Radiation and diversification within the LigulariaCremanthodiumParasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau

https://doi.org/10.1016/j.ympev.2005.09.010Get rights and content

Abstract

The Ligularia–Cremanthodium–Parasenecio (LCP) 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 relationships 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 different 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 Petasites diverged early as a separate lineage, while the remaining 11 genera comprise an expanded LCP complex clade. We suggest that the LCP clade, which is largely unresolved, most likely originated as a consequence of an explosive radiation. The few monophyletic subclades identified in the LCP 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 different parts of the phylogentic tree due to homoplasy of important morphological characters used to delimit them. Molecular-clock analyses suggest that the explosive radiation of the LCP 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 significant increases in geological and ecological diversity that accompanied such uplifting, most likely promoted rapid and continuous allopatric speciation in small and isolated populations, and allowed fixation or acquisition of similar morphological characters within unrelated lineages. This phenomenon, possibly combined with interspecific diploid hybridization because of secondary sympatry during relatively stable stages between different uplifts, could be a major cause of high species diversity in the Qinghai-Tibetan Plateau and adjacent areas of eastern Asia.

Introduction

A central goal of the study of biological diversity is to understand why different regions with similar environments contain different numbers of species (Qian and Ricklefs, 2000, Qian et al., 2005). Determining the causes of high biodiversity in some regions is of primary importance in biology and a principal aim of biogeographic research (Willis and Niklas, 2004, Willis and Whittaker, 2002). Molecular phylogenetic reconstructions of evolutionary relationships between living organisms are increasingly used to infer these putative causes of diversification within an historic and geographic context (Avise, 2000). Recent studies show that high numbers of plant species within regions might be due in part to bursts of speciation that occurred during the last few million years triggered by major geophysical and/or climate change (Richardson et al., 2001a, Richardson et al., 2001b), and that a significant proportion of plant diversity originated during the late Tertiary, i.e., since approximately 10 million years ago (Willis and Whittaker, 2002). However, the number of studies conducted on species rich floras remains low with most centered on groups in the Southern Hemisphere (Pennington et al., 2004). Several areas recognised as biodiversity hotspots in the Northern Hemisphere (Myers et al., 2000, Wilson, 1992), have yet to be subjected to detailed investigation. Here, we report the first molecular phylogenetic investigation of the history and evolution of a component of the flora of the Qinghai-Tibetan (Q-T) Plateau.

The Q-T Plateau is the highest and largest plateau in the world, having a mean elevation of ∼4.5 km and an area of 2.5 × 106 km2 (Zheng, 1996). The eastern part of this region and the adjacent area of southeast China has been listed as one of the world’s 25 or 34 biodiversity hotspots, based on species richness and greatest danger of anthropogenic extinction (Myers et al., 2000, Wilson, 1992; http://www.biodiversityhotspots.org/xp/Hotspots). The Q-T Plateau contains more than 12,000 species of plants in more than 1500 genera, and it is estimated that about 50 genera and more than 20% of the total species are endemic to this region (Wang et al., 1993, Wu and Wu, 1996). Although levels of plant diversity and endemism in this region are much less than those of the Cape flora (Linder, 2003) and tropical rainforests (Richardson et al., 2001a), the flora is more speciose than might be expected based on comparisons made at similar latitudes in the Northern Hemisphere (Wu and Wu, 1996). For example, the Q-T flora contributes to the high plant diversity in eastern Asia (Wang et al., 1993, Wu, 1988, Wu and Wu, 1996), which is roughly twice as rich as that of eastern North America, a region of similar area and climate (Qian et al., 2005). The high species richness of the flora of the Q-T Plateau and adjacent areas has been attributed to two major factors (Axelrod et al., 1996). One hypothesis is that an unbroken gradient of vegetation from tropical rain forest to boreal coniferous forests was maintained in the region and adjacent areas throughout the Quaternary when massive extinctions occurred elsewhere in the Northern Hemisphere. This therefore acted as a major refugium for organisms in the region during the period of marked climatic oscillation. The other scenario assumes that accelerated speciation occurred following the collision of the Indian subcontinent with Asia commencing about 40 Ma. Some ancient taxa, i.e., Trochodendraceae, Cecidiphyllaceae, Eucommiaceae, and several primitive genera found in the area, are monotypic or contain few species (Wang et al., 1993, Wu, 1988, Wu and Wu, 1996), indicating that the existence of Quaternary refugia might not have played an important part in generating great species richness despite having maintained some ancient groups.

