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Population Biology |
2Fonctionnement et Evolution des Systèmes Ecologiques, UMR 7625-CNRS, Ecole Normale Supérieure, 46, rue d'Ulm, F-75252 Paris Cedex 05, France; 3Fonctionnement et Evolution des Systèmes Ecologiques, UMR 7625-CNRS, bat A, 7ème étage, case 237, 7 Quai Saint Bernard, 75252 Paris Cedex 05, France
Received for publication March 14, 2002. Accepted for publication May 31, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: clonal diversity • fire • gene flow • Hyparrhenia diplandra • Poaceae • seed and pollen dispersal • spatial autocorrelation • tropical savannah
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). They can also lack vegetative propagation such as rhizomatous growth. Most of them occasionally reproduce sexually ("facultative agamosperms"; Asker and Jerling, 1992
). However, because of a low rate of sexual reproduction, gene flow through pollen dispersal is negligible most of the time. On the other hand, seed dispersal ability may strongly influence the population genetic structure in such species. Indeed, traits such as limited gene flow through pollen and seeds are known to have important consequences for the genetic structure of dense and continuous populations of several plant species (Epperson, 1993
).
When working on species with limited seed dispersal ability that form continuous populations, spatial autocorrelation methods based on Wright's (1943)
concept of isolation by distance are appropriate to study the population genetic structure at a small spatial scale (Heywood, 1991
; Epperson, 1993
). The concept of isolation by distance is defined as a monotonical decrease in the genetic similarity at neutral loci between individuals with increasing spatial separation. When gene flow is restricted within populations, patches of genetically similar individuals should be found. Moreover, the breeding system strongly affects the spatial structuring of genotypes: self-fertilization increases the potential for isolation by distance (Heywood, 1991
; Williams, 1994
). Most of all, in asexual species, isolation by distance should be very high and populations should be strongly differentiated into patches of one or a few different clones. Sexual reproduction events are very rare in agamospermous species. However, in several asexually reproducing species, genetic diversity has been shown to be much higher than previously thought, both within and among populations (Carter and Robinson, 1993
; Vasseur, Aarssen, and Bennett, 1993
; Hsiao and Rieseberg, 1994
; Noyes and Soltis, 1996
). This paradoxical situation has been reported in numerous agamospermous species (Ellstrand and Roose, 1987
). However, to our knowledge, no attempts to link seed dispersal ability to the genetic diversity of agamospermous species populations are recorded in the literature.
Here, we present a study of the effect of agamospermy and seed dispersal ability on the population genetic structure at different spatial scales of the grass species, Hyparrhenia diplandra (Poaceae). Hyparrhenia diplandra is the dominant species of West African savannahs, its populations are dense and continuous, and this species is a facultative agamosperm with rare events of sexual reproduction (sexual reproduction rate, u = 0.0056; Durand et al., 2000
). In the vast majority of cases, seeds therefore have the same genotype as their maternal plants and are forming a clone. Furthermore, primary seed dispersal is very low: seeds travel distances of about a meter away from the maternal plant (Garnier and Dajoz, 2001b
). Savannahs where H. diplandra is found are burned every year, and fire frequency and intensity are known to play a critical role in the structure and the long-term persistence of plant populations (Whelan, 1995
; Garnier and Dajoz, 2001a
). Furthermore, clones of H. diplandra differ in their diaspore morphology: those with short-awned diaspores have better seed survival and germination rates in conditions where fire is infrequent and/or not very intense, whilst those with long-awned diaspores survive better when fire is frequent and/or very intense (Garnier and Dajoz, 2001b
