Research Article |
Corresponding author: Yu-Jin Wang ( wangyujin@lzu.edu.cn ) Academic editor: Peter de Lange
© 2018 La-Mei Heng, Yu-Lin Zheng, Yong-Bao Zhao, Yu-Jin Wang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Heng L-M, Zheng Y-L, Zhao Y-B, Wang Y-J (2018) Radiation of members of the Soroseris hookeriana complex (Asteraceae) on the Qinghai-Tibetan Plateau and their proposed taxonomic treatment. PhytoKeys 114: 11-25. https://doi.org/10.3897/phytokeys.114.29914
|
The existence of intermediate types is a major obstacle that can hinder the circumscription of species. Elucidating the mechanism responsible for intermediate types is essential for achieving a reasonable taxonomical treatment. In this study, we explored the evolutionary history and taxonomic treatment of the Soroseris hookeriana (C.B.Clarke) Stebbins complex, which comprises six named taxa that may be taxonomically distinct and are all native to the Qingha-Tibetan Plateau (QTP). We made an investigation across the distribution range of Soroseris Stebbins and sampled 27 populations, mostly from the complex. Internal transcribed spacer (ITS) and two chloroplast loci were sequenced and analysed using the neighbour-joining and Bayesian inference methods. The resulting phylogenies show no well supported inconsistence in topologies, in line with the lack of incongruence detected by the length difference test. However, all the trees were largely unresolved within S. hookeriana complex, irrespective of the optimality criterion employed. We interpret these results as an experience of radiation, which is a common process for native genera on the QTP. Thus, we suggest that all of the morphotypes might be different forms, generated by incipient speciation due to recent explosive differentiation, possibly triggered by the drastic environmental changes of the QTP. Given their evolutionary history, we propose a pragmatic method for treating all of these species as subspecies with a total of four new combinations.
Radiation, Soroseris hookeriana complex, taxonomic treatment, Asteraceae
The description and delimitation of species in an evolutionary framework is essential for understanding patterns of biodiversity and distribution, as well as when assessing conservation strategies for natural resources (
Soroseris is a genus comprising seven species and all are endemic to the Qingha-Tibetan Plateau (QTP) according to the latest comprehensive revision (
The second species complex, referred to as the S. hookeriana (C.B.Clarke) Stebbins complex, comprises S. hookeriana and five possibly independent species, where one was accepted as S. erysimoides (Hand.-Mazz.) C. Shih in the latest revision, whereas the other four, i.e. S. occidentalis (Stebbins) Tzvelev, S. hirsuta (J. Anthony) C. Shih, S. gillii (S. Moore) Stebbins and S. gillii subsp. handelii Stebbins, were treated as synonyms of S. hookeriana (
Different taxonomical treatments of the possible members of the Soroseris hookeriana complex. FRPS: Flora Reipublicae Popularis Sinicae; FOC: Flora of China.
|
Shih C (1993) | FRPS (1997) | FOC (2011) |
---|---|---|---|
S. gillii subsp. typica | S. trichocarpa | S. gillii | S. hookeriana |
S. gillii subsp. occidentalis | S. hirsuta | S. hirsuta | S. hookeriana |
S. gillii subsp. hirsuta | S. hirsuta | S. hirsuta | S. hookeriana |
S. gillii subsp. handelii | S. hirsuta | S. hirsuta | S. hookeriana |
S. hookeriana subsp. typica | S. hookeriana | S. hookeriana | S. hookeriana |
S. hookeriana subsp. erysimoides | S. erysimoides | S. erysimoides | S. erysimoides |
S. bellidifolia | S. hirsuta | S. hirsuta | S. glomerata |
In addition to the controversial treatments mentioned above, the circumscription of Soroseris is also disputed. For example, two species of Syncalathium Lipschitz are included in Soroseris in some systems (
Previous studies have resolved the circumscription and sister (Syncalathium) of Soroseris, but the delimitation within the two species complexes remains unresolved (
In total, from the QTP, we collected 35 individuals from 27 populations belonging to Soroseris and two individuals from Syncalathium as an outgroup, according to a previous study (
Genomic DNA was extracted from dried leaves in silica gel using the CTAB method (
Taxa, collection localities, vouchers (or the references for those downloaded from NCBI) and their GenBank accession numbers.
