Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA

Introduced Spartina alterniflora (smooth cordgrass) is rapidly invading intertidal mudflats in San Francisco Bay, California. At several sites, S. alterniflora co-occurs with native S. foliosa (California cordgrass), a species endemic to California salt marshes. In this study, random amplified polymorphic DNA markers (RAPDs) specific to each Spartina species were identified and used to test for hybridization between the native and introduced Spartina species in the greenhouse and in the field. Greenhouse crosses were made using S. alterniflora as the pollen donor and S. foliosa as the maternal plant, and these crosses produced viable seeds. The hybrid status of the crossed offspring was confirmed with the RAPD markers. Hybrids had low self-fertility but high fertility when back-crossed with S. foliosa pollen. Hybrids were also found established at two field sites in San Francisco Bay; these hybrids appeared vigorous and morphologically intermediate between the parental species. Field observations suggested that hybrids were recruiting more rapidly than the native S. foliosa. Previous work identified competition from introduced S. alterniflora as a threat to native S. foliosa. In this study, we identify introgression and the spread of hybrids as an additional, perhaps even more serious threat to conservation of S. foliosa in San Francisco Bay.     

Sexual reproduction of cordgrass hybrids (Spartina foliosa x alterniflora) invading tidal marshes in San Francisco Bay

We genetically analysed cordgrass plants and seedlings throughout the San Francisco, California, USA, estuary and found that hybrids between exotic Spartina alterniflora and native Spartina foliosa are the principal cordgrass invaders and colonizers. We hypothesized that this was due to higher seed set and siring ability by hybrids relative to the native species; too few alien parents remained in San Francisco Bay for our comparative studies. Hybrid seed comprised 91% to 98% of that set in the marsh study plants over the 2 years of the study. Total viable pollen production by hybrid plants was 400 times that of the native plants. Seed and pollen production were highly skewed towards a few hybrid genotypes. In addition to seed produced by hybrid plants, hybrid seed was produced by S. foliosa due to hybrid backcrossing. While the greatest advantage for hybrids was in pollen and seed production, hybrid seeds germinated, and seedlings survived and grew as well or better than the native species. As native S. foliosa becomes increasingly rare, hybrid seed floating on the tides will predominate, overwhelming recruitment sites and resulting in further colonization by hybrids. In an evolutionary context, hybrids with exceptional pollen and seed production will be initially favoured by natural selection, leading to the evolution of even more fertile hybrid genotypes.     

Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA

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 F(1) 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.     

Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization

Hybridization with abundant invaders is a well-known threat to rare native species. Our study addresses mechanisms of hybridization between a rare invader, smooth cordgrass (Spartina alterniflora) and the common native California cordgrass (S. foliosa) in the salt marshes of San Francisco Bay. These species are wind-pollinated and flower in summer. The invader produced 21-fold the viable pollen of the native, and 28% of invader pollen germinated on native stigmas (1.5-fold the rate of the native's own pollen). Invader pollen increased the seed set of native plants almost eightfold over that produced with native pollen, while native pollen failed to increase seed set of the invader. This pollen swamping and superior siring ability by the invader could lead to serial genetic assimilation of a very large native population. Unlike California cordgrass, smooth cordgrass can grow into low intertidal habitats and cover open mud necessary to foraging shorebirds, marine life, navigation, and flood control in channels. To the extent that intertidal range of the hybrids is more similar to the invader than to the native parent, introgression will lead to habitat loss for shore birds and marine life as well to genetic pollution of native California cordgrass.     

