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Genetics and Molecular Biology

Print version ISSN 1415-4757

Genet. Mol. Biol. vol.35 no.4 supl.1 São Paulo  2012

http://dx.doi.org/10.1590/S1415-47572012000600017 

RESEARCH ARTICLE

 

Genetics, evolution and conservation of Bromeliaceae

 

 

Camila M. ZanellaI; Aline JankeI; Clarisse Palma-SilvaII; Eliane Kaltchuk-SantosI; Felipe G. PinheiroI; Gecele M. PaggiIII; Luis E.S. SoaresI; Márcia GoetzeI; Miriam V. BüttowI; Fernanda BeredI

IDepartamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
IIInstituto de Botânica, São Paulo, SP, Brazil
IIILaboratório de Biologia Molecular e Microrganismos, Universidade Federal de Mato Grosso do Sul, Corumbá, MS, Brazil

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ABSTRACT

Bromeliaceae is a morphologically distinctive and ecologically diverse family originating in the New World. Three centers of diversity, 58 genera, and about 3,140 bromeliad species are currently recognized. We compiled all of the studies related to the reproductive biology, genetic diversity, and population structure of the Bromeliaceae, and discuss the evolution and conservation of this family. Bromeliads are preferentially pollinated by vertebrates and show marked variation in breeding systems, from predominant inbreeding to predominant outcrossing, as well as constancy in chromosome number (2n = 2x = 50). Autogamous or mixed mating system bromeliads have a high inbreeding coefficient (FIS), while outcrossing species show low FIS. The degree of differentiation among populations (FST) of species ranges from 0.043 to 0.961, which can be influenced by pollen and seed dispersal effects, clonal growth, gene flow rates, and connectivity among populations. The evolutionary history of the Bromeliaceae is poorly known, although some studies have indicated that the family arose in the Guayana Shield roughly 100 Mya. We believe that genetic, cytogenetic, and reproductive data will be essential for diagnosing species status and for assisting conservation programs.

Keywords: bromeliads, cytogenetics, genetic diversity, population structure, reproductive biology.


 

 

Introduction

The Bromeliaceae is one of the morphologically and ecologically most diverse flowering plant families native to the tropics and subtropics of the New World (Givnish et al., 2011). Its geographical distribution ranges from the states of Virginia, Texas, and California in the USA (latitude 37° N) to northern Patagonia in Argentina (latitude 44° S). The family is known for its recent adaptive radiation. Bromeliads have different habits, varying from terrestrial to epiphytical, and are found from sea level to altitudes above 4,000 m, in both desert and humid regions, as well as in soils subject to regular floods and in places with very low or high luminosity. They can thrive on scalding sands and rocks, and withstand temperatures near 0 °C (Benzing, 2000).

Traditionally, the family has been divided into three subfamilies, Bromelioideae (~650 spp.), Pitcairnioideae (~890 spp.), and Tillandsioideae (~1000 spp.), based on Smith and Downs (1979); this classification is adopted in the present study. However, in a recent phylogeny based on eight plastid regions, with representatives from 46 of 58 genera, Givnish et al. (2011) confirmed the eight-subfamily classification advanced by Givnish et al. (2007). The new classification splits the paraphyletic Pitcar-nioi-deae into six subfamilies and proposes that they are related to each other as follow: (Brocchinioideae, (Lind-manioi-deae, (Tillandsioideae, (Hechtiooideae, (Navioideae, (Pit-carnioideae, (Puyoideae, Bromelioideae))))))).

Bromeliads are especially appreciated for their ornamental value, but some species have proven medicinal properties (e.g., Bromelia antiacantha) or are cultivated as tropical fruits (e.g., pineapple: Ananas comosus). Here, we review the main genetic and evolutionary topics concerning Bromeliaceae, from a conservation standpoint.

