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Population Biology |
2Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina; 3Instituto de Botánica Darwinion, Labardén 200, 1642 San Isidro, Buenos Aires, Argentina
Received for publication July 16, 2002. Accepted for publication August 5, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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Key Words: Acacia • Argentina • Fabaceae • genetic variability • isozymes • mating system parameters • population structure
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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; Ross, 1981
). Australia is the main center of Acacia species diversity, and most genetic variability analyses include species from this continent, providing useful information for domestication, breeding programs, and genetic resource conservation (Moran et al., 1989a
, b
; Muona et al., 1991
; Joly et al., 1992
; Playford et al., 1992
, 1993
; Sedgley et al., 1992
; Fagg et al., 1997
; McGranahan et al., 1997
; Butcher et al., 1998
).
In Argentina the genus is represented by 21 species. Two of them, A. aroma Hook. et Arn. and A. macracantha Willd., are widely distributed in northern and central Argentina (Cialdella, 1984
) because they can tolerate dryness and eroded soils. Both are economically important and promising multipurpose species for agroforesty programs (Dimitri and Biloni, 1973
; Allen and Allen, 1981
; Cialdella, 1984
; Martínez et al., 1996
). The only study on population genetics of Argentinean species of Acacia indicated that A. aroma and A. macracantha are closely related (Casiva et al., 2002
). While data on their genetic structure is just beginning to emerge, little information is avaliable on their mating systems. Mating system analysis in other species of Acacia have shown high levels of outcrossing, sometimes together with self-incompatibility systems, and some species are able to form a hybrid complex (Ali and Qaiser, 1980
; Bernhardt et al., 1984
; Kenrick and Knox, 1985
; Kenrick et al., 1986
; Moran et al., 1989b
; Sedgley et al., 1992
). Studies on the reproductive biology of A. caven from Chile and Argentina showed that this species is protogynous and has a self-incompatibility system (Peralta et al., 1992
; Baranelli et al., 1995
). Analyses of floral morphology and breeding systems in A. aroma and A. macracantha suggested that they are also outcrossers and self-incompatible, when bees, Trigona testaceicornis, Metadontia sp., and Allograpta sp. are considered as the main pollen vector (Zapata and Arroyo, 1978
; Bernhardt et al., 1984
) but mating system parameters have not been studied in these species.
An efficient method to evaluate mating system parameters in natural populations is based on the multilocus mixed mating model and the estimation procedure of Ritland and Jain (1981)
. The method requires grouping the population samples in family arrays and using neutral codominant loci that segregate independently. In the present case, we chose isozyme markers because they fulfill these requirements and give information about the genetic structure and distribution of genetic variability at population and species levels.
Here we tested the hypothesis that A. aroma and A. macracantha are outcrossers, estimated the distribution of genetic diversity, and evaluated the effect of sympatry on the genetic differentiation between populations of different species.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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). The main difference between these species is the length and shape of their thorny stipules. In A. aroma they are 0.80 ± 0.50 cm long (mean ± SD) and conical and circular in cross section, while in A. macracantha they are 1.67 ± 0.79 cm long and laterally compressed and rhomboidal in cross section. No genetic differentiation has been found between these species (Casiva et al., 2001b
, 2002
).
Three populations of A. aroma and two populations of A. macracantha were collected in Argentina (Fig. 1, Table 1). Thirty to 50 pods were collected from at least 10 trees separated from each other by more than 50 m following the method of Vilardi et al. (1988)
and Saidman and Vilardi (1993)
for legumes of genus Prosopis. All seeds (300–500) from each shrub were placed in a single bag from which they were chosen at random for isozyme analysis of progeny arrays.
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). For ADH, we analyzed 12–18-h-old seedlings and used distilled water as the extraction buffer. Buffers and electrophoretic conditions for all systems are outlined in Saidman (1985)
, Saidman and Vilardi (1987)
, and Casiva (2001)
. We used progeny arrays of open-pollinated families to infer genetic control of each enzyme system. Alleles within loci were indicated with superscript numbers with respect to their mobility relative to bromophenol blue, with "1" denoting the fastest allozyme. Bands that did not conform to Mendelian-segregation patterns were omitted from the analysis. For mating system analysis, we chose five polymorphic loci (SOD-1, SOD-3, SOD-4, 6PGD-2, and SKD-1) because they could be evaluated simultaneously in each individual (seed).
Data analysis
We used the program Biosys-1 (version 1.7) (Swofford and Selander, 1981
) to calculate allelic frequencies, mean number of alleles per locus (A), percentage of polymorphic loci (Pp, 0.95 criterion), and unbiased expected heterozygosity (He; Nei, 1978
) in the populations sampled at Tipas. The estimates of He, A, and Pp of the populations sampled at Campo Quijano and Huilla Catina had been previously reported in Casiva et al. (2002)
. Wright's (1951)
fixation index (FIS) was estimated for all five populations using the same program. We used this parameter to estimate the bias from Hardy-Weinberg expectations. Nei's (1978)
genetic distances among all populations were represented in a UPGMA phenogram (Sneath and Sokal, 1973
). Using the method of Sokal and Rohlf (1962)
, we estimated the cophenetic correlation coefficient. Bootstrap support values of each phenogram branch were obtained using PHYLIP (Felsenstein, 1993
). The phenetic relationships among populations were also represented by multidimensional scaling using the program STATISTICA (StatSoft, 1995
).
