Journal of Heredity Advance Access originally published online on September 18, 2006
Journal of Heredity 2006 97(5):466-472; doi:10.1093/jhered/esl031
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Internal Genetic Structure and Outcrossing Rate in a Natural Population of Araucaria angustifolia (Bert.) O. Kuntze
From the Departamento de Fitotecnia, Núcleo de Pesquisas em Florestas Tropicais, Universidade do Estado de Santa Catarina, 88520-000 Lages, Brazil (Mantovani); the Departamento de Botânica, Grupo de Fenologia de Plantas e Dispersão de Sementes, Universidade Estadual Paulista, Instituto de Biociências, Caixa Postal 199, 13506-900 Rio Claro, Brazil (Morellato); and the Departamento de Fitotecnia, Núcleo de Pesquisas em Florestas Tropicais, Universidade Federal de Santa Catarina, Caixa Postal 476, 88034-000 Florianópolis, Brazil (dos Reis)
Address correspondence to A. Mantovani at the address above, or e-mail: mantovani{at}cav.udesc.br.
The internal genetic structure and outcrossing rate of a population of Araucaria angustifolia (Bert.) O. Kuntze were investigated using 16 allozyme loci. Estimates of the mean number of alleles per loci (1.6), percentage of polymorphic loci (43.8%), and expected genetic diversity (0.170) were similar to those obtained for other gymnosperms. The analysis of spatial autocorrelation demonstrated the presence of internal structure in the first distance classes (up to 70 m), suggesting the presence of family structure. The outcrossing rate was high (0.956), as expected for a dioecious species. However, it was different from unity, indicating outcrossings between related individuals and corroborating the presence of internal genetic structure. The results of this study have implications for the methodologies used in conservation collections and for the use or analysis of this forest species.
Studies related to population genetics have helped to provide important assumptions regarding conservation strategies and the regeneration of forests (Bawa 1992; Kitamura and Rahman 1992; Nason and Hamrick 1997; Petit et al. 1998), as well as the elaboration of management strategies (Bawa et al. 1993; Reis et al. 2000). The number of studies related to population genetics and its practical application in forest species is large (e.g., Kitamura and Rahman 1992; Eguiarte et al. 1993; Kaufman et al. 1998; Reis et al. 2000; Mariot et al. 2002), allowing us to infer gene flow, effective population size, and genetic diversity. Information of this nature can assure the better use of the available genetic resources, maximizing the potential responses from germplasm banks or preserved natural populations (Petit et al. 1998).
Many tree species are characterized by high genetic diversity (Hamrick et al. 1992). This diversity is shown by sampling different populations, characterizing the genetic structure in the quantity of variation among and within populations, normally by including a large area of occurrence (e.g., Kitamura and Rahman 1992; Delgado et al. 1999; Reis et al. 2000; Ritland et al. 2001; Auler et al. 2002; Mariot et al. 2002). Studies have established that most of the genetic variation is distributed within populations (Reis et al. 2000; Auler et al. 2002), and in many cases, the internal distribution is not random due to the limited dispersion of pollen and seeds or selection of microhabitat (Loveless and Hamrick 1984; Heywood 1991; Seoane et al. 2001). This therefore promotes structuring of genetic variation within populations.
The presence of genetic structure within populations has important implications for improvement and conservation programs as it can affect estimates of genetic parameters, such as the outcrossing rate in natural populations (Ennos and Clegg 1982), influencing the sampling strategies for improvement or conservation projects ex situ, and aid in the management of populations, where the exploitation patterns can affect the quantity of genetic diversity (Doligez and Joly 1997).
The Mixed Ombrophilous Forest or Araucaria Forest is one of the Brazilian forest types that is most affected by deforestation and is currently made up of only 2–4% of its original area (Guerra et al. 2002). This forest originally occupied around 200 000 km2, a large part of the southern region of Brazil and disjunct areas of the southeast (Golfari 1971). Araucaria, Araucaria angustifolia (Bert.) O. Kuntze (Araucariaceae) has an important role in this typology as it is one of the determinants of its phytophysionomy, occupies the upper stratum of the forest, and has a high density. However, because of its high economic value, it has been intensely exploited and is in the vulnerable category on the endangered species list (Varty and Guadagnin 1999).
