Table of Contents

09 May 2014, Volume 52 Issue 3
Cover illustration: Representative alpine plants from the Qinghai-Tibet Plateau. Top left, Spenceria ramalana Trim. (Rosaceae). Top right, Pomatosace filicula Maxim. (Primulaceae). Bottom left, Cyananthus formosus Diel. (Campanulaceae). Bottom right, Allium wallichii Kunth (Amaryllidaceae). Studies on phylogeography, cytology, and intraspecifi c differentiation of these plants are included in this special issue. Photographed by Hang SUN (top left), Bo XU (top right), and Yang NIU (bottom [Detail] ...
  • Jian-Quan LIU, Yuan-Wen DUAN, Gang HAO, Xue-Jun GE, Hang SUN
    J Syst Evol. 2014, 52(3): 241-249.
    As the highest and largest plateau in the world, the Qinghai–Tibet Plateau, with its numerous endemic species, is one of the important alpine biodiversity hotspots. Only recently have the evolutionary histories and underlying adaptations of these alpine plants become clear, through research mostly based on testable experiments and analyses. In this issue, we collected a total of 13 papers related to such aims. In addition, we selected a few published papers to highlight the major findings in the recent past. We also outlined the outlook and direction of future research.
  • Research Articles
  • Zhi-Qiang LU, Bin TIAN, Bing-Bing LIU, Chen YANG, Jian-Quan LIU
    J Syst Evol. 2014, 52(3): 250-259.
    It remains unknown how Ostryopsis intermedia B. Tian & J. Q. Liu (Betulaceae) originated in the SE Qinghai–Tibet Plateau (QTP). We examined sequence variations of two maternally inherited chloroplast (cp) DNA fragments and amplified fragment length polymorphisms (AFLP) of 32 populations for this species and two congeners, O. davidiana Decne. and O. nobilis Balf. f. W. W. Sm., distributed in northern China and the SE QTP. Each of the two distinct cpDNA haplotype groups was fixed by O. davidiana or O. intermedia, respectively, whereas both were found in O. nobilis. All analyses of AFLP suggested that O. intermedia is more closely related to O. davidiana than to O. nobilis and Bayesian clustering analysis (K = 2) further suggested that the genomic composition of O. intermedia showed a slightly mosaic origin from the other two species, although mostly from O. davidiana. Analyses of AFLP indicated the highest nuclear genetic diversity for O. davidiana and lowest forO. intermedia. The origin of O. intermedia through hybrid speciation due to southward migration of O. davidiana and the following hybridization with O. nobilis may provide the most reasonable explanation for the inconsistency between phylogenetic relationships of three species and degrees of genetic diversity from cpDNA sequences or AFLP datasets. Ostryopsis intermedia may represent one more diploid hybrid species found in the QTP, although further strong tests are needed based on additional data.
  • Guang-Fu CHEN, Wen-Guang SUN, De-Yuan HONG, Zhuo ZHOU, Yang NIU,Ze-Long NIE, Hang SUN, Jian-Wen ZHANG, Zhi-Min LI
    J Syst Evol. 2014, 52(3): 260-270.
    Chromosome numbers and the morphology of members of 24 populations representing 15 species of the Sino-Himalayan endemic genus Cyananthus(Campanulaceae) were studied using karyological and numerical taxonomic techniques. The chromosome numbers of these taxa are 2n = 10, 12, 14, 24, 28, and the basic chromosome numbers for the genus are x = 5, 6, 7. All species except C. inflatus Hook. f. & Thoms. and C. microphyllus Edgew. were examined for the first time and a new ploidy level (tetraploidy) is reported in the genus. Chromosome measurement data were analyzed using cluster analysis. The relationships between three sections within Cyananthus and evolutionary trends within the genus are discussed in the light of karyological data. The cytological data suggest that Cyananthus is a relatively primitive genus in Campanulaceae and there is significant division within the genus, and polyploidization may have played an important role in the chromosome evolution and speciation of Cyananthus in the Himalayan–Hengduan Mountains.
