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Flexible Mating System in a Logged Population of Swietenia Macrophylla King (Meliaceae): Implications for the Management of a Threatened Neotropical Tree Species

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Flexible Mating System in a Logged Population of Swietenia Macrophylla King (Meliaceae): Implications for the Management of a Threatened Neotropical Tree Species Plant Ecol (2007) 192:169–179 DOI 10.1007/s11258-007-9322-9 ORIGINAL PAPER Flexible mating system in a logged population of Swietenia macrophylla King (Meliaceae): implications for the management of a threatened neotropical tree species Maristerra R. Lemes Æ Dario Grattapaglia Æ James Grogan Æ John Proctor Æ Roge´rio Gribel Received: 21 February 2007 / Accepted: 22 May 2007 / Published online: 19 June 2007 Ó Springer Science+Business Media B.V. 2007 Abstract Microsatellites were used to evaluate the crossed matings and that the remaining 6.75% had mating system of the remaining trees in a logged genotypes consistent with self-fertilisation. Apomixis population of Swietenia macrophylla, a highly valu- could be ruled out, since none of the 400 seedlings able and threatened hardwood species, in the Brazil- analysed had a multi-locus genotype identical to ian Amazon. A total of 25 open pollinated progeny its mother tree. The high estimate of the multi-locus arrays of 16 individuals, with their mother trees, were outcrossing rate (tm = 0.938 ± 0.009) using the mixed genotyped using eight highly polymorphic microsat- mating model also indicated that the population in ellite loci. Genotypic data analysis from the progeny this remnant stand of S. macrophylla was predomi- arrays showed that 373 out of the 400 seedlings nantly allogamous. The relatively large difference (93.25%) were unambiguously the result of out- between the multi-locus and single-locus outcrossing estimates (tmÀts = 0.117 ± 0.011) provides evidence that, in spite of the high outcrossing rate, a consid- & M. R. Lemes ( ) Á R. Gribel erable degree of biparental inbreeding has contrib- Laborato´rio de Gene´tica e Biologia Reprodutiva de Plantas, Instituto Nacional de Pesquisas da Amazoˆnia, uted to the genetic structure of this population. Levels Avenida Andre´ Arau´jo, 2936, Manaus, AM 69083-000, of outcrossing were not evenly distributed among Brazil maternal trees (tm ranging from 0.39 to 1.00), sug- e-mail: [email protected] gesting the occurrence of a variable degree of self- M. R. Lemes Á J. Proctor incompatibility and/or dichogamy among individual School of Biological and Environmental Sciences, trees of this monoecious species. Due to its generalist University of Stirling, Stirling FK9 4LA, Scotland, UK pollination system and some level of tolerance for selfing, S. macrophylla seems to be resilient to D. Grattapaglia Laborato´rio de Gene´tica de Plantas, EMBRAPA-Recursos environmental disturbances such as those caused by Gene´ticos e Biotecnologia, C.P. 02372, Brası´lia, DF logging, since it sets fruits with predominantly out- 70770-900, Brazil crossed seeds even at low stand densities. Therefore, the remaining individuals in logged areas or in relict J. Grogan Yale University School of Forestry and Environmental fragments may be very important for long-term pop- Studies, 360 Prospect Street, New Haven, CT 06511, USA ulation recovery and genetic conservation programmes. J. Grogan Keywords Amazon Á DNA microsatellites Á Genetic Instituto do Homem e Meio Ambiente da Amazoˆnia (IMAZON), Rua Domingos Marreiros, 2020, Bairro conservation Á Genetic diversity Á Mahogany Á Fa´tima, Bele´m, PA 66060-160, Brazil Outcrossing 123 170 Plant Ecol (2007) 192:169–179 Introduction gap-colonising tropical trees with light-requiring juve- niles and adults persistent in the mature forest— The mating system determines how the transition of examples include the malvaceous Ceiba pentandra L. genotypic frequencies in a population occurs from one Gaertner and Cavanillesia platanifolia (Bonpl.) Kunth, generation to the next (Ritland 1988). The classifica- the legumes Senna multijuga (Rich.) H. S. Irwin & tion of the mating system in plants is based on the Barneby and Dinizia excelsa Ducke, and Cariniana genetic relatedness between the male and female legalis (Mart.) Kuntze (Lecythidaceae)—tend to be gametes (derived from the pollen and ovule, respec- somewhat tolerant to selfing (Murawski and Hamrick tively) in the newly formed zygotes (Ritland 1983). 1991; 1992a, b;Murawskietal.1994;Gribeletal. The mating system can be characterised in terms of the 1999;Dick2001; Ribeiro and Lovato 2004;Sebbenn proportion of mature seeds resulting from selfing or et al. 2000). outcrossing events (Murawski and Hamrick 1991). The conservation status of Swietenia macrophylla The mating system is an important factor in determin- King (Meliaceae) has been the subject of increasing ing how genetic variation is distributed among subdi- concern due to over-exploitation of this species by visions of a population and among individuals in those selective logging and increasing habitat destruction subpopulations, as well as among progenies, with a (Grogan and Barreto 2005). Despite the high socio- direct impact on the long-term maintenance of genetic economic importance of S. macrophylla, information variation in existing populations. The susceptibility of on