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Radiation and Diversification Within the Ligularia–Cremanthodium

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Radiation and Diversification Within the Ligularia–Cremanthodium Molecular Phylogenetics and Evolution 38 (2006) 31–49 www.elsevier.com/locate/ympev Radiation and diversiWcation within the Ligularia–Cremanthodium– Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau Jian-Quan Liu a,b,¤, Yu-Jing Wang a, Ai-Lan Wang a, Ohba Hideaki c, Richard J. Abbott d a Qinghai-Tibetan Plateau Biological Evolution and Adaptation Laboratory, Northwest Plateau Institute of Biology, Chinese Academy of Sciences, Xining 810001, Qinghai, China b Key Laboratory of Arid and Grassland Ecology, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China c University Museum, University of Tokyo, Hongo 7-3-1, Tokyo 113-0033, Japan d School of Biology, Mitchell Building, University of St. Andrews, St. Andrews, Fife KY16 9TH, UK Received 3 March 2005; revised 3 September 2005; accepted 7 September 2005 Available online 14 November 2005 Abstract The Ligularia–Cremanthodium–Parasenecio (L–C–P) complex of the Tussilagininae (Asteraceae: Senecioneae) contains more than 200 species that are endemic to the Qinghai-Tibetan Plateau in eastern Asia. These species are morphologically distinct; however, their relation- ships appear complex. A phylogenetic analysis of members of the complex and selected taxa of the tribe Senecioneae was conducted using chloroplast (ndhF and trnL-F) and nuclear (ITS) sequences. Phylogenetic trees were constructed from individual and combined datasets of the three diVerent sequences. All analyses suggested that Doronicum, a genus that has been included in the Tussilagininae, should be excluded from this subtribe and placed at the base of the tribe Senecioneae. In addition, the Tussilagininae should be broadly circumscribed to include the Tephroseridinae. Within the expanded Tussilagininae containing all 13 genera occurring in eastern Asia, Tussilago and NSPetasites diverged early as a separate lineage, while the remaining 11 genera comprise an expanded L–C–P complex clade. We suggest that the L–C–P clade, which is largely unresolved, most likely originated as a consequence of an explosive radiation. The few monophyletic subclades identiWed in the L–C–P clade with robust support further suggest that some genera of Tussilagininae from eastern Asia require generic re-circumscriptions given the occurrence of subclades containing species of the same genus in diVerent parts of the phylogentic tree due to homoplasy of important morphological characters used to delimit them. Molecular-clock analyses suggest that the explosive radia- tion of the L–C–P complex occurred mostly within the last 20 million years, which falls well within the period of recent major uplifts of the Qinghai-Tibetan Plateau between the early Miocene to the Pleistocene. It is proposed that signiWcant increases in geological and ecological diversity that accompanied such uplifting, most likely promoted rapid and continuous allopatric speciation in small and isolated popula- tions, and allowed Wxation or acquisition of similar morphological characters within unrelated lineages. This phenomenon, possibly com- bined with interspeciWc diploid hybridization because of secondary sympatry during relatively stable stages between diVerent uplifts, could be a major cause of high species diversity in the Qinghai-Tibetan Plateau and adjacent areas of eastern Asia. 2005 Elsevier Inc. All rights reserved. Keywords: Radiation; DiversiWcation; Qinghai-Tibetan Plateau; Molecular systematics; Senecioneae; Tussilagininae; Eastern Asia 1. Introduction contain diVerent numbers of species (Qian and Ricklefs, 2000; Qian et al., 2005). Determining the causes of high bio- A central goal of the study of biological diversity is to diversity in some regions is of primary importance in biol- understand why diVerent regions with similar environments ogy and a principal aim of biogeographic research (Willis * Corresponding author. Fax: +86 971 6143282. and Niklas, 2004; Willis and Whittaker, 2002). Molecular E-mail addresses: [email protected], [email protected] phylogenetic reconstructions of evolutionary relationships (J.-Q. Liu). between living organisms are increasingly used to infer 1055-7903/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2005.09.010 32 J.-Q. Liu et al. / Molecular Phylogenetics and Evolution 38 (2006) 31–49 these putative causes of diversiWcation within an historic The uplift of the Q-T Plateau began approximately 40 and geographic context (Avise, 2000). Recent studies show million years ago (Ma) (Chung et al., 1998) following the that high numbers of plant species within regions might be collision of India with Asia. Recent evidence indicates that due in part to bursts of speciation that occurred during the the southern margin of the plateau reached its present ele- last few million years triggered by major geophysical and/ vation approximately 15 Ma (Spicer et al., 2003), if not ear- or climate change (Richardson et al., 2001a,b), and that a lier (22 Ma) (Guo et al., 2002), with the total plateau being signiWcant proportion of