  • Bo XU, Zhi-Min LI, Hang SUN
    J Syst Evol. 2014, 52(3): 271-279.
    There have been few studies of the alpine subnival belt flora in the Hengduan Mountains (HM), which host remarkable biodiversity. To extend knowledge of this flora, we examined published florae, herbarium specimens, and field observations (and material) collected by both ourselves and others. In total, 942 seed plant species have been recorded in the belt, representing 168 genera and 48 families. Twenty-four large families (with ≥10 species) are present, represented by 873 species (92.68% of the total). These include Asteraceae, Saxifragaceae, and Brassicaceae (146, 82, and 71 species, respectively). There are also 27 large genera (represented by ≥10 species), collectively contributing 587 species (62.31%) to the flora, including Saxifraga, Corydalis, and Saussurea (75, 55, and 49 species, respectively). Areal elements represented by the highest numbers of genera are the North temperate, Sino-Himalaya, and Old World temperate elements (39.88%, 14.29%, and 12.50%, respectively), while the Hengduan Mountains, Sino-Himalaya, and Qinghai-Tibetan Plateau elements are most species-rich (355, 281, and 161 species, respectively), collectively accounting for 84.61% species of the known flora. Of these, 295 species (31.32%) are endemic to the Sino-Himalayan alpine subnival belt and 151 (16.03%) strictly endemic to the alpine subnival belt of the HM. These findings indicate that the flora is young, strongly differentiated, probably developed as a result of the plateau's uplift, and speciation has been accelerated by the harsh environment and strong heterogeneity of niches.
  • Xin-Hui LI, Xin-Xin ZHU, Yang NIU, Hang SUN
    J Syst Evol. 2014, 52(3): 280-288.
    To better understand the elevational pattern of phylogenetic structure shown by alpine taxa and the underlying causes, we analyzed the phylogenetic structure of each elevational belt of alpine plants in the Hengduan Mountains Region, measured by net related index (NRI) and net nearest taxon index (NTI). We found both the indices of phylogenetic diversity indicated that alpine plants tended to show phylogenetic overdispersion at low elevational belts, implying that the distribution of alpine plants in these belts was mainly determined by interspecific competition. Alpine plants at higher elevational belts tended to phylogenetic clustering indicated by NRI, and NTIrevealed phylogenetic clustering at the belts between 4300 m and 5500 m, which presumably suggested environment filtering and rapid speciation. Above 5500 m,NTI indicated that the phylogenetic structure became random again, perhaps due to the low intensity of filtering and the large distances between plants at the top of the scree slopes. We concluded that phylogenetic structure was, indeed, influenced by the environmental filter, interspecies interaction, rapid speciation during the uplift of the Qinghai–Tibet Plateau, and distance between plants.
  • Gai-Ni WANG, Xin-Yu HE, Georg MIEHE, Kang-Shan MAO
    J Syst Evol. 2014, 52(3): 289-302.
    In order to trace the response of alpine plants on the Qinghai–Tibet Plateau (QTP) to the Quaternary climate oscillations, the phylogeographic history of Pomatosace filicula Maxim. was investigated in the present study. Based on sequence variations of two maternally inherited plastid markers, matK and trnH-psbA, and the biparentally inherited nuclear ribosomal internal transcribed spacer (nrITS), we estimated the population genetic structure, lineage divergence timescale, and population dynamics of P. filicula. Seven plastid haplotypes and two nrITS genotypes were identified across the range-wide sampling of 200 individuals from 24 populations. Although AMOVA revealed a high level of differentiation among populations (FST = 0.560), no significant phylogeographic structure was detected (NST = 0.503, GST = 0.518, P > 0.05). Molecular dating suggested that the divergences between major plastid lineages and nrITS genotypes occurred during the early and middle Pleistocene, and the middle Pleistocene, respectively. This species most likely survived at multiple unglaciated sites on the QTP during the Last Glacial Maximum, with most of these sites located above 4000 m a.s.l. The species probably experienced range expansion at its distribution fringe, but demographic tests did not suggest significant population size changes. We proposed that pronounced effective gene flow (Nem = 0.393) and short generation time may have obscured the phylogeographic and demographic patterns of this species. Our findings will shed new light on the Quaternary evolutionary history of the alpine flora of the QTP.
