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(American Journal of Botany. 2008;95:713-719.) doi: 10.3732/ajb.2007358 © 2008 Botanical Society of America, Inc. |
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Systematics and Phytogeography |
2 Department of Evolution and Ecology, University of California, Davis, California 95616 USA 3 California Coastal Conservancy, Oakland, California 94612 USA 4 Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana 70118 USA 5 Department of Biology, University of Leicester, Leicester LE1 7RH UK 6 Department of Biology, California State University, San Francisco, California 94132 USA
Received for publication 7 November 2007. Accepted for publication 3 March 2008.
ABSTRACT
Rapid evolution in contemporary time can result when related species, brought together through human-aided introduction, hybridize. The significant evolutionary consequences of post-introduction hybridization range from allopolyploid speciation to extinction of species through genetic amalgamation. Both processes are known to occur in the perennial cordgrass genus, Spartina. Here we report the existence of a third recent Spartina hybridization, discovered in 2002, between introduced S. densiflora and native S. foliosa in San Francisco Bay, California, USA. We used nuclear and chloroplast DNA analysis and nuclear DNA content with chromosome counts to examine plants of morphology intermediate between S. densiflora and S. foliosa in a restored marsh in Marin County, California. We found 32 F1 diploid hybrids and two triploid plants, all having S. densiflora and S. foliosa as parents; there is also evidence of a genetic contribution of S. alterniflora in some hybrids. None of these hybrids set germinable seed. In 2007 we found a hybrid over 30 miles away in a marsh where both parental species occurred, suggesting hybridization may not be a localized phenomenon. The presence of diploid and triploid hybrids is important because they indicate that several avenues existed that may have given rise to a new allopolyploid species. However, such an event is now unlikely because all hybrids are targets of eradication efforts.
Key Words: allopolyploid speciation • biological invasions • cordgrass • introgressive hybridization • Poaceae • Spartina
Hybridization is a common and potent mechanism of plant evolution producing 6% of the taxa of the Great Plains of the United States (Great Plains Flora Association, 1986
) and 22% of British taxa (Stace, 1991), for example. Human introductions have greatly accelerated hybridization. In the UK, 13% of hybrid plant taxa resulted from crosses involving introduced and native species, and nearly half of these produce fertile seed (Abbott, 1992). Fertile hybrids may often intercross and backcross with parental species, producing abundant genetic and phenotypic variation for natural selection. Selection favoring invasive genotypes may subsequently lead to the rapid evolution of traits that accelerate invasiveness (Ellstrand and Schierenbeck, 2000). Hybridization may also lead to the formation of new polyploid species if chromosomal doubling or multiplication occurs among hybrids (Abbott, 1992).
Two prior episodes of hybridization have been investigated among Spartina cordgrasses using molecular genetics and cytology. Following introductions of S. alterniflora Loisel. (2n = 62), native to Atlantic, North America tidal marshes to the United Kingdom and west coast of the United States, this species hybridized with both European and Pacific Spartina species, respectively (Table 1). Spartina xtownsendii Groves (2n = 62) a sterile F1 diploid hybrid of S. alterniflora and S. maritima (M. A. Curtis) Fern. (2n = 60) formed in Southampton Water in southern England, early in the 19th century. It gave rise to a new, fertile allotetraploid species, S. anglica C. E. Hubbard, ca. 1890 (Marchant, 1967), which had chromosome numbers that varied from 120 to 124 (Marchant, 1968). Spartina anglica was widely introduced in the early 20th century, and tidally dispersed seed (Huiskes et al., 1995) led to the conversion of estuarine mudflats into meadows of this grass in the United Kingdom, New Zealand, Tasmania, Australia, China, and in Puget Sound, Washington, United States, with mostly deleterious ecological consequences. The genetic evidence implies that S. anglica arose from a single S. xtownsendii plant that had S. alterniflora as the seed parent (Ferris et al., 1997; Ayres and Strong, 2001; Baumel et al., 2001).
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). Chloroplast DNA (cpDNA) haploid sequence analysis showed, because cpDNA is maternally inherited in Spartina (Ferris et al., 1997), that both S. foliosa and S. alterniflora have been seed parents to hybrids (Anttila et al., 2000). Hybrids are fertile, diploid (Daehler et al., 1999), and genetically diverse, as assessed by nuclear DNA markers (Ayres et al., 1999; Blum et al., 2004; Sloop et al., 2005). Some hybrids exceed both parental species in invasive traits for the tidal marsh system (Zaremba, 2000; Ayres et al., 2003,2008; Pakenham-Walsh, 2003). Natural selection acting on these fit hybrids, creating an ever more invasive population, may be responsible for accelerating rates of hybrid spread and the eventual local extinction of the native species (Ayres et al., 2003, 2004; Hall et al., 2006).
