Genetic structure and genetic diversity of Swietenia macrophylla in areas subjected to selective logging in Quintana Roo, Mexico

Estructura y diversidad genética de Swietenia macrophylla en zonas sujetas a tala selectiva en Quintana Roo, México

Raúl Ernesto Alcalá^{1, 3}, Silvia De la Cruz¹ and Gabriel Gutiérrez-Granados²

¹ Departamento de Ecología Evolutiva. Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos. Cuernavaca, Morelos, México.

³ Corresponding author: raul.alcala@uaem.mx.

Received: September 18th, 2014.
Accepted: December 17th, 2014.

Abstract

The hypothesis that selective logging has a negative effect by altering the genetic parameters of tropical tree species was evaluated. The genetic diversity and genetic structure between adult trees (N = 47) and saplings (N = 50) of Swietenia macrophylla were contrasted within an area subjected to selective logging in the Mayan zone. Although differences in the number of alleles and in their frequencies were detected between both groups, the observed and expected heterozygosity and the coefficient of fixation were statistically similar. Evidence of higher genetic structure in the group of saplings was revealed by both, the autocorrelation and the factor correspondence analyses. The genetic differences observed in this study are compatible with those expected under scenarios of disruption in the local pattern of gene flow produced by selective logging. The implication of these results on the conservation genetics of Swietenia macrophylla in the Mayan zone is discussed.

Keywords: autocorrelation analysis, big-leaf mahogany, conservation genetics, Moran's index, tropical timber species.

Se evaluó la hipótesis de que la tala selectiva genera un efecto negativo alterando los parámetros genéticos de las especies de árboles tropicales. Se contrastó la diversidad genética y la estructura genética entre árboles adultos (N = 47) e individuos juveniles (N = 50) de Swietenia macrophylla en una zona sujeta a la tala selectiva en la zona maya. Aunque se detectaron diferencias entre ambos grupos de árboles en el número de alelos y en sus frecuencias, la heterocigosis observada y la esperada, y el coeficiente de fijación fueron estadísticamente similares. Análisis de autocorrelación espacial y factorial de correspondencias mostraron una mayor estructura genética en el grupo de individuos juveniles. Las diferencias genéticas observadas en este estudio son compatibles con las esperadas bajo escenarios de perturbación en el patrón local del flujo de genes producto de la tala selectiva. Se discute la implicación de estos resultados en la conservación genética de Swietenia macrophylla en la zona maya.

Palabras clave: análisis de autocorrelación espacial, caoba de hoja grande, conservación genética, especies tropicales maderables, índice de Morán.

Biodiversity is currently threatened, directly or indirectly by human activities in almost all terrestrial habitats. Due to this, in conservation biology it is important to understand how species respond to anthropic disturbances (Sih et al., 2000; Cushman, 2006). This challenge is particularly relevant for tropical forests because these biomes sustain both, high species richness and a high level of human-induced disturbance (Lowe et al., 2005; Wright and Muller-Landau, 2006). Tropical trees are expected to be particularly susceptible to changes in habitat characteristics because of their low population density (ca. one reproductive tree x ha^-1), self-incompatibility systems and their frequent dependence on animals for pollination (Cunningham, 2000; Lowe et al., 2005; Dick et al., 2008).

The selective logging of target trees with the best characteristics is the commonest strategy in most tropical forests subjected to legal harvesting (Jennings et al., 2001; Sist et al., 2003; Asner et al., 2005; Biscaia-de Lacerda et al., 2008). Selective logging is conceived as a sustainable strategy of forest management due to its intensity is based on growth rates (Snook, 2003; Shono and Snook, 2006). However, it has been proposed that selective logging could impact directly on the local pattern of gene makeup as it tends to reduce population size and/or population density and because it increases the distance between reproductive individuals (Sebbenn et al., 2008). Therefore, the extraction of reproductive trees subsequently reduces outcrossing rates (Murawski et al., 1994; Lee, 2000; Obayashi et al., 2002), increases inbreeding (André et al., 2008) as well as the extent of genetic differentiation (Degen et al., 2006; Cloutier et al., 2007; Biscaia-de Lacerda et al., 2008; Sebben et al., 2008; Silva et al., 2008).