The first studies to consider genetic aspects of A. angustifolia focused on genetic variation between origins and progenies, through quantitative characters, indicating an important variation between origins (Gurgel-Filho 1980; Kageyama and Jacob 1980; Shimizu and Higa 1980). More recent studies, using allozyme markers, have revealed high genetic diversity, most of which is found within populations (Shimizu et al. 2000; Sousa 2000; Auler et al. 2002). However, there are as yet no studies that evaluate the internal genetic structure in natural populations of araucaria.
Thus, the objective of this study was to analyze the internal genetic structure of a natural population of A. angustifolia, as well as its outcrossing rate, using allozyme markers.
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Materials and Methods |
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Study Area
This study was carried out in an area of naturally occurring araucaria (Araucaria angustifolia [Bert.] O. Kuntze—Araucariaceae) located in Campos do Jordão-SP. The area was exploited more than 45 years ago and, since then, has been transformed into a Conservation Unit. The area belongs to the Parque Estadual de Campos do Jordão do Instituto Florestal do Estado de São Paulo and is located in the Mantiqueira Mountain Range (22°45'S and 45°30'W) at an altitude of 1450 m, with an area of 834 186 ha. According to the Koeppen classification, the climate of the region is subtropical highland climate, mesothermic, and humid, with no dry season and an annual rainfall of 2000 mm.
Sampling and Laboratory Procedure
In the study area, was a 10-ha plot in which all the reproductive individuals of araucaria were mapped through georeferenced points. Individuals were numbered with aluminum plates. We collected leaf samples of the 334 reproductive individuals of A. angustifolia in the study area and of the 420 progenies originating from 14 maternal trees (30 individuals per maternal tree). Genetic characterization was carried out using allozyme markers, according to the methodology of Kephart (1990) and Alfenas et al. (1991). For the migration of the enzymes, we used gels prepared with 13% hydrolyzed starch (Penetrose 30). For the extraction of the enzymes, we used leaf tissue that was ground in a mortar using extraction solution 1 of Alfenas et al. (1991). We prepared the gels in horizontal tanks that were submitted to constant electric current. Recipes of the electrode/gel buffers followed Cheliak and Pittel (1984) for the citrate morpholine buffer (CM) and Alfenas et al. (1991) for the histidine (H) buffer. Staining recipes were taken from Shaw and Prasad (1970), Vallejos (1983), Alfenas et al. (1991), and Brune et al. (1998).
Twelve enzyme systems were studied because of the good resolution of their bands and because they permitted a genetic interpretation on the basis of progeny segregation: Shikimate dehydrogenase (loci Skdh-1 and Skdh-2; EC 1.11.25), malate dehydrogenase (loci Mdh-1 and Mdh-2; EC 1.1.1.37 [EC] ), 6-phosphogluconate dehydrogenase (locus 6-Pgdh; EC 1.1.1.44 [EC] ), phosphoglucoisomerase (locus Pgi-1; EC 5.3.1.9 [EC] ), phosphoglucomutase (locus Pgm-1; EC 5.4.2.2 [EC] ), and acid phosphatase (locus Acp-1; EC 2.6.1.1 [EC] ) for the CM buffer; glutamate oxaloacetate transminase (locus Got-1; EC 2.6.1.1 [EC] ), esterase (fluorescent) (loci Est-1 and Est-2; EC 3.1.1.1 [EC] ), leucine aminopeptidase (locus Lap-1; EC 3.4.11.1 [EC] ), isocitrate dehydrogenase (locus Idh-1; EC 1.1.1.42 [EC] ), glucose-6-phosphate dehydrogenase (locus G6pdh-1, EC 1.1.1.49 [EC] ), and peroxidase (locus Po-1; EC 1.11.1.7 [EC] ) for the H buffer.