Here we describe a likely third Spartina hybridization in Creekside Park, a restored salt marsh in San Francisco Bay, California. We found 34 unusual plants that had dense evergreen stems like Spartina densiflora Brongn. (2n = 70), but spread laterally by rhizomes as in S. foliosa and S. alterniflora. Spartina densiflora, native to Chile and Argentina, was introduced during the restoration of Creekside Park in 1978 using plants obtained from an exotic population invading Humboldt Bay, California (Spicher, 1984). Spartina foliosa was also planted during the restoration, and while neither exotic S. alterniflora nor S. alterniflora xfoliosa hybrids have ever been found in Creekside Park, S. alterniflora xfoliosa hybrid plants have been found within a few miles of the Park (http://www.spartina.org/maps.htm). To determine whether these unusual plants were in fact hybrids of S. densiflora and S. foliosa, and possibly involving S. alterniflora, we employed species-specific chloroplast and nuclear DNA markers, as well as the combination of total nuclear DNA amounts with chromosome counts for ploidy assessment, to determine parentage and types of hybrids.
MATERIALS AND METHODS
Plants
All 34 putative Spartina hybrid plants were collected from Creekside Park in San Francisco Bay (Greenbrae, Marin County, California at 37.95°N, 122.54°W). Representative samples of S. alterniflora from the U.S. northeast coast, S. foliosa from throughout the species U.S. range, and S. densiflora plants from Creekside Park were used for comparison in this study.
Random amplified polymorphic DNA (RAPD)
DNA fragments specific to each species were identified by screening 100 RAPD primers (Operon kits A, B, C, D, and G, Operon Technologies, Alameda, California) using DNA extracted according to the protocol in Daehler et al. (1999) from 20 S. alterniflora, 20 S. foliosa and 12 S densiflora individuals. Primers A2, A4, A17, B7, B12, C10, D5, D11, G9, G18 yielded five bands specific to S. alterniflora, 12 bands specific to S. densiflora, three bands specific to S. foliosa, and seven bands found only in S. alterniflora and S. foliosa; species-specific bands were found in 100% of the tested taxa. These primers were used to amplify DNA as described in Daehler et al. (1999) extracted from 31 of the 34 putative hybrids from Creekside Park.
Chromosome counts
Actively growing roots were selected at mid morning and treated overnight in saturated aqueous 
-bromo-napthalene at 4°C, and fixed and stored in 3:1 ethanol:glacial acetic acid until required. Next, roots were soaked in 5 N HCl at room temperature for 10 min to soften them. The meristematic region was cut off, placed on a cleaned microscope slide in a drop of 2% aceto-orcein (Sigma, St. Louis, Missouri, USA), and the meristematic cells teased out with fine tungsten needles. Slides were then heated gently; the tissue was carefully squashed and examined with a Zeiss light microscope and a Planapo 63x objective. Careful drawings were made to count the chromosomes, and suitable preparations were recorded photographically.
Diploids
Ideally two or three undamaged cells with well-condensed and separated chromosomes were examined per accession. Unfortunately, in these plants, even with the rare superb squashes, we could not always distinguish unequivocally between two adjacent small chromosomes and a single larger metacentric. Nevertheless, we obtained at least two good counts for most diploids.
Triploids
For one triploid (CS38), we have only a single good count. For the other (CS15), we have two counts: one of 2n = 96 and one of 2n = 95 or 96. In such circumstances, we think it safer to regard these as circa counts. If they are incorrect, we are sure they will not vary from these counts by more than one or two chromosomes. This material was extremely difficult to work with; the small, numerous chromosomes varied enough in size to make even the finest squash difficult to interpret.
In terms of the "expected" number for a triploid, some caution is needed; in the case of unreduced gamete production, it is quite possible for the occasional bivalent to have separated and become excluded before meiosis I breaks down and the restitution nucleus forms. In such cases, it would be possible to have a range of numbers for basically triploid organisms.
