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Reproductive Biology |
Escuela de Biología, Universidad de Costa Rica, Ciudad Universitaria "Rodrigo Facio," San Pedro de Montes de Oca, San José, Costa Rica
Received for publication July 7, 2000. Accepted for publication February 23, 2001.
ABSTRACT
We studied the breeding systems of four populations of Enterolobium cyclocarpum (guanacaste, earpod tree) in Costa Rica. Multilocus estimates of the outcrossing rate indicate that E. cyclocarpum is a predominant outcrossing species (tm ranged between 0.881 and 0.901) and biparental inbreeding is low (range between 0.058 and 0.079). Overall, our analyses showed significant differences in the gene frequencies between pollen and ovules and significant differences in pollen gene frequencies between the four populations. We also found significant differences in the pollen gene frequencies calculated for single trees in the same population. Outcrossing rates and pollen gene frequencies varied in two consecutive years in two populations of E. cyclocarpum. The correlated mating model revealed that there are differences in the correlation of paternity between populations and years. These findings indicate that there is variation in the average number of trees that father the seed crop of each tree and/or that some fathers are overrepresented in the seed crop of each tree. The implication of these findings for the development of strategies for conservation and management of this species are discussed.
Key Words: correlated mating • correlation of paternity • gene frequencies • isozymes • mixed mating • outcrossing rate
It is well known that mating systems influence the amount as well as the distribution of the genetic variation within and among populations (Wright, 1921
; Stebbins, 1950, 1957
; Baker, 1953
; Grant, 1958
; Hamrick, Linhar, and Mitton, 1979
; O'Malley et al., 1988
; Hamrick and Loveless, 1989
; Hamrick et al. 1991
). The net result of the operation of the various breeding systems is the regulation of the outcrossing rates, which may vary among populations and among geographical regions (Bateman, 1956
; Grant, 1958
). For example, in Gilia achilleifolia the outcrossing rate varies among multiple populations (Schoen, 1982a, b
). This variation is in part explained by the amount of time occurring between anther dehiscence and the start of stigma receptivity within the flower (degree of protandry) (Schoen, 1982a, b
). Similarly, other studies have revealed considerable spatial and temporal variation in outcrossing rates in various species of pines (Shaw and Allard, 1982
; Cheliak, Pitel, and Murray, 1985
; Cheliak et al., 1985
) and Eucaliptus (Moran and Brown, 1980
).
The majority of tropical rain forest species investigated so far appeared to be outcrossers with extensive gene flow (Ashton, 1969
; Bawa, Perry, and Beach, 1985
; Murawski and Hamrick, 1991
; Hamrick et al., 1991
; Hall, Chase, and Bawa, 1994
; Hall, Orell, and Bawa, 1994
; Doligez and Joly, 1997). Isozyme studies conducted to determine the mating system of these species further support the predominance of outcrossing among tropical rain forest trees (O'Malley and Bawa, 1987
; O'Malley et al., 1988
; Murawski et al., 1990
; Hamrick and Murawski, 1991, 1992, 1994
; Hall, Chase, and Bawa, 1994
; Hall, Orell, and Bawa, 1996
; Doliguez and Joly, 1997
; James et al., 1998
). Doliguez and Joly (1997)
and Nason and Hamrick (1997)
recently reviewed the outcrossing rates reported for 28 and 36 species of tropical forest trees in natural populations, respectively. They found that most of these species have estimates of outcrossing rates higher than 0.80.
Only a few studies have examined the variation in the outcrossing rates of tropical plants (Murawski et al., 1990; Murawski and Hamrick, 1991, 1992
; Escalante et al., 1994
; Pascarella, 1997
; James et al., 1998
). For example, it has been reported that the outcrossing rate did not vary significantly among wild and cultivated populations of Phaseolus coccineus in Mexico (Escalante et al., 1994
). However, the same study also revealed great variation in the outcrossing rates among families within each population. In contrast, Pascarella (1997)
showed that outcrossing rates varied significantly among four populations of the tropical shrub Ardisia escallonioides in south Florida. He also showed that outcrossing rates were not correlated with the number of flowering plants within a population. His finding contrasted with those of Murawski and Hamrick (1991)
who reported a significant decrease in the outcrossing rates of Cavanillesia platanifolia as the density of flowering trees declined.