Data Analysis
We recognized the genotypes and estimated the allelic frequencies for the studied population from the interpretation of the zymograms. We used the BIOSYS-2 computer program (Swofford and Selander 1997) to estimate the percentage of polymorphic loci (P), the mean number of alleles per locus (A), the mean heterozygosities observed (Ho) and expected (He), and the fixation indices (F), all in relation to both the adult individuals and the progenies. The value of P was obtained considering the number of loci that presented the most frequent allele with an occurrence of less than 99% in relation to the total number of loci. The value of A was estimated by dividing the total number of alleles by the number of loci. Ho was obtained by counting the heterozygotes. He was obtained by the formula: 
where pi is the mean frequency of allele i in the loci. The fixation indices were estimated as deviations from the expected heterozygosity by: 
We used the MLTR computer program (Multilocus—Ritland 2002) from the mixed outcrossing model proposed by Ritland and Jain (1981) and correlated outcrossing model of Ritland (1989) to estimate the single and multilocus outcrossing rates for family and population. We estimated 1) the population rate of multilocus outcrossing 
by the maximum likelihood method, 2) the population rate of single outcrossing 
, 3) the outcrossing rate between related individuals 
4) the allelic frequencies of the ovules and pollen (o and p), and 5) the paternity correlation 
. The mean standard for the estimates described above was obtained through 1000 bootstraps, where the resampling units were the plants within the families.
We used the Ritland and Jain (1981) model to obtain estimates of the allelic frequencies of pollen and ovules. The homogeneity of these frequencies was tested using the 
estimate of Wright (1965) and the significance of provided by the 
2 test (Workman and Niswander 1970).
Additionally, from the characterization of the spatial distribution of the genotypes, we analyzed the spatial autocorrelation using the SPATIAL GENETIC SOFTWARE computer program of Degen et al. (2001), with an 18-m interval. Estimates of Moran's I index were used for the spatial autocorrelation between distance classes, for each locus and for the population.
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Sixteen loci were resolved into the 12 enzymatic systems, of which 9 were monomorphic (Mdh-1, Skdh-1, Me-1, Pgi-2, G6pdh, Acp, Lap, Idh, Est-1) and the other 7 were polymorphic (Table 1). Twenty-six alleles were found in this population, and the maximum number of alleles per locus was 3 (Table 1). The mean number of alleles per locus was 1.6 for all loci and 2.4 for polymorphic loci, independent of the sex of the individuals. The allelic frequencies were similar when comparing male plants, female plants and progenies, except for the locus Pgm-1, where the second allele was not detected in the progenies (Table 1).
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The absence of this allele can be explained by absence in the 14 maternal plants and by the low frequency in the population (0.047).
The observed and expected heterozygosity values obtained for the classes analyzed show that the different categories (male, female, and progenies) are in panmixia equilibrium, indicating the inexistence of endogamic effects (Table 2). This aspect, allied to the high diversity values obtained, when compared with other studies using this species, suggests that this population is well conserved. We did not find any difference in diversity between male and female individuals.
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The heterozygosity found in this study for both progenies (He = 0.345) and adults (He = 0.389), considering only the polymorphic loci, was greater than that found by Sousa (2000) in forests of the region of Campos do Jordão-SP (He = 0.263), Irati-PR (He = 0.110), and Caçador-SC (He = 0.124). These differences can be associated to the natural history of each of the populations or to the exploitation record of each area. An important difference observed between these studies concerns the size of the sample. Although the current study used 334 plants, Sousa (2000) used only 35 samples for Campos do Jordão and 10 for the other localities. This difference suggests that attention should be drawn to the sampling numbers so that the existing level of variation in the populations can be indicated effectively. Carlini-Garcia et al. (2001) recommend at least 50 individuals per population for this species, so that the deviations associated to the estimates are compatible and adequate.