  • Yi-Xuan KOU, Yu-Xia WU, Yu-Jin WANG, Dong-Rui JIA, Zhong-Hu LI
    J Syst Evol. 2014, 52(3): 303-312.
    Plant species shift ranges in response to climate fluctuation over time. However, differentiation related to heterogeneity in space has been illustrated only rarely. Here we selected Hippophaë neurocarpa S. W. Liu & T. N. Ho (Elaeagnaceae), a shrub endemic to the Qinghai–Tibet Plateau, to exemplify this process. We characterized the genotypic, phenotypic, and climatic variations among 27 populations of this species sampled across its entire distribution. Genotype analyses revealed six highly differentiated groups that may have resulted from expansions in spatial range. Despite recent fluctuation in size, it is likely that most groups survived the last glacial maximum in situ. Instead of two previously described subspecies, we identified four morphotypes (stellate, peltate, and two additional types) that can be characterized based on leaf trichomes. This phenotypic subdivision is consistent with a climate gradient defined by temperature and precipitation, although similar phenotypes may derive from distinct genotypes. Collectively, we propose that the demographic history of H. neurocarpa is characteristic of an early spatial range expansion combined with a recent bottleneck, subsequently subdivided into multiple morphotypes following local adaption to heterogeneous climates.
  • Jin-Ming CHEN, Zhi-Yuan DU, Yang-Yang YUAN, Qing-Feng WANG
    J Syst Evol. 2014, 52(3): 313-325.
    Many phylogeographic studies of terrestrial plant species on the Qinghai–Tibet Plateau (QTP) have been carried out to elucidate the range shifts in response to climatic oscillations in the Quaternary. However, patterns of range shifts for aquatic plants following the climate change on the QTP are poorly understood. Here, we studied the historical range shifts of the aquatic herb Ranunculus bungei Steud. on the QTP using four chloroplast (cpDNA) non-coding spacers. We revealed low within-population genetic diversity (HS = 0.052) and high interpopulation genetic differentiation (GST = 0.914; NST = 0.954). But the high population differentiation was not coupled with a distinct phylogeographic structure (NST > GST, P > 0.05). Phylogenetic analyses revealed two main cpDNA haplotype lineages and the split between these two lineages can be dated back to the late Tertiary (3.84–11.90 Ma). Two independent range expansions within the two intraspecific lineages at approximately 0.15–0.46 and 0.17–0.50 Ma were revealed. Our results suggested that R. bungei survived the Last Glacial Maximum and/or previous glacial periods on the QTP. Colonization or recolonization during the repeated range expansions may have replaced the early haplotypes and the pre-existing genetic structure and could explain the non-significant phylogeographical structure.
  • Liang-Liang YUE, Hang SUN
    J Syst Evol. 2014, 52(3): 326-340.
    Climate oscillations and landscape heterogeneity make the historical population processes of organisms of the Qinghai–Tibet Plateau quite complex. We used chloroplast DNA sequences and amplified fragment length polymorphism (AFLPs) to study the phylogeography and genetic variation of the Qinghai–Tibet Plateau endemic Spenceria ramalana Trimen. The parsimony network contains two star-like evolutionary units, nested into two nested clades, coinciding with geographic population groups indicated by samova software. The central group shows genetic homogeneity, indicating a bottleneck or founder effect of population dynamics. Margin groups contribute more haplotype diversity (CT), indicating potential refugia. Several expansion events during several interglacial periods were detected. The latest expansion of the eastern population contributed to the modern population structure of the central area. Four AFLP clusters were detected. Higher CT, a relict pattern of haplotype distribution and DW values of marginal populations, confirmed the location of potential montane refugia. Relict distribution pattern, nested clade phylogeographic analysis conclusions, and restricted gene flow detected by AFLPs indicated an isolation pattern of the populations of montane areas. Heterogeneity of landscape of the western and southern montane areas could be the main barrier for gene flow. Moisture conditions and ecotype transformation might help to build the phylogeographic pattern of this species. Neither chloroplast DNA markers nor AFLP was able to differentiate the two varieties of this species.