The uplift of the Q-T Plateau began approximately 40 million years ago (Ma) (Chung et al., 1998) following the collision of India with Asia. Recent evidence indicates that the southern margin of the plateau reached its present elevation approximately 15 Ma (Spicer et al., 2003), if not earlier (22 Ma) (Guo et al., 2002), with the total plateau being uplifted to its present altitude by 7–8 Ma (Harrison et al., 1992) or more recently during the late Pliocene and early Pleistocene (Shi et al., 1998). These uplifts since the early Miocene have created high mountains and deep valleys within the plateau (Li et al., 1995), which could have accelerated the production of new species in allopatry, and been partly responsible for the high local and regional species richness. To investigate this possibility, we have conducted a phylogenetic analysis of the LigulariaCremanthodiumParasenecio complex (hereafter referred to as the LCP complex) and possible allies that comprise the subtribes Tussilagininae and Tephroseridinae of the tribe Senecioneae (Asteraceae). This group exhibits high species richness in the region and in adjacent eastern Asia (Liu, 2001, Liu, 2004).

Senecioneae, the largest tribe in the Asteraceae with ∼3200 species and ∼120 genera (Bremer, 1994), has been the subject of much debate with regard to its phylogenetic composition. Nordenstam (1977) recognized two subtribes: Blennospermatinae and Senecioninae, while Jeffrey and Chen (1984) divided the Senecioneae of eastern Asia into three subtribes: Senecioninae, Tussilagininae, and Tephroseridinae. Bremer (1994) incorporated the Tephroseridinae into Tussilagininae, and acknowledged Blennospermatinae and Senecioninae as additional subtribes. But this treatment was rejected by Chen (1999) who maintained the Tussilagininae and the Tephroseridinae as separate subtribes. The LCP complex of the Tussilagininae is composed of ∼120 species of Ligularia, ∼70 species of Cremanthodium, ∼60 species ofParasenecio plus six monotypic or small satellite genera, i.e., Farfugium, Syneilesis, Ligulariopsis, Sinacalia, Miricacalia, and Dendrocacalia (Chen, 1999, Jeffrey and Chen, 1984, Liu, 1989, Liu, 2001, Liu, 2004). Species of Ligularia occur in a great variety of habitats in the Q-T plateau region from forests to high alpine meadows, at elevations ranging from 1000 to 4000 m. Cremanthodium species occur in alpine meadow and scree areas at altitudes ranging from 2400 to 5600 m, while most species of Parasenecio are restricted to coniferous forests. More than 200 species in the complex are endemic to the Q-T Plateau (Liu, 2004) and comprise a typical group which exhibits great diversification in this region (Wu and Wu, 1996). Most endemics are restricted to small hills or valleys, and occur either allopatrically or occasionally sympatrically. These endemics are morphologically well defined and easily recognized in the field (Chen, 1999, Liu et al., 1994, Liu et al., 2002b). However, generic circumscriptions are extremely ambiguous, especially between members of Ligularia, Parasenecio, and Cremanthodium (Liu, 2001, Liu et al., 2001), due to a lack of diagnostic morphological traits (Liu, 2001, Liu, 2004). This may reflect possible bursts of recent speciation and random fixation of similar morphological features among unrelated lineages. Two small satellite genera, Ligulariopsis and Sinacalia, of the three large genera also occur mainly in the Q-T Plateau (Chen, 1999, Liu, 2001, Liu, 2004). Ligulariopsis, a monotypic genus, is distinguished from the three speciose genera in having a morphological combination of radiate capitula and none-vaginate leaf sheathing, while the latter genus comprising four species, differs by having a morphological combination of radiate capitula, none-vaginate leaf sheathing and tuberiform rhizomes (Chen, 1999, Jeffrey and Chen, 1984, Liu, 2001, Liu, 2004). The five genera comprising the core components of the LCP complex mainly distributed in the Q-T Plateau have similar morphology and their delimitation is unclear. Of the remaining four satellite genera, Farfugium and Syneilesis occur from central China to Japan, while Miricacalia, and Dendrocacalia are endemic to Japan. The relationships of the complex to other genera of the Tussilagininae of eastern Asia, i.e., Tussilago, Petasites, and Doronicum, and to genera of the Tephroseridinae, i.e., Sinosenecio, Tephroseris, Nemosenecio, are not well established. Both floral microcharacters and chromosomal data suggest that the LCP complex is more closely related to some species of three genera of the Tephroseridinae than to the remaining genera of the Tussilagininae (Liu, 2001, Liu, 2004).