plant diversity originated during uplifted to its present altitude by 7–8 Ma (Harrison et al., the late Tertiary, i.e., since approximately 10 million years 1992) or more recently during the late Pliocene and early ago (Willis and Whittaker, 2002). However, the number of Pleistocene (Shi et al., 1998). These uplifts since the early studies conducted on species rich Xoras remains low with Miocene have created high mountains and deep valleys most centered on groups in the Southern Hemisphere (Pen- within the plateau (Li et al., 1995), which could have accel- nington et al., 2004). Several areas recognised as biodiver- erated the production of new species in allopatry, and been sity hotspots in the Northern Hemisphere (Myers et al., partly responsible for the high local and regional species 2000; Wilson, 1992), have yet to be subjected to detailed richness. To investigate this possibility, we have conducted investigation. Here, we report the Wrst molecular phyloge- a phylogenetic analysis of the Ligularia–Cremanthodium– netic investigation of the history and evolution of a compo- Parasenecio complex (hereafter referred to as the L–C–P nent of the Xora of the Qinghai-Tibetan (Q-T) Plateau. complex) and possible allies that comprise the subtribes The Q-T Plateau is the highest and largest plateau in the Tussilagininae and Tephroseridinae of the tribe Senecio- world, having a mean elevation of »4.5 km and an area of neae (Asteraceae). This group exhibits high species richness 2.5 £ 106 km2 (Zheng, 1996). The eastern part of this region in the region and in adjacent eastern Asia (Liu, 2001, 2004). and the adjacent area of southeast China has been listed as Senecioneae, the largest tribe in the Asteraceae with one of the world’s 25 or 34 biodiversity hotspots, based on »3200 species and »120 genera (Bremer, 1994), has been species richness and greatest danger of anthropogenic the subject of much debate with regard to its phylogenetic extinction (Myers et al., 2000; Wilson, 1992; http:// composition. Nordenstam (1977) recognized two subtribes: www.biodiversityhotspots.org/xp/Hotspots). The Q-T Pla- Blennospermatinae and Senecioninae, while JeVrey and teau contains more than 12,000 species of plants in more Chen (1984) divided the Senecioneae of eastern Asia than 1500 genera, and it is estimated that about 50 genera into three subtribes: Senecioninae, Tussilagininae, and and more than 20% of the total species are endemic to this Tephroseridinae. Bremer (1994) incorporated the Teph- region (Wang et al., 1993; Wu and Wu, 1996). Although roseridinae into Tussilagininae, and acknowledged Blenno- levels of plant diversity and endemism in this region are spermatinae and Senecioninae as additional subtribes. But much less than those of the Cape Xora (Linder, 2003) and this treatment was rejected by Chen (1999) who maintained tropical rainforests (Richardson et al., 2001a), the Xora is the Tussilagininae and the Tephroseridinae as separate sub- more speciose than might be expected based on compari- tribes. The L–C–P complex of the Tussilagininae is com- sons made at similar latitudes in the Northern Hemisphere posed of »120 species of Ligularia, »70 species of (Wu and Wu, 1996). For example, the Q-T Xora contributes Cremanthodium, »60 species ofParasenecio plus six mono- to the high plant diversity in eastern Asia (Wang et al., typic or small satellite genera, i.e., Farfugium, Syneilesis, 1993; Wu, 1988; Wu and Wu, 1996), which is roughly twice Ligulariopsis, Sinacalia, Miricacalia, and Dendrocacalia as rich as that of eastern North America, a region of similar (Chen, 1999; JeVrey and Chen, 1984; Liu, 1989, 2001, 2004). area and climate (Qian et al., 2005). The high species rich- Species of Ligularia occur in a great variety of habitats in ness of the Xora of the Q-T Plateau and adjacent areas has the Q-T plateau region from forests to high alpine mead- been attributed to two major factors (Axelrod et al., 1996). ows, at elevations ranging from 1000 to 4000 m. Cremantho- One hypothesis is that an unbroken gradient of vegetation dium species occur in alpine meadow and scree areas at from tropical rain forest to boreal coniferous forests was altitudes ranging from 2400 to 5600 m, while most species maintained in the region and adjacent areas throughout the of Parasenecio are restricted to coniferous forests. More Quaternary when massive extinctions occurred elsewhere in than 200 species in the complex are endemic to the Q-T Pla- the Northern Hemisphere. This therefore acted as a major teau (Liu, 2004) and comprise a typical group which exhib- refugium for organisms in the region during the period of its great diversiWcation in this region (Wu and Wu, 1996). marked climatic oscillation. The other scenario assumes Most endemics are restricted to small hills or valleys, and that accelerated speciation occurred following the collision occur either allopatrically or occasionally sympatrically. of the Indian subcontinent with Asia commencing about These endemics are morphologically well deWned and easily 40 Ma. Some ancient taxa, i.e., Trochodendraceae, Cecidi- recognized in the Weld (Chen, 1999; Liu et al., 1994, 2002b).
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