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Issue
Ann. For. Sci.
Volume 67, Number 5, July-August 2010
Article Number 508
Number of page(s) 10
DOI http://dx.doi.org/10.1051/forest/2010010
Published online 18 May 2010

© INRA, EDP Sciences, 2010

1. INTRODUCTION

Species distributed along wide environmental ranges are expected to be either plastic or adapted to local optima. Plasticity implies that a common gene pool shared among populations is capable of acclimation, producing different phenotypes in each environment (Via and Lande, 1987). On the contrary, adaptation means that a specialized gene pool is present in each particular ecological condition, what leads to genetic differentiation. The elucidation of which of these alternatives prevails, is crucial in planning breeding and conservation strategies for not yet domesticated species.

The Instituto Nacional de Tecnología Agropecuaria, INTA, (San Carlos de Bariloche, Argentina) is currently engaged in a domestication program for Patagonian cypress (Austrocedrus chilensis (D. Don) Pic. Ser. et Bizzarri, Cupressaceae). This Argentinean and Chilean conifer presents a valuable breeding potential and is also an important target for conservation since, besides its ecological relevance, it has been classified as a vulnerable species by the IUCN (Conifer Specialist Group, 1998). The most prominent environmental range of its distribution area in the Argentinean side of the Andes Mountains is a steep West-to-East decreasing precipitation gradient. Natural populations of Patagonian Cypress can be found in sites ranging in annual precipitation between less than 400 and more than 2000 mm (Gallo et al., 2004). This wide range for a truly relevant environmental variable gives the possibility of testing whether acclimation or adaptation is the main strategy of this species to survive in a so heterogeneous region.

These alternative scenarios may be tested by means of classic common garden trials: if differentiation is true, phenotypic differences among provenances will arise under common environmental conditions. Sampling a set of natural populations gradually following the precipitation range would help to test clinal variation. However, when the study is aimed at identifying whether differentiation or plasticity takes place, sampling the extremes of the gradient may provide enough more conclusive and certainly simpler evidence.

In nature, the earliest stages of plant development are the most susceptible to selection processes (King, 1990; Moles and Westoby, 2004; Seiwa and Kikuzawa, 1991). Thus, differences in seedling traits would be expected if adaptation has indeed occurred. Seedlings adapted to drought stress would present morphological adjustments related to a more conservative development, with a significantly smaller above-ground size (Cregg, 1994).

The Patagonian Cypress was the subject of previous genetic studies, which constitute valuable antecedents. However, all of them were based on selectively neutral gene markers. Studies performed with isozymes have shown that the allelic frequencies do not differ greatly among natural populations of this species, irrespective of the distances and environmental differences among them (Pastorino and Gallo 2002; Pastorino et al., 2004). Neutral differentiation among 27 populations representing the whole Argentinean range of the species resulted low (Pastorino and Gallo, 2009). This pattern was explained in relation with the post-glacial life history of the species. However, contrasting environments, which are irrelevant for selectively neutral markers, are expected to have an influence on adaptive traits instead. Our main hypothesis is, therefore, that contrasting precipitation regimes significantly affect the genetic variation pattern of susceptible-to-selection traits. The corresponding predictions are: (1) differentiation calculated for seedlings’ morpho/architectural traits will be large among populations developed under contrasting precipitation regimes; (2) intra-population genetic variation will be lower in those populations undergone stronger selective pressure, namely in those suffering drought stress; and (3) populations growing under a similar precipitation regime but genetically isolated from each other (without gene-flow between them), will present no significant differences in adaptive traits.

2. MATERIALS AND METHODS

2.1. Plant material

The variation in morphological traits measured on one-year-old seedlings originating from four natural populations of Austrocedrus chilensis was analyzed in a common garden trial.

