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Population Biology |
2Laboratory of Agricultural Ecology, Faculty of Agriculture, Graduate School, Kyushu University, Kasuya 811-2307 Japan 3Laboratory of Horticultural Science, Faculty of Agriculture, Graduate School, Kyushu University, Fukuoka 812-8581, Japan 4Department of Horticulture, National Chiayi University, Chiayi, Taiwan, Republic of China
Received for publication April 25, 2000. Accepted for publication December 21, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allozyme diversity • biogeography • continental island • insular endemic • Liliaceae • Lilium • Taiwan • the Ryukyu Archipelago
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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as a review). A basic theory holds that genetic depauperization of organisms' populations and genetic differentiation among them, respectively, are promoted by "bottlenecks" created by diminishing population size and restricted gene flow from and into outer populations (Wright, 1931, 1943
; Hartl, 1981
; Kimura, 1983
; Nei, 1987
). Thus, it can be easily assumed that disjunct geographic distributions in islands, along with factors regarding migration (the founder principle) and isolation, greatly affect an organism's genetic structure in terms of its association with historical events. In fact, information on genetic structure obtained using molecular techniques has accumulated recently in regard to flowering plants, further clarifying the way current biogeographic structures have been established in relation to historical events in islands (e.g., Witter and Carr, 1988
; Inoue and Kawahara, 1990
; Crawford et al., 1992
; DeJoode and Wendel, 1992
; Westerberg and Saura, 1994
; Kim et al., 1996
; Weller, Sakai, and Straub, 1996
; Affre, Thompson, and Debussche, 1997
; Ito, 1998
; Baldwin et al., 1999
; Kim et al., 1999
).
These intensive studies simultaneously generated important findings, which are now widely accepted regarding the population and evolutionary biology of insular plants. First, within an isolated island environment, evolution expressing extraordinary morphological and ecological divergence, namely, adaptive radiation, can frequently occur with relatively little molecular divergence within a short time (see Crawford, 1990
, for a review). Second, endemic island taxa often possess relatively limited amounts of genetic variation (see DeJoode and Wendel, 1992
; Weller, Sakai, and Straub, 1996
; Frankham, 1997
, Gemmill et al., 1998
for reviews), though some researchers recently exhibited notable exceptions (Weller, Sakai, and Straub, 1996
; Francisco-Ortega et al., 2000
). These findings, however, have been concerned mostly with the taxa endemic to oceanic islands, upon which organisms are established only through migration events from remote continents.
The archipelago running from Ryukyu to Taiwan consists of nearly 200 islands forming an arc-array in the subtropical area between Kyushu, the southwestern district of mainland Japan, and the southeastern part of China. Since this archipelago is considered geologically to be of continental origin (Kimura, 1996
), unlike oceanic islands such as Hawaii, its biota is largely comprised of relict taxa, which presumably differentiated from their relatives in the adjacent continent or mainland (Kizaki and Oshiro, 1977
). Thus, comparative phylogeographic study between biota in this archipelago and that in oceanic islands may potentially provide significant new insights into island biology. Studies focusing on combinations of genetic population structures in relation to the biogeography of relict organisms in the Ryukyu Archipelago and Taiwan, however, have almost entirely been devoted to animals such as Plecoglossus altivelis (Nishida, 1985
), Iriomote cats (Masuda and Yoshida, 1995
), Gekko hokouensis (Toda, Hikida, and Ota, 1997
), wood-feeding cockroaches (Maekawa et al., 1999
), Indian rice frogs (Toda, 1999
), and pit vipers (Toda et al., 1999
). To our knowledge no such studies have been conducted regarding plants.