  • De-Qing HUANG   Qin-Qin LI   Chun-Jing ZHOU   Song-Dong ZHOU   Xing-Jin HE
    J Syst Evol. 2014, 52(3): 341-354.
    In the present study, we used two chloroplast DNA (cpDNA) fragments (trnL-F and rps16) and the nuclear ribosomal internal transcribed spacer (ITS) sequence data to examine intraspecific differentiation and phylogeographical history of Allium wallichii. Based on wide scale sampling (28 populations and 174 individuals) across the entire distribution range of this species, 33 cpDNA haplotypes and 25 ITS ribotypes were detected in our investigation. These cpDNA haplotypes were divided into three major lineages, which was further supported by the ITS phylogenetic results. High haplotype/ribotype diversity and population differentiation, together with most of the haplotypes/ribotypes being exclusive to single populations, implied restricted gene flow among populations and significant geographical isolation. Nearly all populations with high haplotype/ribotype diversity were found in the Hengduan Mountain Region (HMR), whereas the populations of the Himalayas and Nanling Mountains showed a lower level, suggesting the HMR might serve as a potential divergence center for A. wallichii. The main lineages of A. wallichii diverged from each other between Mid–Late Pliocene and Early Quaternary based on two sets of molecular markers, indicating that the Quaternary climatic fluctuation could not have contributed greatly to the divergence of the main lineages of A. wallichii. Instead, the intricate topography and heterogeneous habitats resulting from the drastic uplift of the Qinghai–Tibet Plateau from the Late Pliocene could be responsible for the intraspecific differentiation of A. wallichii. The present study further highlights the importance of geographic isolation and habitat heterogeneity in shaping and maintaining high species diversity within the HMR.
  • Wen GUO, Lin-Lin WANG, Shan SUN, Yong-Ping YANG, Yuan-Wen DUAN
    J Syst Evol. 2014, 52(3): 355-362.
    Evolution of herkogamy has been ascribed to preventing autonomous selfing within flowers, but this argument has received challenges due to the negative effects of sexual interference on reproductive success of plant species. We examined the effects of the two contrasting modes of herkogamy, detailed by the different patterns of style movement, on the foraging time of pollinators on flowers, pollen removal, and deposition in two Chamerion species. Our results suggested that the duration of foraging time of bumblebees was generally higher in C. angustifolium (L.) Holub than in C. conspersum (Hausskn.) Holub during the male-phase of flowers, but the reverse during the female-phase of flowers. As a result, stigma interfered with pollen removal more in C. conspersum than in C. angustifolium, based on examinations of pollen removal after one visit by a pollinator. However, this negative effect on total pollen removal was covered by the high pollinator diversity and the possible high visitation rate in the study sites. In contrast, we found that almost no difference existed in pollen deposition rate after one visit of a pollinator between the two Chamerion species, and emasculation did not increase the total pollen deposition in either species, indicating that anthers did not interfere with pollen deposition in the two Chamerion species. Our results suggested that, compared with C. conspersum, the derived mode of herkogamy in C. angustifolium reduced interference of stigmas in pollen removal. This might contribute to the wide distribution of C. angustifolium, to some degree, in environments of pollinator scarcity and low activity in newly colonized habitats.
  • Chan ZHANG, Guo-Ying ZHOU, Yong-Ping YANG, Yuan-Wen DUAN
    J Syst Evol. 2014, 52(3): 363-367.
