Recognize Lepisorus sensu lato (Polypodiaceae), by including Ellipinema, Lemmaphyllum, Paragramma, Neocheiropteris, Neolepisorus, Tricholepidium, and Lepidomicrosorium [PASSED]

[weiran007]

Author(s) of proposal

Ran Wei

Name of taxon

Lepisorus

Rank of taxon

Genus

Approximate number of species affected

No response

Description of change

Lumping Lepisorus and its allied genera to keep them as a monophyletic group.

Reason for change

Zhao et al. (2020a) provided a robust phylogenetic topology of Lepisorus and its allies based on plastid markers. The results strongly supported the monophyly of this group of ferns with important synapomorphies, such as scale-like paraphysis and leaves without hairs, and thus proposed a broadly defined Lepisorus with all the allied genera included. This conclusion is further confirmed by Wei et al. (2021) using single or low copy nuclear markers. Inconsistent with plastid data, which recovered Lepidomicrosorium, Lemmaphyllum, Neolepisorus, Neocheiropteris, Paragramma and Tricholepidium together with Lepisorus jakonensis as sisters to Lepisorus s.str., nuclear data resolved these lineages as more closely related to subclades or sections within the latter, indicating possible ancient hybridization events or incomplete lineage sorting may have occurred in their evolutionary history. Moreover, it is well-documented that L. jakonensis can interbreed with L. waltonii to produce fertile offspring: the tetraploid L. inaequibasis (Zhao et al., 2020b). The co-occurrence of L. jakonensis and other Lepisorus species in sections Pachyphyllon, Hymenophyton, Lemmaphyllum, Pseudovittaria and Tricholepidium in the Himalaya regions also indicates that they may have undergone parallel rapid diversification and have experienced similar evolutionary history during the Miocene and Pliocene due to the uplift of the Himalayas and changing of monsoon patterns (Wang et al., 2012). The above evidence, thus, does not support the separation of these lineages (i.e. Lepidomicrosorium, Lemmaphyllum, Neolepisorus, Neocheiropteris, Paragramma and Tricholepidium) from Lepisorus, nor the placement of L. jakonensis in the independent genus Ellipinema. The monotypic Ellipinema was separated from Lepisorus s.str. mainly because of its divergence (during the Miocene; < 23 Ma) (Zhang et al., 2020). Examples in other lineage of leptosporangiate ferns, such as Pteris and Platyzoma may represent similar cases. Platyzoma has an extremely long branch and exhibits a series of unique apomorphies distinct from Pteris, including fronds with farina, heterospory and dioecism in gametophytes and long divergence from Pteris dating back to the Paleogene (Chao et al., 2014) or early Jurassic (Testo and Sundue, 2016). Platyzoma, however, was not segregated from Pteris (Zhang & Zhang, 2018). On the other hand, a number of studies in species-rich genera of ferns have tended to merge recently diverged (since the late Paleogene), small segregates into larger ones, such as in Asplenium (Schneider et al., 2004), Diplazium (Wei et al., 2013), Dryopteris (Zhang et al., 2012), and Polystichum (Le Péchon et al., 2016). The treatment of Lepisorus s.str. and its allies in Zhao et al. (2020a) is an analogous case. The diagnostic morphological feature used to characterize Ellipinema is the elliptic paraphyses (Zhang et al., 2020). However, the detailed observation of L. jakonensis in Wei et al. (2021) demonstrated that the shape of the paraphyses varies continuously from stellar to lanceolate; elliptic forms represent only an intermediate condition. Similar variation pattern in paraphyses also occurs in sect. Hymenophyton (Liu et al., 2008). The statistical analysis of the length/width ratios of paraphyses in Wei et al. (2021) shows that paraphysis features may potentially serve as diagnostic characters in distinguishing L. jakonensis (=sect. Pseudoclathrati) from sect. Hymenophyton within Lepisorus, but the large overlapping part in the range of variation further indicates that paraphyses between them are not substantially distinct, and there is no ground to support the separation of L. jakonensis as a distinct genus. Zhao et al. (2020b) confirmed the hybrid origin of L. inaequibasis based on phylogenetic and morphological evidence and elucidated its allotetraploid origin from its diploid progenitors, L. jakonensis and L. waltonii, providing another evidence for the inclusion of L. jakonensis into Lepisorus. In summary, nuclear phylogenies confirm that many previously recognized segregated genera are nested within Lepisorus and that an expanded Lepisorus containing these species is necessary to make the genus monophyletic as concluded in Zhao et al. (2020a) using plastid data. The recognition of Ellipinema as distinct from Lepisorus rendering the latter paraphyletic, is supported by neither the nuclear data, nor important diagnostic characters, such as rhizome scales and soral paraphyses, and thus should be rejected all together. Although a broadly defined Lepisorus may introduce several novel nomenclatural combinations, our taxonomic philosophy is more concordant with criteria discussed in Schuettpelz et al. (2018), such as morphological diagnosability, phylogenetic monophyly and genetic similarity, and the case of Lepisorus may be applicable for other species-rich fern groups that also have undergone rapid speciation followed by intrageneric introgression and hybridization. The example of cytonuclear discordance in Lepisorus further suggests that taxonomic changes should not rely only on one line of evidence, i.e., plastid DNA in light of faulty morphological interpretations, especially in rapidly evolved groups like Asplenium, Dryopteris, and Polystichum. etc.