Populations were selected in order to represent contrasting precipitation regimes within the species’ Argentinean range (Tab. I and Fig. 1). More than 1000 mm of annual precipitation differentiate both sampled conditions. Two populations separated by more than 100 km represented humid sites: Río Azul and Cerro Catedral. Río Azul is a continuous and compact forest with cypresses taller than 25 m mixed with Nothofagus dombeyi (Mirb.) Oerst., and other secondary species. Cerro Catedral is also a mixed forest but slightly more open and with shorter cypresses (up to 20 m high). Low precipitation sites were represented by two neighbouring populations, Pilcañeu North and Pilcañeu South, situated at the top of two rocky hills in the steppe and distant only 1200 m from each other. These two small stands (with about one-hundred adult individuals each) are the xeric extreme of the species range. Trees are 4 to 6 m tall, with tortuous shape and scattered over some 4 ha in each population. No other tree species accompany these Patagonian cypresses. In a previous work based on neutral markers (Pastorino and Gallo, 2009), these two populations were shown to be genetically quite distant in spite of their geographic proximity. A hindered gene flow between them was inferred by means of isozymes, what is probably caused by their relative position perpendicular to the predominant and strong westerly winds.

Table I

Location and mean annual precipitation (m.a.p.) of the four sampled Austrocedrus chilensis populations.

thumbnail Figure 1

Sampled populations of Austrocedrus chilensis over an isohyet map (from Cordon et al., 1993). A: Río Azul; C: Cerro Catedral; PN: Pilcañeu North, and PS: Pilcañeu South.

In each of the four populations, cones were collected directly from the tree crowns, keeping a minimum distance of 30 m between trees in order to reduce the probability of sampling related individuals.

2.2. Experimental design

Seeds were extracted from the cones and sown in flats at the beginning of spring following a pre-germination treatment. Immediately after germination, a sample of seedlings was transplanted to single 265 cm3 pots of square section and 15 cm depth (HIKOTM HV265 tray type), and ordered according to a totally balanced experimental design.

For each of the four populations, seven open-pollinated families were represented by 30 seedlings each, distributed in three blocks (sub-sampling experimental design, with 10 seedlings per block distributed in two adjacent five-seedling rows; i.e. 210 seedlings per population). The trial was located in a greenhouse under controlled conditions without water limitations (i.e. temperature between 10 °C and 25 °C, 1:1 peat-sand substrate and ferti-irrigation with an N-P-K + micronutrients diet adjusted for the species) at San Carlos de Bariloche city (41° 07′ S lat., 71° 15′ W long., 810 m a.s.l.).

2.3. Variables measured

For each seedling, five primary variables were measured in winter after the first growing season: basal diameter of the main axis (AD), measured immediately above the cotyledons; main axis length (AL), measured from the cotyledons to the apical bud; number of nodes (NN), excluding the cotyledonary node; number of branches of the main axis (NB); and the length of the most basal branch (BL). These five variables are mainly indicative of growth vigour. Lengths and diameters were measured with a digital calliper to the nearest 0.1 mm.

Three additional variables were derived from the previous ones: mean internode length (AL/NN); the ratio between main axis length and basal diameter (AL/AD) which measures stem slenderness; and the ratio between the lengths of the basal branch and the main axis (BL/AL), which evaluates the relative branch development of the seedling and is a sign of the dominance of the main axis on the major branch. These three secondary variables are mainly related to architectural balances of the aerial portion of each seedling.

2.4. Statistical analyses

In order to test the statistical significance of differences among populations and the variability among families, an ANOVA test was performed for each of the considered variables under the following mixed nested model with independent and normally distributed residuals: where yijkl is an observation of the variable for the lth seedling, from the kth family within the ith population located in the jth block; μ is the overall mean for the variable; ρi is the effect (fixed) of the ith population; βj is the effect (random) of the jth block; φki) is the effect (random) of the kth family within the ith population; eijk is the main plot error NID (0, ), and εijkl is the sub-sampling residual NID(0, ).

Tests were performed through the GLM procedure (type III sums of squares) of the SAS software (1989), and components of variance were obtained by restricted maximum likelihood with the MIXED procedure of SAS. The algorithm of the MIXED procedure gives exactly the same result as the VARCOMP procedure due to data balance. Normality of the data was assessed by a histogram and a normal probability plot of the residuals and a Shapiro-Wilk test (Sokal and Rohlf, 1995) for each variable. Homocedasticity was checked by plotting the residuals against the predicted values. In order to compare all possible population pairs through the means, Tukey tests were performed (α = 0.05; SAS, 1989). Bar graphics were drawn with the help of R 2.8.1 (R Development Core Team, 2008).