Extent and degree of hybridization between exotic (Spartina alterniflora) and native (S. foliosa) cordgrass (Poaceae) in California, USA determined by random amplified polymorphic DNA (RAPDs)

Spartina alterniflora, smooth cordgrass, native to the eastern USA, was introduced into south San Francisco Bay ≈ 25 years ago. It has spread by purposeful introduction of rooted plants and dispersal of seeds on the tides. Previous work suggested that S. alterniflora was competitively superior to the native California cordgrass, S. foliosa, and that the two species hybridized. The present study determined the spread of S. alterniflora and S. foliosa × alterniflora hybrids in California and examined the degree of hybridization. We used nuclear DNA markers diagnostic for each species to detect the parental species and nine categories of hybrids. The California coast outside San Francisco Bay contained only the native species. All hybrid categories exist in the Bay, implying that several generations of crossing have occurred and that hybridization is bidirectional. Hybrids were found principally near sites of deliberate introduction of the exotic species. Where S. alterniflora was deliberately planted, we found approximately equal numbers of S. alterniflora and hybrid individuals; S. foliosa was virtually absent. Marshes colonized by water-dispersed seed contained the full gamut of phenotypes with intermediate-type hybrids predominating. The proliferation of hybrids could result in local extinction of S. foliosa. What is more, S. alterniflora has the ability to greatly modify the estuary ecosystem to the detriment of other native species and human uses of the Bay. To the extent that they share these engineering abilities, the proliferation of cordgrass hybrids could grossly alter the character of the San Francisco Bay.     

Spread of Exotic Cordgrasses and Hybrids (Spartina sp.) in the Tidal Marshes of San Francisco Bay, California, USA

Four species of exotic cordgrass (Spartina sp.) occur in the San Francisco estuary in addition to the California native Spartina foliosa. Our goal was to map the location and extent of all non-native Spartina in the estuary. Hybrids of S. alterniflora and S. foliosa are by far the most numerous exotic and are spreading rapidly. Radiating from sites of deliberate introduction, S. alterniflora and hybrids now cover ca. 190 ha, mainly in the South and Central Bay. Estimates of rate of aerial increase range from a constant value to an accelerating rate of increase. This could be due to the proliferation of hybrid clones capable of rapid expansion and having superior seed set and siring abilities. The total coverage of 195 ha by hybrids and other exotic cordgrass species is slightly less than 1% of the Bay's tidal mudflats and marshes. Spartina anglica has not spread beyond its original 1970s introduction site. Spartina densiflora has spread to cover over 5 ha at 3 sites in the Central Bay. Spartina patens has expanded from 2 plants in 1970 to 42 plants at one site in Suisun Bay. Spartina seed floats on the tide, giving it the potential to export this invasion throughout the San Francisco estuary, and to estuaries outside of the Golden Gate. We found isolated plants of S. alterniflora and S. densiflora in outer coast estuaries north of the Bay suggesting the likelihood for the San Francisco Bay populations to found others on the Pacific coast.     

The rapid evolution of self-fertility in Spartina hybrids (Spartina alterniflora × foliosa) invading San Francisco Bay, CA

Plant hybridization can lead to the evolution of invasiveness. We wished to determine whether hybrids between the largely self-sterile Atlantic Spartina alterniflora and California native S. foliosa had evolved self-fertility during their ca 30 year existence in San Francisco Bay, CA. In pollination experiments we found that neither of the parental species was self-fertile, nor were early generation hybrids. A large fraction of later generation hybrids were profusely self-fertile. Inbreeding depression was high in the parental species and early generation hybrids, but was much reduced in later generation hybrids—some even showed outbreeding depression. We found that populations of later generation hybrids and their seedling progeny were almost two-fold more homozygous than early generation hybrids, consistent with the evidence of increased selfing shown by our parentage analyses based upon 17 microsatellite markers. We posit that evolved self-fertility has contributed substantially to the rapid spread of hybrid Spartina in San Francisco Bay.     

Evolution of a new ecotype of Spartina alterniflora (Poaceae) in San Francisco Bay, California, USA