 

Pollination and Reproductive Biology

Among the plant families, Bromeliaceae is the one with the highest diversity of pollination modes (orni-tho-phily, chiropterophily, entomophily, mixed/unspecific, and autogamy) throughout its geographic distribution (Kessler and Krömer, 2000; Canela and Sazima, 2005; Wendt et al., 2008; Schmid et al., 2010). Bromeliads have evolved floral displays with a great diversity of colors, shapes, and scents, which are related to pollinator attraction, with nectar being the usual reward (Benzing, 2000). The presence of Brome-liaceae in the New World has provided an important resource base, largely absent in the Old World, for small, hovering vertebrate pollinators (Fleming and Muchhala, 2008). A recent study (Krömer et al., 2008) strongly supports the hypothesis that the composition of nectar sugars in Bromeliaceae is correlated with the pollinator syndrome (lepidopterophilous, trochilophilous, or chiropterophilous). Although the majority of bromeliads are pollinated by vertebrates, mainly hummingbirds and bats, bees are among the most frequent visitors to some short-corolla species with ornithophilous features. Nevertheless, few studies have identified insects as effective pollinators of these bromeliads (Kamke et al., 2011).

Simultaneously with the divergence of bromeliad sub-families (see "Evolution" below), the first split of modern hummingbird lineages appears to have occurred in the Andes about 13 Mya, with several other Andean lineages diverging during the Pliocene and Pleistocene (Givnish et al., 2011). This might have contributed to the rapid expansion of the range of bromeliads and pollinators throughout the Neotropics. However, plant-pollinator interactions, seed dispersal, and the mechanisms promoting or constraining species diversification via these interactions are complex and poorly studied in the Neotropics (Antonelli and Sanmartín, 2011).

Bromeliads possess specialized floral features such as herkogamy and dichogamy, which prevent spontaneous self-fertilization and facilitate animal-mediated outcrossing (Benzing, 2000; Martinelli G, 1994, PhD Thesis, University of St. Andrews). Floral morphology, hand-polli-nation experiments, and population genetics studies have shown that selfing and mixed are the most common mating systems in a large part of the family (Bush and Guilbeau, 2009; Matallana et al., 2010; Table 1), although self-in-com-patibility systems can be found in all of the subfamilies (Pitcairnioideae: Vosgueritchian and Buzato, 2006; Bro-me-lioideae: Canela and Sazima, 2003, 2005; Schmid et al., 2010; Kamke et al., 2011; Tillandsioideae: Hietz et al., 2006; Ramírez-Morillo et al., 2009). The Tillandsioideae subfamily has a particularly high frequency of selfing and mixed systems in various genera, including Alcantarea, Guzmania, Racinea, Tillandsia, Vriesea, and Werauhia (Benzing, 2000; Lasso and Ackerman, 2004; Paggi et al., 2007, 2012; Matallana et al., 2010; Martinelli G, 1994, PhD Thesis, University of St. Andrews; Table 1). Clonality is another reproductive strategy present in the family (Mu-rawski and Hamrick, 1990; Izquierdo and Pinero, 2000; Sarthou et al., 2001; Sampaio et al., 2002; Sgorbati et al., 2004; Cascante-Marín et al., 2006; Barbará et al., 2009), with important ecological and evolutionary consequences (Gonzales et al., 2008) such as recruitment and population maintenance (Villegas, 2001).

We studied the mating systems of two bromeliad species. Vriesea gigantea presented a high natural production of flowers, fruits, and seeds, with high rates of viable seeds, with an average germination rate of 94% (Paggi et al., 2007, 2010). Furthermore, the species showed regular chro-mo-some segregation and high pollen viability (84-98%, Palma-Silva et al., 2008), which indicated that the populations analyzed were fertile. Manual hand-polli-nation indicated that V. gigantea is self-compatible (Paggi et al., 2007) and showed low to moderate levels of inbreeding depression (δ = 0.02 to 0.39; Sampaio et al., 2012). In a study with Vriesea friburgensis we highlighted that it is pollinated by hummingbirds and produces high flower, fruit, and seeds together with high seed and pollen viability. We concluded that the wild populations studied were fertile. Self-sterility was observed from spontaneous selfing and manual self-pollination treatments, which may be a consequence of late-acting self-incompatibility. We proposed that this self-sterile species depends on pollinator services to maintain its population fitness and viability through cross-pollination (Paggi et al., 2012).

