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Clonality Strongly Affects the Spatial Genetic Structure of the Nurse Species Aechmea Nudicaulis (L.) Griseb. (Bromeliaceae)

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Clonality Strongly Affects the Spatial Genetic Structure of the Nurse Species Aechmea Nudicaulis (L.) Griseb. (Bromeliaceae) bs_bs_banner Botanical Journal of the Linnean Society, 2015, 178, 329–341. With 4 figures Clonality strongly affects the spatial genetic structure of the nurse species Aechmea nudicaulis (L.) Griseb. (Bromeliaceae) ROBERTA LOH1,2,3, FABIO RUBIO SCARANO2,4, MARCIO ALVES-FERREIRA1 and Downloaded from https://academic.oup.com/botlinnean/article/178/2/329/2416415 by guest on 02 October 2021 FABIANO SALGUEIRO3* 1Laboratório de Genética Molecular Vegetal, Departamento de Genética, Centro de Ciências da Saúde, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Av. Prof. Rodolpho Paulo Rocco s/n, prédio do CCS, Sala A2-93, Ilha do Fundão, Rio de Janeiro CEP.: 21949-900, RJ, Brazil 2Laboratório de Ecologia Vegetal, Departamento de Ecologia, Centro de Ciências da Saúde, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Av. Prof. Rodolpho Paulo Rocco s/n, Ilha do Fundão, Rio de Janeiro CEP.: 21941-590, RJ, Brazil 3Grupo de Pesquisa em Biodiversidade Molecular Vegetal, Departamento de Botânica, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro, Av. Pasteur n°458, sala 512, Urca, Rio de Janeiro CEP.: 22290-240, RJ, Brazil 4Conservation International, Rua Buenos Aires n°68, 26° andar, Centro, Rio de Janeiro CEP.: 20070-022, RJ, Brazil Received 9 September 2014; revised 3 February 2015; accepted for publication 15 March 2015 Aechmea nudicaulis is a clonal bromeliad common to the Brazilian Atlantic forest complex and is found abundantly in the sandy coastal plain vegetation (restinga) on the north coast of Rio de Janeiro state, Brazil. This restinga site is structured in vegetation islands, and the species plays a key role as a nurse plant, much favoured by its clonality. We studied the clonal structure and consequences of clonality on the population spatial genetic structure (SGS) of this species using six nuclear microsatellites. Spatial autocorrelation analysis was performed to study the effects of sexual and clonal reproduction on the dispersal of A. nudicaulis. Analyses were performed at the genet (i.e. excluding clonal repeats) and ramet levels. Genotypic richness was moderate (R = 0.32), mostly as a result of the dominance of a few clones. The spatial distribution of genets was moderately intermingled, the mean clone size was 4.9 clonal fragments per genet and the maximum clonal spread was 25 m. Expected heterozygosities were high and comparable with those found in other clonal plants. SGS analyses at the genet level revealed significantly restricted gene dispersal (Sp = 0.074), a strong SGS compared with other herbaceous species. The clonal subrange extended across 23 m where clonality had a significant effect on SGS. The restricted dispersal and SGS pattern in A. nudicaulis, coupled with high levels of genetic diversity, indicated a recruitment at windows of opportunity (RWO) strategy. Moreover, the spatial distribution of genetic variation and the habitat occupation pattern in A. nudicaulis were dependent not only on the intrinsic biological traits of the species (such as spacer size and mating system), but also on biotic interactions with neighbouring species that determined suitable habitats for germination and the establishment of new genets. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 329–342. ADDITIONAL KEYWORDS: Atlantic forest – clonal growth – gene flow – microsatellite – restinga – SGS. INTRODUCTION development of a single zygote and consists of a group of genetically identical semi-autonomous units, Clonal plants are characterized by a hierarchical called ramets (Harper, 1977). Life history traits are organization, in which each genet is the product of the markedly different between clonal and non-clonal plants (Honnay & Jacquemyn, 2008). For instance, *Corresponding author. E-mail: mobility through clonal growth is limited in com- [email protected]. parison with seed dispersal (Eriksson, 1993), and © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 329–341 329 330 R. LOH ET AL. horizontal spread by ramet propagation affects the clonal structure and clonal subrange, which represents spatial distribution of genets, influencing levels of the spatial scale beyond which clonality does not affect dispersal and population structure. It follows that the genetic structure (Alberto et al., 2005; Vallejo- spatial genetic structure (SGS) in clonal plants results Marín et al., 2010). from the combined effects of pollen and seed dispersal, Clonal growth is a common feature among brome- and of clonal growth. Clonality strongly influences liad species (Murawski & Hamrick, 1990; Sampaio spatial