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Wikstrom2009chap13.Pdf Liverworts (Marchantiophyta) Niklas Wikströma,*, Xiaolan He-Nygrénb, and our understanding of phylogenetic relationships among A. Jonathan Shawc major lineages and the origin and divergence times of aDepartment of Systematic Botany, Evolutionary Biology Centre, those lineages. Norbyvägen 18D, Uppsala University, Norbyvägen 18D 75236, Altogether, liverworts (Phylum Marchantiophyta) b Uppsala, Sweden; Botanical Museum, Finnish Museum of Natural comprise an estimated 5000–8000 living species (8, 9). History, University of Helsinki, P.O. Box 7, 00014 Helsinki, Finland; Early and alternative classiA cations for these taxa have cDepartment of Biology, Duke University, Durham, NC 27708, USA *To whom correspondence should be addressed (niklas.wikstrom@ been numerous [reviewed by Schuster ( 10)], but the ebc.uu.se) arrangement of terminal taxa (species, genera) into lar- ger groups (e.g., families and orders) based on morpho- logical criteria alone began in the 1960s and 1970s with Abstract the work of Schuster (8, 10, 11) and Schljakov (12, 13), and culminated by the turn of the millenium with the work Liverworts (Phylum Marchantiophyta) include 5000–8000 of Crandall-Stotler and Stotler (14). 7 ree morphological species. Phylogenetic analyses divide liverworts into types of plant bodies (gametophytes) have generally been Haplomitriopsida, Marchantiopsida, and Jungerman- recognized and used in liverwort classiA cations: “com- niopsida. Complex thalloids are grouped with Blasiales in plex thalloids” including ~6% of extant species diversity Marchantiopsida, and leafy liverworts are grouped with and with a thalloid gametophyte that is organized into Metzgeriidae and Pelliidae in Jungermanniopsida. The distinct layers; “leafy liverworts”, by far the most speci- timetree shows an early Devonian (408 million years ago, ose group, including ~86% of extant species diversity and Ma) origin for extant liverworts. The complex thalloid habit with a gametophyte that is diB erentiated into stem and originated sometime in the Triassic (246–203 Ma). Both leafy leaves; and “simple thalloids” including ~8% of extant and epiphytic habits are indicated as old features, but ana- species diversity and with a more or less anatomically lyses also indicate possible extinctions during the Permian undiB erentiated thalloid gametophyte. and Triassic (299–200 Ma) and rapid family and genus-level divergences during the Cretaceous and early Cenozoic (145–50 Ma). 7 e evolution of land plants marks one of the most important events in earth history. Because of their lengthy and well-documented fossil record, the major patterns in early land plant evolution have mainly been interpreted using macrofossil evidence from the vascular plant lineage (1). Liverworts (Fig. 1), in contrast, have a limited fossil record, they are easily neglected due to their small size, and their role in early land plant evolution is rarely emphasized. Nevertheless, growing evidence (1–7) indicates an early split in land plant evolution between the liverworts and all other land plants. 7 is implies that liverworts occupy a critical position, and that they may help us understand the morphological and repro- ductive changes that favored the successful radiation Fig. 1 Leafy liverwort Schistochila aligera (Nees & Blume) of land plants and their adaptations to life in a terres- J.B. Jack & Stephani, Schistochilaceae, Jungermanniales. trial environment. Here we review recent progress in Credit: X. He-Nygrén. N. Wikström, X. He-Nygrén, and A. J. Shaw. Liverworts (Marchantiophyta). Pp. 146–152 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 114646 11/28/2009/28/2009 11:25:54:25:54 PPMM Eukaryota; Viridiplantae; Streptophyta; Marchantiophyta 147 Calypogeiaceae 28 Arnelliaceae Gymnomitriaceae 27 23 Jungermanniaceae-1 Jungermanniaceae-2 19 Jungermanniaceae-3 Balantiopsidaceae Acrobolbaceae Myliaceae Scapaniaceae 25 20 Cephaloziellaceae 12 16 Cephaloziaceae Adelanthaceae Jungermanniales Lophocoleaceae 26 Plagiochilaceae Herbertaceae 9 18 Jungermanniidae Lepicoleaceae 15 Lepidoziaceae Trichocoleaceae Pseudolepicoleaceae Schistochilaceae Jungermanniopsida Lejeuneaceae 6 22 17 Jubulaceae 13 Frullaniaceae Radulaceae Porellaceae Porellales Porellales Lepidolaenaceae 5 24 Goebeliellaceae Ptilidiaceae (continued on next page) D C P Tr J K Pg Ng PALEOZOIC MESOZOIC CZ 400 350 300 250 200 150 100 50 0 Million years ago Fig. 2 Continues Our understanding of liverwort evolution has (Fig. 2). Together these analyses indicate the pres- improved tremendously over the last 5–10 years, partly ence of three major groups (classes): Haplomitriopsida, through the rapid accumulation of molecular sequence Marchantiopsida, and Jungermanniopsida (15). As