Niche and phenotypic differentiation in fern hybrid speciation, a case study of Pteris fauriei (Pteridaceae).

BACKGROUND AND AIMS: Niche differentiation is a crucial issue in speciation. Although it has a well-known role in adaptive processes of hybrid angiosperms, it is less understood in hybrid ferns. Here, we investigate whether an intermediate ecological niche of a fern hybrid is a novel adaptation that provides insights into fern hybrid speciation. METHODS: Pteris fauriei (Pteridaceae) is a natural hybrid fern, occurring in environments between its parent species. The maternal Pteris minor is found in sunny areas, but the habitat of the paternal Pteris latipinna is shady. We combined data from morphology, leaf anatomy and photosynthetic traits to explore adaptation and differentiation, along with measuring the environmental features of their niches. We also performed experiments in a common garden to understand ecological plasticity. KEY RESULTS: The hybrid P. fauriei was intermediate between the parent species in stomatal density, leaf anatomical features and photosynthetic characteristics in both natural habitats and a common garden. Interestingly, the maternal P. minor showed significant environmental plasticity and was more similar to the hybrid P. fauriei in the common garden, suggesting that the maternal species experiences stress in its natural habitats but thrives in environments similar to those of the hybrid. CONCLUSIONS: Based on the similar niche preferences of the hybrid and parents, we propose hybrid superiority. Our results indicate that the hybrid P. fauriei exhibits greater fitness and can compete with and occupy the initial niches of the maternal P. minor. Consequently, we suggest that the maternal P. minor has experienced a niche shift, elucidating the pattern of niche differentiation in this hybrid group. These findings offer a potential explanation for the frequent occurrence of hybridization in ferns and provide new insights into fern hybrid speciation, enhancing our understanding of fern diversity.

Allotetraploid cryptic species in Asplenium normale in the Japanese Archipelago, detected by chemotaxonomic and multi-locus genotype approaches.

PREMISE OF THE STUDY: Delimitation of cryptic species provides an understanding of biodiversity and opportunities to elucidate speciation processes. Extensive flavonoid variation has been reported in the tetraploid cytotype of the fern, Asplenium normale, although related species have no intraspecific variations in flavonoid composition. We hypothesized that Japanese A. normale still harbors multiple cryptic species with different flavonoid compositions, and tested this hypothesis using chemotaxonomic and multilocus genotyping approaches. METHODS: We determined the multilocus genotypes (MLGs) of 230 samples from 37 populations for one chloroplast DNA region and three nuclear genes. MLGs were used to delimit reproductively isolated lineages by population-genetic approaches. We also tested the correspondence between genetically recognized groups and flavonoid compositions. To identify the origins of putative cryptic species, we conducted phylogenetic analysis of the DNA markers used in genotyping. KEY RESULTS: The genetic clusters and flavonoid compositions showed clear correspondence. We recognized three putative cryptic species in tetraploid Asplenium normale in Japan. Phylogenetic analyses revealed that cryptic species I and III originated from allopolyploidization between a diploid A. normale and an unknown diploid of A. boreale, and cryptic species II originated from allopolyploidization between a diploid A. normale and A. oligophlebium. CONCLUSIONS: Our study demonstrated that intraspecific variation of secondary metabolites can be a good indicator of cryptic species in ferns. The presence of the two cryptic species having the same progenitor diploid pair suggests that speciation between allopolyploid lineages of independent origin may be more common than previously considered.

Phylogeny and character evolution of the fern genus Tectaria (Tectariaceae) in the Old World inferred from chloroplast DNA sequences.

In this study we provide a phylogeny for the pantropical fern genus Tectaria, with emphasis on the Old World species, based on sequences of five plastid regions (atpB, ndhF plus ndhF-trnL, rbcL, rps16-matK plus matK, and trnL-F). Maximum parsimony, maximum likelihood, and Bayesian inference are used to analyze 115 individuals, representing ca. 56 species of Tectaria s.l. and 36 species of ten related genera. The results strongly support the monophyly of Tectaria in a broad sense, in which Ctenitopsis, Hemigramma, Heterogonium, Psomiocarpa, Quercifilix, Stenosemia, and Tectaridium should be submerged. Such broadly circumscribed Tectaria is supported by the arising pattern of veinlets and the base chromosome number (x=40). Four primary clades are well resolved within Tectaria, one from the Neotropic (T. trifoliata clade) and three from the Old World (T. subtriphylla clade, Ctenitopsis clade, and T. crenata clade). Tectaria crenata clade is the largest one including six subclades. Of the genera previously recognized as tectarioid ferns, Ctenitis, Lastreopsis, and Pleocnemia, are confirmed to be members in Dryopteridaceae; while Pteridrys and Triplophyllum are supported in Tectariaceae. To infer morphological evolution, 13 commonly used characters are optimized on the resulting phylogenetic trees and in result, are all homoplastic in Tectaria.

