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Annals of Botany 92: 409-414, 2003
© 2003 Annals of Botany Company

Genetic Diversity of Hibiscus tiliaceus (Malvaceae) in China Assessed using AFLP Markers

TIAN TANG1, YANG ZHONG2, SHUGUANG JIAN1,3 and SUHUA SHI*,1

1 Key Laboratory of Gene Engineering of the Ministry of Education, Zhongshan University, Guangzhou 510275, People’s Republic of China, 2 Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai 200433, People’s Republic of China and 3 South China Botanical Garden, Academia Sinica, Guangzhou 510650, People’s Republic of China

* For correspondence. Fax 86-20-34022356, e-mail lssssh{at}zsu.edu.cn

Received: 9 December 2002; Returned for revision: 20 February 2003; Accepted: 30 May 2003


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 

Amplified fragment length polymorphism (AFLP) markers were used to investigate the genetic variations within and among nine natural populations of Hibiscus tiliaceus in China. DNA from 145 individuals was amplified with eight primer pairs. No polymorphisms were found among the 20 samples of a marginal population of recent origin probably due to a founder effect. Across the other 125 individuals, 501 of 566 bands (88·5 %) were polymorphic, and 125 unique AFLP phenotypes were observed. Estimates of genetic diversity agreed with life history traits of H. tiliaceus and geographical distribution. AMOVA analysis revealed that most genetic diversity resided within populations (84·8 %), which corresponded to results reported for outcrossing plants. The indirect estimate of gene flow based on {phi}ST was moderate (Nm = 1·395). Long-distance dispersal of floating seeds and local environments may play an important role in shaping the genetic diversity of the population and the genetic structure of this species.

Key words: Hibiscus tiliaceus, sea hibiscus, tree hibiscus, AFLP, genetic diversity, China.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
Hibiscus tiliaceus L. (Malvaceae), also known as sea hibiscus (Holtum and Enoch, 1995) or tree hibiscus (Hargreaves and Hargreaves, 1970), has its origin in the Pacific Islands (Konczak, 1996). This fast-growing tree is wind- and salt-resistant and adapted to a wide range of environments. It is found on islands and coasts all over the tropical Pacific (Whistler, 1980; Chin and Enoch, 1988). It is also one of the most common secondary forest trees and is frequently found in disturbed forests (Whistler, 1980). Hibiscus tiliaceus grows well near the ocean, by streams, and on mountainous slopes up to 800 m elevation (Konczak, 1996; Saquet, 1996).

Hibiscus tiliaceus has been used for the stabilization of sand dunes, the formation of coastal windbreaks and in some restoration projects. In addition to the ecological importance of Hibiscus tiliaceus, it is one of the most useful trees throughout tropical and subtropical Polynesia, Melanesia and Micronesia, and is held in high regard for its usefulness to the traditional life of oceanic people (Brown, 1935; Chin, 1992; Field, 1995; Chun, 1995; Wheeler and Carillet, 1997). Hibiscus tiliaceus is sometimes cultivated inland for home landscapes as an ornamental shade tree.

Despite the importance of H. tiliaceus, little is known about its genetics. Its wide geographical distribution and varied habitats indicate that there is probably a large amount of genetic diversity. Amplified fragment length polymorphism (AFLP) (Zabeau and Vos, 1993; Vos et al., 1995) is a DNA fingerprinting technique that approaches the ideal as a marker system for resolving genetic diversity among individuals, populations and species (Mueller and Wolfenbarer, 1999). This technique is highly reproducible, and can be used to survey overall genetic differences in the nuclear genome in a single assay without any prior sequence knowledge (Jones et al., 1997). As a consequence of these features, AFLP has been used to investigate genetic variation in a wide variety of micro-organisms, plants and animals (Janssen et al., 1996; Albertson et al., 1999; Muluvi et al., 1999; Ajmone-Marsan et al., 2001; Sawkins et al., 2001; Terefework et al., 2001; Maguire et al., 2002).

In the current study, AFLPs were used to reveal the extent and distribution of genetic diversity in nine natural populations of H. tiliaceus from the coast of south China as a first step towards gaining a better knowledge of genome diversity in H. tiliaceus.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 LITERATURE CITED
 
Sample collection
A total of 145 individuals of H. tiliaceus, representing nine diverse natural populations, were sampled throughout its range in China (Fig. 1). Leaf material from 13–20 randomly selected trees was collected from each population at intervals of at least 5 m. Leaf material was stored with silica gel in zip-lock plastic bags until use.


Figure 1
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  		Fig. 1. Distribution of the studied populations of Hibiscus tiliaceus. Population codes and numbers of samples are show in Table 2. a Population 9 was excluded from all the analyses because the 20 individuals in the population showed vegetative (clonal) reproduction from a single founder which led to too small a sample (n = 1) for statistical comparison with other populations.

 
DNA extraction and AFLP assay
A modified DNA mini-prep procedure of Doyle and Doyle (1990) was used to extract DNA. The AFLP technique is described by Vos et al. (1995), except that EcoRI selective amplification primers were labelled with fluorescent 6-carboxy fluorescein (6-FAM) on the 5'nucleotide (Table 1). The amplified fragments were separated and detected with an ABI PRISM 377 automated sequencer (PE Applied Biosystems, Foster City, CA, USA).