Nuclear DNA quantification
For each measurement of nuclear DNA, approximately 5 cm2 of freshly harvested leaves of Spartina species or putative hybrid were processed with the equivalent amount of freshly harvested leaves of Hordeum vulgare cv. Sultan as an internal standard (2C = 11.12 pg DNA, seeds obtained from Kew Gardens; Johnston et al., 1999). The nuclei were isolated using a modified method by Galbraith et al. (1983) and stained for 1 h in the dark with 75 mg/ml propidium iodide (Sigma). A laser flow cytometer (FACSCalibur; Becton-Dickinson, San Jose, California) was used to estimate the 2C nuclear DNA amount of each sample, which was measured several times over the next hour to assure the value was constant. Most samples were evaluated on at least two different days, and the measurements were averaged to allow for day to day variation of the flow cytometer. Coefficients of variation were typically under 2%.
Simple sequence repeats (SSRs)
We used nine SSR primers that amplified DNA from S. alterniflora, S. densiflora, and S. foliosa (SPAR.05, SPAR.07, SPAR.10, SPAR.11, SPAR.13, SPAR.15, SPAR.23, SPAR.26, SPAR.30; Blum et al., 2004; Sloop et al., 2005) using genotyping results for an average of six loci per sample. PCR reaction conditions are described in Sloop et al. (2005). Using fluorescently labeled forward primers, PCR products were sized using an ABI 3730 capillary DNA analyzer and the program ABI GeneMapper 3.0 (Applied Biosystems, Cupertino, California). Sixteen S. densiflora from Creekside Park, 41 S. foliosa, and 42 S. alterniflora from San Francisco Bay and the U.S. East Coast were screened for species-specific alleles and to identify polymorphic loci in 33 of the 34 putative hybrids analyzed.
Chloroplast DNA sequencing
Using universal primers listed in Taberlet et al. (1991), we amplified and sequenced the trnT-trnF chloroplast intergenic spacer region. The ca. 1750-bp region was amplified in two sections using the primer pair trnA-trnB to recover the trnT-trnL segment, and primer pair trnC-trnF to recover the trnL-trnF segment (Taberlet et al., 1991). Haplotypes were differentiated by base-pair polymorphism and indel variation across the trnT-trnF region. Sequences from putative hybrids were compared to reference sequences obtained from 12 S. alterniflora from the U.S. northeast coast, 10 S. alterniflora xfoliosa hybrids from San Francisco Bay, five S. densiflora from Creekside Park, and 13 S. foliosa individuals from throughout the species range in California. Sequences representing all distinct haplotypes were subsequently submitted to GenBank (accessions DQ088877–DQ088958).
RESULTS
RAPDs
RAPD (random amplified polymorphic DNA) nuclear markers specific to S. alterniflora,S. densiflora, and S. foliosa showed that the unusual plants were hybrids between S. densiflora and S. foliosa (Table 2). None of the hybrid plants contained any RAPD fragments specific to S. alterniflora. The hybrids in general had an additive pattern of species-specific bands with a frequency close to 1.0 for all species-specific DNA fragments (Table 2). This pattern is distinct from introgressive hybrids in which the frequencies of species-specific fragments in the hybrid population are variable and generally <1.0, as was seen in S. alterniflora xfoliosa introgressive hybrids (Ayres et al., 1999). Some individual hybrids lacked one or a few diagnostic fragments for S. densiflora or S. foliosa likely from a heterozygous individual (band present/band absent) taking part in the hybridization. Because of the dominant nature of RAPD phenotypes, heterozygosity in the parent species is undetectable. A similar additive pattern of RAPD fragments specific to S. alterniflora and S. maritima, respectively, was found in S. xtownsendii and S. anglica (Ayres and Strong, 2001).
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SSRs and chloroplast DNA sequencing
Very little genetic variation in cpDNA haplotypes or SSR loci was observed among S. densiflora and S. foliosa. Only a single chloroplast haplotype was recovered in multiple samples of each species (Table 3), and few SSR loci in each species were found to be polymorphic (SPAR.5 and SPAR.23 for S. foliosa and SPAR.7 for S. densiflora); other apparently polymorphic loci with multiple alleles were fixed genotypes. Fixed heterozygotic genotypes in the parent species were also seen in hybrid genotypes, i.e., S. densiflora had a single genotype for SPAR.15 of 258/275; eight of the nine diploid hybrid plants tested also had these two alleles in addition to the S. foliosa allele at 263 bp. The nondiploid inheritance patterns could be due to the amplification of two loci or the hexaploid nature of the parent species. For uniformity, we listed hybrid genotypes as diploids with the distinguishing parental allele(s) denoted by a single letter code (Table 4). Chloroplast sequence analysis showed that S. densiflora was the seed parent of 29 of the 32 diploid hybrids; S. foliosa was the seed parent to a triploid plant and three of the diploid hybrids (Table 3).