Spatial and temporal variation in the outcrossing rates of tropical rain forest trees has been examined by Murawski and Hamrick (1991, 1992)
, Hall, Chase, and Bawa (1994)
, Hall, Walker, and Bawa (1996)
and Murawski, Dayanandan, and Bawa (1994)
. For example, it has been reported that the outcrossing rates of two populations of Cavanillesia platanifolia in Panama were different (Murawski and Hamrick, 1992
). In addition, this species also showed significant variation in the outcrossing rates in two consecutive years in the population on Barro Colorado Island (Murawski and Hamrick, 1991
). They found that the outcrossing rate was directly correlated to the density of flowering trees (Murawski and Hamrick, 1991, 1992
). In contrast, Hall, Orrell, and Bawa (1994)
did not find differences in the outcrossing rates among nine populations of Carapa guianensis in Costa Rica. They concluded that the high population density and synchronous flowering contributed to the high outcrossing rates. The difference between these two studies could be due to the fact that one species (C. platanifolia) is self-compatible while Carapa guianensis is self-incompatible (J. L. Hamrick, personal communication). Because of that, the later would be expected to have much less flexibility in the amount of outcrossing/selfing.
In another study, Hall, Walker, and Bawa (1996)
reported that outcrossing rates for Pithecellobium elegans did not differ across two consecutive years, while the proportion of flowering trees was significantly different between years. Similar findings were also obtained for Shorea trapezifolia in Sri Lanka, in two consecutive years the estimates of outcrossing rates only varied from 54 to 62% (Murawski, Dayanandan, and Bawa, 1994
). The authors argued that the variation in outcrossing rates among individual trees suggested that the rate of self-incompatibility in this species is also variable.
Here, we report the results of a study aimed at determining the rates of outcrossing of the tropical dry forest tree Enterolobium cyclocarpum in Costa Rica. We also report the variation in gene frequencies in pollen and ovules and in the correlation of paternity among populations in four different geographical areas. Moreover, we report the variation in all estimates for two consecutive years for two of the populations considered in this study.
MATERIALS AND METHODS
Study organism
The guanacaste (Enterolobium cyclocarpum Jacq.) is a native leguminous tree, widely distributed throughout the Neotropics, ranging from Central Mexico to the northern part of South America (Pennington and Sarukhan, 1968
; Little, Woodbury, and Wadworth, 1974
; Janzen, 1983
). It is most frequently found in lowland deciduous and semideciduous dry forests. In Costa Rica, it normally occurs at low densities in intact forests where they tend to be most abundant in areas of frequent local disturbance (Standley, 1937
; Janzen, 1983
; Zamora, 1991
). This species is very important in the communities in which it is present because the few scattered trees are typically quite large (Holdridge and Poveda, 1975
; Janzen, 1983
; Francis, 1988
).
Flowering occurs synchronously throughout the western lowlands of Costa Rica starting in early March, at a time when the tree is leafless or just expanding the first leaves. Each tree produces numerous inflorescences each year. The apetalous flowers are white and borne in loose umbels. The flowers open in the late afternoon and remain open all night. They do not wilt until mid-morning of the following day, i.e., each flower lasts <24 h. Enterolobium cyclocarpum disperses its pollen in polyads consisting of 32 pollen grains (Rubick and Moreno, 1991
). Pollen flow between Guanacaste trees is believed to be mediated by moths, beetles, and other small nocturnal insects (Janzen, 1982
), as well as other diurnal insects such as bees (O. J. Rocha, personal observations).