Lilium longiflorum and L. formosanum are bulbous plants of the Liliaceae endemic to this archipelago and are widely regarded as species of great importance for world horticulture (Miller, 1993
; Okazaki, 1996
; McRae, 1998
). Both species have been taxonomically classified into the subsection of the section Leucolirion by Comber (1949)
, and their interspecific fertile hybrid cultivars, L. x formolongi imply that the two species are genetically close. Lilium longiflorum is geographically distributed from the northernmost islands of the Ryukyu Archipelago to the mainland seacoast and to small islands in the eastern part of Taiwan, exhibiting a disjunct distribution following a pattern of arc-arrayed steppingstones (Wilson, 1925
; Shimizu, 1987
). On the other hand, L. formosanum is natively distributed solely, but widely, within the mainland of Taiwan (Wilson, 1925
; Shii, 1983
). The combined distribution of the two species thus covers the entire archipelago across many islands within an 
1300 km range.
Based on the abovementioned characteristics regarding study sites and plants, we expected that an analysis of the genetic structure of these species would be significant not only in terms of what it might reveal regarding the phylogenetic relationship of the two species, but also for verifying this relationship's association with the historical geography in the Ryukyu to Taiwan archipelago arc and the widely accepted generalization regarding insular evolutionary biology assessed mostly in oceanic islands. Allozyme analysis is often employed for studying types of microevolution such as speciation and conspecific population differentiation (Crawford, 1990
). Thus, we estimated allozyme diversity of L. longiflorum and L. formosanum in order to address the following questions: (1) When and how are the species established? (2) Does the genetic structure of their present populations reflect their ecological nature and/or the historical geography of the archipelago? (3) Are there any properties regarding allozyme diversity expressed by other insular plant taxa?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; M. Hiramatsu, unpublished data). Capsules were collected in the study sites, and plant materials for enzyme analysis were grown in a greenhouse from air-dried seeds. A single progeny individual from each maternal genotype was used for the analysis. Samples of each population comprised 10–55 individuals (33 for L. longiflorum and 25 for L. formosanum, on average).
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) with a sprinkle of polyvinylpolypyrolidone and sea sand. Crude extracts were soaked by paper wicks (11 x 3 mm), and the wicks were inserted into a slit in a starch gel.
Horizontal starch gel electrophoresis was carried out according to the procedures described by Wendel and Weeden (1989)
. Two combinations of gel and electrode buffers were used to resolve 11 enzymes: aspartate aminotransferase (AAT), catarase (CAT), diaphorase (DIA), glucose-6-phosphate isomerase (GPI), glutamate dehydrogenase (GDH), and malic enzyme (ME) were resolved using System 6, and fluorescent esterase (FEST), isocitrate dehydrogenase (IDH), malate dehydrogenase (MDH), phosphoglucomutase (PGM), and phosphogluconate dehydrogenase (6PGD) were determined using System 2. Staining protocols were also carried out according to the method of Wendel and Weeden (1989)
, except for a modification for FEST by dilution of the substrate with 1/20th volume of acetone.
Statistical analysis
Allele frequencies in each population of the species were calculated for 13 loci encoding the 11 enzyme systems. The following parameters concerning genetic diversity were estimated at the population and species level in the manner described by Hamrick and Godt (1990)
: the proportion of polymorphic loci (Pp) at a 95% criterion, the number of alleles per polymorphic loci (Ap), the number of alleles per locus (A), and expected heterozygosity (h), where h was an unbiased estimate (Nei and Roychoudhury, 1974
; Nei, 1978
).
To estimate genetic differentiation among populations, Nei's (1973)
gene diversity statistics, namely, total genetic diversity (HT), genetic diversity within populations (HS), and proportion of the total diversity among populations (GST), were determined. In addition, Wright's (1951)
fixation index (Fis) was estimated at each polymorphic locus as unbiased following the method of Nei and Chesser (1983)
. Chi-square analyses were performed to determine the heterogeneity of allelic frequencies among populations (Workman and Niswander, 1970
) and to determine deviations from genotypic frequencies expected under the Hardy-Weinberg equilibrium (Li and Horvitz, 1953
).