Molecular phylogeny and biogeography of the fern genus Pteris (Pteridaceae).

BACKGROUND AND AIMS: Pteris (Pteridaceae), comprising over 250 species, had been thought to be a monophyletic genus until the three monotypic genera Neurocallis, Ochropteris and Platyzoma were included. However, the relationships between the type species of the genus Pteris, P. longifolia, and other species are still unknown. Furthermore, several infrageneric morphological classifications have been proposed, but are debated. To date, no worldwide phylogenetic hypothesis has been proposed for the genus, and no comprehensive biogeographical history of Pteris, crucial to understanding its cosmopolitan distribution, has been presented. METHODS: A molecular phylogeny of Pteris is presented for 135 species, based on cpDNA rbcL and matK and using maximum parsimony, maximum likelihood and Bayesian inference approaches. The inferred phylogeny was used to assess the biogeographical history of Pteris and to reconstruct the evolution of one ecological and four morphological characters commonly used for infrageneric classifications. KEY RESULTS: The monophyly of Pteris remains uncertain, especially regarding the relationship of Pteris with Actiniopteris + Onychium and Platyzoma. Pteris comprises 11 clades supported by combinations of ecological and morphological character states, but none of the characters used in previous classifications were found to be exclusive synapomorphies. The results indicate that Pteris diversified around 47 million years ago, and when species colonized new geographical areas they generated new lineages, which are associated with morphological character transitions. CONCLUSIONS: This first phylogeny of Pteris on a global scale and including more than half of the diversity of the genus should contribute to a new, more reliable infrageneric classification of Pteris, based not only on a few morphological characters but also on ecological traits and geographical distribution. The inferred biogeographical history highlights long-distance dispersal as a major process shaping the worldwide distribution of the species. Colonization of different niches was followed by subsequent morphological diversification. Dispersal events followed by allopatric and parapatric speciation contribute to the species diversity of Pteris.

Extreme multiple reticulate origins of the Pteris cadieri complex (Pteridaceae).

The Pteris cadieri complex displays extensive morphological variation and seems to have originated through hybridization. However, the members of this complex reproduce by apogamy, which usually limits genetic variation. To evaluate the hypotheses of hybrid origins, the pattern of evolution in this species complex is reconstructed. Multiple methodologies were used. Diploids, triploids, and tetraploids were identified by chromosome counts and flow cytometry. Nuclear DNA markers (cytosolic phosphoglucose isomerase gene, PgiC) were used, together with chloroplast DNA markers (atpB-rbcL spacer and rbcL gene) to infer the biparental and maternal lineages of the Pteris cadieri complex. The three cpDNA haplotype groups and five PgiC alleles found in this study indicate that the evolution of the Pteris cadieri complex has been extremely reticulate. Up to 11 taxa belonging to eight morphs were identified. By comparing genetic variation in the Pteris cadieri in two independent areas, Hainan and Taiwan, we inferred that hybridization has occurred independently in different areas. Furthermore, we found evidence for phenological divergence (evergreen and deciduous) within Taiwan. We propose that the Pteris cadieri complex originated from different genetic lineages through multiple hybridizations in different geographical areas, leading to its present morphological diversity.

Reticulate evolution in the Pteris fauriei group (Pteridaceae).

The Pteris fauriei group (Pteridaceae) has a wide distribution in Eastern Asia and includes 18 species with similar but varied morphology. We collected more than 300 specimens of the P. fauriei group and determined ploidy by flow cytometry and inferred phylogenies by molecular analyses of chloroplast and nuclear DNA markers. Our results reveal a complicated reticulate evolution, consisting of seven parental taxa and 58 hybrids. The large number of hybrid taxa have added significant morphological complexity to the group leading to difficult taxonomic issues. The hybrids generally had broader ranges and more populations than their parental taxa. Genetic combination of different pairs of parental species created divergent phenotypes of hybrids, exhibited by both morphological characteristics and ecological fidelities. Niche novelty could facilitate hybrid speciation. Apogamy is common in this group and potentially contributes to the sustainability of the whole group. We propose that frequent hybridizations among members of the P. fauriei group generate and maintain genetic diversity, via novel genetic combinations, niche differentiation, and apogamy.

Microsatellite primers in the native perennial cycad Cycas taitungensis (Cycadaceae).

PREMISE OF THE STUDY: Microsatellite primers were developed for the native perennial cycad Cycas taitungensis to evaluate the genetic variation of this endangered insular species. METHODS AND RESULTS: Using a magnetic bead enrichment method and EST data, 16 primer sets were developed and identified for the native Taiwan cycad C. taitungensis. The primers amplified dinucleotide, trinucleotide, and complex repeats with 1-9 alleles per locus. Most primers also amplified DNA from C. revoluta and C. debaoensis. CONCLUSIONS: These results indicate the utility of primers for future studies of the genetic structure of C. taitungensis. In addition, the primers are useful for further phylogeographic studies between C. taitungensis and C. revoluta, which is a closely related species.

