Trends and concepts in fern classification

Abstract

Background and aims: Throughout the history of fern classification, familial and generic concepts have been highly labile. Many classifications and evolutionary schemes have been proposed during the last two centuries, reflecting different interpretations of the available evidence. Knowledge of fern structure and life histories has increased through time, providing more evidence on which to base ideas of possible relationships, and classification has changed accordingly. This paper reviews previous classifications of ferns and presents ideas on how to achieve a more stable consensus.

Scope: An historical overview is provided from the first to the most recent fern classifications, from which conclusions are drawn on past changes and future trends. The problematic concept of family in ferns is discussed, with a particular focus on how this has changed over time. The history of molecular studies and the most recent findings are also presented.

Key results: Fern classification generally shows a trend from highly artificial, based on an interpretation of a few extrinsic characters, via natural classifications derived from a multitude of intrinsic characters, towards more evolutionary circumscriptions of groups that do not in general align well with the distribution of these previously used characters. It also shows a progression from a few broad family concepts to systems that recognized many more narrowly and highly controversially circumscribed families; currently, the number of families recognized is stabilizing somewhere between these extremes. Placement of many genera was uncertain until the arrival of molecular phylogenetics, which has rapidly been improving our understanding of fern relationships. As a collective category, the so-called 'fern allies' (e.g. Lycopodiales, Psilotaceae, Equisetaceae) were unsurprisingly found to be polyphyletic, and the term should be abandoned. Lycopodiaceae, Selaginellaceae and Isoëtaceae form a clade (the lycopods) that is sister to all other vascular plants, whereas the whisk ferns (Psilotaceae), often included in the lycopods or believed to be associated with the first vascular plants, are sister to Ophioglossaceae and thus belong to the fern clade. The horsetails (Equisetaceae) are also members of the fern clade (sometimes inappropriately called 'monilophytes'), but, within that clade, their placement is still uncertain. Leptosporangiate ferns are better understood, although deep relationships within this group are still unresolved. Earlier, almost all leptosporangiate ferns were placed in a single family (Polypodiaceae or Dennstaedtiaceae), but these families have been redefined to narrower more natural entities.

Conclusions: Concluding this paper, a classification is presented based on our current understanding of relationships of fern and lycopod clades. Major changes in our understanding of these families are highlighted, illustrating issues of classification in relation to convergent evolution and false homologies. Problems with the current classification and groups that still need study are pointed out. A summary phylogenetic tree is also presented. A new classification in which Aspleniaceae, Cyatheaceae, Polypodiaceae and Schizaeaceae are expanded in comparison with the most recent classifications is presented, which is a modification of those proposed by Smith et al. (2006, 2008) and Christenhusz et al. (2011). These classifications are now finding a wider acceptance and use, and even though a few amendments are made based on recently published results from molecular analyses, we have aimed for a stable family and generic classification of ferns.

Keywords: Bibliography; Cyatheaceae; Polypodiaceae; classification; convergence; cryptogams; fern allies; fern family concepts; ferns; history of botany; homology; lycopods; monilophytes; pteridophytes.

Fig. 1.

Characters of ferns. (A) Gametophyte [Ptisana attenuata (Labill.) Murdock, Marattiaceae]. (B) Sporophyte [Ptisana sp. nov. (Kamau & Christenhusz 638, EA, K), Marattiaceae]. (C) Circinnate vernation (Sphaeropteris excelsa (Endl.) R.M.Tryon, Cyatheaceae). (D) Sporocarps [Salvinia natans (L.) All., Salviniaceae]. (E) Discrete sori with indusia [Polystichum falcatum (L.f.) Diels non Fée, Polypodiaceae]. (F) Acrostichoid sori [Acrostichum durvillei (Fée) C.Presl, Pteridaceae].

Fig. 2.

The first illustration of the germination of spores by Lindsay (1794). 1. Leaf with sori. 2–5. Sporangium opening, showing annulus and spores. 6–7. Spores. 8–11. Developing gametophyte. 15–17. Developing sporophyte.

Fig. 3.

Summary phylogenetic tree showing relationships of a representative selection of fern genera based on molecular (DNA) data, modified from Schuettpelz and Pryer (2007), Lehtonen (2011), Rothfels et al. (2012) and Schneider et al. (2013).

Fig. 4.

Sori of major fern lineages. (A) Equisetales, Equisetum telmateia Ehrh. (B) Ophioglossales, Botrychium virginianum (L.) Sw. (C) Psilotales, Psilotum nudum (L.) P.Beauv. (D) Marattiales, Marattia cicutifolia Kaulf. (E) Osmundales, Todea barbara T.Moore. (F) Hymenophyllales, Trichomanes cupressoides Desv. (G) Gleicheniales, Dicranopteris linearis (Burm.f.) Underw. (H) Schizaeales, Lygodium volubile Sw. (I) Salviniales, Marsilea drummondii A.Braun. (J) Cyatheales, Alsophila dealbata (G.Forst.) C.Presl. (K) Polypodiales, Dennstaedtia punctilobula (Michx.) T.Moore. (L) Pteris usambarensis Hieron. (M) Eupolypods, Asplenium caudatum G.Forst. (N) Dryopteris sieboldii (T.Moore) Kunze.