 

Diversity and Genetic Structure

The genetic diversity of only a few species of Brome-liaceae has been studied. We compiled data from all diversity and genetic structure studies published before June 2011 (Table 1). Of the 58 genera and about 3,140 bromeliad species (Givnish et al., 2011), only 20 species of the following nine genera have been previously evaluated: Aechmea, Alcantarea, Bromelia, Dyckia, Encholirium, Pitcairnia, Puya, Tillandsia, and Vriesea. Most of the studied species are endemic to the Atlantic rainforest in southeastern Brazil.

The use of co-dominant markers has been the preferred method for studying bromeliad population genetics, with nuclear microsatellite markers being the most frequently used molecular markers (nine species), followed by allozymes (eight species). Dominant markers such as amplified fragment length polymorphisms have been used in only one study of one species, and random amplified polymorphic DNA was applied in another study of three species (Table 1). A comparison of genetic diversity parameters among such studies is difficult, as the highly polymorphic SSRs usually show higher observed and expected hetero-zygosity (HO and HE, respectively) compared with other markers. For example, populations of Pitcairnia geyskesii have been evaluated using allozymes (Sarthou et al., 2001) and SSRs (Boisselier-Dubayle et al., 2010). With allozy-mes, HO and HE were 0.188 and 0.246, respectively; with SSRs, HO and HE were 0.293 and 0.324, respectively.

We found low inbreeding coefficient indices (FIS) in almost all species with outcrossing mating systems. The exceptions were B. antiacantha (FIS = 0.431), possibly due to the Wahlund effect and/or null alleles, and Alcantarea glaziouana (FIS = 0.156), owing to biparental inbreeding. Pitcairnia staminea, which is autogamous, had a high inbreeding coefficient (FIS = 0.240; Table 1). V. gigantea and Dyckia ibiramensis, which have a mixed mating system, also showed high inbreeding coefficients (FIS = 0.273 and 0.436, respectively; Table 1). The degree of differentiation among populations (FST) of species evaluated ranged from 0.043 to 0.961. These differences in plant population structure can be influenced by pollen and seed dispersal effects, clonal growth (Gliddon et al., 1987), gene flow rates, and connectivity among populations. Compared with species from continuous forest habitats, species restricted to inselberg habitats (Barbará et al., 2007, 2009; Palma-Silva et al., 2011; Table 1) showed more highly structured populations, with extremely high population differentiation and isolation based on the distance among inselbergs. Thus, rock outcrops could be highly useful venues for studies regarding the molecular ecology and genetics of continental radiations.

 

Cytogenetics

Few cytogenetic studies of Bromeliaceae are available. Chromosome numbers have been determined for nearly 12% of the known species (Cotias-de-Oliveira et al., 2004), most of which are horticulturally important as orna-mentals or fruit producers. Owing to the scarcity of cyto-genetic data, the chromosomal evolution of the family has not been completely elucidated. The major hindrances to cytogenetic studies are probably the very small size and poor staining ability of the chromosomes, together with a marked cytoplasmic content (Sharma and Ghosh, 1971; Brown and Gilmartin, 1986).

Billings (1904) was the first to determine the chromosome number of a bromeliad, using Tillandsia usneoides, after which several studies were carried out. The first reports revealed a great variety of diploid numbers (2n = 16, 34, 36, 46, 48, 50, 52, 54, 56, 64, 96, and 100) and basic numbers (x = 5, 8, 9, 16, 17, and 25; Brown and Gilmartin, 1986; Bellintani et al, 2005). In contrast, most of the 72 bromeliad species studied by Marchant (1967) showed a basic number of x = 25 (except Cryptanthus: x = 17). Since then, studies in several different species have generally found the basic chromosome number to be a multiple of x = 25, corroborating Marchant's finding (Brown and Gil-martin, 1989; Cotias-de-Oliveira et al., 2000, 2004; Pal-ma-Silva et al., 2004; Gitaí et al., 2005; Ceita et al., 2008; Louzada et al., 2010). Polyploidy of this base number (2n = 4x = 100 and 2n = 6x = 150) has been observed in all subfamilies, but with low frequency (Brown and Gilmartin, 1989; Gitaí et al., 2005; Louzada et al., 2010).