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  		Table 1. DNA sequences of amplified fragment length polymorphism (AFLP) primers and adapters
 
Scoring and data analysis
Data were collected using GeneScan software (version 2.1, PE Applied Biosystems). The GeneScan sample files were further analysed using Genotyper (version 1.2; PE Applied Biosystems). The fragments produced by each primer were treated as characters and numbered sequentially. Genotypes were scored for the presence (1) or absence (0) of all polymorphic bands. Population 9 in Xiamen, Fujian was excluded from the analysis below because all 20 individuals shared the same genotype which indicated that all samples must have been the products of vegetative (clonal) reproduction from a single founder, and the genetic diversity in the ‘population’ merely reflects the genotype of the founder individual. Consequently, the sampling in this population (reduced to n = 1) was too small for statistical comparison with the other populations.

From banding patterns of the remaining populations, a matrix of genetic similarity using the Dice coefficient was calculated as GSxy = 2a/(2a + b + c), where a is the number of bands common for samples x and y, b is the number of bands present only in sample x, and c is the number of bands present only in sample y (Dice, 1945). Based on GS values, associations among the remaining 125 individuals were revealed by a neighbour-joining cluster analysis (Saitou and Nei, 1987) using the Njoin procedure of NTSYSpc v2.02j (Rohlf, 1998). The mean similarity values (GS) within populations, the percentage of polymorphic bands (P) and the mean expected heterozygosity (Hexp) (Nei, 1973) were calculated to quantify the degree of within-population diversity with the assistance of TFPGA v1.3 (Miller, 1997). Mean expected heterozygosity was estimated as



Formula

where Pli is the frequency of ith allele of lth loci, k is the number of alleles for a given locus, and m is the number of loci (Nei, 1973). Analyses of molecular variance (AMOVA) based on the pairwise squared Euclidean distances among molecular phenotypes were carried out to partition the genetic diversity among populations using WINAMOVA v1·55 (Excoffier et al., 1992). Gene flow (Nm, number of migrants per generation) among populations was calculated based upon {phi}ST (analogous to FST), using the method of Wright (1951).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
LITERATURE CITED
 
This study is the first application of AFLP to genetic diversity assessment in H. tiliaceus. Population 9, the northernmost population, was the only monomorphic population. The lack of AFLP variation is probably due to a founder effect, since this population is of recent origin. This result also agrees with the prediction that marginal populations should be less variable than populations in the primary range (Brussard, 1984; Blows and Hoffmann, 1993; Johansson, 1994; Stewart and Nilsen, 1995).

Eight primer combinations produced 566 bands across all the 125 individuals (excluding population 9), of which 501 were polymorphic (88·52 % polymorphism). The percentage of polymorphic bands within populations ranged from 47·88 % to 71·38 % (Table 2). One hundred and twenty-five unique AFLP banding patterns were observed, i.e. each individual presented a unique AFLP phenotype, indicating extensive genetic variation in the analysed individuals. There were no population-specific markers (present in one population but absent in the others). However, the mean within-population genetic similarities varied considerably between populations, ranging from 0·761 for population 6 to 0·884 for population 8, with an overall average of 0·826 (Table 2). The average expected heterozygosity at species level was 0·243, which was high compared with other species with similar life history traits (Hamrick and Godt, 1990). Population 6 exhibited the highest expected heterozygosity (0·253) while population 5 exhibited the lowest (0·160). The expected heterozygosity values were consistent with the variation in the percentage of polymorphic bands.


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  		Table 2. Genetic variation within populations of Hibiscus tiliaceus in China based on AFLP data
 
These data indicate that considerable intra-population genetic diversity exists in H. tiliaceus, in agreement with its life history traits and geographical distribution. Hibiscus tiliaceus is a long-lived, insect-pollinated woody perennial and it is spread throughout the tropical and subtropical regions of the Pacific. This combination is expected to result in a high level of genetic diversity (Hamrick and Godt, 1990). Though this species reproduces both sexually and vegetatively by sprouting prostrate stems, this can be viewed as a strategy for both maximal heterozygosity and reproductive success, which is not uncommon in woody plants exposed to adverse environmental conditions (Rafii and Dodd, 1998). The high genetic diversity observed indicates that these populations should be able to adapt to environmental changes. This is reflected in the current adaptive capacity of H. tiliaceus to various habitats (Hamrick et al., 1979; Wills, 1981; Danzmann et al., 1986; Ledig, 1986).

Partitioning of genetic variability by analysis of molecular variance revealed that most of the AFLP diversity was distributed among individuals within populations (84·8 %), with the remaining split among populations within locations (10·5 %) and among locations (4·7 %) (Table 3). The higher {phi}SC value (0·110) compared with the {phi}CT value (0·047) may suggest that ecogenic adaptations to local environments have played a critical role in the genetic differentiation within locations at a small spatial scale. The value of {phi}ST (0·152) is consistent with the life history characteristics of H. tiliaceus. Tropical trees tend to possess the most genetic diversity within populations (Hamrick and Loveless, 1989), and species reproducing both sexually and asexually show less differentiation than species reproducing only sexually (Hamrick and Godt, 1990).