Swietenia macrophylla King in Hook is undoubtedly the most important timber species in Neotropics. It has being traded along its entire geographic distribution, which ranges from the Amazon Basin to South Mexico (Snook, 1998). In Mexico, S. macrophylla has been logged since the late 19^th century. With the implementation of federal regulations (Plan Piloto Forestal) by the 1980s the harvesting plans performed in the so-called Mayan zone (central part of Quintana Roo), included initial inventories and the determination of growth rates. Currently, the management plan is based on polycyclic harvesting with 25-y cutting cycles and a minimum cutting diameter of 55 cm (Bray et al., 2003).

An important consequence of the extraction of largest individuals for timber is that regeneration relies on small-size remnant trees (Gutiérrez-Granados and Dirzo, 2009). As a result, natural regeneration could be limited by a low fruit production, restricted seed shadow, increased seed predation, and a high rate of herbivory in young ontogenetic stages (Snook et al., 2005; Cámara-Cabrales and Kelty, 2009; Gutiérrez-Granados et al., 2011). However, studies addressing the effects of selective logging on genetic parameters are currently absent for Mexican populations of S. macrophylla. If selective logging is exerting some effect on population dynamics, we expect to find genetic differences between the group of adult trees and that derived by the natural regeneration. In particular, it is predicted a higher spatial genetic structure (i.e., higher genetic relatedness at short distances) and lower genetic diversity in saplings rather than in adult trees.

Materials and methods

Sampling design. Some studies sampling only adult trees have shown an apparent absence of negative effects of selective logging, forest fragmentation or deforestation on genetic parameters. This result has been explained by considering these anthropic disturbances as relatively recent processes with regard to the long-life span of adult trees (White et al., 1999; Collevatti et al., 2001; Lowe et al., 2005). Therefore, a more informative approach has been derived from the genetic comparison between adults and their regeneration, assuming that the disruption of processes affecting gene flow between adult trees (i.e., pollination) should produce measurable effects on progeny.

Genetic analyses were performed on 47 adult trees and 50 saplings of Swietenia macrophylla located within a 600-ha forest surface subjected to a first cutting cycle in 1998. Originally 160 individuals were mapped in the area; however, individuals separated from each other by at least 100 m were selected in order to avoid the probability of sampling within genetic families (Gillies et al., 1999; Navarro et al., 2010). Diameter at breast height (DBH 1.30 m) of adult trees ranged from 35 to 45 cm, whereas height of saplings was < 50 cm. For adult trees, a slingshot was used to obtain leaves from the upper part of the crown, whereas a telescopic pruner was used to sample at lower height. Only the leaves free of apparent damage by pathogens and insects were selected. The sampled tissue per plant was kept in previously marked sealed plastic bags containing blue indicator silica gel to stabilize DNA through a rapid desiccation of plant material.

DNA-procedures. Isolation of DNA was performed through a standard Cetyl Trimethyl Ammonium Bromide (CTAB)-based procedure (Doyle and Doyle, 1987). Quality of samples was improved by applying GENECLEAN®. A set of primers Sm01, Sm31, Sm47 and Sm51 were used from those developed for Swietenia macrophylla (Lemes et al., 2002). The final reaction consisted of 15 μl total volume containing 1x PCR buffer, 1 mM MgCl₂, 0.2 mM dNTP's, 1 μL Taq DNA polymerase (Vivantis Technologies, Selangor, Malaysia) and 5 ng of template DNA. Amplification conditions for primer sm47 were: an initial denaturing step of 95 °C 1 min followed by 30 cycles of 95 °C 1 min, 56 °C 1 min and 72 °C 1 min, and a final extension step of 72 °C 10 min. For the other three primers the conditions were: an initial step of 94 °C for 3 min followed by 30 cycles of 1 min at 94 °C, 1 min at 56 °C, 4 min at 72 °C and an extension step of 72 °C 10 min. PCR products were subjected to electrophoresis in 6 % polyacrilamide gel in Tris-Borate Ethylenediaminetetraacetic acid (TBE) buffer. Gels were stained with ethidium bromide and photographed under UV light. Then, the different alleles for each locus were scored according to their molecular mass (White et al., 2002; Céspedes et al., 2003). The allele located closer to anode was arbitrarily identified as "1", and the remaining alleles were identified sequentially (Céspedes et al., 2003).