Each inflorescence initiates 0–3 fruits, but typically only one develops. These minute fruits remain dormant throughout the subsequent rainy season (mid-May to mid-December) and very rapidly expand to full size in late January to February (4–15 cm in diameter) (Janzen, 1982
; Zamora, 1991
). Fruits ripen from March through May, about the time those flowers that will produce fruits the following year are opening. Mature fruits are smooth, shiny, indehiscent, relatively dry, and deep brown. Trees of this species can produce as many as 18 seeds per fruit (Janzen, 1982
).
The mature seeds are hard, ovoid, brown, and weigh from 300 to 1000 mg (Janzen, 1983
). At the beginning of the rainy season, seed germination is abundant after the hard seed coats have been weakened or broken by mechanical or thermal wear, or by microorganism activity (Janzen, 1983
). Often all of the seeds of a fruit will germinate before the fruit wall rots (O. J. Rocha, personal observation).
Fruit collection
Fruits of >100 trees of Enterolobium cyclocarpum (guanacaste) from four locations in Costa Rica (Tárcoles, Ciudad Colón, Cañas, and Térraba) were obtained in 1994. At least 25 open-pollinated fruits were collected from each tree. In addition, we also collected fruits from 21 trees from the Térraba region in 1995 and 15 trees from Tárcoles in 1993. Some trees were collected in both years, so that we could obtain estimates of the outcrossing rates for two consecutive years. All seeds from each fruit were kept in separate paper envelops and stored in the dark at room temperature until used for genetic analyses.
Isozyme electrophoresis procedure
To determine the outcrossing rate of E. cyclocarpum, we determined the genotypes of seeds from each tree, using the sampling schemes described below. All seeds were germinated before enzymes were extracted. To facilitate seed germination, the seed coat of each seed was weakened with a file, soaked in water for 24 h, placed in a glass petri dish, and incubated at 25°C. Seeds were examined twice a day until radicle emergence, which typically occurred between 48 and 72 h. Enzymes were extracted when the germinating seedlings were at least 2 cm long, i.e., between 72 and 96 h after the emergence of the radicle, according to the methods of Mitton et al. (1979)
, Hamrick and Loveless (1986)
, Rocha and Lobo, (1996)
. The extraction buffer had the following components: 0.1 mol/L Tris HCl pH 8.0, 0.02 mol/L DTT, 0.006 mol/L PVP, and 0.1% mercaptoethanol. Starch gel electrophoresis methods followed Hamrick and Loveless (1986)
and Cheliak and Pitel (1984)
. We determined the genotype for five polymorphic enzyme systems markers: EST, PGI, PGM, IDH, and DIA (DDH). Electrophoresis was performed using a continuous histidine-citrate buffer system, with an electrode buffer of 0.065 mol/L L-histidine, 0.019 mol/L citric acid, pH 6.7. The gel buffer was a 1 : 7 dilution of the electrode buffer (Wendel and Weeden, 1989
). For multiple isozymes, the most anodal isozyme was arbitrarily numbered "1," with the remaining isozymes numbered sequentially. The different electromorphs (alleles) for each isozyme (locus) were identified in a similar fashion, the most anodal allele was arbitrarily identified as "A," with the remaining alleles identified sequentially.
Data analyses
To examine the differences in the relatedness among progenies from each tree, i.e., among pods and within pods, we used two sampling schemes: (1) in the first, we scored the genotype of 20–25 seeds per tree, each from a different pod. The first sampling scheme should allow us to determine, more precisely, the maternal genotype and also provide us with a good estimate of the gene frequencies in the pollen pool. This sampling was conducted in all four populations in 1994 (Table 1). In addition, we also sampled seeds from 15 trees from Tárcoles that were collected in 1993 and seeds from 21 trees from Térraba that were collected in 1995.