). This is because awn length determines seed burial depth into the soil, and the soil depth range where lethal temperatures for seeds are recorded varies with fire intensity (Garnier and Dajoz, 2001b
). Therefore, variations in fire intensity may be important for the maintenance of clonal diversity, because the mortality rate of seeds issued from the different clones varies according to this fire intensity. Few studies have been carried out on the population structure of species growing in fire-prone habitats (Krauss, 1997
). In this clonal species, we predicted that (1) isolation by distance should be easily detected within populations and should occur within very short distances if there is no secondary seed dispersal; (2) if seed dispersal is restricted, maternal lineages should be fixed in place, resulting in a patchy clonal structure within populations, and; (3) this patchy clonal structure should be maintained by environmental factors such as fire frequency and intensity. In this study, we analyzed the genetic diversity and distribution of clones and thus the macro and microspatial population structure of H. diplandra. To explore the consequences of seed dispersal ability on the population genetic structure at different spatial scales, we added to the use of nuclear DNA markers a chloroplast DNA marker, which is maternally inherited in angiosperms (Palmer, 1987
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Garnier and Dajoz [2001b]
for a detailed site description). At the Lamto Research Station (Ivory Coast), H. diplandra is the dominant grass species and represents 80% of the total herbaceous biomass (Menaut and César, 1979
). Hyparrhenia diplandra grows in densely packed tussocks but as there is no underground vegetative reproduction, dispersal can only occur through seeds and/or pollen. The fruit dispersal unit is a diaspore containing one seed and ornamented with a long and robust hygroscopic awn (Jacques-Felix, 1962
) that effects seed burial (Garnier and Dajoz, 2001b
). Diaspores are mature in early December. Germination occurs after the annual fire and the first rains of January–March (see Garnier and Dajoz, 2001a
for a complete description of the species life cycle).
Sampling procedure
In July 1998, during vegetative growth, two 10 x 10 m2 quadrats separated by at least 30 m (Q1 and Q2) were chosen at random in one population of the Lamto savannah. All H. diplandra individuals were mapped precisely in each quadrat in order to perform spatial autocorrelation analyses. Samples of young leaves (length = 5–6 cm; dry mass = 10–20 mg) were collected at the base of the sheath of each individual (N = 171 in Q1 and N = 246 in Q2) with a basal diameter of at least 5 cm.
DNA extraction and microsatellite analysis
All samples were oven dried at 65°C for 48 h immediately after collection and kept for several months at room temperature before DNA extraction. Total DNA was extracted following Doyle and Doyle's (1987)
rapid procedure. Two nuclear loci were used (Hd1 and Hd2, which have been described in a previous study, Durand et al., 2000
). One chloroplast locus was used for quadrat samples (HdcpA). This locus amplifies at (AA)n dinucleotide repeats. Amplification of the cpDNA was performed using either a TB1 (Biometra, Göttingen, Germany) or a PCT 100 (MJ Research, Waltham, Massachusetts, USA) thermocycler. Each polymerase chain reaction (PCR) was conducted in 0.4 µmol/L of each primer, 200 µmol/L dCTP-dGTP-dTTP, 5 µmol/L dATP, 0.025 µCi/µL 
-33Q-dATP, 50 mmol/L KCl, 10 mmol/L Tris-HCl pH 9.0, 1.5 mmol/L MgCl2, 0.01% Triton X-100, 0.01% gelatin, 1 unit Taq polymerase. Amplification was proceeded by, first, a denaturing step at 94°C for 5 min followed by 35 cycles at 94°C for 1 min, 56°C or 60°C for 1 min, and 72°C for 1 min. A final extension was carried out at 72°C for 5 min. Annealing was carried out at 55°C for locus HdcpA. Amplification products were denatured in 40% formamide for 5 min at 95°C and run on a sequencing gel using a M13mpl18 plasmid sequence as a molecular weight scale.