2.5. Intra-population genetic parameters

Additive genetic variance is the basic parameter to estimate genetic variation within a population. In open-pollinated families, relationships among their members are expected to be closer than those among members of true half-sib families, but not as close as those of full sibs. Since A. chilensis is a dioecious species, selfing is not possible. Nonetheless, individuals were shown to mate not randomly but in groups (Pastorino and Gallo, 2006). Consequently, the additive genetic variance was estimated as three times the family variance, namely an intermediate factor between 4 and 2, corresponding to half and full sibs respectively (Squillace, 1974): where is the additive genetic variance and is the family variance.

Since additive genetic variance values are a function of the units used, an additive genetic coefficient of variation (CVA; Houle, 1992) was calculated so as to render direct comparisons among variables meaningful: where x is the variable mean.

Narrow-sense heritabilities (h2) were calculated for each variable taking each population separately and also pooling the data across populations, according to the equation: where is the phenotypic variance, is the block variance, and is the error variance, which is the sum of the variances of the main plot and the sub-sampling residuals.

The standard error (SE) of the heritability was also calculated with factor 3: where f is the number of families and n is the number of individuals within each family (Falconer and Mackay, 1996).

Phenotypic and additive genetic correlations (Pearson’s correlation coefficient rP and rA respectively) were calculated for the four populations as a pool for all the possible combinations of primary variables according to the formulae: where Covxy is the covariance between variables x and y, and are the variances of both variables, and are the family variances of the variables, and Covfxy is the family covariance of the variables, which is calculated by where is the family variance of a variable built by the sum of both variables (O’Neill et al., 2001).

Standard errors of phenotypic and genetic correlations were computed by where N is the total number of individuals sampled (Visscher, 1998).

2.6. Inter-population genetic parameters

Partitioning the phenotypic variance of each variable into its components, and particularly distinguishing within- and among-populations components lead to a straightforward calculation of genetic differentiation among populations for quantitative traits, Qst (Spitze, 1993), for each variable by means of: where σ is the variance among populations calculated after considering the original model but with populations as a random effect factor.

3. RESULTS

3.1. Comparisons among populations throughphenotypic values

The plants from the xeric population Pilcañeu South were, on average, the least vigorous as revealed by the mean values of all five primary variables. The most vigorous seedlings, according to these variables, were those of Cerro Catedral and Río Azul (Fig. 2).

thumbnail Figure 2

Means and confidence intervals (α = 0.05) for eight seedling traits in four natural populations of Austrocedrus chilensis: Río Azul (Azul), Cerro Catedral (Cat.), Pilcañeu North (PilN) and Pilcañeu South (PilS). Different letters indicate significant differences (pairwise Tukey tests).

Significant differences among populations were revealed by means of ANOVA tests for phenotypic values of all traits but axis length (AL), internode length (AL/NN) and the ratio between axis length and basal diameter (AL/AD) (Tab. II). Tukey tests showed no differences between Río Azul and Cerro Catedral, and between Pilcañeu North and Pilcañeu South in the phenotypic values of all variables. Pilcañeu North could not be differentiated from the humid populations (it showed significant differences with Cerro Catedral only regarding the number of branches; Fig. 2).

Table II

Results of the type III tests of hypotheses for Mixed Model ANOVA on morpho/architectural traits of Austrocedrus chilensis seedlings in a common garden experiment. Fisher’s F and probability values P. df: degrees of freedom.

Variability among families was shown to be significant for all primary and secondary variables. The block factor was not significant in all but two secondary variables (Tab. II).

3.2. Intra-population genetic variation

From the values of additive genetic coefficient of variation, but especially from those of additive genetic variance (), it becomes evident that Pilcañeu South was the least variable population whereas Río Azul and Pilcañeu North were the most variable populations in almost all of the traits (Tab. III).

All primary variables were moderately to highly positively correlated (all rP and rA were higher than 0.4, Tab. IV). Pearson phenotypic correlations were all significant (P < 0.001), with additive genetic correlations higher than phenotypic correlations in all cases but NN vs. NB. The highest genetic correlations were those between: AL and AD, BL and NB, and AL and NN (rA > 0.9), while the lowest correlation was that between NB and NN (Tab. IV). The estimated phenotypic correlation between AD and AL was among the lowest correlations. The highest phenotypic correlations were those between BL and NB and between AL and NN (rP > 0.71; Tab. IV).