Reference(s) for publication of the name

Chao, Y.S., Rouhan, G., Amoroso, V.B., Chiou, W.L., 2014. Molecular phylogeny and biogeography of the fern genus Pteris (Pteridaceae). Annals of Botany, 114, 109–124. Le Péchon, T., He, H., Zhang, L., Zhou, X.M., Gao, X.F., Zhang, L.B., 2016. Using a multilocus phylogeny to test morphology-based classifications of Polystichum (Dryopteridaceae), one of the largest fern genera. BMC Evolutionary Biology, 16, 55. Liu, Q.R., Ming, G.H., Ge, Y., Zhang, X.C., 2008. A taxonomic revision of Lepisorus sect. Hymenophyton (Polypodiaceae) from China. Journal of Systematics and Evolution, 46, 906–915. Schneider, H., Russell, S.J., Cox, C.J., Bakker, F., Henderson, S., Rumsey, F., Barrett, J., Gibby, M., Vogel, J.C., 2004. Chloroplast phylogeny of asplenioid ferns based on rbcL and trnL-F spacer sequences (Polypodiidae, Aspleniaceae) and its implications for biogeography. Systematic Botany, 29, 260–274. Schuettpelz, E., Rouhan, G., Pryer, K.M., Rothfels, C.J., Prado, J., Sundue, M.A., Windham, M.D., Moran, R.C., Smith, A.R., 2018. Are there too many fern genera? Taxon, 67, 473–480. Testo, W., Sundue, M.A., 2016. A 4000-species dataset provides new insight into the evolution of ferns. Molecular Phylogenetics and Evolution, 105, 200–211. Wang, L., Schneider, H., Wu, Z.Q., He, L.J., Zhang, X.C., Xiang, Q.P., 2012. Indehiscent sporangia enable the accumulation of local fern diversity at the Qinghai-Tibetan Plateau. BMC Evolutionary Biology, 12, 158. Wei, R., Schneider, H., Zhang, X.C., 2013. Toward a new circumscription of the twinsorus-fern genus Diplazium (Athyriaceae): A molecular phylogeny with morphological implications and infrageneric taxonomy. Taxon, 62, 441–457. Wei, R., Zhao, C.F., Xiang, Q.P., Zhang, X.C., 2021. Ellipinema and × Ellipisorus? Just Lepisorus (Polypodiaceae)! Molecular Phylogenetics and Evolution, 161, 107176. Zhang, L., Zhang, L.B., 2018. Phylogeny and systematics of the brake fern genus Pteris (Pteridaceae) based on molecular (plastid and nuclear) and morphological evidence. Molecular Phylogenetics and Evolution, 118, 265–285. Zhang, L., Zhou, X.M., Liang, Z.L., Fan, X.P., Lu, N.T., Song, M.S., Knapp, R., Gao, X.F., Sun, H., Zhang, L.B., 2020. Phylogeny and classification of the tribe Lepisoreae (Polypodiaceae; pteridophyta) with the description of a new genus, Ellipinema gen. nov., segregated from Lepisorus. Molecular Phylogenetics and Evolution, 148, 106803. Zhang, L.B., Zhang, L., Dong, S.Y., Sessa, E.B., Gao, X.F., Ebihara, A., 2012. Molecular circumscription and major evolutionary lineages of the fern genus Dryopteris (Dryopteridaceae). BMC Evolutionary Biology, 12, 180. Zhao, C.F., Wei, R., Zhang, X.C., Xiang, Q.P., 2020a. Backbone phylogeny of Lepisorus (Polypodiaceae) and a novel infrageneric classification based on the total evidence from plastid and morphological data. Cladistics, 36, 235–258. Zhao, C.F., Wei, R., Xiang, Q.P., Zhang, X.C., 2020b. The origin of allotetraploid Lepisorus inaequibasis (Polypodiaceae) and paternal bias in its morphology and abiotic niche. Taxon, 69, 43–55.