Gene diversity and F statistics
We first used a classical infinite island model (Wright, 1951
) in order to estimate the genetic differentiation. Statistical analyses were conducted using the GENEPOP version 1.2 software (Raymond and Rousset, 1995
). For quadrat 1 and 2 and for each locus, allelic frequencies, observed heterozygosity (HO), and expected heterozygosity (HE) were calculated. Values of FST were estimated following the Weir and Cockerham (1984)
model for diploid data, because a previous study had shown that H. diplandra is an allotetraploid species with a transmission of alleles similar to that found in diploid species (Durand et al., 2000
). To estimate the genetic differentiation at different spatial scales, each quadrat was divided into 4 and 16 squares of 25 m2 and 6.25 m2 area, respectively. When quadrats were divided into four squares, the number of individuals in each square was found to be similar in quadrat 1 (Q1), between 36 and 44 tussocks, and in quadrat 2 (Q2), between 50 and 69 tussocks. When quadrats were divided into 16 squares, much more variation in the number of individuals per square was apparent: in Q1, this number ranged from 3 to 19 tussocks and in Q2, from 9 to 22 tussocks. The tussock distribution was uniform in both quadrats with a mean (standard deviation) density of 3.13 (1.74) tussocks/m2 in Q1 and 4.00 (1.94) tussocks/m2 in Q2 (Durand et al., 2000
). In each quadrat, FST values were calculated among the 4 squares and among the 16 squares. The two quadrats were also compared using the FST. The FIS indices were not calculated because they are not statistically appropriate when studying an agamospermous species: indeed, in both quadrats, some genotypes represented half of the individuals. For example, in Q1, most individuals were homozygous, thus calculation of FIS indices may have greatly overestimated the heterozygous deficiency.
Spatial genetic structuring within populations
We applied spatial autocorrelation analysis on the microsatellite data from quadrats Q1 and Q2 (Sokal and Oden, 1978a
, b
). Spatial autocorrelation measures the dependence of a character at each location with the character values at other nearby locations, with no assumptions on the scale of the spatial patterns. We considered that H. diplandra transmitted its alleles like a diploid species (Durand et al., 2000
). Alleles with a frequency of less than 5% were not used in the analysis. The genetic data were obtained at each nuclear locus in the following way: each individual was assigned a frequency value of 0.0 (allele not present), 0.5 (two different alleles at the locus: heterozygosity), or 1.0 (same allele at the locus: homozygosity), for all alleles whose frequency was higher than 5%. Seven individuals with three alleles at locus Hd2 and one individual with four alleles at the same locus were not included in the analysis. In Q2, since there were three alleles at the chloroplast locus and one had a frequency less than 5%, the autocorrelation analysis was conducted for only one allele (the other one would offer identical information). The chloroplast genome is haploid so each individual was assigned a frequency value of 0.0 or 1.0 depending on the presence or absence of the allele. The resulting data were analyzed using SAAP version 4.3 (Wartenberg, 1989
), which calculates Moran's coefficient of spatial autocorrelation (I). In both Q1 and Q2, eight distance intervals were considered: 0–<0.5 m, 0.5–<1 m, 1–<1.5 m, 1.5–<2 m, 2–<4 m, 4–<6 m, 6–<8 m, and 8–14 m. For each distance interval, Moran's I was computed (Sokal and Oden, 1978a
). Moran's I varies between –1 and +1 and its expected value is given by E(I) = –1/(n – 1) with n = the total number of individuals in the sample (Sokal and Oden, 1978a
). Departures from the expected value of I for each distance class were tested for each allele by SAAP version 4.3. Overall statistical significance of the correlograms was assessed using Bonferroni's corrected P values (Sakai and Oden, 1983
).
