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Hedging in a Rare Yet Widespread Rainforest Tree, Syzygium

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Hedging in a Rare Yet Widespread Rainforest Tree, Syzygium bs_bs_banner Austral Ecology (2012) 37, 936–944 Reproductive bet-hedging in a rare yet widespread rainforest tree, Syzygium paniculatum (Myrtaceae)aec_2353 936..944 KATIE A. G. THURLBY,1,2,3 PETER G. WILSON,1* WILLIAM B. SHERWIN,2 CAROLYN CONNELLY1 AND MAURIZIO ROSSETTO1 1National Herbarium of NSW,Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia (Email: [email protected]), 2School of Biological, Earth and Environmental Sciences, and 3School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia Abstract The rare rainforest tree species, Syzygium paniculatum, is the only known Australian species of the genus to produce seeds that regularly have multiple embryos. Evidence from other species suggests that this is a case of adventitious polyembryony, with the embryos arising from maternal nucellar tissue. In the present study we use microsatellite data to determine whether sexual reproduction does occur and, if it does, to investigate the relative fitness of asexual versus sexual seedlings. Genotyping suggested that the species is a polyploid and our results found very little genetic diversity within and among populations (with a total of nine genotypic combinations across the entire species).The only significant variation was between the three northernmost populations and the other eight populations sampled. Analysis of individual embryos showed that sexually derived embryos did occur in some seeds but that these were not necessarily the fittest. In general, the seedling from the largest embryo is the first to emerge and maintains a competitive advantage over the other seedlings from the same seed. We discuss the ramifications of the low levels of genetic diversity and consider whether there is a direct relationship between polyembryony and the inferred polyploidy of the species. We consider the possible advantages of reproductive bet-hedging but also highlight the susceptibility of a species with low genetic diversity to extreme stochastic events. Syzygium paniculatum occurs in areas heavily impacted by human activity and these findings should contribute to improved management of this threatened species. Key words: agamospermy, clonality, littoral rainforest, polyembryony, polyploidy, Syzygium. INTRODUCTION tions unfavourable for sexual reproduction, such as strong pollen limitation in species-rich communities (Whitton et al. 2008); they could also increase the Sexual versus asexual reproduction survival of advantageous genotypes, enable a geno- type to sequester space and monopolize resources The major benefit of sexual reproduction is generally (including establishment of new populations from a believed to be the ability of an organism to produce single individual), or provide the potential to accu- new and potentially advantageous combinations of mulate variability through extended lifespan (Cal- genes, an advantage that is only available to obligate laghan et al. 1992; Hörandl 2004; Houliston & asexual species through somatic mutation. However, Chapman 2004; Paun et al. 2006; Vallejo-Marín et al. sexual reproduction can also be disadvantageous. A 2010; van der Merwe et al. 2010). As a result, some sexual parent transmits only 50% of its genes to its asexual species are as genetically diverse and wide- offspring, which could potentially lead to the break- spread as sexual species (Gitzendanner & Soltis down of favourable genic combinations and the loss of 2000; Paun et al. 2006). Asexual reproduction also local adaptation (Otto 2009). poses possible disadvantages, particularly if it results Asexual reproduction may provide genetic and in loss of genetic diversity. Reduced genetic variation ecological advantages, particularly in the short term and drift (Harper 1978; Eckert et al. 1999; Paun (e.g. van Dijk & van Damme 2000). These advan- et al. 2006) can result in the loss of short-term fitness tages might include the ability to persist in condi- and of long-term adaptive potential (Richards 2003; Zhang & Zhang 2007). *Corresponding author. Interestingly, models show that the benefits Accepted for publication December 2011. of sex may be obtained through facultative sexual © 2012 The Authors doi:10.1111/j.1442-9993.2011.02353.x Austral Ecology © 2012 Ecological Society of Australia REPRODUCTIVE BET-HEDGING IN SYZYGIUM PANICULATUM 937 reproduction without the cost (Green & Noakes 1995).This suggests that the combination of a range of reproductive mechanisms may provide the benefits of both sexuality and asexuality while reducing overall costs (Green & Noakes 1995; Paun et al. 2006; Vallejo- Marín et al. 2010). Agamospermy One particular case of asexual reproduction is agamo- spermy, the