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Reproductive Biology |
2Departamento de Botânica, Universidade Federal do Rio de Janeiro, CCS, IB, cep 21941-590, Rio de Janeiro-RJ, Brazil; 3Departamento de Ecologia, Universidade Federal do Rio de Janeiro, CCS, IB, Caixa Postal 68020, cep 21941-590, Rio de Janeiro-RJ, Brazil
Received for publication August 11, 2000. Accepted for publication March 9, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: breeding systems • Bromeliaceae • conservation biology • hybrid fitness • hybridization • Pitcairnia • pollination biology; • selfing
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Arnold, 1992, 1997
). It has been estimated that from 30 to 70% of all flowering plant species have hybridization events in their phylogenetic histories (Grant, 1981
; Ehrlich and Wilson, 1991
; Whitham, Morrow, and Potts, 1991
; Masterson, 1994
; Soltis and Soltis, 1999
). Characterization of interspecific hybridization in plants has been the focus of various studies over the past several decades (Anderson, 1949
; Stebbins, 1950
; Heiser, 1973
; Arnold, 1992, 1997
). Numerous methods have been used to show hybridity, including intermediate morphology (Wilson, 1992
; Valverde, Vite, and Zavala-Hurtado, 1996
; McDade, 1997
), artificial hybridization (Motley and Carr, 1998
), isozymes (Standley, 1990
; Lack, 1995
), and more recently DNA (Smith, Burke, and Wagner, 1996
; Hollingsworth et al., 1999
). However, the role of hybridization in plant evolution is still unclear, partly due to the scarcity of studies dealing with hybrid formation, maintenance, and fitness (sensu Rieseberg, 1995
; Arnold and Hodges, 1995
). Nevertheless, the stabilization of the reproductive behavior of hybrid plants is an essential part of the process of speciation by hybridization (Grant, 1981
).
It is known that bromeliad species easily hybridize by hand manipulation (McWilliams, 1974
). However, little is known about natural hybridization within Bromeliaceae. Few records of natural hybrids are available for genera such as Tillandsia (Gardner, 1984
; Luther, 1985
), Vriesea (Read, 1984
), and Pitcairnia (Luther, 1984
; Wendt, Paz, and Rios, 2000
). This paper investigates the reproductive biology of hybridizing populations of two closely related Pitcairnia species: P. albiflos Herb. and P. staminea Lodd. They are rare, saxicolous plants, narrowly distributed on granite outcrops near the ocean in Rio de Janeiro state, Brazil. Their few populations are frequently allopatric, but they occur sympatrically at Pão de Açúcar outcrop, where morphological intermediacy between these two species has been demonstrated (Wendt, Paz, and Rios, 2000
). The reproductive biology of most Pitcairnia species is unknown. In the present study we investigated basic aspects of reproductive biology of these two species and their putative hybrids to answer the following questions: (1) What are their breeding systems? (2) How are hybrids formed, and are hybrids backcrossing with parental species? (3) Are hybrids fit or unfit compared to their parents?
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Although they are broadly sympatric along this rocky slope, their populations tend to be separated due to distinct habitat preferences: P. albiflos forms small patches on sun-exposed rock surfaces, whereas P. staminea occurs in large patches associated with shrubs and trees. Hybrids frequently occur in disturbed sites invaded by weeds and subjected to fire, where the original vegetation was partialy removed and landslide occurred. At the study site, the distance from a given hybrid to the nearest individuals of P. albiflos and P. staminea varied from a few meters (
5 m) to no more than 1000 m. These plants show marked vegetative reproduction by offshoots, with each ramet blooming only once in its lifetime. Hermaphroditic flowers are borne on a single racemose inflorescence. Branched inflorescences were rarely observed on parental species, though they were more frequent on hybrid plants. The perianth is actinomorphic and dichlamydeous, consisting of three free sepals and three free petals, which are held close together, like a corolla tube. The petals became spiralled during the anthesis. They have six stamens, and a one-pistil gynoecium. The ovary is semi-inferior with three locules. Putative hybrids show a large range of pink floral colors, rarely red (as in P. staminea) or white flowers (as in P. albiflos). In this study Pitcairnia ramets were classified phenotypically as P. albiflos, P. staminea, or hybrids based on the morphological characters listed in Table 1. These phenotypic patterns were defined by our previous morphometric study (Wendt, Paz, and Rios, 2000
).