Taxon (FOC, 2011) | Collection locality | Latitude (°N) / Longitude (°E) | Altitude (m) | Voucher | Genbank number (ITS, matK, psbA-trnH) |
---|---|---|---|---|---|
S. erysimoides | Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN30 (LZU) | MG932859; MG946722; MG932893 |
Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN47 (LZU) | MG932861; MG946724; MG932895 | |
Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN48 (LZU) | MG932862; MG946725; MG932896 | |
Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN49 (LZU) | MG932863; MG946726; MG932897 | |
Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN50 (LZU) | MG932864; MG946727; MG932898 | |
Cuona, Tibet, China | 27.9269, 91.8789 | 4519 | Y.-J. Wang, CN51 (LZU) | MG932865; MG946728; MG932899 | |
Geermu, Qinghai, China | 35.4158, 96.3409 | 4665 | Y.-J. Wang, GEM3 (LZU) | MG932858; MG946721; MG932892 | |
Yadong, Tibet, China | 27.5518, 88.9306 | 3059 | Y.-J. Wang, YD46 (LZU) | MG932860; MG946723; MG932894 | |
Xingu, Sichuan, China | – | – |
|
HQ436213; JF956518; HQ436180 | |
Tibet, China | – | – |
|
JF978800; JF956516; JN047244 | |
Deqin, Yunnan, China | – | – |
|
HQ436212; JF956517; HQ436179 | |
Sichuan, China | – | – |
|
JF978799; JF956515; JN047243 | |
S. hookeriana | Chayu, Tibet, China | 29.3252, 97.0390 | 4705 | Y.-J. Wang, CY39 (LZU) | MG932868; MG946742; MG932910 |
Chayu, Tibet, China | 29.3252, 97.0390 | 4705 | Y.-J. Wang, CY53 (LZU) | MG932869; MG946743; MG932917 | |
Daocheng, Sichuan, China | 29.2953, 100.1466 | 4404 | Y.-J. Wang, DC9 (LZU) | MG932871; MG932921; MG932921 | |
Kangding, Sichuan, China | 29.4446, 101.4339 | 4657 | Y.-J. Wang, KD11 (LZU) | --; MG946729; MG932900 | |
Kangding, Sichuan, China | 30.0411, 101.9532 | 2861 | J.-Q. Liu, KD54 (LZU) | MG932870; MG946732; MG932918 | |
Kangding, Sichuan, China | 30.0411, 101.9532 | 2861 | Y.-J. Wang, KD7 (LZU) | MG932877; MG946750; MG932914 | |
Xiangcheng, Sichuan, China | 28.9312, 99.7835 | 2927 | Y.-J. Wang, XC10 (LZU) | MG932876; MG946747; MG932915 | |
Xiaojin, Sichuan, China | 30.5473, 102.5373 | 4519 | Y.-J. Wang, XJ4 (LZU) | MG932873; MG946739; MG932911 | |
Xiaojin, Sichuan, China | 30.5473, 102.5373 | 4519 | Y.-J. Wang, XJ5 (LZU) | MG932874; MG946740; MG932914 | |
Xiaojin, Sichuan, China | 30.5473, 102.5373 | 4519 | Y.-J. Wang, XJ6 (LZU) | MG932875; MG946741; MG932920 | |
Zhiduo, Qinghai, China | 33.5845, 96.3409 | 4689 | Y.-J. Wang, ZD2 (LZU) | MG932866; MG932902; MG932902 | |
Sichuan, China | – | – |
|
HQ446097; JF956522; JN047246 | |
Sichuan, China | – | – |
|
HQ436227; JF956521; JN047245 | |
Kangding, Sichuan, China | – | – |
|
HQ436214; JF956520; HQ436181 | |
Cuomei, Tibet, China | 28.7853, 91.7549 | 5048 | Y.-J. Wang, CN25 (LZU) | MG932883; MG946734; MG932905 | |
Dingri, Tibet, China | 28.5755, 87.1136 | 4305 | Y.-J. Wang, DR55 (LZU) | MG932886; MG946737; MG932919 | |