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The outcrossing rate was conducted using the method of Ritland and Jain (1981)
and the MLT Program provided by Ritland (1990)
. This method is based on the mixed-mating model proposed by Ritland and Jain (1981)
, where the mating parameters are estimated based on the assumption that the seed crop of a tree is made up of a proportion, t, of outcrossed seeds and a proportion, 1 – t = s, of self-fertilized seeds. It also assumes that each tree receives a sample of pollen with the allele frequencies representative of the population. Moreover, it also assumes that the gene frequencies in the pollen pool, as well as the outcrossing rates, are constant from one tree to another in the same population. According to this model, any increase in the number of homozygotes in the progeny, in relation to a totally outcrossed progeny, is due to selfing. For this reason, s is an estimate of the effective selfing rate, which includes real selfing, as well as biparental inbreeding (Ritland, 1989
). The analysis uses the electrophoretic data from each family to calculate multilocus estimates of outcrossing, tm, as well as the coefficient of inbreeding, F, for the population, and the gene frequencies for all alleles of each of the loci examined. Moreover, it can also provide separate estimates of the gene frequencies in the pollen pool and the ovules. This program also provides estimates of outcrossing rates and pollen allele frequencies for each tree. We tested for heterogeneity between the gene frequencies in the pollen and ovules as proposed by Wier (1996) and James et al. (1998)
.
Data was also analyzed using the correlated mating model proposed by Ritland (1989)
. This model introduces a modification to the mixed mating model, where the outcrossing rate is not expected to be the same for each tree and the gene frequencies in the pollen that each tree receives are allowed to be different. This modification allows one to investigate the proportion of matings occurring with the same sire, as well as the correlation of mating within progenies. Under this model, the observations are taken from the genotypes of pairs of progenies drawn from a random sample of all genotypes in the progeny of each tree. With this new arrangement of our data, we consider the probability of obtaining pairs of genotypes in a model where they are distributed according to the type of mating that produced each pair of progeny, i.e., self–self, self–outcrossed, and both outcrossed. The last group could be further subdivided according to the identity of the sire into fullsibs and halfsibs. The proportion of fullsibs among the outcrossed progeny is measured by the correlation of paternity, rp, and it serves as an indicator of the variation in the gene frequencies of the pollen received by each plant. This is expected in natural populations where trees differ in their flowering time, their degree of isolation, and the species composition and behavior of the pollinators that visit them (see Ritland, 1989
). In addition, the correlated mating model also provides an estimate of the correlation of outcrossing rate within progeny arrays. This parameter describes the correlation of outcrossing between two sibs; i.e., it is equal to 1, when sib pairs are either both self or both outcrossed.
RESULTS
Outcrossing rates
The analyses of the breeding system of the four populations of Enterolobium cyclocarpum using the mixed-mating model are shown in Table 2. These findings indicate that this species is predominantly outcrossed, as the multilocus estimators of the outcrossing rates are all high. Our results also show that the biparental inbreeding, as shown by the difference between the multilocus estimate and the mean single locus estimate, is low (Ritland, 1989
). These analyses also allowed an examination of the variation in outcrossing rates, rt, among sites. We found that, for the progeny collected in 1994, there are some differences in the multilocus estimates of outcrossing rates between the four locations tm ranging from 0.812 to 0.913).
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Correlated mating model
The analyses of the correlation of paternity of the four populations of E. cyclocarpum using the correlated mating model are shown in Table 5. Estimates using the first sampling scheme show that the correlation of outcrossing and the correlation of paternity vary not only from one location to another, but also among years (Tables 4A and 5). For 1994, the estimates of the correlation of outcrossing, rt, as well as the estimates of paternity, rp, show important differences in the breeding behavior among the four locations. In addition, when we compare our two estimates for the location of Térraba, we found that the estimate of rp for 1995 is only 37% of that estimated for 1994.
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DISCUSSION
The goal of this study was to determine the breeding behavior of the tropical dry forest tree Enterolobium cyclocarpum (guanacaste) at four different locations in Costa Rica. In particular, we wanted to estimate the outcrossing rates, as well as other breeding parameters such as the rate of biparental inbreeding and the correlation of paternity and outcrossing among the progeny. In addition, we determined the levels of spatial and temporal variation in all estimates. Finally, we also obtained the allele frequencies of the pollen that sired the seed crop of the trees examined.
