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High Mountain Origin, Phylogenetics, Evolution, and Niche Conservatism of Arctic Lineages in the Hemiparasitic Genus Pedicularis (Orobanchaceae)

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High Mountain Origin, Phylogenetics, Evolution, and Niche Conservatism of Arctic Lineages in the Hemiparasitic Genus Pedicularis (Orobanchaceae) Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2014 High mountain origin, phylogenetics, evolution, and niche conservatism of arctic lineages in the hemiparasitic genus Pedicularis (Orobanchaceae) Tkach, Natalia ; Ree, Richard H ; Kuss, Patrick ; Röser, Martin ; Hoffmann, Matthias H Abstract: The origin of the arctic flora covering the northernmost treeless areas is still poorly understood. Arctic plants may have evolved in situ or immigrated from the adjacent ecosystems. Frequently arctic species have disjunctive distributions between the Arctic and high mountain systems of the temperate zone. This pattern may result from long distance dispersal or from glacial plant migrations and extinctions of intermediate populations. The hemiparasitic genus Pedicularis is represented in the Arctic by c. 28 taxa and ranks among the six most species-rich vascular plant genera of this region. In this study, we test the hypothesis that these lineages evolved from predecessors occurring in northern temperate mountain ranges, many of which are current centers of diversity for the genus. We generated a nuclear ribosomal and chloroplast DNA phylogeny including almost all of the arctic taxa and nearly half of the genus as a whole. The arctic taxa of Pedicularis evolved 12-14 times independently and are mostly nested in lineages that otherwise occur in the high mountains of Eurasia and North America. It appears that only three arctic lineages arose from the present-day center of diversity of the genus, in the Hengduan Mountains and Himalayas. Two lineages are probably of lowland origin. Arctic taxa of Pedicularis show considerable niche conservatism with respect to soil moisture and grow predominantly in moist to wet soils. The studied characteristics of ecology, morphology, and chromosome numbers of arctic Pedicularis show a heterogeneous pattern of evolution. The directions of morphological changes among the arctic lineages show opposing trends. Arctic taxa are chiefly diploid, the few tetraploid chromosome numbers of the genus were recorded only for arctic taxa. Five arctic Pedicularis are annuals or biennials, life forms otherwise rare in the Arctic. Other genera of the Orobanchaceae consist also of an elevated number of short-lived species, thus hemiparasitism may favor this life form in the Arctic. DOI: https://doi.org/10.1016/j.ympev.2014.03.004 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-94778 Journal Article Accepted Version Originally published at: Tkach, Natalia; Ree, Richard H; Kuss, Patrick; Röser, Martin; Hoffmann, Matthias H (2014). High mountain origin, phylogenetics, evolution, and niche conservatism of arctic lineages in the hemiparasitic genus Pedicularis (Orobanchaceae). Molecular Phylogenetics and Evolution, 76:75-92. DOI: https://doi.org/10.1016/j.ympev.2014.03.004 Molecular Phylogenetics and Evolution 76 (2014) 75–92 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev High mountain origin, phylogenetics, evolution, and niche conservatism of arctic lineages in the hemiparasitic genus Pedicularis (Orobanchaceae) ⇑ Natalia Tkach a, Richard H. Ree b, Patrick Kuss c, Martin Röser a, Matthias H. Hoffmann a, a Martin Luther University Halle-Wittenberg, Institute of Biology, Geobotany and Botanical Garden, Neuwerk 21, 06108 Halle, Germany b Department of Botany, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA c Institute of Systematic Botany, Zollikerstrasse 107, 8008 Zurich, Switzerland article info abstract Article history: The origin of the arctic flora covering the northernmost treeless areas is still poorly understood. Arctic Received 23 May 2013 plants may have evolved in situ or immigrated from the adjacent ecosystems. Frequently arctic species Revised 25 February 2014 have disjunctive distributions between the Arctic and high mountain systems of the temperate zone. This Accepted 3 March 2014 pattern may result from long distance dispersal or from glacial plant migrations and extinctions of Available online 12 March 2014 intermediate populations. The hemiparasitic genus Pedicularis is represented in the Arctic by c. 28 taxa and ranks among the six most species-rich vascular plant genera of this region. In this study, we test Keywords: the hypothesis that these lineages evolved from predecessors occurring in northern temperate mountain Pedicularis ranges, many of which are current centers of diversity for the genus. We generated a nuclear ribosomal Arctic Biogeography and chloroplast DNA