structure, not only because of the potential et al., 2004; Sampaio, Pico & Scarano, 2005; Barbará aggregation of clones, leading to a spatial concentra- et al., 2009). However, there are few studies describ- tion of genetic variation, but also because clonal ing clonal structure in bromeliads using molecular growth itself is a component of dispersal (Alberto et al., markers (e.g. Murawski & Hamrick, 1990; Izquierdo 2005; Arnaud-Haond et al., 2007). Moreover, patterns & Piñero, 2000). Aechmea nudicaulis (L.) Griseb. is a Downloaded from https://academic.oup.com/botlinnean/article/178/2/329/2416415 by guest on 02 October 2021 of aggregation also vary into guerrilla (genets distrib- nurse bromeliad common to the Brazilian Atlantic uted in an irregular fashion and widely spread ramets) forest complex. This species has several features or phalanx (regularly distributed genets and clonal which make it an interesting model species for SGS copies densely aggregated near the parental ramet) studies in clonal and non-clonal bromeliads. First, (Lovett-Doust, 1981); although guerrilla growth leads being a self-incompatible species (Matallana et al., to high genet intermingling and clonal dispersal, 2010), the issue of selfing resulting in identical geno- phalanx growth results in spatially aggregated clones types can be disregarded, making it easier to compute and an increase in SGS (Vallejo-Marín, Dorken & the amount of sexual reproduction vs. clonal growth. Barrett, 2010). Seedling recruitment dynamics is also Moreover, in certain habitats, the species presents a important in determining SGS in clonal plants, and terrestrial growth habit, which means that individu- contemplates a spectrum of strategies between two als can be considered to be distributed in a two- endpoints: initial seedling recruitment (ISR), charac- dimensional space. In addition, it is a ubiquitous terized by a colonization by a single sexual recruitment species, which makes it easier to obtain large sample event and associated with long-distance dispersal sizes suited for SGS studies. leading to a decrease in SGS; and repeated seedling This study aims to provide information on the recruitment (RSR), characterized by the continuous clonal and genetic structure of this nurse bromeliad. establishment of new genets through seed germination Thus we: (1) evaluated the clonal structure of A. nudi- and associated with short-distance dispersal leading to caulis by describing the diversity components and the an increase in SGS (Eriksson, 1993). In between, two spatial components of clonal growth; (2) characterized more categories were later described to elaborate this the clonal subrange of A. nudicaulis in the population dichotomy further: RWO (recruitment at windows of studied; and (3) evaluated the small-scale SGS in opportunity) and RSR/ISR (systematic large-scale the population studied. For this purpose, a detailed variation between RSR and ISR) (Eriksson, 1993, analysis of the distribution of genetic variation among 1997, 2011). In the RWO model, there is continuous ramets of A. nudicaulis was conducted in the field site seedling recruitment, but only under specific condi- using a set of six polymorphic microsatellite markers. tions that are spatially unpredictable. In the RSR/ISR category, there is a source/sink dynamic between a MATERIAL AND METHODS group of local populations, in which some are RSR, acting as seed sources, and some are ISR, acting as STUDY SITE seed receptors. The Brazilian Atlantic forest complex is one of the most In addition, the amount and distribution of genetic threatened ecosystems on the planet (Ribeiro et al., diversity within clonal populations may have an 2011). It is composed of a core rain forest surrounded impact on the evolvability of these populations by a number of marginal ecosystems that range from (Eriksson, 1993; Dorken & Eckert, 2001; Honnay & open to forest formations. One such peripheral habitat Jacquemyn, 2008). In addition, a small effective popu- is the so-called ‘restinga’, which is a coastal sandy lation size, which can be expected in clonal popula- plain vegetation, separating the rain forest from the tions, may lead to high levels of inbreeding and thus a sea (Scarano, 2009). On the northern coast of Rio de strong genetic drift. Therefore, the characterization of Janeiro state, restinga is typically structured in veg- levels of genetic variability and SGS in clonal plants is etation islands separated by a matrix of bare sand, and essential for understanding the evolutionary dynamics its dynamics are intimately dependent on nurse plant and conservation status of these species. species, such as the tree Clusia hilariana Schltdl. and When describing SGS in clonal plants, it is essential the clonal bromeliad Aechmea nudicaulis (Scarano, to account for the effects of clonality on the estimate. 2009). Therefore,
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