Low genetic diversity indicating the threatened status of Rhizophora apiculata (Rhizophoraceae) in Malaysia: declined evolution meets habitat destruction

Gandhi, S. & Jones, T. G. Identifying mangrove deforestation hotspots in South Asia, Southeast Asia and Asia-Pacific. Remote Sens. 11, 728 (2019).

ADS  Article  Google Scholar 

Hamdan, O., Khali-Aziz, H., Shamsudin, I. & Raja-Barizan, R.S. Status of Mangroves in Peninsular Malaysia. 153 (Forest Research Institute Malaysia, 2012).

Taillardat, P., Friess, D. A. & Lupascu, M. Mangrove blue carbon strategies for climate change mitigation are most effective at the national scale. Biol. Lett. 14, 20180251 (2018).

Article  CAS  Google Scholar 

Richards, D. R. & Friess, D. A. Rates and drivers of mangrove deforestation in Southeast Asia, 2000–2012. Proc. Natl. Acad. Sci. USA 113, 344–349 (2016).

ADS  CAS  Article  Google Scholar 

Friess, D. A. et al. Mangroves give cause for conservation optimism, for now. Curr. Biol. 30, R153–R154 (2020).

CAS  Article  Google Scholar 

Polidoro, B. A. et al. The loss of species: mangrove extinction risk and geographic areas of global concern. PLoS ONE 5, e10095 (2010).

ADS  Article  CAS  Google Scholar 

Matesanz, S., Rubio-Teso, M. L., García-Fernández, A. & Escudero, A. Habitat fragmentation differentially affects genetic variation, phenotypic plasticity and survival in populations of a gypsum endemic. Front. Plant Sci. 8, 843 (2017).

Article  Google Scholar 

Furches, M. S., Small, R. L. & Furches, A. Genetic diversity in three endangered pitcher plant species (Sarracenia; Sarraceniaceae) is lower than widespread congeners. Am. J. Bot. 100, 2092–2101 (2013).

Article  Google Scholar 

Yan, Y. B., Duke, N. C. & Sun, M. Comparative analysis of the pattern of population genetic diversity in three Indo-West Pacific Rhizophora mangrove species. Front. Plant Sci. 7, 1434 (2016).

PubMed  Google Scholar 

Wan-Ismail, W. N., Wan-Ahmad, W. J., Salam, M. R. & Latiff, A. Structural and floristic pattern in a disturbed mangrove tropical swamp forest: a case study from the Langkawi UNESCO Global Geopark Forest, Peninsular Malaysia. Sains Malays. 47, 861–869 (2018).

Article  Google Scholar 

Setyawan, A.D., Ulumuddin, Y.I. & Ragavan, P. Mangrove hybrid of Rhizophora and its parentals species in Indo-Malayan region. Nusantara Biosci. 6 (2014).

Lahjie, A.M., Nouval, B., Lahjie, A.A., Ruslim, Y. & Kristiningrum, R. Economic valuation from direct use of mangrove forest restoration in Balikpapan Bay, East Kalimantan, Indonesia. F1000Res. 8 (2019).

Omar, H., Misman, M.A. & Musa, S. GIS and remote sensing for mangroves mapping and monitoring. Geographic Information Systems and Science. IntechOpen https://www.intechopen.com/books/geographic-information-systems-and-science/gis-and-remote-sensing-for-mangroves-mapping-and-monitoring (2019).

Takayama, K., Tamura, M., Tateishi, Y., Webb, E. L. & Kajita, T. Strong genetic structure over the American continents and transoceanic dispersal in the mangrove genus Rhizophora (Rhizophoraceae) revealed by broad-scale nuclear and chloroplast DNA analysis. Am. J. Bot. 100, 1191–1201 (2013).

CAS  Article  Google Scholar 

Ng, W. L. et al. Closely related and sympatric but not all the same: genetic variation of Indo-West Pacific Rhizophora mangroves across the Malay Peninsula. Conserv. Genet. 16, 137–150 (2015).

Article  Google Scholar 

Yahya, A. F. et al. Genetic variation and population genetic structure of Rhizophora apiculata (Rhizophoraceae) in the greater Sunda Islands, Indonesia using microsatellite markers. J. Plant Res. 127, 287–297 (2014).