Table III

Additive genetic variance (), additive genetic coefficient of variation (CVA) and heritability (h2) for eight variables measured in Austrocedrus chilensis seedlings from four natural populations. Heritabilities for the pooled populations and genetic differentiation between them (Qst) are indicated for each variable in the right columns. Standard errors (SE) are shown between brackets. AD: main axis basal diameter, AL: main axis length, NN: number of nodes, NB: number of branches, BL: basal branch length.

Table IV

Phenotypic (above diagonal) and genetic (below diagonal) correlations between five morpho/architectural traits of Austrocedrus chilensis seedlings and their standard errors (between brackets).

3.3. Heritability

Single-population heritabilities were quite variable among populations, with the lowest values in Pilcañeu South for all traits, and the highest in Río Azul or eventually in Pilcañeu North (Tab. III).

Besides single-population heritabilities, a value of narrow sense heritability was calculated for a hypothetic population built by pooling the 28 families corresponding to the four populations surveyed. This procedure allows to better extract a measure of the genetic control for each trait, since the calculation of this pooled heritability is more accurate (lower standard errors) due to the larger sampling. According to this, the traits with the highest genetic control were BL (h2 = 0.53) and NB (h2 = 0.51). In general terms, all the primary variables presented a moderate to high heritability. The lowest pooled heritability corresponded to the AL/AD ratio (; Tab. III).

3.4. Genetic differentiation

The mean differentiation calculated for all five primary variables was Qst = 0.122, and that for all primary and secondary variables 0.088. The Qst calculated for the AL/AD ratio was 0. This result was caused by a null component of variance of the factor “population”, that is, seedlings belonging to different populations were as different among them (with respect to this variable) as those belonging to the same population. The highest differentiation corresponded to AD (Qst = 0.172; Tab. III), which could be considered moderate.

4. DISCUSSION

4.1. Phenotypic differences among populations

The results of this trial showed that Patagonian Cypress seedlings whose parent trees belonged to populations growing under similar precipitation levels (namely, Río Azul – Cerro Catedral and Pilcañeu North – Pilcañeu South) did not differ regarding phenotypic values of morphological and architectural traits. However, seedlings of one of the xeric populations (Pilcañeu North) did not differ from those of the humid populations either. Thus, the precipitation regime would not be a selective pressure determining seedling morphology and architecture, at least for the traits considered in the present study. Working on a sample of only five seedlings per provenance, Gyenge et al. (2005) consistently found no differences among populations of A. chilensis with contrasting precipitation levels regarding several physiological parameters (photosynthetic and stomatal responses to drought, leaf water content, hydraulic resistance and xylem cavitation vulnerability).

The length of the main axis is determined by the number of nodes and internodes produced on the axis and, most importantly, by the degree of extension of its internodes. It has been pointed out that internode extension in plant axes is more dependent upon microenvironmental conditions than the number of nodes, which would be more closely tied to endogenous regulation (Puntieri et al., 1998). Consistently, it has been suggested that early height growth would lack adaptive value in stress-tolerant conifers (López et al., 2007). This seems to be the case in Patagonian Cypress, since the sampled populations differed regarding the number of nodes of the main axis but not internode length which, in turn, brought about non-significant differences in height. Differencesbetweenpopulations in height growth have been shown to increase with plant age, especially in conifers (e.g. Foster, 1986; Namkoong and Conkle, 1976; Namkoong et al., 1972). Thus, differences among A. chilensis populations regarding plant height cannot be dismissed to become significant in further years.

4.2. Genetic variation and correlations

Additive genetic variances of all traits but the main axis slenderness were highest for Río Azul and Pilcañeu North populations, intermediate for Cerro Catedral, and lowest for Pilcañeu South. It can be seen in general that the two most variable populations (with similar levels of variation) belong to sites with contrasting precipitation regimes. This is again supporting that the precipitation level does not represent a strong selective force for the surveyed variables. Otherwise, humid and the xeric populations would have been clearly differing in terms of genetic variation (considering that those traits under strong selective pressure would present the lowest levels of variation; Reich et al., 2003). In other words, the lack of adaptive value of the considered traits in regard to the precipitation condition might be postulated. In that respect, we should distinguish two types of traits among those considered here: traits concerning main axis development, and traits concerning branch development. The former presented lower additive genetic coefficients of variation in the four populations, and lower single population and pooled heritabilities. These are evidences of lower adaptive value.