    In plants with infrequent pollinator services, the benefits of reproductive assurance could be eroded by severe ovule discounting and inbreeding depression (ID). However, it remains unclear how selfing evolves under complete pollinator failure and strong ID. We examined the mating system and ID under netting and robbing conditions in Comastoma pulmonarium (Turcz.) Toyok. (Gentianaceae), an alpine annual experiencing a high ratio of nectar robbery on the Qinghai–Tibet Plateau.Comastoma pulmonarium produced seeds via selfing at the study site. No pollinator was observed and thus the nectar was consumed exclusively by robbers. Inbreeding depression occurred in the life stages of seed mass and germination, and the cumulative ID was much higher than 0.5 under netting and robbing conditions. Overall, in comparison with netting, the magnitude of ID under robbing conditions tended to decrease. Our results suggested that selfing could assure reproduction for plants under complete pollinator failure and strong ID, supporting the “better than nothing” role of selfing and providing one of the few cases of the evolution of selfing under strong ID.
  • De-Li PENG, Xiao-Kun OU, Bo XU, Zhi-Qiang ZHANG, Yang NIU, Zhi-Min LI, Hang SUN
    J Syst Evol. 2014, 52(3): 368-377.
    Plant sexual systems can be affected by various environmental factors, and thus show a range of morphological differences. The associations between plant sexual systems and morphology are unique, for example, the subnival belt of the Hengduan Mountains has harsh climatic conditions, but hosts remarkable biodiversity. However, these associations have received surprisingly little attention. We analyzed the associations in this region, and compared the pattern of sexual systems with that of other floras, and we also reviewed the breeding system of 36 alpine species. Information on plant sexual systems and these traits were mainly based on published information, herbarium collections, and field observations. The results showed that there was a high proportion of hermaphroditic species and a low proportion of dioecious and monoecious species. Hermaphroditism was strongly associated with showy floral displays, specialist entomophily, and perennial forbs. Dioecy was strongly associated with inconspicuous, pale-colored flowers, anemophily, and shrubs, whereas monoecy was strongly associated with inconspicuous, pale-colored flowers, generalist entomophily, and perennial grasses. Although no association was found between sexual systems and fruit type, plants with dry fruits (98.1%) were predominant in our study region. With respect to the plant breeding systems in the alpine region of southwest China, we predicted that pollination service might be particularly low; most of the plants lacked enough outcrossing pollinators. Our data revealed that 97.1% of the hermaphroditic species were self-compatible, and 88.2% of them showed autonomous or facilitated selfing. The plant sexual systems identified might serve to optimize the probability of pollination and thus ensure reproductive success.
  • Reviews
  • Hang SUN, Yang NIU, Yong-Sheng CHEN, Bo SONG, Chang-Qiu LIU, De-Li PENG, Jian-Guo CHEN, Yang YANG
    J Syst Evol. 2014, 52(3): 378-396.
    The Qinghai–Tibet Plateau (QTP) is the highest and largest plateau in the world. It covers correspondingly wide geological, topographical, and climatic gradients, and thus hosts greater biodiversity than surrounding lowlands and other high elevation regions. Due to its extreme environmental and biological diversity, the QTP is an ideal region for studying adaptations of plant species under harsh environmental conditions at multiple evolutionary levels. Many recent ecological studies have revealed functions of distinctive morphological features of various plants in the region that improve their reproductive success. Examples include large and showy bracts, hairy inflorescences, and drooping flowers. Numerous other investigations have examined QTP plants' sexual systems, patterns of biomass allocations, and biotic interactions. This paper summarizes recent advances in understanding of morphological adaptations, plant–plant interactions, plant–pollinator interactions, floral color patterns, pollination adaptations, and resource allocation patterns of alpine plants of the QTP. The overall aim is to synthesize current knowledge of the general mechanisms of plant survival and reproduction in this fascinating region.