Our data supports the notion that E. cyclocarpum is a predominantly outcrossing species. All estimates indicate that >80% of the progeny produced from each tree were sired by pollen from another plant (tm ranges between 0.81 and 0.91). In addition, our findings also revealed very low levels of biparental inbreeding (tm – ts was only 
5%). Bawa, Perry, and Beach (1985)
reported that the majority of tropical rain forest species investigated so far appeared to have traits that enhance outcrossing. Moreover, the majority of isozyme studies conducted to determine the mating system of these species further support the predominance of outcrossing among tropical rain forest trees (Doliguez and Joly, 1997
; Nason and Hamrick, 1997
). However, only few neotropical dry forest trees have been studied in some detail, but they also appear to experience high rates of outcrossing (James et al., 1998
).
The reproductive phenology of dry forest species has been described by other authors (Frankie, Baker, and Opler, 1974
; Opler, Frankie, and Baker, 1980
). They found that, in contrast with wet forest species, most dry forest treelet and shrub species show a pronounced seasonal pattern, exhibiting a sharp peak of flowering at the beginning of the rainy season (Opler, Frankie, and Baker, 1980
). For trees, they found two peak periods of flowering activity, one during the long dry season and another at the onset of the rainy season (Frankie, Baker, and Opler, 1974
). In the case of Enterolobium cyclocarpum, the pattern is different. Flowering is synchronized among most trees in the population and typically occurs a few weeks before the beginning of the rainy season (Rojas, 2001
). However, a few trees consistently flowered earlier than the majority of the trees (O. J. Rocha, personal observation).
Synchronization of flowering among trees of E. cyclocarpum may play an important role in their breeding behavior. Individual tree estimates of outcrossing may suggest that there is important variation in the outcrossing rates among trees. If such variation is not an artifact of the estimation procedure, it is likely that deviation from the peak of flowering among trees can result in variation in the estimates of the rate of outcrossing for individual trees, as pollen allele frequencies may differ over time. Deviation from the peak of flowering that result in little overlap with other flowering trees is likely to result in geitonogamy and self-fertilization.
Heterogeneity of pollen allele frequencies among maternal trees was observed for all loci examined in this study. Pollen allele frequencies are estimated from the pollinations that sired seeds. This observation suggests that near-neighbors might be overrepresented in the progeny of a given tree as they might contribute more pollen than more distant trees. Thus, it is likely that each maternal tree mated with a different group of pollen donors. Alternatively, overrepresentation of one or a few pollen donors in the seed crop of a given tree might result from selective abortion of fruits and seeds (Rocha and Aguilar, 2001
). It has been well documented that pollen donors differ in their likelihood to sire seeds upon pollination. Therefore, differences in the ability to sire seeds among different pollen donors might also explain the high correlation of paternity observed in E. cyclocarpum.
Our estimates of outcrossing rates indicate that there is substantial movement of pollen among trees of E. cyclocarpum. Such estimates of outcrossing rates, accompanied by low values in the estimates of the correlation of paternity, strongly suggest that the number of pollen donors represented in the seed crop of E. cyclocarpum may be high. Such numbers could be explained on the basis of the behavior of its pollinators. Other authors have proposed that insect pollinators have the ability to disperse pollen widely in tropical forests (Gilbert, 1975
; Frankie, Opler, and Bawa, 1976
; Frankie et al., 1983
; Haber and Frankie, 1989
). In addition, Frankie and Haber (1983)
studied the movement of insect pollinators in the dry forest of Costa Rica, and they proposed that the variation in flowering phenology, nectar flow, volume, and quality is continually monitored by pollinators and that they are prompt to make intertree movements as they detect changes in these characters. Moreover, hawkmoths, as most tropical insect pollinators, are considered to have extensive foraging ranges (Haber and Frankie, 1989
). Thus, it might result in significant movement of pollen among mass flowering trees, such as E. cyclocarpum, which in turn, affect the outcrossing rates, the number of pollen donors in the seed crop, and the correlation of paternity.