CAS  Article  Google Scholar 

Chen, Y. et al. Applications of multiple nuclear genes to the molecular phylogeny, population genetics and hybrid identification in the mangrove genus Rhizophora. PLoS ONE. 10 (2015).

Guo, Z. et al. Genetic discontinuities in a dominant mangrove Rhizophora apiculata (Rhizophoraceae) in the Indo-Malesian region. J. Biogeogr. 43, 1856–1868 (2016).

Article  Google Scholar 

Cheng, A. et al. Molecular marker technology for genetic improvement of underutilised crops. In Crop improvement (eds Abdullah, S. et al.) 47–70 (Springer, Cham, 2017).

Google Scholar 

Ali, A. et al. Genetic diversity and population structure analysis of Saccharum and Erianthus genera using microsatellite (SSR) markers. Sci. Rep. 9, 1–10 (2019).

Article  CAS  Google Scholar 

Shinmura, Y. et al. Isolation and characterization of 14 microsatellite markers for Rhizophora mucronata (Rhizophoraceae) and their potential use in range-wide population studies. Conserv. Genet. Resour. 4, 951–954 (2012).

Article  Google Scholar 

Xu, S. et al. The origin, diversification and adaptation of a major mangrove clade (Rhizophoraceae) revealed by whole-genome sequencing. Natl. Sci. Rev. 4, 721–734 (2017).

CAS  Article  Google Scholar 

Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).

CAS  Article  Google Scholar 

Nei, M., Tajima, F. & Tateno, Y. Accuracy of estimated phylogenetic trees from molecular data. J. Mol. Evol. 19, 153–170 (1983).

ADS  CAS  Article  Google Scholar 

Maguire, T.L., Edwards, K.J., Saenger, P. & Henry, R. Characterisation and analysis of microsatellite loci in a mangrove species, Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Theor. Appl. Genet. 101, 279–285 (2000).

Torre, S. et al. RNA-seq analysis of Quercus pubescens leaves: de novo transcriptome assembly, annotation and functional markers development. PLoS ONE 9, e112487 (2014).

ADS  Article  CAS  Google Scholar 

Ye, Y. et al. Characterization, validation, and cross-species transferability of newly developed EST-SSR markers and their application for genetic evaluation in crape myrtle (Lagerstroemia spp). Mol. Breed. 39, 26 (2019).

Article  CAS  Google Scholar 

Nei, M. Molecular Evolutionary Genetics (Columbia University Press, London, 1987).

Google Scholar 

Wee, A. K. et al. Vicariance and oceanic barriers drive contemporary genetic structure of widespread mangrove species Sonneratia alba, J. Sm in the Indo-West Pacific. Forests 8, 483 (2017).

Article  Google Scholar 

Ellstrand, N. C. & Elam, D. R. Population genetic consequences of small population size: implications for plant conservation. Annu. Rev. Ecol. Evol. Syst. 24, 217–242 (1993).

Article  Google Scholar 

Feder, J. L., Gejji, R., Yeaman, S. & Nosil, P. Establishment of new mutations under divergence and genome hitchhiking. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 461–474 (2012).

Article  Google Scholar 

Annuar, A. S. & Latip, N. A. Mangrove contributions towards environmental conservation and tourism in Balik Pulau. Adv. Conserv. Sci. Technol. 1, 1–7 (2020).

Google Scholar 

Wee, A.K. et al. Oceanic currents, not land masses, maintain the genetic structure of the mangrove Rhizophora mucronata Lam. (Rhizophoraceae) in Southeast Asia. J. Biogeogr. 41, 954–964 (2014).

Ismail, M. H., Zaki, P. H. & Hamed, A. A. Wood density and carbon estimates of mangrove species in Kuala Sepetang, Perak, Malaysia. Malays. For. 78, 115–124 (2015).

Google Scholar 

Vitorino, C. A., Nogueira, F., Souza, I. L., Araripe, J. & Venere, P. C. Low genetic diversity and structuring of the Arapaima (Osteoglossiformes, Arapaimidae) population of the Araguaia-Tocantins basin. Front. Genet. 8, 159 (2017).

Article  Google Scholar 

Wright, S. The genetical structure of populations. Ann. Eugen. 15, 323–354 (1951).