production of seed without sex (Talent 2009). It is a mechanism that affords offspring the advantages of seed production normally only available to sexually produced progeny: protection, disease resistance, dormancy and improved dispersal (Rich- ards 2003; Silvertown 2008). Sex can exist simultaneously with agamospermy because most forms of agamospermy require the initial development of a sexual embryo or, at the very least, fertilization and development of the endosperm (Ganeshaiah et al. 1991; Koltunow & Grossniklaus 2003; Whitton et al. 2008). So, in some polyembryonic seeds, sexual embryos may persist alongside the devel- oping agamospermic embryos (Ganeshaiah et al. 1991; Asker & Jerling 1992; Richards 2003; Whitton et al. 2008). However, stable coexistence of both sexual and asexual progeny may be difficult to accom- plish within a single population (Silvertown 2008) because embryos must compete for the resources afforded by the endosperm. As a result, the percentage Fig. 1. Distribution and sampling sites of Syzygium paniculatum. The asterisks identify collection sites along the of fruits containing sexual embryos will vary depend- New South Wales coast. ing on the outcome of this competition (Roy 1953, 1961; Narayanaswami & Roy 1960; Naumova 1992; Whitton et al. 2008). Studies in Citrus indicate that the zygotic embryo develops rather slowly, and may be 1961). In adventitious polyembryony the embryos outcompeted by the more vigorous nucellar embryos are genetically identical and are derived from the and fail to survive in seeds where many of these occur integument or the nucellus (the parts of the ovule (Koltunow 1993). adjacent to the embryo sac). The embryos in S. pan- iculatum vary in size and often have markedly unequal storage cotyledons. Embryos with cotyledons Study system of this type are cryptocotylar and germination is often hypogeal. The rare Australian rainforest tree Syzygium panicu- Syzygium paniculatum is locally rare and represented latum Gaertn. (Myrtaceae) may prove to have a by small populations distributed across a geographical complex mating system, combining multiple repro- range of about 400 km (Fig. 1). Because of its mode of ductive mechanisms. Fruits contain a single seed reproduction, the species is likely to have low diversity, which is usually polyembryonic, a trait not seen in which may be detrimental to fitness. Understanding any other Australian native Syzygium species. Poly- the relative contribution of sexual and asexual repro- embryony can arise by several means. One possible duction might help us to understand the causes of mechanism is cleavage polyembryony (the separation rarity in S. paniculatum, and this species may provide a of a zygote into two or more units; see Webber means for exploring the consequences of mating 1940), although this happens more often in gymno- mechanisms on the expansion or decline of rare sperms than angiosperms (Batygina & Vinogradova species. To better understand the impact of sexual 2007). It is most likely that polyembryony in S. pan- reproduction on rarity, current distribution and long- iculatum is due to agamospermy, as has been docu- term potential, this study aims to test the hypotheses mented in some Asian Syzygium species (Roy 1953, arising from the following points: © 2012 The Authors doi:10.1111/j.1442-9993.2011.02353.x Austral Ecology © 2012 Ecological Society of Australia 938 K. A. G. THURLBY ET AL. 1. Despite its wide distribution range, the rare the PCR and genotyping conditions reported in Thurlby S. paniculatum has low genetic diversity. The level et al. (2011). Genotyping traces were analysed using Gen- and distribution of genetic diversity are important emapper v4.0 (Applied Biosystems). To test genotyping elements in the development of appropriate con- accuracy, PCRs were repeated for each primer across 20% servation planning for this species. of the individuals. Fewer than 5% of repeats identi- fied errors needing confirmation with further PCR and 2. As suggested by other studies, there are asso- genotyping. ciations between polyembryony, apomixis and During the development of the SSR markers, it was polyploidy. noticed that multiple loci produced polyploid amplification 3. If both sexual and asexual reproduction mecha- patterns (Thurlby et al. 2011). In order to confirm the nisms are identified, it is expected that they polyploid nature of S. paniculatum and to verify the number could result in differential levels of fitness (as of alleles per locus, genotyping traces were obtained for measured by germination success and seedling three other Syzygium species: Syzygium corynanthum growth). (F.Muell.) L.A.S.Johnson, Syzygium francisii (F.M.Bailey) L.A.S.Johnson and Syzygium jambos (L.) Alston. Of the four Syzygium species tested, S. corynanthum and S. fran-
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