We can search further evidence by comparing populations with the same precipitation regime. As mentioned above, Pilcañeu South is the least genetically variable population in terms of for all traits. However, its neighbouring population, Pilcañeu North, exhibited the opposite pattern. This difference between the two xeric populations does not match an adaptation process. This is especially true for the main axis traits, for which the differences in terms of CVA between both populations are the largest. Since both populations are quite small, genetic drift appears to have been a reasonable cause of such differences, together with the already mentioned hindered gene flow.

The estimations of heritability in the Pilcañeu South population can also help to distinguish two types of traits. Basal diameter, number of nodes and main axis slenderness presented heritabilities close to zero for Pilcañeu South, even though they exhibited moderate to high heritabilities for the other populations. On the other hand, basal branch length, number of branches and the branch-length/main-axis-length ratio for Pilcañeu South population had moderate heritabilities, closer to those of the other populations.

In the present study, the genetic correlation between main axis basal diameter and main axis length surpassed the highest theoretical value of 1. This is a hardly reported but not uncommon result. It must be taken into account when assessing these correlations that they are estimations of the true correlations in which additive epistatic interactions are potentially included in the estimates of the genetic variances and covariances (Lynch and Walsh, 1998). The large standard error of the mentioned correlation (0.453) indicates that the true correlation lies within a confidence interval that includes the value 1. In any case, it is clear that height and basal diameter are closely tied at this early growth stage.

The low number of families per population in our trial does not allow for an analysis of correlations within each population, so that the calculated values should be taken as indicative. However, a general trend is evident, since additive genetic correlations were higher than phenotypic correlations in almost all cases. This means a low environmental correlation and renders more support for combining these surveyed traits as early selecting criteria. For example, the relatively high genetic control of branch development may be beneficial for an early selection of seedlings, what could be performed either by the number of branches or the length of the basal branch because these traits are highly correlated (both phenotypically and genetically).

4.3. Differentiation

Fst (Wright, 1978) is a differentiation parameter analogous to Qst but especially designed for neutral markers. Their conceptual analogy makes them possible to be compared in a direct way, thus allowing to understand the role played by selection and other evolutionary forces in modeling the partition of the genetic variation among and within populations (McKay and Latta, 2002; Merilä and Crnokrak, 2001).

Differentiation among 27 natural populations of A. chilensis measured by means of isozyme markers was Fst = 0.060 (Pastorino and Gallo, 2009). Although the present study is not based on those 27 populations, this Fst value can be taken as a reference. Comprehensive reviews have demonstrated that, on average, Qst is typically higher than Fst (Leinonen et al., 2008; McKay and Latta, 2002; Merilä and Crnokrak, 2001).

According to a scale proposed by Bower and Aitken (2008), in our results the differentiation among populations resulted low for all variables, but especially for the secondary ones. We can further distinguish three ranges of Qst values: very low (Qst < 1%), low (8% < Qst < 13%) and moderate (Qst = 17%). For the traits with very low Qst values, which are clearly below the Fst. value reported, we should presume that natural selection has favoured the same mean phenotype in different populations. On the other extreme, we could deduce directional natural selection favouring different basal diameter phenotypes in different populations, since QstAD > Fst (Merilä and Crnokrak, 2001). However, our calculated mean quantitative differentiation (Qst = 0.088) was not much higher than the reported Fst, but in fact quite similar. This similarity does not evidence a selection process; instead, the observed quantitative differentiation can be simply explained by genetic drift and restricted gene flow, particularly considering that the populations sampled represent quite contrasting environments.

In some species of the Cupressaceae family, the development of branches in terms of number, angle and size compared to that of the trunk, is considered to be relevant in distinguishing taxonomical varieties (Grosfeld, 2002; Grosfeld and Barthélémy, 2004). If, as discussed above, we distinguish between the two types of traits in A. chilensis, we have a mean Qst for main axis traits of 0.075 and a mean Qst for branch traits of 0.109. This difference is in accordance with the expectation. However, differentiation based on neutral markers seems not so different from differentiation based on quantitative traits, especially those of the main axis.