phylogeny including almost all of the arctic taxa and nearly half of the genus as a Ecology whole. The arctic taxa of Pedicularis evolved 12–14 times independently and are mostly nested in lineages Niche conservatism that otherwise occur in the high mountains of Eurasia and North America. It appears that only three arctic Phylogeny lineages arose from the present-day center of diversity of the genus, in the Hengduan Mountains and Himalayas. Two lineages are probably of lowland origin. Arctic taxa of Pedicularis show considerable niche conservatism with respect to soil moisture and grow predominantly in moist to wet soils. The studied characteristics of ecology, morphology, and chromosome numbers of arctic Pedicularis show a heterogeneous pattern of evolution. The directions of morphological changes among the arctic lineages show opposing trends. Arctic taxa are chiefly diploid, the few tetraploid chromosome numbers of the genus were recorded only for arctic taxa. Five arctic Pedicularis are annuals or biennials, life forms otherwise rare in the Arctic. Other genera of the Orobanchaceae consist also of an elevated number of short-lived species, thus hemiparasitism may favor this life form in the Arctic. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction thus of nature protection concern. Altogether, c. 2800 vascular plant species and subspecies presently occur in the Arctic, and The Arctic is a large, but young biome, of which major parts are considered ‘‘arctic’’ species if their whole (arctic endemics) or were repeatedly devastated by Pleistocene glaciations. It provides only a part of their ranges are situated in the arctic biome an excellent setting for studying, for example, range shifts, specia- (Fig. 1; Panarctic Flora, Elven et al., 2011). The now treeless and tion and polyploidy. It is of interest to the study of plant evolution cold region of the Arctic (Fig. 1) was covered during much of the because its extreme environmental conditions require responses Tertiary with deciduous and coniferous forests (e.g., Mai, 1995; like adaptation to seasonality, and freezing and desiccation toler- Murray, 1995). In the late Tertiary and the ice ages of the Quater- ance. Furthermore, this area is strongly affected by global change, nary, cooling and the retreat of the forests created new habitats available for colonisation by plants, especially herbaceous lineages ⇑ Corresponding author. Address: Martin Luther University Halle-Wittenberg, that were able to tolerate or adapt to the harsh environmental con- Institute of Biology, Geobotany and Botanical Garden, Am Kirchtor 3, 06108 Halle, dition. Evidence of early arctic vegetation composition based on Germany. fossil deposits is confined to a rather limited number of taxa E-mail addresses: [email protected] (N. Tkach), rree@ (e.g., Cerastium, Draba, Dryas, Ranunculus, Saxifraga, Silene, Stellaria; fieldmuseum.org (R.H. Ree), [email protected] (P. Kuss), martin.roeser@ Bennike and Bøcher, 1990; Bennike et al., 2010; Matthews and botanik.uni-halle.de (M. Röser), [email protected] (M.H. Hoffmann). Ovenden, 1990). Floristic analyses have suggested that the present http://dx.doi.org/10.1016/j.ympev.2014.03.004 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. 76 N. Tkach et al. / Molecular Phylogenetics and Evolution 76 (2014) 75–92 GREENLAND ALASKA NORTHERN EAST ASIA (Chukotka, SIBERIA Kamchatka) NORTH AMERICA (Canada, USA - excluding Alaska ) EUROPE EAST ASIA SOUTHERN SIBERIA (Altai), (Russian MONGOLIA Far East, Korea, Japan) CENTRAL ASIA (Turkmenistan, Uzbekistan, C Kazakhstan, Kyrgystan) TS Arctic border (tree line) CHINA Polar circle H Distribution regions High mountains ranges C Caucasus TS Tian-Shan H Himalaya Fig. 1. Delineation of the Arctic following the Panarctic Flora (Elven et al., 2011) and geographical regions outside of the arctic region that are used in this study to circumscribe the southerly distribution of Pedicularis taxa. The selection of these arbitrary geographical regions follows the availability of distribution data in various sources explored for this study (see Section 2 for details). arctic flora originated from different sources, including autochtho- studied in a species-level phylogenetic context despite the occur- nous elements of the Arcto-Tertiary vegetation that evolved in situ rences of frequent arctic–alpine disjunctions. by adapting to the increasingly cold climate, Quaternary migrants Here we concentrate on the hemiparasitic genus Pedicularis L. from adjacent forests and saline coastal habitats that may have (Orobanchaceae), which includes as many as 800 described species been pre-adapted to arctic conditions and migrants from more re- (Mill, 2001). It is distributed primarily in colder regions throughout mote southern mountains (Tolmachev, 1960, for example,
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