Our data revealed that there is some spatial and temporal variation in the outcrossing rates of E. cyclocarpum. Such variation could be due to variation in the degrees of self-incompatibility among trees and/or to differences in flowering time, where asynchronous individuals are more likely to have higher rates of selfing. The multilocus mixed mating model proposed by Ritland and Jain (1981)
assumes that all maternal genotypes outcross at the same rate to a homogeneous pollen pool. In this study we found that allele frequencies in the pollen pool vary in space and time, i.e., they vary among locations, among trees within locations, and among years for given locations and trees. This finding suggests that the variation in outcrossing rates is most likely to be explained by the composition of the pollen pool that each tree receives and the levels of geitonogamy that they experience.
We found that the single tree estimates of pollen gene frequencies vary from one year to another. These changes may result in different estimates of the outcrossing rate. Moreover, two trees found growing in pastures, separated from continuous forest, flowered earlier than most trees in the area for three consecutive years. Under these circumstances of temporal and spatial isolation, the scarse nonself-pollen available limited fruit production to only a few pods, indicating that self-incompatibility is very strong.
The correlated mating model proposed by Ritland (1989)
revealed that the correlation of paternity varied significantly among locations and from one year to the next. These findings could be explained, at least in part, by the heterogeneity in the allele frequencies in the pollen pool, which in turn might be correlated to the mean number of pollen donors contributing to the seed crop of the trees. This is expected in natural populations where trees differ in their flowering time, their degree of reproductive isolation, and the species composition and behavior of the pollinators that visit them. But high estimates of the correlation of paternity may also be due to selective abortion of seeds and fruits (Rocha and Aguilar, 2001
).
Implications for conservation and management
The results presented here have implications for the conservation and management of E. cyclocarpum and other dry forest species. First, they show that given the high levels of genetic variation and the high levels of outcrossing, a moderate amount of seed trees could provide an adequate sample of the genetic constitution of this species. However, in another study, one of us found that there is a significant effect of the location of origin of the seeds on early indicators of plant vigor in E. cyclocarpum (O. J. Rocha and U. Estrada, unpublished results). This finding indicates that isozyme markers may not be representative of the variation of quantitative traits, especially those that are adaptative and sensitive to natural selection (Hamrick and Godt, 1996
; Lynch, 1996).
Second, the variation in the outcrossing rates among locations and among reproductive episodes also needs to be considered when defining sampling strategies (Kanowski and Boshier, 1997
). This is important not only for ex situ conservation or for restoration of locally extinct populations, but also for the establishment of commercial plantations (Boshier, Chase, and Bawa, 1995
). This issue should also be considered in areas where selective logging is being conducted (Hall, Orrell, and Bawa, 1994
; Murawski, Dayanandan, and Bawa, 1994
; Nason and Hamrick, 1997
), as the reduction in effective population size could increase the levels of inbreeding.
FOOTNOTES
1 The authors thank M. E. Zaldivar, A. G. Stephenson, J. L. Hamrick, and an anonymous reviewer for advice, comments, and/or criticisms on a previous version of this manuscript; L. Castro, E. Castro, O. Chaves, M. Artavia, J. I. Mena, and A. Cartín for laboratory, field, and greenhouse assistance and the Servicio de Parques Nacionales and the staff of Parque Nacional Carara and Parque Nacional Santa Rosa for their collaboration. This work was supported by the International Foundation for Science grant (grant IFS 1943), the International Plant Genetic Resources Institute and the Center for International Forestry Research (grants 96/ 073, 97/052, and 98/049), and a University of Costa Rica grant (VI-111-91-223) to O. J. Rocha. 
2 Author for reprint requests (ojrocha{at}cariari.ucr.ac.cr
).
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