The diversity of A. angustifolia (He = 0.170) was similar to that of other Gymnosperms. Considering also the monomorphic loci, Auler et al. (2002) found lower indices of diversity for all the populations of A. angustifolia studied. These authors studied degraded populations (He = 0.059) and conserved populations (He = 0.112), suggesting a loss of variability in the degraded ones. Shimizu et al. (2000) studied a population in the Parque Nacional do Iguaçu and found an He of 0.248, a little over the He found in the current study, although only 10 loci were analyzed against 16 loci in our study. The number of loci analyzed directly affects the estimate of mean heterozygosity by locus, so care must be taken when comparing different studies. The heterozygosities found for another species of Araucariaceae, Agathis borneensis (HT = 0.122; Kitamura and Rahman 1992), and for a tropical forest species (H = 0.111; Hamrick and Loveless 1986) are below the heterozygosity found in this study. Similar values have been found for other Gymnosperms (H = 0.169; Hamrick et al. 1992). Hamrick and Godt (1989) found an He of 0.123 for wind-pollinated species. In more recent studies with Gymnosperms, Pinus rzedowskii presents an He of 0.219 (Delgado et al. 1999), 4 species of Abies have values between 0.069 and 0.113 (Aguirre-Planter et al. 2000), Chamaecyparis nootkatensis has an He of 0.147 (Ritland et al. 2001), and Taxus cuspidate has an He of 0.192 (Chung et al. 1999).
Mating System
Significant differences between the allelic frequencies in the pollen/ovule group for the loci Pgm-1, Prx-1, Fes-2, and Got-1 (Table 3) were found in the adhesion test of the loci in the multilocus model, showing that these 4 loci did not adapt to the mixed mating model of Ritland and Jain (1981). In the other 3 loci, the allelic frequencies in ovules and pollen can be considered homogeneous. We therefore found deviations to the mixed mating model in Araucaria angustifolia. According to Ritland and El-Kassaby (1985), these deviations do not compromise the estimates of the outcrossing rate. The estimate of single outcrossing rate varied between 7 loci from 0.593 (Skdh-1) to 1.20 (Got-1), and in 4 loci the outcrossing rate was less than unity (confidence interval, CI ± 0.0021; 
= 0.05). The 
mean was 0.897 (0.029) (Table 4). The estimate of multilocus outcrossing rate for the families varied from 0.835 to 1.121, and the mean for the population was 0.956 (0.022) (Table 4). The difference between the multilocus and unilocus rates 
for the population was 0.058 (0.020), indicating the existence of outcrossings between related individuals. The outcrossing rate obtained in this study (tm = 0.956) indicates that this species behaves like an allogamous species, which is expected, as it is dioecious. However, the estimate obtained (0.956 ± 0.00215) is different from unity, and the difference between the multilocus and unilocus rates was significant and positive, indicating that 5.8% of the outcrossings occur between related individuals. As we are dealing with a dioecious species, with obligatory outcrossing, deviations from unity in the outcrossing rate can be attributed to outcrossings between related or preferential individuals as discussed by Ritland and Jain (1981) and Ritland and El-Kassaby (1985).
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The outcrossings between related individuals in araucaria was not expected since this species is wind pollinated. However, Sousa (2000) has demonstrated that the size of the araucaria pollen grain is larger than that of most wind-pollinated species. Therefore, the dispersion of pollen from this species probably does not occur over long distances, especially because it lacks wings. In this case, the dispersion of pollen over long distances is dependent on the climatic conditions at the moment when the pollen is released. Moreover, data raised by Solórzano-Filho (2000) show that the dispersion of the seeds occurs over short distances, on average 2.5 m (max = 13 m). These characteristics suggest that the chances of outcrossings between neighboring individuals is greater, and outcrossings can therefore occur between related individuals. The spatial distribution of the reproductive individuals found in the study area tended toward being "aggregated" (Mantovani 2003), which points to the occurrence of outcrossings between related individuals. Moreover, the heterozygosity values of the progenies were smaller than those of the parents, which reinforce the possibility of family structure.
The correlation of the paternity estimate was significant 
=0.192±0.086) (Table 4) which allowed to conclude that approximately 18.3% 
of the offspring derived from correlated outcrossing (full sibs) and 77.2% 
derived from random mating, related as half sibs. The estimated number of effective pollinators (1/
) exceed 5. Thus, the A. angustifolia families in this population are mainly half sibs.