Bolbitis lianhuachihensis (Dryopteridaceae), a new species from Taiwan.

A new species of Bolbitis, B. lianhuachihensis sp. nov., was found in central Taiwan. It most resembles B. virens var. compacta and B. hainanensis. A phylogenetic tree of Taiwanese and other Asian species of Bolbitis species supports the recognition of the new species. Morphologically, the combination of anastomosing venation and fewer sterile pinnae are critical characters to discriminate B. lianhuachihensis from other Taiwanese Bolbitis species. Bolbitis lianhuachihensis can be further distinguished from B. virens var. compacta and B. hainanensis by having lanceolate sterile pinnae and absent or fewer free veinlets in small areoles of sterile pinnae. The morphological descriptions, illustration, ecology and distribution of the new species are presented. A key to all Taiwanese Bolbitis is also provided.

Spore morphology and its systematic implication in Pteris (Pteridaceae).

Pteris (Pteridaceae) spores are usually trilete and can be distinguished by the perine ornamentation. The systematic value of spore morphology in Pteris is unclear, especially based on the renewed infrageneric classification of Pteris. In the present study, we used scanning electron microscopy (SEM) to understand spore characters in 57 Pteris species, one Onychium species, and two Astrolepis species; 40 species are reported here for the first time. The observed spore characters combined with published spore data, totaling 100 species from 16 sections of Pteris, were mapped onto a reconstructed phylogenetic tree. Seven characters (five proposed in previous studies), including an equatorial flange, laesural ridges, proximal ridges, distal ridges, tubercula on distal faces, coarse reticula on distal faces, and a row of extervermiculi between the distal face and equatorial flange, were analyzed to investigate spore morphology evolution in Pteris. However, the results showed no synapomorphies with other genera in Pteridaceae. Most of the characters were found to have arisen independently several times in different lineages or were even frequently reversed. Equatorial flanges and tubercula on distal faces are plesiomorphies and present in most Pteris species. Overall, the application of spore morphology in section circumscription is limited. Thus, we suggest combining spore morphology with leaf characters for Pteris infrageneric classification.

Pteris latipinna sp. nov. (Pteridaceae), a new species segregated from Pteris fauriei.

Pteris fauriei is widely distributed in Eastern Asia and has high morphological variation. Some morphologically similar plants related to this species are difficult to distinguish. We showed that the new Pteris species from Taiwan, previously identified as P. fauriei, can be morphologically distinguished by its wide pinnae, larger terminal pinnae than the lateral pinnae in sterile fronds, and triangular basal segments of the lateral pinnae. It was confirmed that this species is phylogenetically separated from the other East Asian Pteris species, except for a morphologically distinct species P. arisanensis, by means of chloroplast genes, rbcL and matK. The new species is named as Pteris latipinnasp. nov., referring to its wide pinnae. Here, we provide a key to facilitate the identification of the morphologically similar Pteris species in Asia. The morphological descriptions, images, ecology, and distribution are also presented.

New Species of the Fern Genus Lindsaea (Lindsaeaceae) from New Guinea with Notes on the Phylogeny of L. sect. Synaphlebium.

To determine the taxonomic identities and the systematic positions of some collections of Lindsaea sect. Synaphlebium (Lindsaeaceae) from Papua New Guinea, we conducted morphological comparisons and phylogenetic analyses on the whole section. A total of 22 morphological characters were selected and coded for each of all known taxa in L. sect. Synaphlebium, and were analyzed using maximum parsimony. The datasets containing either of or combined two plastid DNA sequences (trnL-trnF spacer and trnH-psbA spacer) of 37 taxa were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference. Morphological comparisons revealed two new species which are formally published here as L. subobscura and L. novoguineensis. Lindsaea subobscura is similar to sympatric L. obscura and L. modesta but differs in the obviously reduced upper pinnules and other characters. Lindsaea novoguineensis is most similar to L. pacifica from Melanesia but differs in having rhomboid pinnules with truncate apices and concave soral receptacles. Molecular analyses resolved L. sect. Synaphlebium and allied species into five well-supported clades, namely L. rigida clade, L. obtusa clade, L. pulchella clade, L. multisora clade, and L. cultrata clade. The new species L. novoguineensis is included in L. obtusa clade; L. subobscura is in L. pulchella clade; whereas the majority of L. sect. Synaphlebium is clustered in L. cultrata clade. As the section Synaphlebium sensu Kramer is strongly suggested as polyphyletic, we propose the concept of a monophyletic L. sect. Synaphlebium in a broad sense that comprises five lineages. The morphological circumscription of L. sect. Synaphlebium sensu lato and the divergence in morphology, habit, and distribution between the five lineages are briefly discussed. Further molecular study is needed to test the systematic positions of 16 other species which are supposed to be within L. sect. Synaphlebium sensu lato but have not been included in this and previous molecular analyses.