Statistical analyses. The genetic differences between adults and saplings of Swietenia macrophylla were analyzed with four different approaches, allelic frequencies, heterozygosity-based information, autocorrelation analysis and factor correspondence analysis. For the allelic information, the total number of alleles found in the population, the number of alleles per locus and their respective allelic frequencies were described. In addition, the alleles present in eight frequency classes for adults and saplings were counted. The statistical differences between both groups were tested by a contingency table (Sokal and Rohlf, 1995). Second, the mean values for both the observed heretozygosity (H_O) and expected heterozygosity (H_E) were calculated using ARLEQUIN (Excoffier et al., 2005). The coefficient of fixation (F_IS) that indicates departures of genotypic frequencies from Hardy-Weinberg equilibrium was also estimated. The significance of the coefficients F_IS, were tested using a Monte Carlo chain with 1,000 iterations (Excoffier et al., 2005). Genetic differences between adults and saplings regarding these tree estimates were evaluated performing independent Mann-Whitney tests (Sokal and Rohlf, 1995).

Third, three independent spatial autocorrelation analyses were performed to investigate differences between both groups in the fine-scale genetic structure (Degen et al., 2001). The autocorrelation analysis has been used to identify a series of processes that affect the local pattern of gene flow and that consequently shape the fine-scale genetic structure (Smouse and Peakall, 1999; Degen et al., 2001; Vekemans and Hardy, 2004). The spatial autocorrelation analysis performed on the molecular information evaluates if the pairwise genetic relatedness varies depending on the separation distance of the compared individuals. From this relationship, a spatial random distribution is expected as a null hypothesis. Instead, a higher genetic relatedness at shorter distances is expected under conditions restricting gene movement.

The SGS software utilized in this study to perform the autocorrelation analyses returned correlograms displaying the variation in the magnitude of the Moran's Index (genetic relatedness) obtained for multilocus genotypes according with the separation distance of pairs of individuals. Along the x-axis of the correlograms, the variation in the separation distance between compared individuals is displayed in the form of ranges (distance classes; Degen, 2000). A permutation procedure using Monte-Carlo simulations was applied to test for significant deviation from the spatial random distribution. For each one of the spatial distance classes, observed values were compared with the distribution obtained after 1,000 permutations. Then, a 95 % confidence interval for the parameters was obtained. Thus, positive values of Moran's Index located beyond the confidence limit represent statistically significant deviations of the random distribution (positive fine-genetic structure). The consistency of the genetic spatial pattern was evaluated varying the number of distance classes. To do this, three analyses per group were performed using 5, 7, and 15 distance classes. In all cases, at least 30 pairs of data points per distance class were used (Degen, 2000).

Finally, a factorial correspondence analysis was carried out using GENETIX 4.05.2 (Belkhir et al., 1996-2000). With this analysis, the genetic structure was qualitatively examined by comparing the extent of genetic variation displayed for both groups in a multivariate space. A strong overlapping in the distribution pattern between adults and saplings would indicate the absence of genetic differences between them.

Results

Genetic diversity. The information extracted from the four loci utilized in this study revealed a total of 25 alleles. The genetic polymorphism varied lightly among loci. The lowest number of alleles (5) was observed for locus Sm22, whereas loci Sm51 and Sm 47 revealed the occurrence of seven alleles (Table 1). In the group of adults, 21 alleles showed a frequency equal or higher to 0.05. In contrast, in the group of saplings seven alleles showed a low frequency (< 0.05). In fact, two alleles present in adult trees were absent in that group, whereas all alleles present in saplings were detected in adult trees.

The analysis of the distribution of allelic frequencies showed significant differences between adults and saplings (χ² = 23.37, df = 7, P = 0.0014, Figure 2). Differences were present in most of the frequency categories, in particular on alleles at frequencies < 0.25 (Figure 2). With regard the genotypic information, in both groups, the observed heterozygosity (H_O) was markedly lower than expected heterozygosity (H_E) for all loci. In consequence, positive values for the coefficient of fixation (F_IS) were obtained that indicate a statistically significant deficiency of heterozygotes (Table 2). No statistical differences in H_O, H_E , and F_IS between adults and saplings were detected by the independent Mann-Whitney tests (Table 2).

Genetic structure. The three autocorrelation analyses performed for both adults and saplings showed consistent results. This means that the relationship between the genetic relatedness of individuals with spatial distance was not affected by the variation in the number of distance classes (5, 7 or 15). No departures from a random pattern were detected in the analysis corresponding to adults. This is because the values for the Moran's Index were constrained within the confidence limits along the variation in the separation distance between compared individuals (Figure 3). In contrast, a statistically significant fine-scale genetic structure was observed for saplings. In this group, positives values of the Moran's Index (ca. 0.05 of magnitude) were situated beyond the confidence limit along the first 1,000 m of separation distance (Figure 3). This indicates the occurrence of individuals that are more genetically related than the expected by random.