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400 m). Although this is a tourist attraction, situated in the heart of the city, it still bears native vegetation, as described in the last century (Martius, 1842
). The regional rainforest climate has mean annual rainfall of 1500 mm and mean annual temperature of 24°C (Niemer, 1979
). This kind of outcrop forms edaphically and microclimatically "xeric islands" (sensu Porembski et al., 1998
). Open exposed rocks are subject to high amounts of insolation, in combination with high evaporation rates (Mattos et al., 1997
). The temperatures on the surface of dark colored rocks regularly reach 60°C at noon, and relative humidity falls below 30% (Porembski et al., 1998
). These outcrops appear as bald mountain with vegetation usually installed on a thin soil layer, forming elliptical soil-islands with great variability of sizes related to substrate inclination (Meirelles, Pivello, and Joly, 1999
). Here, bromeliads (Pitcairnia and Alcantarea) are important physiognomic elements and have the capacity to establish directly on bare rock.
Flowering phenology
Flowering phenology was assessed during 3 yr of field observations (1996, 1997, 1998). Plants were censused fortnightly between February and August. The census was conducted by walking along the Claudio Coutinho trail, which is parallel to many clumps of the parental species, and by climbing a trail that leads to a large group of hybrids. For each phenotypic group (Table 1) a tally of flowering ramets was counted on each census date.
Floral visitors
Pollinator visitations were observed for around 400 plants in the field for >50 h, during 1996, 1997, and 1998. Periods of observation ranged from 30 min to 4 h and took place during daylight (from 0700 to 1700) and nightime (from 1800 to 0300). The foraging behavior was observed by naked eye and recorded. Insect visitors were collected for identification. Bird visitors were photographed for identification. Bat visitors were caught in nylon mistnets set in front of flowering Pitcairnia plants and examined for pollen by rubbing a cube of gelatin over the bat's body. In the laboratory, the cube was placed on a microscope slide, melted, stained, and covered with a cover slip for microscopic examination.
Experimental crosses
Manipulated pollinations were conducted in a greenhouse using plants transplanted from the field. In 1997 and 1998, plants were transplanted at the outset of inflorescence formation; most flowered and fruited normally. Evaluation of natural open pollination was done on plants left in the field throughout the experiments. The option of conducting artificial pollination in a greenhouse was justified in an urban site such as this to avoid problems due to human interference and damage to plants manipulated during the course of the study. Each phenotypic group produced different numbers of flowers per inflorescence, therefore different numbers of plants and flowers were used for the controlled pollination tests: on P. albiflos, 749 flower buds (276 hand-manipulated) from 37 plants (26 in the greenhouse); on P. staminea, 1572 flower buds (416 hand-manipulated) from 39 plants (12 in the greenhouse); and on hybrids, 1312 flower buds (433 hand-manipulated) from 46 plants (18 in the greenhouse). Different treatments were often applied to different flowers on the same inflorescence. Each flower received one of the following treatments: (1) agamospermy, in which flower buds were emasculated and the inflorescence enclosed in a paper bag; (2) self-pollination, in which inflorescences with flower buds were bagged, and when flowers opened they were hand-pollinated using fresh pollen obtained from the same flower; (3) spontaneous selfing, in which inflorescences were enclosed as above and left unmanipulated; (4) cross-pollination, in which flower buds were emasculated and the inflorescence bagged, and when flowers opened they were hand-pollinated using fresh pollen obtained from another plant of the same species (we made sure that these two plants were from different patches in the field to avoid using ramets of the same clone); (5) interspecific cross-pollination, as for cross-pollination except that flowers were hand-pollinated using fresh pollen obtained from a flower of the other species or from a hybrid. Two days after the last flowers of each inflorescence opened, the paper bags were removed to prevent accidental injury. Inflorescences were monitored until fruit set could be evaluated. Each inflorescence in the greenhouse was labeled and the flower sepals were color-coded by pollination treatment with acrylic paint. For natural pollination, plants were randomly selected in the field. Since pedicels remain on the inflorescence regardless of whether a fruit is produced, the number of pollinated and nonpollinated flowers per plant can be obtained by a simple counting of pedicels with and without fruits.