Brown and Gilmartin (1989) have proposed a model to explain the evolution of the chromosome base number. In their model, two paleodiploids (x = 8 and x = 9) hybridized, resulting in a paleotetraploid lineage (x = 17), which in turn hybridized with the x = 8 paleodiploid, and the poliploidization stabilized at the hexaploid level of x = 25. Eletrophoretic data (Soltis et al., 1987) suggest that a "di-ploidization" of the dibasic paleohexaploid occurred. The dibasic model could explain the origin of the distinctive chromosome number in Cryptanthus, which may represent a paleotetraploid with 2n = 34. One alternative hypothesis is that Cryptanthus evolved from x = 25 via aneuploidy (Brown and Gilmartin, 1989). Flow cytometric results obtained by Ramírez-Morillo and Brown (2001) indicated that the Cryptanthus chromosome number originated by descending aneuploidy.

Bromeliaceae chromosomes are usually exceedingly small (0.21-2.72 m), although the size varies widely among species. According to Gitaí et al. (2005), larger chromosomes are usually found at lower ploidy levels, with diploids exhibiting a higher contrast between maximal and minimal chromosome sizes compared with polyploids. Chro-mosome banding and triple staining with CMA3/Actinomycin/DAPI has revealed that bromeliads have relatively little heterochromatin, with only one or two CMA+/DAPI- terminal bands corresponding to nucleolus organizing regions. B chromosomes have been reported in three Bromelioideae species (Cotias-de-Oliveira et al., 2000, 2004; Bellintani et al., 2005).

 

Evolution

Recently, Givnish et al. (2011) reinforced the i.e. of Smith (1934) that bromeliads arose in the Guayana Shield roughly 100 Mya during the Cretaceous Period, with the extant subfamilies beginning to diverge only about 19 Mya. Givnish et al. (2011) also suggested that about 15.4 Mya, bromeliads began to spread from that hyper-humid, extremely infertile center to other parts of tropical and subtropical America, and probably arrived in tropical Africa about 9.3 Mya, in a recent long-distance dispersal event. During the evolution of this family, events such as climatic oscillations throughout the Pleistocene have resulted in the dispersion of some clades, including Bromelioidae (Givnish et al., 2011). As of the current time, V. gigantea has survived glaciation periods in two fragmented refugia in southeastern Brazil (Palma-Silva et al., 2009).

The "bromeliad revolution" probably occurred after the uplift of the northern Andes and shift of the Amazon to its present course (Givnish et al., 2007). Some morphological and physiological adaptations, including crassulacean acid metabolism (CAM) photosynthesis and the formation of rosettes and leaf absorptive scales, might have been crucial to the adaptive radiation of bromeliads (Benzing, 2000; Crayn et al., 2004).

An ecological peculiarity of Bromeliaceae, compared with other families of the order Poales, is their epiphytic habit (Linder and Rudall, 2005). Based on plastid loci, Crayn et al. (2004) proposed that the epiphytic habit of bromeliads evolved a minimum of three times, most likely in response to geological and climatic changes in the late Tertiary.

The more than 3,000 bromeliad species that currently occupy the Neotropical region have evolved to fill numerous niches, with an incredible diversity of adaptations. Some aspects of the complex evolutionary history of this family are still unclear, indicating the need for further molecular studies, in combination with paleontological data, to explain the evolutionary gaps in the wide diversity of bromeliad forms and adaptations.

 

Conservation

Bromeliads are widely distributed in the Neotropics, with three centers of diversity: the Brazilian Atlantic rainforest; the Andean slopes of Peru, Colombia, and Ecuador; and Mexico and adjacent Central America (Zizka et al., 2009). Many species are presently distributed in endangered biomes, are endemic, or have a relict distribution, threatening the survival of many members of this family. For example, the Brazilian Atlantic rainforest is a diverse biome with multiple extremely endangered vegetation ty-pes occupying only 7.91% of the extent of their original distribution (Fundação SOS Mata Atlântica and Instituto Na-cional de Pesquisas Espaciais, 2009; Carnaval and Mo-ritz, 2008). As the Atlantic rainforest contains at least 803 bromeliad species, 653 of which are endemic and 40% of which are endangered, the preservation of the Atlantic rainforest is vital for the conservation of Bromeliaceae (Mar-tinelli et al., 2008).