The information summarized by the first two axes derived from the factorial correspondence analysis explained 37 % of the total variance and showed genetic differences between adults and saplings (Figure 4). In this multivariate space, the scores of saplings along Axis 1were constrained between -0.7 and 0.7. In contrast, the scores of adult trees ranged between -1 and 1.5 for the same Axis 1. The coefficients of adults also showed a higher variation on the Axis 2 (Figure 4).

Discussion

The management implemented in the Mayan zone has received international acknowledgement as a low impact, socially fair and a community-based forestry program (Bray et al., 2003). However, recent ecological evidence obtained for Swietenia macrophylla indicates the existence of negative effects of selective logging on different components related with its natural regeneration. For example, selective logging limits fruit production (Snook et al., 2005), seed dispersal (Cámara-Cabrales and Kelty, 2009) and increase both, the risk of herbivory and seedlings mortality (Gutiérrez-Granados et al., 2011). In accordance with our prediction, the genetic differences detected in this study between adults and saplings of S. macrophylla are compatible with those expected under conditions of selective logging.

Genetic diversity. Overall, our results were similar to those reported for other Mexican populations of Swietenia macrophylla sampled within the Yucatan peninsula and analyzed with microsatellite loci. For example, Trujillo-Sierra et al. (2013) reported from 21 to 26 alleles per population (29 alleles in total), whereas 25 alleles were reported in this study (in the group of adults for comparison). Mean values of the observed heterozygosity (H_O) of 0.420 and 0.410 has been reported respectively by Trujillo-Sierra et al. (2013) and by Alcalá et al. (2014), which coincide with our estimate of 0.451. These two studies also showed a statistically significant deviation of the genotypic frequencies, revealing a high coefficient of fixation (0.309 and 0.449, respectively). In this study, a mean value for the F_IS was 0.43. All the results involving allelic and genotypic information indicate that Mexican populations could maintain overall low levels of genetic diversity and high scores for the coefficient of fixation by historic reasons. This is because there is evidence that suggests that northern populations of Swietenia macrophylla maintain lower heterozygosity due to the colonization toward northern latitudes from South America (Lemes et al., 2003, Novick et al., 2003), a pattern that is still observed along the distribution of this species in Mexico (Alcalá et al., 2014).

Statistically significant differences between adults and saplings were detected for the number of alleles present at different frequency categories. In fact, saplings of Swietenia macrophylla showed lower polymorphism, lacking of two alleles that were present in adult trees. These results are similar to the reported for other tree species subjected to selective logging (Rajora et al., 2000; Silva et al., 2008). Interestingly, no statistical differences between adults and saplings of S. macrophylla were found for the mean values of H_O, H_E, and the coefficient of fixation (F_IS). Although a clear reduction in H_O and a statistically significant increase in the coefficient F_IS have been reported for S. macrophylla as a result of selective logging (André et al., 2008), most studies in other tree species have not reported at a short-term, genetic differences between logged and unlogged populations (Rajora et al., 2000; Cloutier et al., 2007; Sebbenn et al., 2008; Silva et al., 2008), fragmentation and habitat degradation (Lowe et al., 2005), and even at a long-term as revealed by simulation models (Young et al., 1996; Degen et al., 2006; Sebbenn et al., 2008). Therefore, although changes in allelic frequencies and loss of rare alleles produced by selective logging have been commonly detected (Rajora et al., 2000, Silva et al., 2008, this study), heterozygosity seems to be highly resilient to the reduction in population size. This is because under neutrality, the theoretically per generation rate of loss of heterozygosity is set at 1/2Ne (Franklin, 1980). At this rate, population reductions should occur at a very high magnitude to produce marked reductions, as the loss of rare alleles (those that are lost first) shows a limited effect on this parameter in the short-term (Hedrick, 2000). However, the absence of differences in heterozygosity between adults and saplings may be explained by the overall low levels of genetic diversity that Mexican populations sustain as a result of the expansion of its geographic range, as explained above (Lemes et al., 2003, Novick et al., 2003; Alcalá et al., 2014).

Genetic structure. The occurrence of a fine-scale genetic structure has been commonly detected in plant populations through the implementation of autocorrelation analysis. In particular, some ecological factors affecting local patterns of gene movement have been advanced to explain the fine-scale genetic structure observed in tropical trees. For example, in adults of Dicorynia guianensis Amshoff the within-population genetic structure resulted from tolerance to selfing, overlapping generations or selection (Latouche-Hallé et al., 2004). In adults of Swietenia macrophylla (Lowe et al., 2003) and Simarouba amara (Hardesty et al., 2005) autocorrelation resulted as a consequence of restricted seed dispersal, whereas in Bagassa guianensis Aubl. the genetic structure was due to biparental inbreeding (Silva et al., 2008).