Fruit and seed set
Fruit development was monitored periodically until fruit maturation. Evaluation of fruiting success was based on counts of mature fruits. The fruits were collected at the onset of capsule dehiscence. Number of seeds per fruit was determined for all mature fruits (except those that were preyed upon or dehisced before collection) from the six hand-pollination treatments, and for a sample from the field to represent natural pollination (42 fruits of P. albiflos, 30 fruits of P. staminea, and 21 fruits of hybrids). The seeds are small and were counted on a paper grid using a hand tally counter. We discriminated between developed and aborted or unfertilized seeds. All seeds (viable and aborted) in each fruit were weighed on precision scales.
Breeding systems
The reproductive strategy was determined following the indices described by Ramirez and Brito (1990)
. The self-compatibility index was estimated by dividing number of seeds per self-fertilized flower by number of seeds from cross-pollinated flowers. Self-compatible or partially self-compatible species (SC) have values between 0.30 and 1.00. Below 0.30, species are considered self-incompatible (SI). The autogamy index (AI) is calculated as the relationship between seeds from spontaneous selfing and self-pollination. Autogamous and partially autogamous species show indices between 0.30 and 1.00, and nonautogamous show values below 0.30.
Seed germination
We compared germination rates among treatments for parental species and hybrids using seeds produced in 1998. Because seeds were produced from agamospermy only in 1997, we do not have germination results for this treatment. For each pollination treatment, seeds from one mature fruit from each of five different plants were planted on a tree fern trunk substrate in aluminum containers (21 x 16 x 5 cm) in a greenhouse. One container was used for each fruit. The containers were covered by plastic film to avoid seed loss by wind and promote high humidity at the onset of germination. A commercial plant insecticide was sprayed over each container before covering to prevent insect attack. The number of germinating seeds was estimated by counting the seedlings over a period of 6 mo and was recorded as percentage germination of the total number of viable seeds planted from each fruit from each treatment.
Pollen viability
Mature buds or recently opened flowers were collected from individuals of P. albiflos (N = 16), P. staminea (N = 16), and hybrids (N = 21). Pollen grains from two anthers per flower were placed on separate microscope slides, one of which was stained with buffalo-black, the other with acetocarmine. For each anther, the viability of 500 pollen grains was recorded by counting the number of viable (stained) and malformed (unstained) pollen.
Fitness measures
Hybrid fitness influences the likelihood of backcrossing and subsequent introgression. We examined four components of fitness—fruit set, seed production, seed germination, and pollen viability—and compared the hybrids results with those from plants of parental species. As the artificial environment condition at the greenhouse could affect fitness components, the results of seed production from manipulated pollination (self, cross, interspecific cross) conducted at the greenhouse were averaged and compared between hybrids and parental species. Thus, the natural pollination treatment was compared separately between hybrids and species. The result of seed production from agamospermy and spontaneous selfing were not utilized in fitness comparison.
Data analysis
Data expressed as percentages were transformed (x' = arcsin 
) prior to statistical analysis (Sokal and Rohlf, 1995
). The means of viable and aborted seeds per fruit and the means of total seed mass per fruit among treatments were compared using one-way ANOVA. Significant differences (P < 0.05) between treatments were assessed with Tukey's honestly significant difference (HSD, unequal N) multiple-range tests. Differences in seed production, seed germination, and pollen viability between hybrid and parental species were analyzed by one-way ANOVA followed by Tukey's HSD multiple-range test. All these analyzes were performed using the software package Statistica 4.2 for Windows.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2100. First, the bat flew over the blooming plants without making contact with the flowers. It often made one or more circles over the plants, perhaps assessing the inflorescence's condition. Contact lasted 1 sec, and intervals between feeding bouts varied greatly from 10 to 120 min. On the last night of observation, when the bats of two species were caught, no more visits were recorded during the hours following capture, suggesting that only one individual for each species were visiting the flowers. Other observed night visitors to P. albiflos flowers included an unidentified species of hawk moth (Sphingidae). The hawk moth probed the open flowers with its tongue, while hovering; during this visit the tongue and head occasionally touched the flower's reproductive organs, and contact lasted 1 min. Apparently, a single hawk moth visited the flowers in regular intervals of 40–60 min. Hawk moth and bats did not visit simultaneously. Hawk moth was the most frequent night visitor, but was not observed during one night when the weather was cold and damp. No nocturnal visitors were recorded in 9 h of observation (spread over two nights) of a total of 15 inflorescences of P. staminea. Flowers of this species also showed nocturnal anthesis between 2400 and 0200. Nocturnal pollinator observation was not conducted on the hybrid plants, because access at night to their location was unsafe. Nocturnal observation at the greenhouse showed that hybrid anthesis occurred between 2200 and 0100.