The mean expected heterozygosity was calculated at the population level (HP), species level (HC), and for the whole sample (HT). We performed a hierarchical analysis of population structure (Wright, 1978
), considering variation within populations (1 – FST), among populations, within species (FST – FCT) and between species (FCT). These statistics were estimated according to Nei (1987)
as FST = 1 – HS/HT; FCT = 1 – HC/HT; FSC = 1 – HS/HC.
To test isolation by distance between populations and species, we compared the matrix of Nei's genetic distances with that of geographic distances among populations. The latter was estimated using the measurement tool of Encarta World Atlas (Microsoft 1995–1996
). The significance of that correlation was estimated with Mantel's (1976)
test using the ISOLDE program in the GENEPOP package (Raymond and Rousset, 1995
).
Using MLTR 2.2 (Ritland, 2002
), we calculated the following mating system parameters: multilocus outcrossing rate (tm), single locus outcrossing rate (ts), correlation of outcrossed paternity (rp), correlation of tm between progeny arrays (rt), and fixation index of maternal parents (FISM). Because the mixed mating model assumes independent segregation of alleles at different marker loci, we tested possible genotypic association among loci using GENEPOP (Raymond and Rousset, 1995
). This method performs a probability test (or Fisher exact test) for each contingency table using a Markov chain.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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genetic distances and represented in two ways, a UPGMA tree and a multidimensional scaling (MDS) plot (Fig. 2). Genetic distances among populations were low, from 0.004 between populations from Tipas to 0.048 between A. macracantha from Tipas and A. aroma from Huilla Catina. The UPGMA tree showed little distortion from the original distance matrix (cophenetic correlation = 0.90). Both intraspecific and interspecific clusters were formed (Fig. 2A). The closest populations (Tipas) belong to different species, whereas A. aroma from Huilla Catina and Campo Quijano are separated from A. macracantha from Campo Quijano. The MDS plot (Fig. 2B) is consistent with the tree. Dimension 1 associates both populations from Tipas and both populations from Campo Quijano. There is not consistency between the groups in the MDS and the morphological determination.
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and geographical distance was not significant (P = 0.62) according to Mantel's (1976)
test (Table 5).
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The single locus inbreeding coefficient of maternal parents (FISM) was in all cases lower than that estimated for their offspring (Tables 3, 7). In A. aroma (Tipas) FISM was negative, indicating some heterozygosity excess in the maternal plants. For the other four populations, FISM was near zero, suggesting no Hardy-Weinberg deviations in the populations.
In most populations, significant differences were observed for several loci between pollen and ovule allelic frequencies (confidence intervals of estimated frequencies do not overlap) (Table 8).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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; Joly et al., 1992
). For Argentinean species of Acacia, Casiva et al. (2002)
obtained estimates of H ranging from 0.036 to 0.238 for isozyme loci and from 0.045 to 0.121 for RAPD markers. The populations studied here and those belonging to A. aroma and A. macracantha studied by Casiva et al. (2002)
had similar variability. The available information suggest that Argentinean populations of these species would have high levels of genetic variability. No significant departures from Hardy-Weinberg expectations were found in these populations, suggesting that they mate at random.
In the hierarchical analysis, we found no differences among species, and the most variability occurred within populations. These results agree with the predictions of Hamrick and Godt (1990)
that plant species, on average, maintain high levels of allozyme variation within populations. This same pattern was observed by Playford et al. (1993)
in populations of Acacia melanoxylon, for which most of the genetic diversity was found within populations. However, they found a high level of genetic patterning in the species and a strong differentiation among populations and geographic zones. Although in other studies on Acacia geographical patterns of differentiation of populations was found (Brain, 1986
; Joly et al., 1992
; Playford et al., 1993
), we found no geographic isolation and no genetic differentiation between species, suggesting a wide area of distribution of the allelic variants among all populations of these species. In all the studied populations of A. aroma and A. macracantha, polymorphic loci had the same allelic variants. Seed dispersal by livestock and/or human activity may explain the lack of correlation between genetic distances and geographic distances.
The FCT index indicated no significant differences between species. The high similarity was also revealed by Nei's genetic distances. The UPGMA phenogram and the MDS plot showed a similar trend, i.e., the populations are not grouped as expected according to morphological determination. The small genetic distance between these two taxa was also noticed previously by Casiva et al. (2002)
. In fact, the distances recorded between populations belonging to these species are as low as those corresponding to conspecific populations of other Acacia species (e.g., A. caven; Casiva et al., 2002
) or populations of some species of the mimosoid genus Prosopis that belong to a syngameon (see Saidman and Vilardi, 1987
).