S. hookeriana | Dangxiong, Tibet, China | 29.9018, 90.1370 | 5400 | Y.-J. Wang, DX17 (LZU) | MG932882; MG946733; MG932901 |
Dangxiong, Tibet, China | 29.9018, 90.1370 | 5400 | Y.-J. Wang, DX43 (LZU) | MG932885; MG946736; MG932912 | |
Longzi, Tibet, China | 28.6027, 92.2142 | 4906 | Y.-J. Wang, LZ27 (LZU) | MG932884; MG946735; MG932906 | |
Longzi, Tibet, China | 28.6371, 92.2175 | 5106 | Y.-J. Wang, LZ52 (LZU) | MG932878; MG946749; MG932916 | |
Yadong, Tibet, China | 27.5527, 88.9315 | 3059 | Y.-J. Wang, YD21 (LZU) | MG932867; MG946731; MG932904 | |
Hongshan, Yunnan, China | – | – |
|
HQ436218; JF956532; HQ436185 | |
Tibet, China | – | – |
|
JF978806; JF956530; JN047250 | |
Longzi, Tibet, China | 28.6371, 92.2175 | 5106 | Y.-J. Wang, LZ33 (LZU) | MG932872; MG946738; MG932909 | |
Cuona, Tibet, China | 27.9269, 91.8788 | 4519 | Y.-J. Wang, CN29 (LZU) | MG932880; MG946745; MG932907 | |
Cuona, Tibet, China | 27.8476, 91.8929 | 4732 | Y.-J. Wang, CN32 (LZU) | MG932881; MG946746; MG932908 | |
S. glomerata | Angren, Tibet, China | 29.5021, 86.2770 | 4753 | Y.-J. Wang, AR18 (LZU) | MG932887; MG946744; MG932922 |
Tibet, China | – | – |
|
JF978802; JF956523; JN047247 | |
Daxueshan, Yunnan, China | – | – |
|
HQ436217; JF956527; HQ436184 | |
Deqin, Yunnan, China | – | – |
|
HQ436216; JF956528; HQ436183 | |
Tibet, China | – | – |
|
JF978804; JF956525; JN047248 | |
S. teres | Yadong, Tibet, China | 27.5503, 88.9316 | 3059 | Y.-J. Wang, YD44 (LZU) | MG932888; MG946752; MG932924 |
Yadong, Tibet, China | 27.5503, 88.9316 | 3059 | Y.-J. Wang, YD45 (LZU) | MG932889; MG946753; MG932925 | |
S. umbrella | Zhonggashan, Yunnan, China | – | – |
|
HQ436197; HQ436164; HQ436131 |
Hongshan, Yunnan, China | – | – |
|
HQ436198; HQ436165; HQ436132 | |
Soroseris sp. | Chayu, Tibet, China | 29.3252, 97.0390 | 4705 | Y.-J. Wang, CY40 (LZU) | MG932879; MG946748; MG932923 |
Syncalathium disciforme | Heishui, Sichuan, China | 32.1326, 102.3633 | 4016 | Y.-J. Wang, HS12 (LZU) | MG932890; MG946754; MG932926 |
Syncalathium kawaguchii | Luozha, Tibet, China | 28.2504, 91.0481 | 4112 | Y.-J. Wang, LZ24 (LZU) | MG932891; MG946755; MG932927 |
Three datasets were constructed for the ITS sequences, the combination of psbA–trnH and matK and the combination of all the three fragments. For the first two datasets, genetic distance was calculated with Mega (
The aligned ITS dataset comprised 607 base pairs (bp) with 58 variable sites, where 36 sites were potentially parsimony informative. A total of 12 mosaic sites are detected from eight individuals, mostly with one or two. The K-2P distance, ranged from 0 to 2.4%, is 0.6% on average within the ingroup, while 0.3% on average or 1% maximally within the complex. The NJ tree was mostly congruent in terms of its topology with the 50% majority rule consensus tree derived from Bayesian analysis and the latter is shown in Fig.