Subtribal relationships in the Senecioneae remain poorly known despite the accumulation of molecular data for the group within recent years (e.g., Bain and Golden, 2000, Comes and Abbott, 2001, Fernandez et al., 2001, Pelser et al., 2002, Pelser et al., 2003). Blennospermatinae has been widely assumed to be the basal group of the Senecioneae (Bain and Golden, 2000, Bremer, 1994, Pelser et al., 2002); however, Swenson and Bremer (1999) found that Abrotanella, a genus of the Blennospermatinae, is only weakly (one step) associated with four sampled genera (Blennosperma, Syneilesis, Senecio, and Lopholaena) of the Senecioneae, casting doubt upon which genus is basal to the tribe. Doronicum has traditionally been placed in the Tussilagininae based on its cylindrical anther-collars and x = 30, suggesting a close relationship with the LCP complex (Bremer, 1994, Chen, 1999, Jeffrey and Chen, 1984). However, its “Helianthoid” pollen and small chromosomes indicate an aberrant position in this subtribe (Liu, 2001, Liu, 2004). Recently, Fernandez et al. (2001) placed it at the base of the sampled genera of the Senecioneae, sister to a clade containing Blennosperma, Lopholaena, Senecio, and Syneilesis (one genus of the LCP complex). These findings suggest that the traditionally circumscribed Asian Tussilagininae might not be monophyletic. However, except for these aberrant genera, other genera of Senecioneae that occur out of Asia have been shown to form two monophyletic clades: the Senecioninae group and the Tussilagininae group (Bain and Golden, 2000, Panero et al., 1999, Pelser et al., 2002, Pelser et al., 2003). Although not all non-Asiatic genera of Senecioneae have been examined, the available morphological traits indicate that most un-sampled genera fit well within the Senecioninae and Tussilagininae groups (Jeffrey, 1992). Most genera of Senecioneae whose phylogenetic position is unresolved occur in eastern Asia, within two subtribes: the Tussilagininae and the Tephroseridinae (Chen, 1999, Jeffrey, 1992, Liu, 2001). Therefore, our sampling strategy focused on the LCP complex, but extended to cover the most representative genera of the Tussilagininae, the Tephroseridinae and a few of the Senecioninae in eastern Asia.

Following a survey of newly sequenced chloroplast and nuclear DNA data of representative species of the LCP complex and related genera of the Senecioneae, we aimed to (1) evaluate the relationship of the LCP complex to the Tephroseridinae, and to refine its circumscription in eastern Asia; (2) examine the generic delimitation of the complex against the previous classification based on morphological characters; and (3) determine underlying causes of the radiation and diversification within the LCP complex, which might be correlated with past geological changes in the Q-T plateau.

Section snippets

Sampling strategy, plant materials, and datasets

Our sample of species within the LCP complex included 20 species representing eight of the nine sections in Ligularia and Cremanthodium, five species representing three of five sections in Parasenecio, and eight species representing the satellite genera: Sinacalia, Ligulariopsis, Farfugium, Syneilesis, Miricacalia, and Dendrocacalia from eastern Asia (Fig. 1). We further sampled four species representing the other three genera of Tussilagininae: Doronicum, Tussilago, and Petasite. Only the

Phylogenetic analyses of ndhF dataset

The ndhF sequence dataset analyzed comprised 52 species of the Senecioneae, representing all recognized subtribes, and 12 species representing eight additional tribes of Asteraceae. The aligned dataset contained 2131 sites of which 276 were variable but phylogenetically uninformative, and 191 that were variable and informative (gaps excluded). Five indels (one of 3-bp, another of 9-bp, and the remainder of 6-bp) were restricted to single species, and therefore yielded no phylogenetic

Discussion

A localized lack of phylogenetic signal and poorly resolved phylogenetic relationships has been interpreted as a signature of explosive speciation or rapid radiation in some floras (see Baldwin and Sanderson, 1998, Richardson et al., 2001a, Richardson et al., 2001b, Verboom et al., 2003). Our investigation into the evolution of a morphologically diverse group of species of Ligularia, Cremanthodium, Parasenecio and closely related taxa, most of which are endemic to the Q-T Plateau, revealed that

Conclusions

Several molecular phylogenetic studies conducted on species-rich plant groups that occur in biodiversity hotspots have now yielded similar findings with regard to species diversity being the product of recent bursts of speciation triggered most likely by geophysical and/or climatic changes within these regions since the middle Miocene (Richardson et al., 2001a). In the Neotropics, however, it has been argued that a mixture of both ancient and recent diversification should be involved to explain

Acknowledgments

We are grateful to Dr. Stephen Harris for his constructive comments on an earlier version of this paper. We thank Profs. Chen Zhiduan, Lu Anmin, Liu Shangwu, Ho Tingnong, Lu Xuefeng, Shuichi Norshiro, Richard Milne, and George Miehe for their help in collecting materials in the fields, sequencing and analysis, and fruitful discussions during the past 10 years. Support for this research was provided by Key Innovation Plan KSCX-SW-106, Special Fund of Outstanding Ph.D. Dissertation, FANEDD 200327

References (85)

  • R.J. Abbott

    Evolution. Sex, sunflowers, and speciation

    Science

    (2003)
  • Z.S. An et al.