data. A series of large-scale and more A ne-scaled phylo- expected, they do not strictly correspond to the three genetic analyses (9, 15–24) have contributed to a robust types of gametophyte, and the presence of a more and well-supported hypothesis of liverwort relationships or less undiB erentiated simple thalloid gametophyte HHedges.indbedges.indb 114747 11/28/2009/28/2009 11:25:56:25:56 PPMM 148 THE TIMETREE OF LIFE (continued from previous page) Makinoaceae 21 Aneuraceae 14 4 7 Metzgeriaceae Pleuroziaceae Metzgeridae Pallaviciniaceae 10 Hymenophytaceae 2 Fossombroniaceae Jungermanniopsida Pelliidae Pelliidae Pelliaceae Marchantiales 1 11 Sphaerocarpales 8 Blasiales Treubiales Marchantiopsida 3 Haplomitriales D C P Tr J K Pg Ng Haplomitriopsida PALEOZOIC MESOZOIC CZ 400 350 300 250 200 150 100 50 0 Million years ago Fig. 2 A timetree of liverworts. Divergence times are shown in Table 1. Abbreviations: C (Carboniferous), CZ (Cenozoic), D (Devonian), J (Jurassic), K (Cretaceous), Ng (Neogene), P (Permian), Pg (Paleogene), and Tr (Triassic). Jungermanniaceae-1 includes Nardia scalaris and Jungermannia obovata; Jungermanniaceae-2 includes Jungermannia ovato-trigona and Leiocolea collaris; and Jungermanniaceae-3 includes Saccogyna viticulosa, Harpanthus fl otovianus, and Geocalyx graveolens in the original analyses by Heinrichs et al. (23). may be an ancestral feature for liverworts as a whole, markers, commonly used in the more inclusive analyses, although formal reconstructions of ancestral morpho- display too little variation to establish well-supported logical states have not been undertaken. 7 e ancestral relationships in this group (9). Some analyses place body plan is ambiguous because the Haplomtriopsida, Sphaerocarpales as the closest relative of all remaining which is well resolved as closest to Marchantiopsida and taxa (15, 16, 22, 23), and this is also reP ected in the clas- Jungermanniopsida, includes both leafy and more or siA cation by He-Nygrén et al. (16), who recognized two less thallose types. Haplomitriopsida, the least diverse orders in the complex thalloid clade, Sphaerocarpales group in terms of living taxa, includes only the three and Marchantiales. genera Haplomitrium, Treubia, and Apotreubia. 7 e Relationships within each of the three Jungermanni- Marchantiopsida include a monophyletic complex thal- opsida groups are better explored. A series of analyses loid clade that is closest to the Blasiales, which has a have included a comprehensive sample of the simple simple thalloid morphology. 7 e Jungermanniopsida, thalloid groups Pelliidae and Metzgeriidae (9, 20, 22). by far the most diverse group and possibly comprising Family-level relationships are comparatively well under- 86% of extant species diversity, includes three distinct stood in both of these groups, although some of this groups (subclasses): Pelliidae (including simple thal- knowledge has yet to be incorporated in a classiA catory loid taxa and the more or less leafy Fossombroniales), framework. Also the leafy group (Jungermanniidae) Metzgeriidae (including simple thalloid taxa but also the has been the focus of several analyses ( 15, 16, 18, 19, leafy Pleuroziales), and Jungermanniidae (including all 23). 7 ese consistently identify two major groups the leafy liverworts except Pleuroziales). Clearly, transi- (orders), Porellales and Jungermanniales, plus a smaller tions between thallose and leafy body types have hap- order, the Pitilidiales (containing Ptilidiaceae and pened multiple times. Neotrichocoleaceae), whose relationship to the two lar- With the exception of the analyses by Wheeler (24) and ger clades is currently unresolved. Some analyses place Boisselier-Dubayle et al. (17), there are no recent studies the Ptilidiales in Jungermanniales (9, 19), but others targeting the resolution of relationships among complex indicate a closer relationship with the Porellales (16, 18, thalloid taxa in Marchantiopsida. Standard molecular 23). 7 e Ptilidiales may also be closest to a clade that HHedges.indbedges.indb 114848 11/28/2009/28/2009 11:25:56:25:56 PPMM Eukaryota; Viridiplantae; Streptophyta; Marchantiophyta 149 Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among liverworts. Timetree Estimates Node Time Ref. (23)(a) Ref. (23)(b) Ref. (23)(c) Ref. (27) Time CI Time CI Time CI Time CI 1407.7407.7411–405– – – – – – 2 370.9 372.6 383–362 – – – – 369.2 403–338 3360.0––––––360.0396–316 4307.9328.5335–322– – – – 287.3331–262 5290.6308.7317–301– – – – 272.5310–243 6 265.1 – – 288.3 290–286 274.8 277–273 232.1 275–207 7 263.3 – – 269.9 272–268 256.6 259–255 – – 8245.7––––––245.7268–231 9 235.5 – – 240.5 251–230 230.5 240–221 – – 10 229.0 – – 235.3 269–202 222.7 252–194 – – 11 203.0 – – – – – – 203.0
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