Few studies of Bromeliaceae connect genetic data and conservation planning. All of the works cited in the above section "Diversity and genetic structure" contain data that could be used in making conservation decisions. Considerations of the clonal and sexual reproduction, demography, genetic structure within and among populations, gene flow, and mating systems of Bromeliaceae are of primary importance in developing successful conservation strategies (Bizoux and Mahy, 2007).

Our group has studied mainly Brazilian bromeliads, and our field records show a significant reduction in the current distribution of species, compared with the first records in the literature. We believe that genetic, cytogenetic, and reproductive data will be essential for diagnosing species status and for assisting conservation programs and will help to elucidate aspects of evolution and environmental and climate change for Bromeliaceae and the Brazilian Atlantic rainforest.

 

References

Alves GM, Filho AR, Puchalski A, Reis MS, Nodari RO and Guerra MP (2004) Allozymic markers and genetic characterization of a natural population of Vriesea friburgensis var. paludosa, a bromeliad from the Atlantic Forest. Plant Genet Resour 2:23-28.         [ Links ]

Antonelli A and Sanmartín I (2011) Why are there so many plant species in the Neotropics? Taxon 60:403-414.         [ Links ]

Barbará T, Martinelli G, Fay MF, Mayo SJ and Lexer C (2007) Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude 'inselbergs', Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Mol Ecol 16:1981-1992.         [ Links ]

Barbará T, Martinelli G, Palma-Silva C, Fay MF, Mayo SJ and Lexer C (2009) Genetic relationships and variation in reproductive strategies in four closely related bromeliads adapted to neotropical 'inselbergs': Alcantarea glaziouana, A. regina, A. geniculata and A. imperialis (Bromeliaceae). Ann Bot 103:65-77.         [ Links ]

Bellintani MC, Assis JGA and Cotias-de-Oliveira ALP (2005) Chromosomal evolution of Bromeliaceae. Cytologia 70:129-133.         [ Links ]

Benzing DH (2000) Bromeliaceae: Profile of an Adaptative Radiation. Cambridge University Press, Cambridge, 690 pp.         [ Links ]

Billings FH (1904) A study of Tillandsia usneoides. Bot Gaz 38:99-121.         [ Links ]

Bizoux JP and Mahy G (2007) Within-population genetic structure and clonal diversity of a threatened endemic metallo-phyte, Viola calaminaria (Violaceae). Am J Bot 94:887-895.         [ Links ]

Boisselier-Dubayle MC, Leblois R, Samadi S, Lambourdière J and Sarthou C (2010) Genetic structure of the xerophilous bromeliad Pitcairnia geyskesii on inselbergs in French Guiana - A test of the forest refuge hypothesis. Ecography 33:175-184.         [ Links ]

Brown GK and Gilmartin AJ (1986) Chromosomes of the Brome-liaceae. Selbyana 9:88-93.         [ Links ]

Brown GK and Gilmartin AJ (1989) Chromosome numbers in Bromeliaceae. Am J Bot 76:657-665.         [ Links ]

Bush SP and Guilbeau JE (2009) Early autonomous selfing in the hummingbird-pollinated epiphyte Pitcairnia brittoniana (Bromeliaceae). J Torr Bot Soc 136:313-321.         [ Links ]

Canela MBF and Sazima M (2003) Aechmea pectinata: A hummingbird-dependent bromeliad with inconspicuous flowers from the rainforest in south-eastern Brazil. Ann Bot 92:731-737.         [ Links ]

Canela MBF and Sazima M (2005) The pollination of Bromelia antiacantha (Bromeliaceae) in southeastern Brazil. Plant Biol 7:1-6.         [ Links ]

Carnaval AC and Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187-1201.         [ Links ]

Cascante-Marín A, De Jong M, Borg ED, Oostermeijer JGB, Wolf JHD and Den Nijs JCM (2006) Reproductive strategies and colonizing ability of two sympatric epiphytic bromeliads in a tropical premontane area. Int J Plant Sci 167:1187-1195.         [ Links ]