Unbiased genetic identity and genetic distance were calculated based on allele frequencies in accordance with the formula derived by Nei (1978)
. The resulting distance matrix among all populations of the two species was then used to construct a neighbor-joining tree (Saitou and Nei, 1987
) using the NEIGHBOR and DRAWTREE programs of PHYLIP (Felsenstein, 1993
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1.2–2.2 times larger than those for L. formosanum.
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Genetic population structure and intraspecific differentiation
Fixation indices (Fis) varied greatly among populations of each species, although no significant excess of heterozygotes was observed (Table 3). Fifty-five loci (44%) out of 119 loci tested for L. longiflorum showed significant deviation from 0. Relatively high frequencies of the deviated loci within a population occurred in LYA, LAM1, LAM2, LOE, LYR, LOK2, and LOK3, which are located in the relatively northern part of the archipelago. For L. formosanum, ten loci (30%) out of 33 loci tested were significant.
Chi-square analyses for heterogeneity indicated significant (P < 0.01) allele frequency differences among populations in all and seven loci for L. longiflorum and L. formosanum, respectively (Table 4). On average, the indices of genetic differentiation (GST) were prominently different between the two species. The total gene diversity was moderately (35%) apportioned among populations of L. longiflorum, whereas the majority (92%) was apportioned within populations of L. formosanum.
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unbiased genetic identity (I) and standard genetic distance (D) values within and between species are summarized in Table 5. The I values between populations within L. longiflorum ranged widely from 0.592 to 1.000 with the mean of 0.850, whereas those within L. formosanum ranged much more narrowly from 0.946 to 0.997 with the mean of 0.977.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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demonstrated that insular endemic species tend to have lower genetic variability than the continental taxa. DeJoode and Wendel (1992)
summarized the allozyme variability of 55 insular endemic plant taxa, which in general was seen to express relatively limited amounts of variability at the species or infraspecific taxon with Pp = 25.0 (0.0–57.0), A = 1.32 (1.00–1.93), and h (HT) = 0.064 (0.000–0.195) as an average (range) across them. On the other hand, notable exceptional cases indicating relatively high estimated values were reported recently. For example, in Hawaiian Schiedea and Alsinidendron, respective Pp, A, and h values (and ranges) averaged across 25 populations from 20 species were 43.1 (0–88.9), 1.80 (1.00–3.00), and 0.183 (0–0.371) (Weller, Sakai, and Straub, 1996
); in Hawaiian Metrosideros, the latter two values (and ranges) averaged across 14 populations from three species were 3.0 (2.7–3.3) and 0.371 (0.296–0.470), respectively (Aradhya, Mueller-Dombois, and Ranker, 1991
), and in endemics of the Canary Islands, the h (HT) value (and range) averaged across 69 species from 18 genera was 0.186 (0.000–0.456) (Francisco-Ortega et al., 2000
). Compared with the variability values of the reported insular taxa, those of L. longiflorum (Pp = 100, A = 3.46, and h = 0.312 at the species level, and Pp = 48.2, A = 1.72, and h = 0.187 at the population level) are comparable to higher or the highest ones.
The both species-level and population-level allozyme variability of L. longiflorum exceeded that averaged across the species in various ecological categories, which mainly comprised continental species, such as monocotyledonous species (Pp = 59.2, A = 2.38, and h = 0.181 at the species level for 111 species, and Pp = 40.3, A = 1.66, and h = 0.144 at the population level for 80 species), endemic species (Pp = 40.0, A = 1.80, and h = 0.096 at the species level for 81 species, and Pp = 26.3, A = 1.39, and h = 0.063 at the population level for 100 species) and outcrossing animal-pollinated species (Pp = 50.1, A = 1.99, and h = 0.167 at the species level for 172 species, and Pp = 35.9, A = 1.54, and h = 0.124 at the population level for 164 species) (Hamrick and Godt, 1990
), though the wide range of variations was observed among population-level values of L. longiflorum. Among Liliaceous species, the species-level allozyme variability in L. longiflorum is almost comparable to the highest one reported in Hemerocallis hakuunensis (Pp = 83.0, A = 6.08, and h = 0.279), which is native to the Korean Peninsula and a bulbous plant with similar life history to L. longiflorum (Kang and Chung, 1997
). Thus, L. longiflorum is a plant species with remarkably high allozyme variability.
