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Population Structure and Mating System in Tachigali Versicolor, a Monocarpic Neotropical Tree

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Population Structure and Mating System in Tachigali Versicolor, a Monocarpic Neotropical Tree Heredity 81 (1998) 134–143 Received 28 May 1997, accepted 24 November 1997 Population structure and mating system in Tachigali versicolor, a monocarpic neotropical tree M. D. LOVELESS*%, J. L. HAMRICK^ & R. B. FOSTER§ %Department of Biology, The College of Wooster, Wooster, OH 44691, U.S.A., ^Departments of Botany and Genetics, University of Georgia, Athens, GA 30602, U.S.A. and §Department of Botany, Field Museum of Natural History, Chicago, IL 60605, U.S.A. Patterns of genetic differentiation among six populations of Tachigali versicolor (Fabaceae: Papilionoideae) on Barro Colorado Island, Panama were investigated. Average gene diversity within any one population (He) was 0.073 (SD 0.010), and He over all populations was 0.080. Populations showed relatively little genetic differentiation (mean GST = 0.069), suggesting high levels of gene flow. A direct estimate of pollen flow indicated that 21% of the pollen received by a cluster of five trees had travelled at least 500 m. Genetic analyses of the mating system showed complete outcrossing (tm = 0.998, SE¹0.054; mean ts = 1.001, SE¹0.063). Estimates of F at different life stages showed a slight deficiency of heterozygotes in the six population samples, a slight excess among the 25 flowering adult trees, and no significant deviation in heterozygosity in progeny arrays. These differences may reflect the monocarpic life history of T. versicolor, in which adults flowering in a given year represent a temporal genetic bottleneck, producing a Wahlund effect in genotype frequencies in the overall population. This interpretation of genetic structure in T. versicolor suggests the overriding importance of ecological factors and life history on genetic processes in natural populations. Keywords: gene flow, genetic diversity, genetic structure, mating system, monocarpy, Tachigali versicolor. Introduction evolutionary and ecological dynamics of the population. Population genetic structure and the mating system Recent studies have examined the genetic make- are closely interrelated aspects of a species’ up of tropical tree populations (reviewed in Love- ecological genetics. The amount of genetic variation less, 1992; Hall et al., 1994; Boshier et al., 1995a,b; in a species is affected by various ecological pheno- Gibson & Wheelwright, 1995). In general, tropical mena (Loveless & Hamrick, 1984; Hamrick & Godt, plant species have levels of allozyme variability 1990), as well as by the mating system (Holtsford & equal to those of their temperate counterparts Ellstrand, 1989). Furthermore, the way in which (Hamrick & Godt, 1990; Loveless, 1992). Analyses genetic variation is distributed among populations is of genetic differentiation at a local scale on Barro closely tied to gene flow, both by pollen and seed Colorado Island, Panama (hereafter BCI) show that movement (Levin & Kerster, 1974; Loveless & populations separated by one to several kilometres Hamrick, 1984). Because genetic structure is gener- have relatively little genetic differentiation, implying ated by the dispersal, survival and reproduction of high levels of gene flow. Such patterns of population individuals in a population over time, an apprecia- differentiation can be correlated with breeding tion of the evolutionary genetics of a species must biology, individual distribution, and pollen and seed take into account not only strictly genetic events, dispersal (Hamrick & Loveless, 1989; Hamrick & such as fertilization and the mating system, but also Murawski, 1990). Evidence suggests that gene flow ecological and life history traits as they influence the in tropical forests is often substantial, tying together populations of even relatively rare tropical trees into *Correspondence. E-mail: [email protected] large demes or breeding units (Hamrick & Muraw- 134 ©1998 The Genetical Society of Great Britain. GENETIC STRUCTURE IN TACHIGALI VERSICOLOR 135 ski, 1990; Chase et al., 1996; Nason et al., 1996; Stacy peccaries and fungal infection) mortality (Kitajima et al., 1996). & Augspurger, 1989). Information on the reproductive biology and Seeds lack dormancy, and germination occurs at mating systems of tropical trees provides an inde- the start of the rainy season, in late April and early pendent corroboration of high levels of gene flow. May. Germination of undamaged seeds is high, and Initial studies of tropical plant mating systems seedling shadows may be dense beneath adults. demonstrated that dioecy and other sexual systems Seedlings are shade-tolerant, persisting for many which enforce outcrossing were more common in years in the understorey. However, seedlings in tropical than in temperate species (Bawa & Opler, light-gaps grow rapidly, forming a cohort that is 1975). High levels of outcrossing have been heterogeneous in size (Kitajima & Augspurger, confirmed by genetic analyses of tropical tree mating 1989). To reach canopy size, several gap-mediated systems (reviewed in Loveless, 1992). Fewer data are growth spurts are probably necessary. available for seed dispersal; however, the preponder- ance of animal-mediated seed dispersal suggests that dispersal should have a high variance, permitting Field collections long-distance seed movement (Hamrick & Loveless, Genetic diversity on BCI was sampled at two spatial 1986; Hamrick et al., 1993). scales. Four collection areas located about 200 m In this paper, local patterns of genetic organiza- apart were chosen within a 50 ha mapped forest plot tion in populations of Tachigali versicolor (Fabaceae: established in 1980 (the Forest Dynamics Plot, or Papilionoideae) on BCI, Panama, are described and FDP; Hubbell & Foster, 1983). Within each area, 72 the mating system is analysed using allozyme individuals were sampled. Two additional off-plot markers. These data allow calculation of indirect sites, each located at least 1 km from the FDP, were and direct estimates of gene flow in a natural popu- also identified. Fifty individuals were sampled in lation of this tropical tree. these sites. In all locations, individuals of different size classes were sought over an area of 6–8 ha. Leaf Materials and methods collections were kept cool in the field, vacuum-dried for at least 48 h, packaged with dessicant, and The study species returned to the U.S.A. Dried samples were kept at Tachigali versicolor (Fabaceae: Papilionoideae) is 70°C until used for electrophoresis. found from Costa Rica to western Colombia (Croat, Seed collections were made in February and 1978). It is a relatively common canopy tree in March 1985, when mature fruits from the 1984 secondary and primary forests on BCI (Foster, 1977; flowering episode (Fig. 1) were being dispersed. Kitajima & Augspurger, 1989). Tachigali versicolor is Seeds were collected directly beneath 25 adult trees. monocarpic: adults die after flowering (Foster, In those cases where seed shadows of different 1977). Other, South American species of Tachigali adults might have overlapped, collections were made are also apparently monocarpic (Gentry, 1993). Age in a direction away from other seed sources. Seeds at flowering is unknown, but growth rates vary were germinated in a growing house on BCI, and widely, depending on the light environment of seed- leaf tissue was vacuum-dried. lings and saplings (Augspurger, 1984; Kitajima & Augspurger, 1989), and trees may flower in a wide Laboratory procedures range of size classes (Foster, pers. obs.; Loveless, pers. obs.). Flowering is pulsed at intervals of 4 to Horizontal starch gel electrophoresis was performed 6 years (Foster, 1977, pers. obs.). On BCI, flowering on the samples. The dried leaves were crushed occurred in 1970, 1974, 1978, 1983, 1984, 1989 and under liquid nitrogen, mixed with an extraction 1994 (Foster, 1977, pers. obs.). Although individuals buffer and adsorbed onto filter paper wicks. A total sometimes flower (and die) out of synchrony, in of 31 allozyme loci in 17 enzyme systems were most off-years there is no flowering. resolved in the population samples. Isozymes and Flowering occurs from January to July. Individual buffers used in this study are given in Table 1, and trees flower for 6–12 weeks. The mature fruit is a are modified from Soltis et al. (1983). large, wind-dispersed, single-seeded samara. Most Four loci (Idh, Dia, Fe1 and Fe3) were used to fruits fall s100 m from the parent (Kitajima & assess mating systems. In all cases, progeny banding Augspurger, 1989). Fruits suffer both pre- (bruchid patterns were consistent with a simple Mendelian beetles and parrots) and postdispersal (rodents, interpretation of the allozyme loci. © The Genetical Society of Great Britain, Heredity, 81, 134–143. 136 M. D. LOVELESS ET AL. Table 1 Enzyme systems resolved in electrophoretic analyses of Tachigali versicolor. Buffer systems are taken from Soltis et al. (1983) Abbreviation and loci Buffer system Enzyme system scored (n) 6 Fluorescent esterase Fe (3) Peroxidase Per (2) Leucine amino peptidase Lap (2) Acid phosphatase Acp (1) Malic enzyme Me (1) Colorometric esterase Ce (3) Triose-phosphate isomerase Tpi (3) Phosphogluco isomerase Pgi (2) Phosphoglucomutase Pgm (2) 4 6-Phosphate dehydrogenase 6Pgdh (2) Aldolase Ald (1) 5 Isocitrate dehydrogenase Idh (1) Diaphorase Dia (1) Fig. 1 Map showing the location of flowering individuals Malate dehydrogenase Mdh (4) and sampled trees (squares) of Tachigali versicolor on 7 Glutamic-oxaloacetic Got (1) Barro Colorado Island, Panama, in 1984. The forest transaminase dynamics plot is shown by the box in the centre of the Diaphorase Dia (1) island. The five trees indicated
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