    Evolution of Asian monsoons and phased uplift of the Himalayan-Tibetan Plateau since late Miocene times

    Nature

    (2001)
  • B.S. Arbogast et al.

    Estimating divergence times from molecular data on phylogenetic and population genetic timescales

    Ann. Rev. Ecol. Sys.

    (2002)
  • J.C. Avise

    Phylogeography: The History and Formation of Species

    (2000)
  • D.I. Axelrod et al.

    History of the modern flora of China

  • B.G. Baldwin et al.

    Age and rate of diversification of the Hawaiian silversword alliance (Compositae)

    Proc. Natl. Acad. Sci. USA

    (1998)
  • R.J. Bayer et al.

    Tribal phylogeny of the Asteraceae based on two non-coding chloroplast sequences, the trnL intron and trnL/trnF intergenic spacer

    Ann. Mol. Bot. Gard.

    (1998)
  • R.J. Bayer et al.

    Phylogeny of South African Gnaphalieae (Asteraceae) based on two non-coding chloroplast sequences

    Am. J. Bot.

    (2000)
  • K. Bremer

    Asteraceae, Cladistics and Classification

    (1994)
  • L. Bromham et al.

    The modern molecular clock

    Nat. Rev. Genet.

    (2003)
  • Y.L. Chen

    Compositae-Senecioneae. Flora Reipublicae Popularis Sinicae

    (1999)
  • H.P. Comes et al.

    Molecular phylogeography, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae)

    Evolution

    (2001)
  • S.L. Chung et al.

    Diachronomous uplift of the Tibetan plateau starting 40 Myr ago

    Nature

    (1998)
  • J.J. Doyle et al.

    A rapid DNA isolation procedure for small quantities of fresh leaf materials

    Phytochem. Bull.

    (1987)
  • J.S. Farris et al.

    Testing significance of incongruence

    Cladistics

    (1995)
  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • J. Francisco-Ortega et al.

    Molecular evidence for a Mediterranean origin of the Macaronesian endemic genus Argyranthemum (Asteraceae)

    Am. J. Bot.

    (1997)
  • J. Francisco-Ortega et al.

    Origin and evolution of the endemic genera of Gonosperminae (Asteraceae: Anthemideae) from the Canary Islands: evidence from nucleotide sequences of the internal transcribed spacers of the nuclear ribosomal DNA

    Am. J. Bot.

    (2001)
  • Z.T. Guo et al.

    Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China

    Nature

    (2002)
  • T.M. Harrison et al.

    Raising Tibet

    Science

    (1992)
  • M.A. Hershkovitz et al.

    Ribosomal DNA sequences and angiosperm systematics

  • J.P. Huelsenbeck et al.

    MTBAYES: Bayesian inference of phylogeny

    Bioinformatics

    (2001)
  • C. Jeffrey et al.

    Taxonomic studies on the tribe Senecioneae (Compositae) of eastern Asia

    Kew Bull.

    (1984)
  • C. Jeffrey

    The tribe Senecioneae (Compositae) in the Mascarene Islands with an annotated world check-list of the genera of the tribe

    Notes on Compositae VI. Kew Bull.

    (1992)
  • H.G. Kim et al.

    Molecular evidence for an African origin of the Hawaiian endemic Hesperomannia (Asteraceae)

    Proc. Natl. Acad. Sci. USA

    (1998)
  • K.J. Kim et al.

    ndhF sequence evolution and the major clades in the sunflower family

    Proc. Natl. Acad. Sci. USA

    (1995)
  • J.J. Li et al.

    Uplift of the Qinghai-Xizang (Tibet) Plateau and Global Change

    (1995)
  • W.H. Li

    Molecular Evolution

    (1997)
  • K.F. Liem

    Key evolutionary innovations, differential diversity, and symecomorphosis

  • H.P. Linder

    The radiation of the Cape flora, southern Africa

    Biol. Rev.

    (2003)
  • J.Q. Liu

    Floral microcharacters of the subtribe Tussilagininae (Asteraceae: Senecioneae) of eastern Asia and their systematic and taxonomic significance

    Bull. Bot. Res.

    (2001)
  • J.Q. Liu

    Uniformity of karyotypes in Ligularia (Asteraceae: Senecioneae), a highly diversified genus of the eastern Qinghai-Tibet Plateau highlands and adjacent areas

    Bot. J. Linn. Soc.

    (2004)
  • Cited by (0)

    View full text