Comparison in genetic identity value (I) within a species also revealed that L. longiflorum is highly diverged as a single species (see Crawford, 1990
, for a review). The minimum I value between populations within L. longiflorum (0.592), which was recorded between northernmost (LYA) and southernmost (LLA) populations, has rarely been reported within the flowering plant. For example, extensive minimum I values have been reported within a selfing insular species, Bidens discoidea (0.688; Roberts, 1983
), in Limnanthes floccosa (0.575; McNeill and Jain, 1983
), and between subspecies pairs of Lens culinaris (0.65; Pinkas, Zamir, and Ladizinsky, 1985
).
Generally, among insular plants, lower minimum I values have been rarely recorded in very limited "congeneric" or "intergeneric" population pairs in a large complex of morphologically and ecologically highly radiating taxa; e.g., Alsinoideae in Hawaii (0.242; Weller, Sakai, and Straub, 1996
), silversword alliance in Hawaii (0.426; Witter and Carr, 1988
), woody Sonchus alliance in the Canary Islands (0.490; Kim et al., 1999
), and Robinsonia in the Juan Fernandez Islands (0.560; Crawford et al., 1992
). Unlike morphological and ecological phenotypes, protein molecules such as allozymes are assumed to evolve much more consistently because of their neutral relationship to natural selection, as described by the neutral theory of molecular evolution (Kimura, 1983
). The fact that the amount of allozyme divergence in L. longiflorum is close to that in the maximally radiating insular plant taxa indicates that they originated, roughly, at the same time. Nevertheless, they show a great contrast in terms of phenotypic divergence.
A large number of reports for insular plants have been concerned with the highly radiating taxa in their morphological and ecological phenotypes in combination with very little molecular divergence (see Crawford, 1989, 1990
; Gemmill et al., 1998
; Ito, 1998
, for reviews). The opposite pattern, in which genetically highly diverged insular taxa showed little divergence in their morphological and ecological phenotypes, was rarely observed until the present study on L. longiflorum. Although it may be difficult to conclude the reason why such contrasting evolution occurs under "insular" environments, it could be attributed to differences in the environmental and ecological properties of oceanic and continental islands. Diverse ecologically unoccupied niches, which is presumably a major factor affecting radiating evolution, are expected to be rather few and small even at the birth of continental islands such as the Ryukyu Archipelago and Taiwan.
Nei (1987)
demonstrated a method for estimating divergence time based on allozyme data, given certain assumptions about mutation rates and the operation of a molecular clock: time (t) = D/2a, where D is the standard genetic distance and a is the substitution rate per locus per year. Usually, a is assumed to be 10–7 per locus per year. Then, t may be calculated as (5 x 106)D. Using this formula, the initiation of divergence has been estimated in the aforementioned highly radiating insular taxa, e.g., 3.6 x 106 yr ago (MYA) for the woody Sonchus alliance in the Canary Islands (Kim et al., 1999
) and 2.9 MYA for Robinsonia spp. in the Juan Fernandez Islands (Crawford et al., 1992
). Since the maximum D within L. longiflorum was 0.524, initiation of divergence is assumed to be 2.62 MYA. As pointed out by Nei (1987)
, however, this value may sometimes be an overestimate because the genetic distance tends to increase when the population experiences "bottlenecks." This is likely to occur under insular environments and for colonizing plants like L. longiflorum.
From the geological point of view, Kimura (1996)
described that at the end of the Tertiary Period (1.7–2.0 MYA), the area around Ryukyu and Taiwan was a continuous coastal margin in East Asia. The archipelago had developed during the Pleistocene Era. It is, therefore, realistic to presume that L. longiflorum existed as early as around at the end of the Tertiary Period, and then experienced the Quaternary dynamics that generated the current Ryukyu to Taiwan arc. The extremely high allozyme variability and divergence in L. longiflorum presumably reflect the relict endemism with the relatively longtime persistence of the present distribution in this species.