List the numbers of any related issues

46

Code of Conduct

• [X] I agree to follow the PPG Code of Conduct

[gonggashan88]

Hi Dr. Wei, I see 9 problems in your proposal:

1. Caobangia and Weatherbya were resolved in Lepisorus and have been treated as part of Lepisorus since Wang et al. (2010), PPG I (2016), and Wei et al. (2017). They are not controversial at all.
2. The taxon samplings in neither Zhao et al. (2020) nor Wei et al. (2021) were large. In fact, only 1-2(-5) accessions from each of the critical genera were sampled. In contrast, Zhang & Zhang (2020) achieved complete or near-complete sampling of the tribe, as estimated by PPG I.
3. Your two nuclear trees in Wei et al. (2021) are conflicting each other and not as reliable as the plastid trees in Zhao et al. (2020) or Zhang et al. (2020).
4. Lepisorus is paraphyletic only if you include L. jakonensis. The former will be monophyletic if the latter is included in a different genus, Ellipinema (Zhang et al., 2020).
5. In order to keep L. jakonensis (Ellipinema) in Lepisorus, you lumped 6 other well-established genera in Lepisorus, and transferred a number of species to Lepisorus to make new combinations, nomenclaturally being not parsimonious.
6. Your lumping Ignores the deeply diverged and morphologically diagnosable lineages (genera) consistently found in quite a few studies.
7. The 6 genera you lumped in Lepisorus have long been recognized in various floristic and taxonomic works in Asia and Africa and also by PPG I. Your approach will inevitably cause disruption of current application of ca. 30 generic and species names.
8. At least two of the genera you lumped in Lepisorus, Neocheiropteris and Neolepisorus, have high horticultural values, and thus your lumping caused inconvenience and confusion in horticulture industry.
9. Two out of the 6 generic names you lumped in Lepisorus, Lemmaphyllum (1851) and Neocheiropteris (1905), are much older than Lepisorus (1933), threatening the application of Lepisorus.

As stated in detail in proposal #46, the best and simplest practice is to recognize Ellipinema instead of lumping all 6 other well-established genera in Lepisorus.

[weiran007]

Hi Dr. Wei, I see 9 problems in your proposal:

1. Caobangia and Weatherbya were resolved in Lepisorus and have been treated as part of Lepisorus since Wang et al. (2010), PPG I (2016), and Wei et al. (2017). They are not controversial at all.
2. The taxon samplings in neither Zhao et al. (2020) nor Wei et al. (2021) were large. In fact, only 1-2(-5) accessions from each of the critical genera were sampled. In contrast, Zhang & Zhang (2020) achieved complete or near-complete sampling of the tribe, as estimated by PPG I.
3. Your two nuclear trees in Wei et al. (2021) are conflicting each other and not as reliable as the plastid trees in Zhao et al. (2020) or Zhang et al. (2020).
4. Lepisorus is paraphyletic only if you include L. jakonensis. The former will be monophyletic if the latter is included in a different genus, Ellipinema (Zhang et al., 2020).
5. In order to keep L. jakonensis (Ellipinema) in Lepisorus, you lumped 6 other well-established genera in Lepisorus, and transferred a number of species to Lepisorus to make new combinations, nomenclaturally being not parsimonious.
6. Your lumping Ignores the deeply diverged and morphologically diagnosable lineages (genera) consistently found in quite a few studies.
7. The 6 genera you lumped in Lepisorus have long been recognized in various floristic and taxonomic works in Asia and Africa and also by PPG I. Your approach will inevitably cause disruption of current application of ca. 30 generic and species names.
8. At least two of the genera you lumped in Lepisorus, Neocheiropteris and Neolepisorus, have high horticultural values, and thus your lumping caused inconvenience and confusion in horticulture industry.
9. Two out of the 6 generic names you lumped in Lepisorus, Lemmaphyllum (1851) and Neocheiropteris (1905), are much older than Lepisorus (1933), threatening the application of Lepisorus.

As stated in detail in proposal #46, the best and simplest practice is to recognize Ellipinema instead of lumping all 6 other well-established genera in Lepisorus.

Hi Prof. Zhang,

Thank you so much for your questions! Actually, I DO NOT think there are problems at all as you stated.

Reply to your concern #1: Yes, Caobangia and Weatherbya are not controversial any more.

Reply to your concern #2: The taxon samplings in Zhao et al. (2020) and Wei et al. (2021) are both typical and representative with all extant clades and critical genera/species included. Actually, species sampling of Zhang & Zhang (2020) is superficially “complete”, and I DO NOT think it is substantially different from Zhao et al. (2020) and Wei et al. (2021). If checking in details, the "comprehensive" sampling in Zhang & Zhang (2020) only means multiple accessions or individuals of one species, none of which shows different phylogenetic clustering from Zhao et al. (2020) and Wei et al. (2021) using quantitatively fewer species sampling.