Experimental crosses and breeding systems
All experimental treatments resulted in fruit set, except that flowers of hybrids showed no fruit production from emasculated, bagged buds, although their parental species showed a limited capacity to produce agamospermous fruits (Table 2). For all three taxa, there was no significant difference in seed production between self-pollinated and outcrossed flowers, suggesting that they are largely self-compatible with SC index 1.0. Furthermore, many fruits and seeds were set by spontaneous selfing treatments for P. staminea and hybrids; they are thus classified as autogamous, with AI indices of 0.62 and 0.78, respectively. Although P. albiflos is a self-compatible species, few fruits and seeds were formed without manipulated pollination. Its index of autogamy (AI = 0.1) was typical of a nonautogamous species. In P. albiflos, P. staminea, and the putative hybrids, there were no significant differences in seed production between interspecific crossing vs. self- and cross-pollination, suggesting the absence of interspecific genetic barriers. Seed set in naturally pollinated flowers of P. albiflos and P. staminea was significantly lower than in self-, cross-, or interspecific cross-pollination, whereas the hybrids had similar reproductive output in all treatments (Table 3).
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The number of seeds per fruit produced by manipulated pollination (self-, cross-, interspecific cross; F = 234.08) and natural pollination (F = 70.79) showed significant differences between P. albiflos, P. staminea, and hybrids (P < 0.0001), with the hybrids intermediate between the parental species (Fig. 2A). The percentage of viable seeds per fruit produced by manipulated pollination for hybrids was significantly lower than for the parental species (F = 75.96, P < 0.0001). However, percentage viable seeds per fruit produced by natural pollination had similar results for parental species and hybrids (F = 0.15, P = 0. 857; Fig. 2B). Seed mass per fruit produced by manipulated pollination was lower for hybrids than for the parental species (F = 198.35, P < 0.0001). However, the seed mass per fruit produced by natural pollination did not differ between P. staminea and hybrids (F = 7.56, P < 0.0001; Fig. 2C). Apparently, hybrids fitness decreased in the artificial pollination conducted at the greenhouse, but did not in natural conditions.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Solbrig and Rollins, 1977
; Jarne and Charlesworth, 1993
). There is a general consensus that outcrossing is favored because it produces more variable genotypes and creates new allelic combinations each generation (Darwin, 1876
; Charlesworth and Charlesworth, 1987
). Conversely, inbreeding could preserve traits adapted to particular environmental conditions under which outcrossed offsprings would likely have lower fitness (Jarne and Charlesworth, 1993
). Pitcairnia albiflos and P. staminea are adapted to the harsh environmental conditions found on rocky outcrops. They do not occur in other habitats. Probably one explanation for the evolution of SC in these species is associated with the narrow distribution of their populations. Many studies support the idea that species with limited distribution tend to be more self-compatible and have less genetic variation than more widespread species (Kruckeberg and Rabinowitz, 1985
; Wyatt, Evans, and Sorenson, 1992
). Thus selfing is expected to be favored when density is low, such as during colonization, because one seed produced in one plant is potentially capable of establishing a new population (Stebbins, 1957
; Solbrig and Rollins, 1977
). It is worth mentioning that self-compatible species can still be outcrossed. Therefore, the understanding of breeding system evolution of these taxa will require knowledge of selfing rates in natural populations. Additional studies using genetic markers will give us estimates of selfing rates that will permit additional inferences about breeding systems evolution on the taxa.