Lilium formosanum
Lilium formosanum possessed a subset of L. longiflorum alleles for 11 (85%) loci and exhibited less allozyme variability than L. longiflorum (76.9 vs. 100 for Pp 2.46 vs. 3.46 for A, and 0.142 vs. 0.312 for h at the species level). These facts agree with previous data describing progenitor-derivative species pairs (e.g., Gottlieb, 1973, 1974
; Crawford, Ornduff, and Vasey, 1985
; Rieseberg et al., 1987
; Loveless and Hamrick, 1988
; Pleasants and Wendel, 1989
; Maki et al., 1999
). The three species-specific alleles (Fest-2b, Fest-2f, and Gpi-2e) were detected for L. formosanum. However, such numbers of unique alleles are not uncommon in recently derived species (0–8 in the 11 species; see Pleasants and Wendel, 1989
). The mean I value of population pairs between L. formosanum and L. longiflorum (0.816) is close to the lowest values among those 11 progenitor-derivative species pairs listed by Pleasants and Wendel (1989)
. This result can be undoubtedly attributed to the unusually extreme genetic differentiation within a progenitor species, L. longiflorum. Restricted among populations within the mainland of Taiwan, where the speciation between the two species presumably occurred, estimation of the mean I between L. formosanum and L. longiflorum was 0.954 (0.925–0.978). This indicates that the two species are genetically very close in the manner typical of progenitor-derivative species pairs. Selfing is considered a key characteristic necessary for the rapid expansion of a species (Maki et al., 1999
), and the occurrence of selfing natures shown by several recently derivative species such as Stephanomeria malheurensis (Gottlieb, 1973
), Polygonella articulata, P. americana (Lewis and Crawford, 1995
), and Tricyrtis nana (Maki et al., 1999
) are very similar to the case of derivation of self-compatible L. formosanum from self-incompatible L. longiflorum. The accumulated evidence above demonstrates that L. formosanum could be a recent local derivative from the southern peripheral populations of L. longiflorum.
Naturalized populations of L. formosanum are found in vegetation dominated by relatively tall grasses with wide geographical ranges in often-disturbed inland areas of the mainlands of Japan, and sometimes they comprised thousands of individuals (M. Hiramatsu, personal observation). In contrast, L. longiflorum populations are never seen in such contexts. In South Africa, L. formosanum is widely naturalized under vegetation similar to that found in the mainlands of Japan (Walters, 1983
). These facts imply that unlike L. longiflorum, L. formosanum can be distributed rapidly and widely in adaptable competitive and disturbed environments. Similar adaptable environments develop in adjacent regions such as the Ryukyu Archipelago and the Chinese continent. Nevertheless, native populations of L. formosanum persist solely within the mainland of Taiwan. Thus, it is assumed that L. formosanum has been prevented from migrating to adjacent regions because of its isolation on the mainland of Taiwan prior to species initiation. The isolation of the mainland of Taiwan is assumed to have occurred during the late stage of the archipelago's development as early as the last glaciation at the end of the Pleistocene Era (Kimura, 1996
). Examples of recent derivative species whose initiation times are assumed to be around the Pleistocene glaciation include Cirsium pitcheri (Loveless and Hamrick, 1988
), Erythronium propullans (Pleasants and Wendel, 1989
), Polygonella articulata, and P. americana (Lewis and Crawford, 1995
).
The progenitor and derivative relationship between L. longiflorum and L. formosanum based on our results contradicts the speculation made by Dubouzet and Shinoda (1999)
, who demonstrated only a sister relationship between the two species based on the internal transcribed spacer sequences of the species' nrDNA and regarded L. longiflorum as a species derived from L. formosanum. Since our results demonstrate that L. longiflorum is highly diverged as a single species, the accuracy of resolution for the two species' phylogenetic relationships will depend on the sample size used in the study. Thus, the very small number of samples (presumably one for each species) in the study by Dubouzet and Shinoda (1999)
is assumed to be a cause of their inaccurate determination of the phylogenetic relationship between the two species.