The paternity correlation found in this study can be associated to 1) a higher probability of male plants closer to female plants, increasing the females chances of receiving the pollen; and 2) the asynchrony in the flowering, a fact that was not verified in this study. Significant paternity correlations have been found for other tree species such as Cariniana legalis (Sebbenn et al. 2000), Tabebuia cassinoides (Sebbenn et al. 2001), Esenbeckia leicarpa (Seoane et al. 2001), and Chorisa speciosa (Sousa et al. 2003).
Spatial Autocorrelation
The analysis of spatial autocorrelation showed that 21 of the 140 values of I (Moran's index) were significant (not shown). Eleven, or 40%, of these significant values were found in the first 4 distance classes (Figure 1), indicating genetic structure in these classes (up to 70 m). These results indicate the presence of low structuring of the genotypes within the population, which is, however, distinct from a complete panmitic distribution. Similar structuring levels were found for other conifers, such as Pinus ponderosa (Linhart et al. 1981) and Pinus contorta (Epperson and Allard 1989). In his review, Heywood (1991) shows that 25 out of 32 analyzed species presented spatial structure within populations. This author remarks that the magnitude of this structure is relatively low in allogamous plants.
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Araucaria angustifolia is a dioecious species and presents compatible structuring results, which are low. However, the presence and level of genetic structuring within populations varies among populations (Xie and Knowles 1991), as reported for Larix laricina, probably as a function of different occupation histories (Knowles et al. 1992). Therefore, we can expect the presence and magnitude of the internal structure to vary for each population since the density of individuals in the araucaria remnants is variable.
The positive and significant autocorrelations found in this study, in the first distance classes (up to 70 m), indicate that the plants share common alleles with a frequency greater than random, corroborating the outcrossing rate results that indicate outcrossings between related individuals and the lower heterozygosity found in the progenies. As the distance between individuals increases, the autocorrelation values are no longer significant and individuals are generally less related than would be expected with a random distribution. The structuring of genotypes over short distances within populations has been verified for several species (e.g., Schnabel et al. 1991; Wagner et al. 1991; Shapcott 1995; Berg and Hamrick 1995). This structuring can result from spatial variation in selection (environmental heterogeneity) or of local genetic drift (isolation by distance) (Heywood 1991). One of the sources of genetic structure may be linked to demographic patterns, where populations formed by individuals of similar age have a greater chance of possessing a given genetic structure (Perry and Knowles 1991).
The observed values of Moran's I statistics for distance class 1 (average value 0.09) can be used to estimate total dispersal under the standard isolation by distance model (Epperson et al. 1999), and thus the observed value corresponds approximately to a Wright's neighborhood size of 70 individuals. This number of individuals is contained in an area approximately equal to 2 ha, in agreement with the density of 32 individuals per hectare actually found in the study area (Mantovani et al. 2004). Within this neighborhood size, the individuals exchange alleles randomly, in such a way that the reduction in this value would cause alterations to the genetic structure of the populations and consequently the loss of less frequent alleles by the more accentuated effect of genetic drift, thereby reducing the genetic diversity.
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Acknowledgments |
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We are grateful to the Instituto Florestal do Estado de São Paulo for providing a research license for the Parque Estadual de Campos do Jordão; to the Fundação de Amparo a Pesquisa no Estado de São Paulo—FAPESP (Process 95/9626-0) and National Scientific and Technological Development Council—CNPq (Process 582920/2001-9) for financial aid; to the Núcleo de Pesquisa em Florestas Tropicais da UFSC for help during the field work; to the Laboratório de Fisiologia do Desenvolvimento e Genética Vegetal da Universidade Federal de Santa Catarina for providing the infrastructure for isoenzyme analysis. A.M. received a doctoral scholarship from Capes and L.P.C.M. and M.S.R. received Research Productivity scholarships from CNPq.
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Footnotes |
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Corresponding Editor: James Hamrick
Received May 30, 2006
Accepted June 16, 2006
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