Basal diameter was the trait that most differentiated the four populations. In contrast, main axis length, another trait indicative of aerial vigour, was the least discriminating primary variable. Coincidently, this variable measured in two similar trials on Pinus sylvestris L. and Ulmus laevis Pall. provided similar results (QstALPs = 0.08, Notivol et al., 2007; QstALUl = 0.077, Whiteley et al., 2003). These results further support the idea of low adaptive value of main axis length.

The generally low differentiation among A. chilensis populations found in the present study might be due to the early ontogenic stage on which this type of traits was assessed (Cavender-Bares and Bazzaz, 2000). The contrasting environments of the populations sampled may indeed be acting as selective forces but over traits directly related to hydraulic balances and tolerance to drought stress. Higher differentiation among these populations might be found by analysing the traits of underground tissues or physiological mechanisms conditioning the water economy (carbon isotope discrimination, δ13C, is a good alternative for genetic studies with hundreds of individuals, as shown by Lauteri et al., 2004).

4.4. Concluding remarks

The results gave not support for our three original predictions: (1) differentiation was low; (2) intra-population genetic variation was not the lowest in the two most stressed populations and (3) populations growing under a similar precipitation regime showed no significant differences in their seedlings’ traits but populations growing under contrasting precipitation regimes were also similar in this regard. Therefore, we have not evidence to accept the hypothesis that the Patagonian Cypress genetic pool is adapted to local optima. Rather this species appears to be phenotypically plastic, at least regarding early traits relative to above ground growth vigour.

The moderate to high estimated CVA for the traits concerning branch development would be indicative of good adaptive potential of A. chilensis natural populations and genetic improvement potential of the species with regards to these traits. These are wanted features considering the intention of domesticating this species to commercial plantations and in view of the current global climate-change scenario. However, inflation of CVA values due to maternal effects should be considered. At early stages of development, the similarity among half-sibs could be deeply influenced by non-genetic features (Roach and Wulff, 1987). Unfortunately, the dioecious condition of this conifer impedes reciprocal crosses, which is the common procedure to test maternal effects. Therefore, these results should at least be confirmed at more advanced ages, that is, when maternal effects are considered to be diluted.

Finally, evidence was presented supporting that early traits relative to the main axis size would be not adaptively meaningful. This additional result should be taken into account for future studies.

Acknowledgments

We gratefully thank Priscila M. Willems and Eduardo P. Cappa for their helpful guidance in the statistical labyrinth. Alejandro Aparicio must also be mentioned for his help with the R graphics. Comments and literature suggestions by one anonymous reviewer are most appreciated. Seed collection and seedling production were funded by PIA 02/01, Proyecto Forestal de Desarrollo, SAGPyA “Selección para productividad y resistencia a la sequía en poblaciones marginales de Ciprés de la Cordillera ”. The study was partly supported by Fundación BBVA “Fragmentación y conservación de recursos genéticos de coníferas ”.

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All Tables

Table I

Location and mean annual precipitation (m.a.p.) of the four sampled Austrocedrus chilensis populations.

Table II

Results of the type III tests of hypotheses for Mixed Model ANOVA on morpho/architectural traits of Austrocedrus chilensis seedlings in a common garden experiment. Fisher’s F and probability values P. df: degrees of freedom.

Table III

Additive genetic variance (), additive genetic coefficient of variation (CVA) and heritability (h2) for eight variables measured in Austrocedrus chilensis seedlings from four natural populations. Heritabilities for the pooled populations and genetic differentiation between them (Qst) are indicated for each variable in the right columns. Standard errors (SE) are shown between brackets. AD: main axis basal diameter, AL: main axis length, NN: number of nodes, NB: number of branches, BL: basal branch length.

Table IV

Phenotypic (above diagonal) and genetic (below diagonal) correlations between five morpho/architectural traits of Austrocedrus chilensis seedlings and their standard errors (between brackets).

All Figures

thumbnail Figure 1

Sampled populations of Austrocedrus chilensis over an isohyet map (from Cordon et al., 1993). A: Río Azul; C: Cerro Catedral; PN: Pilcañeu North, and PS: Pilcañeu South.

In the text
thumbnail Figure 2

Means and confidence intervals (α = 0.05) for eight seedling traits in four natural populations of Austrocedrus chilensis: Río Azul (Azul), Cerro Catedral (Cat.), Pilcañeu North (PilN) and Pilcañeu South (PilS). Different letters indicate significant differences (pairwise Tukey tests).

In the text