in tropical Australia. Mar Biol 96:193–205CrossRefGoogle Scholar
- Savolainen V, Manen JF, Douzery E, Spichiger R (1994) Molecular phylogeny of families related to Celastrales based on rbcL 5′ flanking sequences. Mol Phylogenet Evol 3:27–37CrossRefPubMedGoogle Scholar
- Schwarzbach AE, Ricklefs RE (2000) Systematic affinities of Rhizophoraceae and Anisophylleaceae, and intergeneric relationships within Rhizophoraceae, based on chloroplast DNA, nuclear ribosomal DNA, and morphology. Am J Bot 87:547–564CrossRefPubMedGoogle Scholar
- Sheue CR, Yong JWH, Yang YP (2005) The Bruguiera (Rhizophoraceae) species in the mangroves of Singapore, especially on the new record and the rediscovery. Tawania 50:251–260Google Scholar
- Spalding MD, Kainuma M, Collins L (2010) World atlas of mangrove. Earthscan. Routledge, LondonGoogle Scholar
- Sun M, Lo EYY (2011) Genomic markers reveal introgressive hybridization in the Indo-West Pacific mangroves: a case study. PLoS One 6:e19671CrossRefPubMedPubMedCentralGoogle Scholar
- Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefPubMedGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analisis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
- Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
- Tomlinson PB (1978) Rhizophora in Australasia, some clarification of taxonomy and distribution. J Arnold Arbor 59:159–169Google Scholar
- Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, CambridgeGoogle Scholar
- Tomlinson PB, Womersley JS (1976) A species of Rhizophora new to New Guinea and Queensland, with notes relevant to the genus. Contr Herb Aust 19:1–10Google Scholar
- Urashi C, Teshima KM, Minobe S, Koizumi O, Inomata N (2013) Inference of evolutionary history of a widely distributed mangrove species, Bruguiera gymnorrhiza, in the Indo-West Pacific region. Ecol Evol 3:2251–2261CrossRefPubMedPubMedCentralGoogle Scholar
- Valiela I, Bowen JL, York JK (2001) Mangrove forests: one of the world’s threatened major tropical environments. BioScience 51:807–815CrossRefGoogle Scholar
- Wang R, Chen Z, Chen E, Zheng X (1999) Two hybrids of the genus Sonneratia (Sonneratiaceae) from China. Guihaia 19:199–204Google Scholar
- Wee AKS, Low SY, Webb EL (2014) Pollen limitation affects reproductive outcome in the bird-pollinated mangrove Bruguiera gymnorrhiza (Lam.) in a highly urbanized environment. Aquat Bot 120:240–243CrossRefGoogle Scholar
- Wee AKS, Takayama K, Chua JL, Asakawa T, Meenakshisundaram SH, Onrizal, Adjie B, Ardli ER, Sungkaew S, Malekal NB, Tung NX, Salmo SG, Yllano OB, Saleh MN, Soe KK, Tateishi Y, Watano Y, Baba S, Webb EL, Kajita T (2015) Genetic differentiation and phylogeography of partially sympatric species complex Rhizophora mucronata Lam. and R. stylosa Griff. using SSR markers. BMC Evol Biol 15:57CrossRefPubMedPubMedCentralGoogle Scholar
- White AT, Martosubroto P, Sadorra MSM (1989) The coastal environmental profile of Segara Anakan-Cilacap, South Java, Indonesia. International Center for Living Aquatic Resources Management on behalf of the Association of Southeast Asian Nations/United States Coastal Resources Management ProjectGoogle Scholar