Cavallari MM, Forzza RC, Veasey EA, Zucchi MI and Oliveira GCX (2006) Genetic variation in three endangered species of Encholirium (Bromeliaceae) from Cadeia do Espinhaço, Brazil, detected using RAPD Markers. Biodivers Conserv 15:4357-4373.         [ Links ]

Ceita GO, Assis JGA, Guedes MLS and Oliveira ANPC (2008) Cytogenetics of Brazilian species of Bromeliaceae. Bot J Linn Soc 158:189-193.         [ Links ]

Cotias-de-Oliveira ALP, Assis JGA, Bellintani MC, Andrade JC and Guedes MLS (2000) Chromosome numbers in Bro-meliaceae. Genet Mol Biol 23:173-177.         [ Links ]

Cotias-de-Oliveira ALP, Assis JGA, Ceita G, Palmeira ACL and Guedes MLS (2004) Chromosome number for Brome-liaceae species occurring in Brazil. Cytologia 69:161-166.         [ Links ]

Crayn DM, Winter K and Smith JAC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proc Natl Acad Sci USA 101:3703-3708.         [ Links ]

Excoffier L, Smouse PE and Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes - application to human mitochondrial - DNA restriction data. Genetics 131:479-491.         [ Links ]

Fleming TH and Muchhala N (2008) Nectar-feeding bird and bat niches in two worlds: Pantropical comparisons of vertebrate pollination systems. J Biogeogr 35:764-780.         [ Links ]

Fundação SOS Mata Atlântica and Instituto Nacional de Pes-quisas Espaciais (1993) Atlas dos Remanescentes Florestais da Mata Atlântica Período 2005-2008. Fundação SOS Mata Atlântica, São Paulo, 156 pp.         [ Links ]

Gitaí J, Horres R and Benko-Iseppon AM (2005) Chromosomal features and evolution of Bromeliaceae. Plant Syst Evol 253:65-80.         [ Links ]

Givnish TJ, Millam KC, Berry PE and Sytsma KJ (2007) Phylogeny, adaptive radiation, and historical biogeography of Bro-me-liaceae inferred from Ndhf sequence data. Aliso 23:3-26.         [ Links ]

Givnish, TJ Barfuss MHJ, Ee BV, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, et al (2011) Phylogeny, adaptive radiation, and historical bio-geography in Bromeliaceae: Insights from an eight-locus plastid phylogeny. Am J Bot 98:872-895.         [ Links ]

Gliddon C, Belhassen E and Gouyon pH (1987) Genetic neighborhoods in plants with diverse systems of mating and different patterns of growth. Heredity 59:29-32.         [ Links ]

Gonzales E, Hamrick JL and Smouse PE (2008) Comparison of clonal diversity in mountain and piedmont populations of Trillium cuneatum (Melanthiaceaae-Trilliaceae) a forest under-story species. Am J Bot 95:1254-1261.         [ Links ]

González-Astorga J, Cruz-Angon A, Flores-Palacios A and Vovi-des AP (2004) Diversity and genetic structure of the Mexican endemic epiphyte Tillandsia achyrostachys E. Morr. ex Baker var. achyrostachys (Bromeliaceae). Ann Bot 94:545-551.         [ Links ]

Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633-1638.         [ Links ]

Hietz P, Winkler M, Cruz-Paredes L and Jiménez-Aguilar A (2006) Breeding systems, fruit set, and flowering phenology of epiphytic bromeliads and orchids in a Mexican humid mountain forest. Selbyana 27:156-164.         [ Links ]

Hmeljevski KV, Reis A, Montagna T and Reis MS (2011) Genetic diversity, genetic drift and mixed mating system in small subpopulations of Dyckia ibiramensis, a rare endemic bromeliad from southern Brazil. Conserv Genet 12:761-769.         [ Links ]

Izquierdo LY and Piñero D (2000) High genetic diversity in the only known population of Aechmea tuitensis (Bro-meliaceae). Aust J Bot 48:645-650.         [ Links ]