The biogeographic structure of L. longiflorum involving insular historical events
Detailed comparisons of allozyme diversity among L. longiflorum populations revealed biogeographic structures highly associated with the historical geography of the Ryukyu to Taiwan archipelago arc, which has been assumed based on geology and the biogeography of other organisms.
First, the depauperization in allozyme variability for some populations closely correlated with the maximum altitude of their islands, i.e., the populations that did not exhibit as much allozyme variability as did the adjacent island populations, LKI, LOE, LYR, LMI, and LYO, were located on islands lower than 231 m (Tables 1, 3). Because the sea level was at one time 200 m higher than that at present, lower islands were submerged largely or completely and then pushed upward during the late Pleistocene Era (0.4–1.0 MYA) (Kimura, 1996
). This evidence suggests that those L. longiflorum populations had recently experienced very severe bottlenecks either by diminishing population size or by subsequent migration from relict populations on adjacent islands not highly submerged and with higher altitudes. Similarly, another substantially genetically eroded population on the small but high volcanic island southeast of the mainland of Taiwan (LLA) seems to have also experienced severe bottlenecks, although the initiating time of this island is not known. A similar geohistory-associated biogeographic hypothesis regarding this archipelago has been proposed to explain the mosaic distribution pattern of pit vipers (Trimeresurus spp.), whether they are present or absent in each island (Takara, 1962
). However, no evidence has been based on population genetic diversity until the present study.
Secondly, by excluding the islands with genetically eroded populations (LKI, LOE, LYR, LMI, LYO, and LLA), three major vicariant splits generating large genetic differentiation on the neighbor-joining tree correspond to interisland splits between Yaku Shima and Amami O Shima, between Tokuno Shima and Okinawa, and between Iriomote Jima and the mainland of Taiwan, though a northernmost population in Okinawa (LOK1) is included as an exception in the geographically different cluster group over the splits (Figs. 1 and 2). The northernmost split has long been recognized as the first strait formed in the archipelago land bridge (Kizaki and Oshiro, 1977
; Kimura, 1996
) and as a vicariant border called Watase's Line (Kuroda, 1931; Hotta, 1974
; Ono, 1989
), since it corresponds to distribution borders dividing Japanese biota (Kuroda, 1931; Inger, 1950
; Hotta, 1974
; Ono, 1989
; Ota, 1998
) and to the Tokara Tectonic Strait (Kimura, 1996
). Thus, due to the persistence of such an old strait, the population of L. longiflorum on Yaku Shima (LYA) seems to have been isolated from the other southern populations for a long time. Whereas the vicariant border between Tokuno Shima and Okinawa had scarcely been recognized based on the distribution patterns of organisms until the accumulation of recent molecular data regarding such species as Japanese newts, Cynops ensicauda (Hayashi and Matsui, 1988
), semi-aquatic annual ferns, Ceratopteris thalictroides (Watano and Masuyama, 1994
), wood-feeding cockroaches, Salganea taiwanensis (Maekawa et al., 1999
), and pit vipers, Trimeresurus flavoviridis (Toda et al., 1999
) exhibits considerable genetic differentiation between Okinawa and Tokuno Shima. Our results together with those regarding other organisms may suggest the possibility that another noticeable vicariant border limiting gene flow has long persisted between Okinawa and Tokuno Shima. At present, we do not know why the remaining major vicariant split exists between Iriomote Jima and the mainland of Taiwan, only that the separation of this region is assumed to have originated during a relatively late stage of the archipelago's development (Kimura, 1996
).