MathSciNet  CAS  MATH  Article  Google Scholar 

Slatkin, M. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462 (1995).

CAS  PubMed  Google Scholar 

Goodman, S. J. RST calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol. Ecol. 6, 881–885 (1997).

CAS  Article  Google Scholar 

Moulin, N. L., Wyttenbach, A., Brüunner, H., Goudet, J. & Hausser, J. Study of gene flow through a hybrid zone in the common shrew (Sorex araneus) using microsatellites. Hereditas. 125, 159–168 (1996).

Article  Google Scholar 

Ge, X. J. & Sun, M. Population genetic structure of Ceriops tagal (Rhizophoraceae) in Thailand and China. Wetl. Ecol. Manag. 9, 213–219 (2001).

Article  Google Scholar 

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

Rizal, S. et al. General circulation in the Malacca strait and Andaman Sea: a numerical model study. Am. J. Environ. Sci. 8, 479–488 (2012).

Article  Google Scholar 

Nathan, R. et al. Mechanisms of long-distance seed dispersal. Trends Ecol. Evol. 23, 638–647 (2008).

Article  Google Scholar 

Drexler, J.Z. Maximum longevities of Rhizophora apiculata and R. mucronata propagules. Pac. Sci. 55, 17–22 (2001).

Li, J. et al. Pronounced genetic differentiation and recent secondary contact in the mangrove tree Lumnitzera racemosa revealed by population genomic analyses. Sci. Rep. 6, 29486 (2016).

ADS  CAS  Article  Google Scholar 

Murray, M. G. & Thompson, W. F. Rapid isolation of high molecular weight plant DNA. Nucl. Acids Res. 8, 4321–4326 (1980).

CAS  Article  Google Scholar 

Andrews, S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics https://www.bioinformatics.babraham.ac.uk/projects/fastqc (2010).

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinform. 30, 2114–2120 (2014).

CAS  Article  Google Scholar 

Grabherr, M. G. et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 29, 644 (2011).

CAS  Article  Google Scholar 

Varshney, R. K., Thiel, T., Stein, N., Langridge, P. & Graner, A. In silico analysis on frequency and distribution of microsatellites in ESTs of some cereal species. Cell Mol. Biol. Lett. 7, 537–546 (2002).

CAS  PubMed  Google Scholar 

Rozen, S. & Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers in Bioinformatics methods and protocols. 365–386 (Humana Press, 2000).

Van-Oosterhout, C., Hutchinson, W. F., Wills, D. P. & Shipley, P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes. 4, 535–538 (2004).

CAS  Article  Google Scholar 

Lewis, P.O. & Zaykin, D. Genetic Data Analysis (GDA) version 1.1: a computer program for the analysis of allelic data. UConn https://phylogeny.uconn.edu/software/ (2002).

Rice, W. R. Analyzing tables of statistical tests. Evol. 43, 223–225 (1989).

Article  Google Scholar 

Park, S.D.E. Trypanotolerance in West African cattle and the population genetic effects of selection. Ph. D (University of Dublin, 2001).

Goudet, J. FSTAT version 2.9.3.2: a program to estimate and test gene diversities and fixation indices. Unil https://www2.unil.ch/popgen/softwares/fstat.htm (2002).

Nei, M., Tajima, F. & Tateno, Y. Accuracy of estimated phylogenetic trees from molecular data. J. Mol. Evol. 19, 153–170 (1983).

Liu, K. & Muse, S. V. PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinform. 21, 2128–2129 (2005).

CAS  Article  Google Scholar 

Nei, M. F-statistics and analysis of gene diversity in subdivided populations. Ann. Hum. Genet. 41, 225–233 (1977).

CAS  MATH  Article  Google Scholar 

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

CAS  Article  Google Scholar 

Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

CAS  PubMed  Google Scholar 

Li, Y. L. & Liu, J. X. StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Mol. Ecol. Resour. 18, 176–177 (2018).

Article  Google Scholar 

Goudet, J. PCAGEN version 1.2: a program to perform a principal component analysis (PCA) on genetic data. Unil https://www2.unil.ch/popgen/softwares/pcagen.htm (1999).

Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

CAS  Article  Google Scholar