Hybrid formation and introgression
Isolation mechanisms in plants can be grouped into three main classes: (1) geographic isolation, (2) ecological isolation, and (3) reproductive isolation that can be divided in premating and postmating processes (Grant, 1981
). The few known populations of P. albiflos and P. staminea rarely co-occur (Wendt, 1994
). They grow sympatrically on the Pão de Açúcar rocky outcrop but show adaptations to different ecological settings. Hybrids are common in this mixed population because geographic and ecological isolation between these species have been broken down possibly facilitated by human disturbance. Seasonal differences in flowering periods and pollinator behavior (premating reproductive isolation) among sympatric species often contribute significantly to their separation. Pitcairnia albiflos and P. staminea flower together for the majority of the flowering season. The two species possess different pollination syndromes—P. albiflos with white and scented flowers are night pollinated by bats and hawk moths, while P. staminea with red and nonscented flowers are diurnally pollinated by butterflies—however, both species are intensely visited by trigonid bees all day long. This common visitor is probably responsible for interspecific crosses. Cross incompatibility and hybrid inviability (postmating isolation) can, in principle, impede hybridization, but our results suggest that hybridization may not be limited by cross incompatibility in P. albiflos and P. staminea. Similarly, our results of germination and hybrid fertility suggest that hybridization and backcrossing are not strongly limited by hybrid inviability. Although there is evidence for introgression in the direction of both parental species, the results of seed germination indicate the existence of a partial introgression barrier in P. staminea. When this species was used as an ovule source and crossed with hybrids (pollen donor), percentage seed germination was significantly lower (P < 0.001) than that of the other treatments. The results of this study suggest that reproductive barriers to interspecific gene flow between P. albiflos and P. staminea are rather weak. One might expect to find hybrid swarms involving these species to be complicated assemblages of parental types mixed with early- and late-generation backcrossed individuals and early- and late-generation hybrids.
Hybrid fitness
Many authors have concluded that natural hybridization is of little evolutionary importance because hybrids, in general, are unfit relative to their progenitors (Mayr, 1963, 1992
; Wagner, 1970
). However, recent analyses have found that hybrids are not uniformly unfit, but, rather, are genotypic classes that possess lower, equivalent, or higher levels of fitness relative to their parental taxa (see review in Arnold and Hodges, 1995
). As the putative hybrids are relatively common on Pão de Açúcar, it seems likely that they do not suffer any major reduction in fitness. Our measurements of fitness components for hybrids and parental individuals allowed direct comparisons of fruit set, seed set, seed germination, and pollen viability and showed that hybrids had equivalent fitness to the parental taxa, except for pollen viability, which was significantly lower in hybrids.
Interspecific hybridization in rare species
Pitcairnia albiflos and P. staminea are locally abundant on Pão de Açúcar. However, they have a very narrow geographic distribution and are restricted to rocky outcrops in the state of Rio de Janeiro; they can both be considered rare and endangered species (Kruckeberg and Rabinowiitz, 1985
; Frankham, 1998
). There are two viewpoints from which to consider natural hybridization as it relates to conservation (Rhymer and Simberloff, 1996
; Arnold, 1997
). The first regards natural hybridization as deleterious because of loss of biodiversity. Hybridization within natural populations could lead to the replacement of the parental form by hybrid individuals or the reduction in fitness due to outbreeding depression if the hybrids have reduced vigor or are partly sterile (Ellstrand and Elam, 1993
). The second perspective on natural hybridization and conservation is more positive. In this case, hybridization involving one species that is rare and another that is more numerous potentially results in a genetic enrichment of the endangered form (Stebbins, 1942
). The rare form is aided by such interaction through increased fitness, the addition of genetic variability that facilitates habitat expansion, and the hybrid population may act as a genetic reservoir for reconstituting the parental genotypes/phenotypes (Anderson, 1949
). In the case of P. albiflos and P. staminea on Pão de Açúcar, we did not find evidence for outbreeding depression and the complex of populations, as a whole is healthy. Thus, in this case hybridization probably contributes to the expansion in the number of individuals on the slope of Pão de Açúcar. However, further disturbance at this or other sites could lead to a breakdown in the distinctiveness of the two parents each losing to some extent their special ecology and pollination system.
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FOOTNOTES |
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4 Author for reprint requests (e-mail: twendt{at}biologia.ufrj.br
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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