Kamke R, Schmid S, Zillikens A, Lopes BC and Steiner J (2011) The importance of bees as pollinators in the short corolla bromeliad Aechmea caudata in southern Brazil. Flora 206:749-756.         [ Links ]

Kessler M and Krömer T (2000) Patterns and ecological correlates of pollination modes among bromeliad communities of Andean Forests in Bolivia. Plant Biol 2:659-669.         [ Links ]

Krömer T, Kessler M, Lohaus G and Schmidt-Lebuhn AN (2008) Nectar sugar composition and concentration in relation to pollination syndromes in Bromeliaceae. Plant Biol 10:502-511.         [ Links ]

Lasso E and Ackerman JD (2004) The flexible breeding system of Werauhia sintenisii, a cloud forest bromeliad from Puerto Rico. Biotropica 36:414-417.         [ Links ]

Linder HP and Rudall PJ (2005) Evolutionary history of Poales. Annu Rev Ecol Evol Syst 36:107-24.         [ Links ]

Louzada RB, Palma-Silva C, Corrêa AM, Kaltchuk-Santos E and Wanderley MGL (2010) Chromosome number of Orthophytum species (Bromeliaceae). Kew Bull 65:53-58.         [ Links ]

Marchant CJ (1967) Chromosome evolution in Bromeliaceae. Kew Bull 21:161-170.         [ Links ]

Martinelli G, Vieira CM, Gonzalez M, Leitman P, Piratininga A, Costa AF and Forzza RC (2008) Bromeliaceae da Mata Atlântica Brasileira: Lista de espécies, distribuição e conser-vação. Rodriguésia 59:209-258.         [ Links ]

Matallana G, Godinho MAS, Guilherme FAG, Belisario M, Coser TS and Wendt T (2010) Breeding systems of Bromeliaceae species: Evolution of selfing in the context of sympatric occurrence. Plant Syst Evol 289:57-65.         [ Links ]

Murawski DA and Hamrick JL (1990) Local genetic and clonal structure in the tropical terrestrial bromeliad, Aechmea magdalenae. Am J Bot 77:1201-1208.         [ Links ]

Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321-3323.         [ Links ]

Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225-233.         [ Links ]

Paggi GM, Palma-Silva C, Silveira LCT, Kaltchuk-Santos E, Bodanese-Zanettini MH and Bered F (2007) Fertility of Vriesea gigantea Gaud. (Bromeliaceae), in southern Brazil. Am J Bot 94:683-689.         [ Links ]

Paggi GM, Sampaio JAT, Bruxel M, Zanella CM, Goetze M, Büttow MV, Palma-Silva C and Bered F (2010) Seed dispersal and population structure in Vriesea gigantea, a bromeliad from the Brazilian Atlantic Rainforest. Bot J Linn Soc 164:317-325.         [ Links ]

Paggi GM, Silveira LCT, Zanella CM, Bruxel M, Bered F, Kal-tchuck-Santos E and Palma-Silva C (2012) Reproductive system and fitness of Vriesea friburgensis, a self-sterile bromeliad species. Plant Spec Biol doi: 10.1111/j.1442-1984.2012.00374.x.         [ Links ]

Palma-Silva C, Santos DG, Kaltchuk-Santos E and Bodanese-Zanetini MH (2004) Chromosome numbers, meiotic behavior, and pollen viability of species of Vriesea and Aechmea genera (Bromeliaceae) native to Rio Grande do Sul, Brazil. Am J Bot 91:804-807.         [ Links ]

Palma-Silva C, Paggi GM, Felicetti RA, Ferraz RS, Kaltchuk-Santos E, Bered F and Bodanese-Zanettini MH (2008) Meiotic behavior and pollen viability of wild populations of the neotropical species Vriesea gigantea (Bromeliaceae). Plant Spec Biol 23:217-221.         [ Links ]

Palma-Silva C, Lexer C, Paggi GM, Barbará T, Bered F and Bodanese-Zanettini MH (2009) Range-wide patterns of nuclear and chloroplast DNA diversity in Vriesea gigantea (Bromeliaceae), a Neotropical forest species. Heredity 103:503-512.         [ Links ]

Palma-Silva C, Wendt T, Pinheiro F, Barbará T, Fay MF, Coz-zolino S and Lexer C (2011) Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs. Mol Ecol 20:3185-3201.         [ Links ]