Reply to your concern #3: It is quite normal that there exists conflict between nuclear trees because Lepisorus might have undergone complex evolutionary process such as hybridization/introgression and incomplete lineage sorting, and there are a lot of papers discussing phylogenetic conflict using genomic nuclear sequences, and this is one of the main reasons for the development of multi-species coalescent methods for tree inference. This also indicates that it is not necessary to just use plastid to reveal the phylogenetic relationship among these ferns. So, Wei et al. (2021) included updated information from Zhao et al. (2020).

It is important that both nuclear markers recovered the monophyly of Lepisorus with the allied genera. So, the major point here I want to respond is that both nuclear markers show mixed phylogenetic clustering among Lepisorus s.s. and the allied segregates based on the representative sampling size. This is strong evidence that these ferns show very close relationship and reticulate evolution, and it is rather rational to lump them all into a single genus. Surely, there will be more and more relevant species from these allied segregates mixed with Lepisorus s.s. when the sampling size are larger.

Reply to your concern #4: Lepisorus is not paraphyletic when L. jakonensis and other allied genera are recognized as members of Lepisorus, and they should be recognized as Lepisorus. Leaf morphology is variable in these ferns, but scale-like paraphyses and lack of trichomes are obvious synapomorphies of these ferns. As we mentioned in Wei et al. (2021), shape of paraphyses is not elliptic, instead, it well represents a continuous variation from ovate to lanceolate, and elliptic-shape is just an intermediate state. Also, paraphyses and rhizome scales of L. jakonensis show much similarity to sect. Hymenophyton. Thus, it is not necessary to recognize Ellipinema.

Reply to your concern #5: By stating this, I think you might be showing the self-contradiction. Since you mentioned that lumping Lepisorus and the allied genera is not parsimonious, why lumping Dryopteris and the allied genera such as Peranema, Nothoperanema, Acrophorus, Diacalpe and Acrorumohra in Zhang et al. (2012), which is a similar case to Lepisorus?

Reply to your concern #6: The same as concern #5 showing self-contradiction: Platyzoma are quite different from Pteris in ferns based on some unique morphological characters and has split from the latter since the Paleogene (> 56 Ma in Chao et al., 2014) or early Jurassic (> 174 Ma in Testo & Sundue, 2016), but Zhang & Zhang (2018) still lumped this genus into the latter. In comparison, the split time among L. jakonensis, other Lepisorus and the allied genera is much younger during the Miocene (< 23 Ma), obviously not as old as stated in your concern. Considering splitting time is not rational for the separation of L. jakonensis and other allied genera from Lepisorus.

Reply to your concern #7: This is the same question as your concern #5 and 6.

Reply to your concern #8: I DO NOT think this should be borrowed as a reason, and take Selaginella as an example, again: Selaginella kraussiana is much more well-known than Lepisorus (Neolepisorus) ensatus and L. (Neocheiropteris) palmatopedatus as horticultural plants, however, Zhou & Zhang (2023) still give it a new GENUS name: Gymnogynum. According to your logic, we should reject this treatment on Selaginella kraussiana. Actually, there is a lot of instances on the changing of generic level of ornamental plants, such as Juniperus chinensis (formerly Sabina chinensis) and many horticultural species in Magnoliaceae, all current generic status of which are widely accepted by both scientists and consumers nowadays. The changing of generic circumscription will not substantially make confusion in their common names for commercial usage.

Reply to your concern #9: Theis is already proposal submitted and voted in IAPT for conserving Lepisorus against Lemmaphyllum (1851) and Neocheiropteris (1905). I DO NOT think there will be any threatens. In a word, recognition of Ellipinema and other allied genera from Lepisorus is supported by neither the nuclear/plastid data, nor important diagnostic characters, and also is not a parsimonious way as stated.

[SchneiderHarald]

Actually, the proposal is arguably the best approach to handle this lineage by avoiding the messiness associated with narrower genera concepts. This proposal is actually an excellent example how the fern community can avoid the troubles created by the unnecessary introduction of very small generic units — arguably only reflecting the personal motivation of particular authors instead of scientific common sense. Instead of splitting hairs about details, it is crucial to be integrative and comprehensive as the original draft of the proposal.

[joelnitta]

This proposal was voted on during PPG Ballot 5 (voting period November 2023). A total of 65 votes were cast. There were 49 'Yes' votes (75.4%) and 16 'No' votes (24.6%). The proposal passes.