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DISCUSSION
F1 nature of the diploid interspecific hybrids
We found 34 plants at Creekside Park, Marin County, California to be hybrids between exotic S. densiflora and native S. foliosa. The 32 diploid plants are F1 interspecific hybrids. The F1 nature of the hybridization was established by the additive pattern of species-specific RAPD bands (Table 2). The diploid status of these hybrids, as determined by their intermediate chromosome number and nuclear DNA amounts between the parental species (Table 1), supports this interpretation of the RAPD data. In 2006, another F1 hybrid was found in a nearby marsh, Piper Park, and in 2007, two hybrids were found nearby, along Corte Madera Creek in Marin County, and a single hybrid plant was in a third location, Sanchez Marsh, over 48 km south, near the San Francisco International Airport (see Fig. 2 in Ayres et al., 2004). All sites have S. densiflora growing among S. foliosa, suggesting that hybridization between the two species is not restricted to a single marsh. Most hybrid plants grew in a midmarsh position, at an elevation overlapping that of S. densiflora; S. foliosa occurred at a lower elevation in the marshes. Both parent species have been the seed parent to hybrids although S. densiflora has been the predominant maternal parent. The low genetic variation in the parental species made it difficult to determine the total number of plants participating in the densiflora xfoliosa hybridization at Creekside Park. We estimate a minimum of three plants have been seed parents of hybrids (cpDNA haplotypes: one S. foliosa, one S. densiflora, one S. alterniflora; Table 3), and at least six plants have been pollen parents (SSR genotypes: two S. foliosa, one S. densiflora, three S.alterniflora hybrids).
Triploid hybrids
The two triploid hybrids we found were morphologically similar to the diploid hybrids. They both appear to have the karyotype of DFF based on 2C nuclear DNA amounts larger than both parental species and arithmetically equivalent to that identity. Although the chromosome numbers of the two triploids plants (94 and 96) for this karyotype are not the expected 97, this discrepancy may be due to a loss of chromosomes in the formation of these triploids or simply to the difficulty in accurately counting so many chromosomes. Spartina foliosa was determined to be the seed parent for one of the triploids, while the other triploid had the same chloroplast sequence as S. alternifolia from Point Lookout, New York City, NY or a San Francisco Bay S. alterniflora xfoliosa hybrid (Table 3).
Sources of S. alterniflora alleles
The S. alterniflora alleles in the S. densiflora xfoliosa hybrids (CS 25, 26, 38; Tables 1, 4) may have come from two possible sources. The S. densiflora in Creekside Park might have hybridized with one or more S. alternifloraxfoliosa hybrids so highly backcrossed to S. foliosa that no RAPD bands and few SSR alleles specific to S. alterniflora remained. The chloroplast haplotype of the three-species triploid supports this hypothesis because the S. alterniflora haplotype in this hybrid is a common haplotype in S. alterniflora xfoliosa plants in San Francisco Bay and has been found in Mid-Atlantic coast and northeastern Atlantic coast populations of native S. alterniflora (Blum et al., 2007; Table 3). In addition, in the triploid plant, presumed S. alterniflora SSR nuclear alleles replaced S. foliosa alleles at two loci, which were heterozygous with a S. densiflora allele at these loci (Table 4).
Alternatively, or in addition to the foregoing, the source of the S. alterniflora alleles could be from highly introgressed S. alterniflora xdensiflora hybrids. An exotic population of S. densiflora from Humboldt Bay, 370 km north of San Francisco, was the source of the plants used in the Creekside Park restoration. Baumel et al. (2002) inadvertently demonstrated that the Humboldt Bay population appears to include hybrids between S. densiflora and a member of the S. alterniflora-S. foliosa phylogenetic clade. Additional genomic studies using RAPDs showed the Humboldt Bay S. densiflora sample used by Baumel et al. (2002) contained no S. alterniflora or S. foliosa fragments (D. Ayres, unpublished). This result, together with the wide geographic separation of Humboldt Bay populations ofS. densiflora from the closest populations of S. foliosa and S. alterniflora, suggests that the putative hybrids in Humboldt Bay may have originated from hybridization with S. alterniflora prior to their introduction into Humboldt Bay. In support of this second possibility, recent molecular investigations of S. densiflora using chloroplast and nuclear DNA sequences indicates that S. densiflora has a reticulate origin in its native range, involving a lineage related to the clade formed by S. alterniflora, S. foliosa, and S. maritima (P. M. Fortuné, K. Schierenbeck, D. R. Ayres, A. Bortolus, O. Catrice, S. Brown and M. Aïnouche, University of Rennes, unpublished manuscript). Both S. densiflora and S. alterniflora co-occur in Argentina, and plants intermediate in morphology have been observed there. Although there is no confirming molecular evidence yet for hybridization, these individuals have been designated as hybrids and are often referred to as S. longispica (S. xlongispica Hauman & Parodi ex St.-Yves) (Cabrera, 1970).