The 50% majority rule consensus tree derived from Bayesian inference of the nuclear internal transcribed spacer. Posterior probabilities and bootstrap percentages are indicated above and below the branches, respectively. The samples named according to FOC (2011) or NCBI,
The combined psbA–trnH and matK sequences measured 870 bp, where 54 nucleotide sites were variable and 23 were phylogenetically informative. The K-2P distance is estimated to be 0.2% on average and ranged from 0 to 1.8% within the ingroup, while 0.1% on average or 0.6% maximally within the complex. The NJ tree was congruent with the 50% major consensus tree obtained by BI and the latter is presented in Fig.
The 50% majority rule consensus tree derived from Bayesian inference of the combined sequences of psbA-trnH and matK. Posterior probabilities and bootstrap percentages are indicated above and below the branches, respectively. The samples named according to FOC (2011) or NCBI,
ILD test (P = 0.289000) detected no strong evidence of incongruence between the data partitions. Thus, the three fragments are combined and the resulting topologies from NJ and BI (Suppl. material 2) are concordant. Being highly similar to that from ITS, three major clades within Soroseris were recovered and the relationship within S. hookeriana complex remains largely unresolved.
Aside from S. umbrella, no species were recovered in a monophyletic clade. In particular, S. glomerata was revealed to be present in all the three major clades (Figs
In most cases, hybridisation is considered to explain the occurrence of intermediates. It is not possible to exclude this mechanism in the S. hookeriana complex, but it appears to conflict with the status of Soroseris because of the following reasons. First, hybridisation often results in different topologies when phylogenetic trees are reconstructed based on ITS and chloroplast sequences, which was not the case for Soroseris. Second, hybridisation might only affect the tree obtained based on a nuclear marker, but the grouping of the chloroplast sequences was also not species-specific for Soroseris. Third, the occurrence of hybridisation might be determined by the distribution of the parent species, where it usually occurs in areas where the ranges of the two species meet and thus the diversity of these populations might be higher than that of others. We found no evidence of hybridisation based on these three reasons in Soroseris. In addition, mosaic sites in nuclear ITS sequences, which are characteristic of many taxa generated by hybridisation, are rare in Soroseris.
Alternatively, we suggest that radiation might be the main mechanism responsible for the various forms of intermediates in Soroseris. Radiation involves the rapid differentiation of a lineage within a short time interval, which is mostly triggered by environmental change or morphological innovation (
According to the phylogenetic context and little genetic differentiation (ITS: 0.3% on average while 1% maximally; concatenated cp: 0.1% on average while 0.6% maximally), all members of the S. hookeriana complex (include S. teres and part of S. glomerate) could be treated as single species. However, this revision will make it difficult to describe an assemblage. In addition, this treatment might fail to reflect the evolutionary history discussed above and the biodiversity may be underestimated. However, the alternative treatment is also not perfect because separating all of the species will make identification difficult, especially when encountering intermediates, which is common in the field. In order to address these issues, we propose to treat all of the morphotypes, especially those with the typical morphology and widespread distribution, as subspecies of S. hookeriana because this is the earliest name of a species reported within the complex. However, we abandoned, for the time being, assigning new names to S. teres and S. glomerate due to insufficient sampling as well as distinct morphology. In addition, the name S. hookeriana subsp. erysimoides (Hand.-Mazz.) Stebbins has been published previously and we suggest that it is restored. Thus, a total of eight taxa, including four new combinations, are proposed and a key is provided in the following.