Clonal diversity
We also used ecological indices to measure clonal diversity following Ellstrand and Roose (1987)
. In both Q1 and Q2, we used "the proportion distinguishable" (Ellstrand and Roose, 1987
, p. 125); to measure clonal diversity. G/N, where G is the number of genotypes and N the number of individuals sampled in the population, defines this statistic. The number of alleles found at the three loci used varies between two and six (Table 3), which gives a fairly low probability of considering two genetically different individuals as identical. We also used Pielou's (1969)
corrected version of the Simpson's index, which summarizes clonal diversity. This index gives the probability that two plants selected at random from a population of N plants will have different genotypes:
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 123.93, P = 0.0001; Fig. 1B). In both quadrats, the genetic diversity (i.e., expected heterozygosity) was high, varying between 0.61 and 0.69 (Table 3). The linkage disequilibrium was significant between the nuclear loci in both quadrats (P < 10–5) showing that few recombination events occurred, which was suspected in this agamospermous grass.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Spatial genetic structure
Spatial autocorrelation analysis showed that on average individuals of H. diplandra located within a 5 m diameter were more genetically similar to each other than they were to plants beyond that distance. Moreover, the genetic differentiation within quadrats when divided into 4 squares of 25 m2 or 16 squares of 6.25 m2 was substantial when studied with the nuclear and chloroplast genetic markers. However, between quadrats, the genetic differentiation was extremely high (FST = 0.417) when studied with the chloroplast locus and relatively low (FST = 0.0895, 1 SD = 0.037, although significantly different from 0) when using the nuclear loci. The FST value for the chloroplast locus was nearly five times greater than that of the nuclear loci. These results suggest that gene flow by pollen transfer may occur rather frequently between quadrats, but that seed flow is rare between them. This gene flow is very unlikely due to rapid mutation of one (or some) of the microsatellite loci, since in the populations studied, the alleles found in the progeny issued from sexual reproduction events are the same as the ones found in the adult plants. Recent studies have also reported a greater genetic structuring of maternally inherited genomes than co-parental nuclear ones (McCauley, 1994
, 1998
; Tarayre et al., 1997
). Furthermore, the dissemination rate of nuclear genes by both pollen and seeds may be higher than for chloroplast genes that are only dispersed by seeds (McCauley, 1995
). Our results also show this same trend. However, we also confirm that gene flow by seed dispersal is very restricted in H. diplandra. Diaspores of this species possess no adaptation for secondary dispersal processes by animals (L. K. M. Garnier, personal observation). Seeds fall straight to the ground, are subsequently rapidly buried, and thus, stay within the neighborhood of their mother plant (1 m on average; Garnier and Dajoz, 2001b
). Surprisingly, patches of plants showing significant isolation-by-distance patterns formed clonal groups approximately 5 m in diameter. However, we suggest that the size of a clonal patch may increase because of the asexual reproduction and localized seed dispersal of the clonal progenies located at the neighborhood of their mother plant.
Because there is only very limited gene flow via seeds in H. diplandra, long-distance gene flow may only occur through long-distance wind pollination. Long-distance pollen dispersal has been reported for wind-pollinated species (Bos, Harmens, and Vrieling, 1986
) and in particular for grass species (Wagner and Allard, 1991
; Nurminiemi et al., 1998
). Unequal dispersal of pollen and seeds has been recorded in many species (Ennos, 1994
). In oaks, pollen may disperse over distances 200 times greater than seeds, whilst in wild barley, pollen dispersal is only 4 times greater than seeds (Ennos, 1994
; Streiff et al., 1998
). According to Ennos (1994)
, the ratio of pollen over seed flow in H. diplandra is 5.27, very similar to the situation observed in wild barley. However, in barley, Wagner and Allard (1991)
found that pollen could disperse up to distances of 60 m.
The importance of pollen dispersal in determining the genetic structure of H. diplandra populations is a surprising result because in an agamospermous species, pollen dispersal is expected to be negligible (Heywood, 1991
). However, the rather low genetic differentiation between quadrats and among populations recorded using nuclear markers (Durand et al., 2000
) can only be explained by long-distance pollen dispersal in this species.
The study of the microspatial genetic structure using both nuclear and chloroplast genomes also revealed differences in the spatial pattern of genotype distribution between quadrats. Our data obtained from Q1 showed a high diversity of nuclear genotypes whereas only one chloroplast genotype was found in the vast majority of individuals. Tarayre et al. (1997)
have argued that local chloroplast differentiation may be maintained for longer periods of time than nuclear differentiation because of higher gene flow via pollen. We may thus hypothesize that the differences in the patterns of spatial distribution exhibited by nuclear and chloroplast genomes in Q1 not only provide evidence for gene flow through pollen occurring during events of sexual reproduction in H. diplandra, but also reveal variation in the genetic structure over time. In the past, a single clone might have colonized the quadrat, and because of pollen flow and the occurrence of sexual reproduction, the nuclear genotypes might have evolved conversely to the chloroplast ones. Thus, in H. diplandra, the relatedness among neighboring individuals is due probably more to restricted seed dispersal than to a decrease in gene flow (via pollen and seed) with increasing distance (Heywood, 1991
).