Reproduction of the diploid and triploid hybrids
Preliminary results indicate that diploid plants fail to set seed, whereas the three-species triploid plant set seed in 4% of its flowers in 2004, and the two-species triploid had less than 0.1% seed set. However, the seeds produced by the triploid plants are apparently not viable; none germinated in preliminary trials. Thus, we found no genetic or fertility evidence of selfing or intercrossing among the hybrids, or backcrossing to the parent species. While there is apparently no sexual reproduction, the hybrids are clonal perennials that reproduce vegetatively by rhizomes, spreading laterally to form patches ranging in diameter from 0.50 to 6.0 m (D. Ayres and K. Zaremba, unpublished data). Similarly, failure to produce seed was noted in clonally spreading S. xtownsendii for about two decades before it gave rise to S. anglica (Marchant, 1967).
Evolutionary consequences
Here we have identified and described newly formed cordgrass hybrids in nature; the eventual fate of this hybridization, however, is unknown. Nonetheless, a new species may have arisen from within this group of plants. First, the genus has already produced one and possibly two allopolyploid species, S. anglica and S. longispica. Spartina longispica formed despite the disparity of chromosome numbers between the parental species (S. densiflora: 2n = 70 vs. S. alterniflora: 2n = 62)—the same disparity that exists between S. densiflora and S. foliosa. Further, S. alterniflora and S. foliosa have been described as "weakly differentiated sister species" (Baumel et al., 2002, p. 308), form introgressive interspecific hybrids (Ayres et al., 1999), and might be expected to share similar interspecific crossing abilities with S. densiflora. Second, the presence of both diploid and triploid hybrids suggests several avenues by which an allopolyploid species could form (Fig. 1). Once a F1 hybrid forms, the union of unreduced gametes from the F1 hybrid would give rise to an allotetraploid, a sequence of steps thought to be common in the origin of allotetraploids (Ramsey and Shemske, 1998). An alternate route, the fusion of an unreduced F1 gamete and the gamete of a parental species, gives rise to a triploid backcross hybrid. These 3n individuals can produce allohexaploids via selfing (3n + 3n) or allotetraploids through what is termed a triploid bridge (3n + 1n).
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). While the triploid could have arisen according to Fig. 1, step IV–V, the two aneuploid plants may have formed from a triploid-produced gamete uniting with a gamete from S. alterniflora or S. maritima, which suggests that a triploid plant was producing viable gametes. As unreduced triploid gametes can vary from expected chromosome numbers by 1–3 chromosomes (Ramsey and Shemske, 1998), the triploid bridge alone could have produced the chromosomal variation seen in S. anglica. The union of unreduced gametes from the F1 could have also formed S. anglica, or both mechanisms could have contributed to the origins of S. anglica.
The future of these new Spartina hybrids: Epilogue
Studying the dynamics of polyploid origins and unraveling the exact route by which a new allopolyploid species develops has not been possible before as the technologies to decipher key features of interspecific hybrids, such as seed parentage and nuclear DNA patterns, have not been available. Here we have identified and described new natural hybrids. However, it is unlikely that the population will persist or that a new allopolyploid species will arise in nature. The Invasive Spartina Project of the California Coastal Conservancy began an aggressive eradication program against all nonnative Spartina including S. densiflora xfoliosa hybrids in San Francisco Bay in 2003. The Creekside Park population of hybrids was treated with herbicides in 2005 and is currently extirpated; outlying plants have been targeted for eradication. Most of the hybrid genotypes (24 plants) survive only in a glasshouse at the University of California–Davis.
FOOTNOTES
1 The authors thank their team of laboratory assistants, especially A. Lee and H. McGray; and anonymous reviewers who substantially improved the manuscript. They acknowledge the financial support of the California Coastal Conservancy Invasive Spartina Project and California Sea Grant R/CZ-176. 
7 Author for correspondence (e-mail: drayres{at}ucdavis.edu)
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