We report the discovery and spread of a dwarf ecotype of Spartina alterniflora in San Francisco Bay. Relative to typical S. alterniflora, this dwarf ecotype has one-fifth the tiller height (～21 cm), tenfold the tiller density (～4000 tillers/m(2)), and is restricted to growth in the upper intertidal zone. Chromosome counts of the dwarfs are identical to typical smooth cordgrass (2n = 62), and smooth cordgrass-specific random amplified DNA markers confirm the species identity of the dwarf. Field-collected clonal fragments of the dwarf grown for 2 yr under high-nutrient conditions maintained the dwarf syndrome, as did plants grown from the seed of a dwarf. The dwarf condition is not caused by endophytic fungi. The first dwarf smooth cordgrass patch was discovered in 1991, and by 1996 five separate dwarf patches had appeared within 200 m of the original. Since 1991, total area covered by the dwarf ecotype has increased sixfold to 140 m(2). The ecological range of the dwarf smooth cordgrass ecotype is similar to that of S. patens, a competitor on the Atlantic coast. We suggest that the absence of S. patens from most of San Francisco Bay has allowed the dwarf ecotype of smooth cordgrass to survive and spread.     

Molecular phylogeny of hybridizing species from the genus Spartina Schreb. (Poaceae)

Interspecific hybridization events have been reported in the genus Spartina Schreb. (Poaceae), involving the east American species Spartina alterniflora, and including either introgression (e.g., with the western American Spartina foliosa) or allopolyploid speciation (e.g., with the Euro-African Spartina maritima). Molecular phylogenetic analysis of the genus has been undertaken in order to understand phylogenetic relationships and genetic divergence among these hybridizing species. Twelve Spartina species have been sequenced for two nuclear DNA regions (ITS of ribosomal DNA, and part of the Waxy gene) and one chloroplast DNA spacer (trnT-trnL). Separate and conditional combined phylogenetic analyses using Cynodon dactylon as the outgroup have been conducted. Spartina is composed of two lineages. The first clade includes all hexaploid species: the Euro-African S. maritima (2n = 60), the East-American S. alterniflora (2n = 62) and the West-American S. foliosa (2n = 60). Spartina alterniflora appears as a closely related sister species to S. foliosa. Although belonging to the same lineage, Spartina maritima appears consistently more genetically differentiated from S. alterniflora than S. foliosa. The tetraploid species S. argentinensis (2n = 40) is placed at the base of this first clade according to the Waxy data, but its position is not well resolved by the other sequences. The second well-supported main lineage within genus Spartina includes the other tetraploid American species. Significant incongruence has been encountered between the waxy based tree and both the ITS and trnT-trnL trees concerning the position of S. densiflora, suggesting a possible reticulate evolution for this species. The results agree with hybridization patterns occurring in Spartina: introgression involving closely related species (S. alterniflora and S. foliosa) on one hand, and alloploid speciation involving more differentiated species (S. alterniflora and S. maritima) on the other hand.     

An examination of hybridization between the cattail species typha latifolia and typha angustifolia using random amplified polymorphic DNA and chloroplast DNA markers

Typha glauca represents a significant portion of the biomass of the wetlands surrounding the Great Lakes, USA. It is generally accepted to be a form of hybrid between T. latifolia and T. angustifolia, which itself appears to be an exotic introduction from Europe. Based on morphological and isozyme data, conflicting theories have been proposed for the hybrid nature of T. glauca: it has been described as a hybrid swarm, a distinct hybrid species and an F1 hybrid. Therefore, we developed random amplified polymorphic DNA (RAPD) and chloroplast DNA markers, specific to the parental species, to assess hybrids. Ten RAPD primers gave 17 fragments specific to T. angustifolia and 13 fragments specific to T. latifolia. All of the interspecific hybrids contained each of the species-specific markers, indicating an F1 hybrid status. Furthermore, all hybrids tested contained the T. angustifolia chloroplast haplotype, which is consistent with differential interspecific crossing success found previously. Additional confirmation of an F1 hybrid status was gained by examining seedlings from T. glauca. These progeny were expected to be advanced-generation hybrids, as opposed to the F1 hybrid parent. Analysis of the seedlings revealed segregating marker patterns consistent with patterns observed in experimental advanced-generation hybrids, although these advanced hybrids do not appear to be a significant part of mature stands. Our data do not provide support for extensive gene flow between T. latifolia and T. angustifolia. However, our results suggest that hybridization between the native and introduced Typha species has impacted the native population through the spread of the F1 hybrid, T. glauca.