Ramírez-Morillo IM and Brown GK (2001) The origin of the low chromosome number in Cryptanthus (Bromeliaceae). Syst Bot 26:722-726.         [ Links ]

Ramírez-Morillo IM, May FC, Carnevali G and Pat FM (2009) It takes two to tango: Self incompatibility in the bromeliad Tillandsia streptophylla (Bromeliaceae) in Mexico. Rev Biol Trop 57:761-770.         [ Links ]

Sampaio MC, Perissé LE, de Oliveira GA and Rios RI (2002) The contrasting clonal architecture of two bromeliads from sandy coastal plains in Brazil. Flora 197:443-451.         [ Links ]

Sampaio JAT, Paggi GM, Zanella CM, Bruxel M, Palma-Silva C, Goetze M, Büttow MV and Bered F (2012) Inbreeding depression in Vriesea gigantea, a perennial bromeliad from southern Brazil. Bot J Lin Soc 169:312-319.         [ Links ]

Sarthou C, Samadi S and Boisselier-Dubayle MC (2001) Genetic structure of the saxicole Pitcairnia geyskesii (Bromeliaceae) on inselbergs in French Guiana. Am J Bot 88:861-868.         [ Links ]

Sgorbati S, Labra M, Grugni E, Barcaccia G, Galasso G, Boni U, Mucciarelli M, Citterio S, Benavides Iramátegui A, Venero Gonzales L, et al. (2004). A survey of genetic diversity and reproductive biology of Puya raimondii (Bromeliaceae), the endangered queen of the Andes. Plant Biol 6:222-230.         [ Links ]

Schmid S, Schmid VS Zillikens A, Harter-Marques B and Steiner J (2010) Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biol 13:41-50.         [ Links ]

Sharma AK and Ghosh I (1971) Cytotaxonomy of the family Bromeliaceae. Cytologia 36:237-247.         [ Links ]

Smith LB (1934) Geographical evidence on the lines of evolution in Bromeliaceae. Bot Jahrb Syst, Pflanzengesch Pflan-zen-geogr 66:446-468.         [ Links ]

Smith LB and Downs RJ (1979) Bromelioideae (Bromeliaceae). In: Flora Neotropica Monograph 14. Hafner Press, New York, pp 1658-1660.         [ Links ]

Soltis DE, Gilmartin AJ, Rieseberg L and Gardner S (1987) Genetic variation in the epiphytes Tillandsia ionatha and T. recurvata (Bromeliaceae). Am J Bot 74:531-537.         [ Links ]

Villegas AC (2001) Spatial and temporal variability in clonal reproduction of Aechmea magdalenae, a tropical understory herb. Biotropica 33:48-59.         [ Links ]

Vosgueritchian SB and Buzato S (2006) Reprodução sexuada de Dyckia tuberosa (Vell.) Beer (Bromeliaceae, Pitcair-nioi-deae) e interação planta-animal. Rev Bras Bot 29:433-442.         [ Links ]

Wendt T, Coser TS, Matallana G and Guilherme FAG (2008) An apparent lack of prezygotic reproductive isolation among 42 sympatric species of Bromeliaceae in southeastern Brazil. Plant Syst Evol 275:31-41.         [ Links ]

Zanella CM, Bruxel M, Paggi GM, Goetze M, Buttow MV, Cidade FW and Bered F (2011) Genetic structure and phe-no-typic variation in wild populations of the medicinal tetra-ploid species Bromelia antiacantha (Bromeliaceae). Am J Bot 98:1511-1519.         [ Links ]

Zizka G, Schimidt M, Schulte K, Novoa P, Pinto R and König K (2009) Chilean Bromeliaceae: Diversity, distribution and evaluation of conservation status. Biodivers Conserv 18:2449-2471.         [ Links ]

 

 

Send correspondence to:
Fernanda Bered
Laboratório de Genética Molecular Vegetal
Instituto de Biologia
Caixa Postal 15053, 91501-970 Porto Alegre, RS, Brazil
E-mail: fernanda.bered@ufrgs.br

 

 

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