Population structure with respect to its relation to reproductive and breeding system, and geographic distribution of the two species
In general, the breeding system of flowering plant species greatly affects their GST values, e.g., outcrossed and mixed animal-pollinated species have 39 and 42% GST values of selfing species, respectively (Hamrick and Godt, 1990
). Most Lilium species including L. longiflorum secrete nectaries to attract pollinating insects (McRae, 1998
; M. Hiramatsu, personal observation), and L. longiflorum is generally regarded as self-incompatible (Miller, 1993
). These facts imply that L. longiflorum is an obligate outcrossed, insect-pollinated species. Nevertheless, the GST value of L. longiflorum (0.348) was 77% higher than that of the mean across 124 outcrossed, animal-pollinated species (0.197) and 61% higher across 60 mixed, animal-pollinated species (0.216) (Hamrick and Godt, 1990
). This shows conspicuously limited gene flow between L. longiflorum populations. The distribution of L. longiflorum ranges 1300 km between its northernmost and southernmost populations, but is disconnected in the manner of steppingstones (Fig. 1). Since the 19 populations treated in the present study are located widely across 14 different islands, it is highly unlikely that pollen transfer by insects and seed dispersal across the sea occurs for these populations.
The frequent occurrence of the loci with significant excesses of homozygous genotypes in some northern populations from Okinawa (LYA, LAM1, LAM2, LOE, LYR, LOK2, and LOK3) is also an unexpected result, because L. longiflorum is a putative self-incompatible, outcrossed species. Because of the lack of additional evidence, this result is difficult to interpret. For the moment, it could only be said that this is either because of the random drift of a small specimen as seen in Okinawa (LOK2 and LOK3), the relatively restricted gene flow of the metapopulation structure within a large population, or possibly the lack of random mating within a population, namely, the selfing of self-compatible individuals.
Likewise, the frequency of loci deviating significantly toward an excess of homozygotes varied between populations within L. formosanum and tended to be high in populations with relatively low percentages of polymorphic loci (Table 3). Lilium formosanum is generally recognized as self-compatible (Shii, 1983
; M. Hiramatsu, unpublished data). These facts thus indicate that facultative breeding occurs in L. formosanum, i.e., within some populations, outcrossing dominates, while selfing dominates within others. Selfing must play an important role, particularly in rapidly establishing new colonies from only single introductions, as described by Baker's law (Baker, 1955, 1967
; Stebbins, 1957
).
The GST value of L. formosanum (0.078) was 60% smaller than the mean of 124 outcrossed, animal-pollinated species and 64% smaller than the mean of 60 mixed, animal-pollinated species (Hamrick and Godt, 1990
). This shows frequent gene flow between populations. Unlike in L. longiflorum, L. formosanum populations are distributed solely on the mainland of Taiwan. Further, L. formosanum produces thinner seeds with a wider winged margin than those of L. longiflorum and has an advantage in natural seed dispersal by wind (Shii, 1983
; McRae, 1998
). Gene flow between the populations of the species, therefore, seems to be maintained by frequently repeated pollen flow by insects and seed dispersal by wind or human activities within Taiwan without a major restriction by the sea.
Conservational aspects
We are confident that natural populations of L. longiflorum and L. formosanum are gradually diminishing because of such human activities as robbery for horticultural purposes and developmental destruction on islands, even though they are exempted from inclusion in the red data book at present. From the viewpoint of conservation biology, our present study is quite educational; the diminishment of natural populations and genetic assimilation caused by reckless human activities will eventually erase the natural history written within the genes of these attractive lilies.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Crawford D. J. 1989 Enzyme electrophoresis and plant systematics. In D. E. Soltis and P. S. Soltis [eds.], Isozymes in plant biology, 146–164. Dioscorides Press, Portland, Oregon, USA
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———, T. F. Stuessy D. W. Haines M. B. Cosner M. Silva P. Lopez 1992 Allozyme diversity within and divergence among four species of Robinsonia (Asteraceae: Senecioneae), a genus endemic to the Juan Fernandez Islands, Chile. American Journal of Botany 79: 962-966[CrossRef][ISI]
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) and L. formosanum (
) populations studied. Closed areas of a small map are enlarged. Abbreviations of population names are the same as those in 