The levels and distribution of genetic variability may also be related to mating system (Hamrick and Godt, 1990
). Mating system analysis showed high levels of outcrossing in all populations studied in our work. On average, only 2% of progeny would result from selfing. The small differences between tm and ts and the differences between pollen and ovule allelic frequencies are consistent with the lack of biparental inbreeding. The rp values suggest that individuals within progeny arrays are full rather than half sibs. This pattern could be a consequence of hierarchical mating, previously noted for Acacia species (Muona et al., 1991
). This is the result of the composite pollen grains, which are distributed in polyads. The number of pollen grains per polyad varies among Acacia species, with four, eight, 16, and 32 grains per polyad (Vassal, 1972
; Guinet and Vassal, 1978
; Cialdella, 1984
). A correlation between polyad grain number (pgn) and maximum pod seed number (mpsn) was suggested by Kenrick and Knox (1982)
, who observed that pgn 
mpsn and proposed that polyads in Acacia could be a mechanism helping to ensure seed set following a single pollination event (a single polyad fertilizing all available ovules at a single ovary). However, A. macracantha might be an exception to the predictions of Kenrick and Knox (1982)
. In fact, although both A. aroma and A. macracantha have 16 pollen grains per polyad, A. aroma presents 6–16 seeds per fruit and A. macracantha pods may have as many as 20 seeds (Cialdella, 1984
). Therefore, in A. macracantha two pollination events might be involved in some single pods.
Nonrandom pollination between pods may also occur because flowers are grouped into clusters, which often form parts of a complex raceme. Because all flowers within a cluster often open simultaneously, the probability that the same insect pollinates several flowers with polyads from the same paternal tree may be high (Muona et al., 1991
). Because we sampled randomly seeds from different pods, the high proportion of full sibs in our sample suggests that pollinating insects tend to visit many flowers in the same shrub before moving to a different plant.
Based on the results from our study of mating system parameters, we can reject selfing as a mechanism of isolation between these sympatric entities. The high variability observed by Casiva et al. (2002)
and the present estimates of He and tm indicate that these species are outcrossers.
The actual relationships between A. aroma and A. macracantha are under debate. The morphological criteria differ between authors. According to Cialdella (1984
, 1997
) and Casiva et al. (2002)
, the most important characters for morphological differentiation are the shape and length of the thorny stipules. On the other hand, Ebinger et al. (2000)
hold that A. aroma and A. macracantha could be differentiated by fruit and petiolar gland morphology. However, in Argentinean material we observed variation in fruit morphology within individuals, the range of peduncle length in both species overlaps, and both species have sessile petiolar glands. The biochemical evidence is also intriguing. Lamarque et al. (2000)
found that seed chemical components (moisture, fat, protein, ash, and fatty acid profiles) permit separation of A. aroma from A. macracantha. On these grounds, they support recognition of two distinct species. However, the associations among species obtained from morphology by Cialdella (1984
, 1997)
and from isozymes and RAPDs by Casiva et al. (2002)
differ from those obtained by Lamarque et al. (2000)
.
The high genetic similarity between A. aroma and A. macracantha is not expected for different biological species. The hierarchical analysis indicated absence of differentiation between them. The low estimates of genetic distances are compatible with very short divergence between these entities (see Nei, 1987
). Indirect estimations of gene flow suggested that these species are able to exchange genes (Casiva et al., 2001a
, 2002
). The outcrossing system is not compatible with sympatric speciation if the species undergo significant gene flow.
Casiva et al. (2002)
advanced three possible hypothesis: (1) A. aroma and A. macracantha may be varieties of a single species, (2) they may be members of a single species where thorny stipule shape and length are determined by a few linked loci, or (3) they are different species that diverged very recently and have yet to accumulate significant genetic differences. The geographical range together with the present results on the mating system constitute evidence against the possibility that A. aroma and A. macracantha are varieties or subspecies unless they could be isolated by different pollen vectors. In Venezuelan populations of A. macracantha, Trigona testaceicornis, Metadontia sp., and Allograpta sp. are described as pollinators (Zapata and Arroyo, 1978
), but no information is available for A. aroma. Entomological studies in Argentinean populations showed no differences in the insect fauna hosted by both species (Di Iorio, in press
). According to Cialdella (1984)
and to our field observations, they are sympatric and their flowering and fruiting periods overlap. Because interspecific Nm estimates are high and the hierarchical analysis does not provide evidence of isolation between these entities, the present results rule out hypothesis 1. Because the morphological differences between these species refer to a single trait (thorny stipule), the condition resembles that of Prosopis glandulosa for which a polymorphism was described for the presence of the nectarium (Golubov et al., 1999
). Although hypothesis 3 cannot be ruled out, the lack of genetic divergence between A. aroma and A. macracantha favors the hypothesis that they may be a single polymorphic species.
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FOOTNOTES |
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LITERATURED CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURED CITED |
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