Sources of spatial genetic variation
Breeding system
Hyparrhenia diplandra populations exhibited high genetic (high heterozygosity rates) and clonal diversity (diversity indices). Also, as in many other clonal species, multiple clones occurred within the quadrats studied (Carter and Robinson, 1993
; Vasseur, Aarssen, and Bennett, 1993
; Hsiao and Rieseberg, 1994
; Montalvo et al., 1997
). Total clonal diversity index (0.85) in H. diplandra was comparable to the one found in other nonagamospermous Poaceae species such as Festuca rubra (0.76) and in some non-Poaceae agamospermous species (Ellstrand and Roose, 1987
). To explain this unexpected clonal diversity, many authors have suggested that in asexual plant species, and particularly in agamospermous ones, the rate of sexual reproduction must have been underestimated (Ellstrand and Roose, 1987
; Asker and Jerling, 1992
; Carter and Robinson, 1993
; Noyes and Soltis, 1996
). A small amount of sexual recruitment could maintain the genetic diversity in clonal species (Watkinson and Powell, 1993
). In a previous study (Durand et al., 2000
), we showed that H. diplandra produced few sexually obtained seeds (u = 0.0056) either through selfing (60% of all fertilisations) or outcrossing. Thus, the occurrence of a little sexual reproduction in H. diplandra might create and maintain (through apomixis) a high genetic diversity in this clonal species. Another key factor that maintains high genetic diversity is the very low dispersal ability of seeds that leads to the occurrence of patches of plants belonging to the same clone over short distances. Extensive pollen flow could act as an homogenizing factor and might disrupt patches of clones produced by low seed dispersal. But, surprisingly, the relative importance of pollen flow in this species does not appear very different from species with sexual reproduction and high outcrossing rate (Montalvo et al., 1997
; Gehring and Delph, 1999
). This shows that patterns of seed dispersal in H. diplandra are mainly responsible for the clear isolation-by-distance patterns recorded here.
Role of fire
Several authors have suggested that clonal diversity could be maintained by environmental heterogeneity that permits coexistence of clones through diversifying selection (Burdon, 1980
; see also Asker and Jerling, 1992
). Fire is a common phenomenon in savanna ecosystems (Frost and Robertson, 1985
). In a previous study, we showed that fire intensity (i.e., soil temperature elevation) significantly varied between different years in Lamto savanna (Garnier and Dajoz, 2001b
). Furthermore, we observed that, each year, some patches of savanna are left unburned (L. K. M. Garnier, personal observation). Thus, after a fire, Lamto savanna is constituted of a patchwork of unburned and burned areas that may or may not burn in the following year, an observation that joins Frost and Robertson (1985)
views: when fires are less intense, they burn more patchily. The proportion of unburned biomass determines future fire intensity (Whelan, 1995
); therefore, the spatial heterogeneity of fire and its temporal dynamics may greatly influence future fire intensities.
Clones of H. diplandra differ in their diaspore morphology: long-awned seeds are buried deeper into the ground than short-awned ones and survive better when fire is frequent and/or very intense, whilst short-awned diaspores have better seed survival and germination rates in conditions where fire is infrequent and/or not very intense (Garnier and Dajoz, 2001b
). Since awn length variation is highly heritable (Garnier and Dajoz, 2001b
), the nondirectional selective pressure induced by fire intensity variations selects for different awn lengths and therefore different clones of H. diplandra. That may thus contribute to the maintenance of high clonal diversity. However, we might also hypothesize that some clones have been consistently selected for from one year to another and that their spatial distribution is the result of their expansion through apomixis. Clones showing isolation-by-distance patterns might thus be in a phase where they have an advantage caused by environmental conditions. In sum, the mating system coupled with the unpredictable dynamics of fire may be one of the main factors acting on the genetic structure of H. diplandra populations in the long term.
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FOOTNOTES |
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4 Author for reprint requests (lisa.garnier{at}wanadoo.fr
)
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