In this study, no evidence of fine-scale genetic structure in the group of adult trees was found. However a positive genetic structure was found in the group of saplings. The genetic information of adult trees (not deviated from a random pattern) may represent conditions of higher gene flow that were present before or very close to the implementation of the first cutting cycle in the stand (ca. 16 years ago). Consequently, the positive spatial autocorrelation observed in saplings is interpreted as evidence of disruption in the local pattern of gene flow probably produced by selective logging.

Even under random mating, in conditions of limited seed dispersal it can be expected an increase in relatedness at decreasing spatial scales (Vekemans and Hardy, 2004). Seeds of Swietenia macrophylla remain viable for only few months, so seedlings present in the area have resulted unequivocally from seeds recently produced. Therefore, progeny could reflect the occurrence of current ecological conditions that affect gene admixture in sites subjected to selecting logging. For example, it has been documented that small-remnant trees of S. macrophylla in the Mayan zone seems to show a limited seed dispersal (Cámara-Cabrales and Kelty, 2009). So the higher genetic relatedness in the group of saplings should be linked to the limited seed dispersal caused by selective logging. This is because the progeny has been produced mainly by small and nearby remnant trees, as the largest individuals have been almost entirely removed (Santos-Jiménez et al., 2005).

In addition, a restricted gene movement could also be explained by a limited pollen movement, as anthropogenic activities have the potential to disrupt mutualistic interactions. First, changes in behaviour of pollinators affecting reproductive success in tropical trees have been detected in disturbed forests (Ghazoul et al., 1998; Ghazoul and McLeish, 2001). Second, outcrossing rates may be also diminished by a reduction in the proportion of flowering trees in logged forests (Murawski and Hamrick, 1991; Murawski et al., 1994; Obayashi et al., 2002). Third, the average effective number of pollen donors and the number of sires per mother were lower in isolated patches than in continuous forests (Rosas et al., 2011). These three effects suggest that in our study, saplings could have been derived from a subset of adult trees, whereas a higher number of reproductive individuals were involved in the production of current adult trees. Therefore it seems that both, the alteration of the interaction with pollinators and the limited seed dispersal produced by selective logging could be involved in the higher genetic structure observed in the group of saplings (Lourmas et al., 2007).

The results derived from the autocorrelation analyses were supported by the results obtained from the factorial correspondence analyses that indicated a higher genetic structure within the saplings groups. Although the factorial correspondence analysis is not an explicit spatial approach to test for genetic structure, it showed that the multi-locus genotypic variation of adult trees was twice as much as the observed in the group of saplings. This result agreed with the observed for other tropical tree species. For example, a reduction in the number of genotypes has been documented as a result of selective logging (Degen et al., 2006), whereas the number of mutilocus genotypes registered in seedlings was a half compared with those present in adult trees of Swietenia macrophylla located in a forest fragment of Brazil subjected to selective logging (André et al., 2008).

The integration of ecological data available in literature with the genetic information about Swietenia macrophylla in the Mayan zone provided by this study, indicates that the current management program performed under the current conditions (i.e. 25-y cycles, minimum cutting diameter ≥ 55 cm), should be reviewed in order to assure not only natural regeneration, but the maintenance of genetic diversity. It is important to note that the genetic differences (loss of alleles, higher genetic structure) observed between adults and saplings in this study, are related to the implementation of the first cutting cycle, some 16 y ago. Therefore, future cutting cycles of adult reproductive trees could reduce the effective population size, which in consequence could produce higher negative impact on allelic richness and heterozygosity. The protection of several large individuals as pollen donors and seed sources should occur to increase gene flow and the effective population size. Large individuals are crucial to maintain the genetic diversity of the northernmost big-leaf mahogany populations, and the Mayan zone inhabitants' income as well.

Acknowledgements

Authors are grateful to the Organización de Ejidos Productores Forestales de la Zona Maya, S. C., in particular to Ing. V. J. Santos Jiménez for the access to the site. Field assistance was provided by H. Salazar, L. Y. Bustos and M. Chan. We also acknowledge the comments and suggestions provided by two anonymous reviewers that greatly improved the quality of this manuscript. This study was funded by the Comisión Nacional para el estudio de la Biodiversidad (CONABIO).

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