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  		Table 3. AMOVA analysis of Hibiscus tiliaceus from eight populations using 566 AFLP markers
 
For a wide range of plant species, the mating system plays a critical role for the patterns of genetic variation both within and among populations. However, our investigation provides no direct information on the mating system of H. tiliaceus due to the dominant nature of AFLP markers. Using AFLP markers, Maguire et al. (2002) found that 80 % of the total genetic diversity was among individuals within populations for Avicennia marina based on AMOVA. They suggested that this widespread, long-lived, woody mangrove had a trend towards outcrossing. RAPD-based GST values for 35 plant species averaged 15·5 % for 27 outcrossing species, and 59·6 % for eight inbreeding species (Bussell, 1999). Summaries of allozyme analyses yield similar results: average GST < 19 % for outcrossing species compared with 51 % for selfers (Hamrick and Godt, 1990). Furthermore, most forest trees have been found to have mating systems with high levels of outcrossing (Muona, 1990), and some studies suggest that outcrossing is the main form of reproduction of tropical coastal trees (Primack and Tomlinson, 1980; Ge and Sun, 1999; Maguire et al., 2000). Therefore, by comparing the proportion of genetic diversity found among populations of outcrossing species as presented above, it could be speculated that H. tiliaceus is mainly outcrossing.

The indirect estimate of gene flow (Nm) based on {phi}ST was moderate (1·395), which means the numbers of migrants per generation are larger than one, and the level of genetic diversity maintained within a population is less susceptible to genetic drift. This Nm value of 1·395 is in accordance with what is expected for tropical trees in general. Reis (1996) stated that values above 1·0 are common among populations of tropical trees. It is also comparable with the average values reported for outcrossing animal-pollinated species (Nm = 1·154) and higher than that of mixed-mating species (Nm = 0·727) (Hamrick and Godt, 1990). Gene flow between populations occurs when migrant genes arriving by pollen or seed become established in new genets. Though H. tiliaceus is frequently visited by insects, leading to pollen exchange, there is no information to suggest that it has a long-distance pollinator. Considering the geographical distance between the populations in our study (average 476·5 km), it is suggested that the importance of long-distance dispersal of floating seeds for the genetic profile of H. tiliaceus should be explored in the future. Kudoh and Whigham (1997, 2001) studied both historical gene flow and current-year seed dispersal of Hibiscus moscheutos, and inferred that the observed genetic patterns could be explained by patterns of water dispersal of seeds rather than by exchange of pollen among populations.

Cluster analysis revealed that most of the individuals of a specific population were arranged in population-specific clusters, despite confusing patterns mainly occurring among the individuals of two populations where these occurred in the same location (Fig. 2). Each two populations from the same location tended to cluster together except for populations 5 and 6, indicating the relatively high geographic proximity. The apparent genetic discrepancy observed between the two populations in Dongzhai, Hainan, may be attributed to their different habitats. Population 5 was the only population located on a physically isolated small island. The limited gene flow from the source (continental) populations made the genetic diversity more susceptible to genetic drift. Supposing this population was recently established from a small number of individuals colonizing from population 6, the closest population located on the mainland, the genetic diversity has not recovered since the founder event. The genetic drift and founder effect may simultaneously influence the genetic diversity of population 5 and contribute to low levels of variation. In contrast, population 6 grew in association with the mangrove marsh and was regularly inundated; the greater opportunities of gene exchange via seeds may account for the higher genetic diversity. Though AMOVA analysis also suggested an effect of ecogeographic parameters on genetic diversity, critical tests are needed to determine such correlations.


Figure 2
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  		Fig. 2. Neighbour-joining tree of 125 individuals of Hibiscus tiliaceus in China based on genetic similarity (Dice, 1945) from AFLP data.

 
In conclusion, the results of this study indicate that H. tiliaceus is characterized by a relatively high within-population genetic diversity. The estimates of genetic differentiation and gene flow suggest that the species is primarily outcrossing. Long-distance dispersal of floating seeds and microscale ecogeographic factors may play important roles in the genetic diversity of the populations and the genetic structure of this species.


   ACKNOWLEDGEMENTS
 
We thank Dr Junchao Huang for advice on techniques, Dr Shichu Liang for helping us in sampling, Dr Peng Nan for analysis of NTSYS-pc, and Xun Gong, Xin Liu, Changchun Yuan, Yuguo Wang, Yaqing Du, Fengxiao Tan, Yalin Peng, Jianzi Huang and Yelin Huang for DNA extraction. This study was supported by grants from the National Natural Science Foundation of China [39825104, 301(0071) and 302(0030)], the Natural Science Foundation of Guangdong Province (001223), and the Ministry of Education Special Foundation (20010558013) and Key Member Teachers Project, and the Qiu Shi Science and Technology Foundation.


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