Phylogeny of liverworts (Hepaticae), the least known group of early land plants

Xiaolan He-NygrÉn, inkeri ahonen, aino juslÉn, sinikka piippo & david glenny

The objective of our research is to understand the evolutionary history of liverworts including their origin, patterns of diversification, and adaptive innovations. To date this has been done using a phylogenetic approach based on morphological, genomic, developmental, ultrastructural and palaeontological evidence. We emphasize the use of systematics in comparative biology.

The evolution of land plants marks one of the most important events in Earth's history. Because of their lengthy and well documented fossil record, major patterns in early land plant evolution has mainly been interpreted using macrofossil evidence from vascular plant lineage. Liverworts, in contrast, have a limited fossil record, they are easily neglected due to their small size, and the role they have played in early land plant evolution is rarely emphasized. However, considerable evidence has now accumulated in support of the hypothesis that land plants are of monophyletic origin from a freshwater charophyte algal ancestor, with liverworts the earliest diverging land plant group (e.g. He-Nygrén et al., 2004). Thus liverworts are in a critical position for the understanding of morphological and reproductive changes that favored successful radiation of land plants and adaptation to life in terrestrial environments. Simultaneously, the diversification of this ancient plant lineage, accompanied by various morphological innovations, sheds light on understanding of character transformations and adaptive strategies within the group.

Extant liverworts comprise 5000–8000 species. They exhibit tremendous diversity in their morphology, including complex thalloid, simple thalloid and leafy gametophytes, various apical cell geometries, and several types of sporophyte dehiscence. However, the identification of morphological homologies has been hindered by very significant morphological changes that have occurred over a long historical time period, by possible rapid radiations over short periods, and, more essentially, by the lack of an overall phylogenetic framework. Our understanding of liverwort origin and evolution has been hampered by extinction, a poorly known early fossil record, and insufficient knowledge of the processes underlying the diversification of the group.

Over the last few years, significant progress has been made in resolving phylogenetic relationships of major groups of liverworts using DNA sequence data alone and combined morphological and multiple gene sequence data. These studies have converged on a new hypothesis on evolutionary relationships of liverworts. Our study based on three chloroplast genome sequence data (He-Nygrén et al., 2004) proposed the simple thalloid form with a cuneate apical cell as the ancestral gametophyte type for the liverworts, and thus overturned the long standing theory that liverworts initiated from an erect, leafy gametophyte with a tetrahedral apical cell and three identical leaves around the stem. We recognized the presence of three major groups (classes) in liverworts, Treubiopsida, Marchantiopsida and Jungermanniopsida (He-Nygrén et al, 2006).

Another advance of our studies lay in largely resolving relationships within the leafy liverworts, which includes approximately 90 % of liverwort diversity. Because of their remarkable morphological variation and great complexity of structure, comprehending the evolution and taxonomy of the leafy liverworts has been difficult and challenging. Since the 1970s, based on morphological observations, the leafy liverworts have been assumed to have a “bush-like” phylogeny and have been classified in as many as 15 suborders or orders representing independent evolutionary lines. Therefore the evolutionary relationships between these suborders have largely remained obscure. There are no morphological characters providing clear-cut distinctions between these suborders.

Our studies (He-Nygrén et al., 2004, 2006) clearly demonstrate that, aside from the very isolated Pleurozia, two major clades, the Porellales and the Jungermanniales, constitute the leafy liverworts. This result has initiated new trends and opened up new questions in the study of leafy liverwort evolution. It also requires that our current understanding of the morphology, ontogeny and development of many groups, especially of the leafy liverworts should be reassessed.

Publications

Ahonen, I., J. Muona, J. & Piippo, S. 2003: Inferring the phylogeny of the Lejeuneaceae (Jongermanniopsida): a first appraisal of molecular data. – The Bryologist 106: 297-308.
Ahonen, I. 2004: Molecular phylogeny of the liverwort order Porellales (Marchantiophyta, Jungermanniopsida). – In Goffinet, B., V.C. Hollowell, and R.E. Magill (eds.). Molecular Systematics of Bryophytes: Progress, Problems & Perspectives.  Monogr. Syst. Bot. Missouri Bot. Gard. 98: 87-118.
Ahonen, I. 2005: The taxonomic position of the genus Nipponolejeunea (Steph.) Hattori. – J. Hattori Bot. Lab. 99: 319-342.
Ahonen, I., A. Sass-Gyarmati & Pócs, T. 2005: Molecular, morphological, and taxonomic evaluation of the Ptychanthus striatus complex. – Acta Bot. Hungarica 47: 225-246.
He-Nygrén, X. 2007: Multi-gene phylogeny supports single origin of jungermannioid perigynium. – Ann. Bot. Fennici 44:450-462.
He-Nygrén, X., I., Ahonen, A. Julén, D. Glenny, & S. Piippo, 2004: Phylogeny of liverworts -    beyond a leaf and a thallus. – In Goffinet, B., V.C. Hollowell, and R.E. Magill (eds.). Molecular Systematics of Bryophytes: Progress, Problems & Perspectives.  Monogr. Syst. Bot. Missouri Bot. Gard. 98: 87-118.
He-Nygrén, X., Juslén, S., Ahonen, I., Glenny, D. & Piippo, S. 2006: Illuminating evolutionary history of liverworts- towards a natural classification. – Cladistics 22: 1-31.  
He-Nygrén, X. & Piippo, S. 2003: Phylogenetic relationships of generic complex Chiloscyphus-Lophocolea-Heteroscyphus (Geocalycaceae): Insights from three chloroplast genes and morphology. – Ann. Bot. Fennici 40 (5): 317-329.   
Juslén, A. 2004: Bryophyte flora of Hunan Province, China. 7. Herbertus (Herbertaceae, Hepaticae). – Annales Bot. Fennici 41: 393-404.
Juslén, A. 2006: Revision of Asian Herbertus Gray (Herbertaceae, Marchantiophyta). – Annales Bot. Fennici 43: 409-436.
Juslén, A. 2006: Phylogeny of Vetaformaceae, Lepicoleaceae, and Herbertaceae (including Mastigophoraceae) inferred from chloroplast trnL-F, nuclear ITS2, and morphology. – Annales Bot. Fennici: 43: 349-362.