1a | Cataphylls numerous on the lower part of the stem; leaf blades elliptic or spatulate; ligule of corollas mostly equal to or shorter than the tube | S. glomerata (only those closely related to the S. hookeriana complex) |
1b | Cataphylls few or none; leaf blades lanceolate or oblanceolate; ligules distinctly exceeding the tube of the corolla | 2 |
2a | Synflorescence elongate and cylindric | S. teres |
2b | Synflorescence hemispheric | 3 |
3a | Leaves entire or denticulate, obtuse at the apex; upper leaves, bracts of the inflorescence and peduncles glabrous or sparingly hirsute | S. hookeriana subsp. erysimoides |
3b | Leaves pinnatifid, acute at the apex; upper leaves, bracts of the inflorescence and peduncles strongly hirsute4a. Involucral bracts sparsely to strongly hirsute | 4 |
4a | Involucral bracts sparsely to strongly hirsute | 5 |
5a | Leaves sinuate-pinnatifid, sinuate-dentate or merely denticulate; inner bracts sparsely to moderately hirsute | S. hookeriana subsp. occidentalis (new combination) |
5b | Leaves runcinate-pinnatifid; inner bracts densely hirsute | 6 |
6a | Stem tall, 4–20 cm; leaf blade pinnately lobed, lobes narrowly triangular | S. hookeriana subsp. typica |
6b | Stem short, less than 6 cm tall; leaf blade pinnately lobed, lobes irregular | S. hookeriana subsp. hirsuta (new combination) |
4b | Involucral bracts glabrous | 7 |
7a | Leaf blade 3–8cm long, 0.7–1.8 cm wide | S. hookeriana subsp. gillii (new combination) |
7b | Leaf blade 2–4cm long, 0.5–1.3 cm wide | S. hookeriana subsp. handelii (new combination) |
≡Crepis gillii S. Moore in Journ. Bot. 37: 170. 1899 (Syntype: K000250191); ≡Soroseris gillii (S. Moore) Stebbins in Mem. Torrey Bot. Club 19 (3): 41. 1940; S. Y. Hu in Quart. Journ. Taiwan Mus. 21 (3–4): 166. 1968; Higher Plants of China 4: 686, figure 6786. 1975; Flora Reipublicae Popularis Sinicae. 80 (1): 199. 1997; ≡Soroseris gillii subsp. typica Stebbins in Mem. Torrey Bot. Club. 19 (3): 42. 1940; S. Y. Hu in Quart. Journ. Taiwan Mus. 21 (3–4): 166. 1968; ≡Soroseris trichocarpa (Franch.) Shih in Act. Phytotax. Sin 31: 446. 1993; Flora Reipublicae Popularis Sinicae. 80 (1): 199. 1997.
≡Crepis gillii var. hirsuta J. Anthony in Notes Royal Bot. Gard. Edinb. 18: 193. 1934 (Syntype: E00383690); ≡Soroseris gillii subsp. hirsuta (J. Anthony) Stebbins in Mem. Torrey Bot. Club 19 (3): 44. 1940 (Syntype: E00383690); S. Y. Hu in Quart. Journ. Taiwan Mus. 21 (3–4): 166. 1968; ≡Soroseris hirsuta (J. Anthony) C. Shih in Act. Phytotax. Sin 31: 446.1993; Flora Reipublicae Popularis Sinicae. 80 (1): 201. 1997.
≡Soroseris gillii subsp. occidentalis Stebbins in Mem. Torrey Bot. Club. 19 (3): 44. 1940 (Type: K000250154); Babcock in Univ. Calif. Publ. Bot. 22: 922. 1937; S. Y. Hu in Quart. Journ. Taiwan Mus. 21 (3–4): 166. 1968; ≡Soroseris occidentalis (Stebbins) Tzvelev in Bot. Zhurn. 92: 1753. 2007.
≡Soroseris gillii subsp. handelii Stebbins in Mem. Torrey Bot. Club. 19 (3): 42. 1940 (Isotype: E00383689); S. Y. Hu in Quart. Journ. Taiwan Mus. 21 (3–4): 166. 1968.
We thank Jian-Quan Liu and Zhong-Hu Li for helping with our field investigation. We are very grateful to Dr. Christina Flann and Dr. Rob Smissen for their valuable comments that contributed greatly to our manuscript. This study was supported by the National Natural Science Foundation of China (81274024).
The main morphological difference amongst members of the Soroseris hookeriana complex and the closely related species
Data type: measurement
The 50% majority rule consensus tree derived from Bayesian inference of the combined sequences of nuclear internal transcribed spacer, psbA-trnH and matK
Data type: molecular data
Explanation note: Posterior probabilities and bootstrap percentages are indicated above and below the branches, respectively. The samples named according to FOC (2011) or NCBI,