the processes maintaining genetic variation in a population to the loss of genetic diversity and natural populations of this species is scarce. Studies inbreeding depression following for example logging on the population genetics of S. macrophylla have or habitat fragmentation will depend, to a considerable focused mainly on estimates of genetic diversity and extent, on the characteristics of its mating system. population structure in Central and South America The pattern of mating in tropical trees is complex, and implications for its conservation (Gillies et al. reflecting the influence of several genetic and ecological 1999; Lemes et al. 2003; Novick et al. 2003). factors such as the demography of adult trees, flower- In this study, the outcrossing rate (tm) and other ing intensity, synchrony of flowering among and mating system parameters (ts = the single-locus within individuals, the nature and intensity of self- population outcrossing rate, F = the single-locus incompatibility mechanisms, the foraging behaviour of inbreeding coefficient of maternal parents, and pollinators, and the selective abortion of young fruits. rp = the correlation of paternity) were estimated for a Although many plant populations and species appear to population of S. macrophylla in the Brazilian Amazon, produce mixtures of selfed and outcrossed progeny using eight highly polymorphic microsatellite loci (Barrett and Husband 1990), most tropical tree species (SSR—simple sequence repeat). The main aims were appear to exhibit morphological and physiological to understand how the mating system may contribute to adaptations, which promote outcrossing and prevent shaping and maintaining the levels of genetic variation or reduce selfing (Bawa 1990). As a result, the mating of the population and to infer how logging and habitat system of the majority of neotropical trees investigated fragmentation may affect the reproduction of remain- so far by using molecular markers, such as allozymes or ing individuals and the recovery capacity of the DNA microsatellites showed predominant or complete population. These findings, coupled with information outcrossing(seereviewinWardetal.2005). Addition- on pollination and seed dispersal mechanisms, have ally, a number of studies have shown that inbreeding of important implications for the long-term conservation biparental origin is frequently very low or undetectable and management of this valuable hardwood species. among tropical trees, at least with isozyme markers (Eguiarte et al. 1992;MurawskiandHamrick1992a, b; Hall et al. 1994; Boshier et al. 1995; Doligez and Joly Materials and methods 1997; James et al. 1998; Loveless et al. 1998). These findings contrast with previous ideas that autogamy Study site and inbreeding would be favoured in widely spaced conspecific tropical forest trees (Fedorov 1966). Based Field work was conducted at the Marajoara Manage- on data available so far, species of fast growing, ment Project site (c. 078 500S, 508 160W) in southeast 123 Plant Ecol (2007) 192:169–179 171 Para´ State, Brazil. The project site of about 4,100 ha and mother trees were genotyped at eight highly (13 · 3.15 km) of selectively logged forest was sub- polymorphic microsatellite loci previously developed divided into 12 plots of approximately 340 ha each and optimised in multiplexed fluorescence-based (1.08 · 3.15 km). Samples for the present study were systems for Swietenia macrophylla (Lemes et al. collected from trees randomly selected in plots 1, 2, 2002). and 3 (c. 1,020 ha) at the northern end of the project Microsatellite amplification was carried out in a area. These plots were selectively logged between final volume of 10 or 25 ml for single and multiplexed 1992–1994 at a relatively low intensity because the reactions, respectively, containing 1.25–2.0 mMof intended showcase status of the management project. each forward and reverse primer, 1 unit Taq DNA Even so, a full inventory covering an area of 204 ha polymerase, 200 mM of each dNTP, 1· reaction within the study area at Marajoara demonstrated that buffer (10 mM Tris-HCl, pH 8.3, 50 mM KCl, À1 only 16% of commercial-sized trees (45 cm diam- 1.5 mM MgCl2), BSA (2.5 mg ml ), 5.0 ng of eter at breast height (dbh) at the time of cutting) template DNA, and distilled ultrapure H2O. Ampli- remained after logging, compared to c. 8% survival fications were performed using a MJ Research PTC- after conventional logging (and 5% survival by 100 thermal controller using the following program trees >60 cm dbh, the current legal minimum cutting for all loci: an initial denaturation at 968C for 2 min, limit for mahogany; Grogan et al. in press). Stand followed by 30 cycles of 948C for 1 min, 568C for density of mahogany trees 45 cm dbh was therefore 1 min, and 728C for 1 min, and a final elongation step reduced from approximately one tree per 2 ha at 728C for 7 min. PCR products were electrophor- (0.51 haÀ1) to one tree per 12 ha (0.08 haÀ1). Within esed on a 5% denaturing polyacrylamide gel in an the study area, Swietenia macrophylla is nearly ABI Prism 377 sequencer. GeneScan and Genotyper always found at highest densities along the banks of software (Applied Biosystems Inc.) were used for small seasonally dry streams and in adjacent low- data collection and allele size estimation.
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