Table of Contents

06 June 2019, Volume 57 Issue 3

Cover illustration: Four closely related Rhododendron species growing on the Sejila Mountain, Tibet, China. Top left to right: Rh. tanastylum, Rh. phaeochrysum, Rh. principis, Rh. lulangense. Middle: Four genetic clusters (corresponding to the order of the species above) identified by STRUCTURE based on 15 SSR loci, indicating the numerous hybrids or introgressive progenies. Bottom: A view of the flowering Rhododendron landscape on Mt. Sejila. Photographs by Jian Luo, Lei Zhang and Xin-Xin Mao. Designed by Jian-Quan Liu. See Wang et al., pp. 278–286 in this issue. [Detail] ...

  

• Awards of JSE Outstanding Papers (2017)

  Song Ge and Jun Wen

  J Syst Evol. 2019, 57(3): 209-210.
  https://doi.org/10.1111/jse.12506

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Research Articles
• Phylogenetics of Annona cherimola (Annonaceae) and some of its closest relatives

  Nerea Larranaga, Federico J. Albertazzi, and Jose I. Hormaza

  J Syst Evol. 2019, 57(3): 211-221.
  https://doi.org/10.1111/jse.12473

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  Annona cherimola is a woody perennial species in the Annonaceae family that produces edible fruits and has economic importance in several regions of the world with subtropical climates. Together with other 10‐12 species, A. cherimola belongs to the section Atta of the Annona genus with a center of origin in Central America and the Caribbean. Species of the section Atta produce soft skin ripe fruits with raised areoles bounded by recessed furrows. Annona cherimola is the only species of the section naturally found in the Andean region of South America. Currently, no information is available at the molecular level on the phylogenetic relationships of most of the species of Atta and closely related sections in Annona. In order to fill this gap, in this work a phylogenetic approach was performed using five coding and non‐coding plastid DNA regions, to determine the phylogenetic relationships between A. cherimola and other related species included in Atta and other sections of the genus. The results obtained support recent studies that demonstrated the likely Mesoamerican origin of A. cherimola based on biogeographical analysis with SSR markers, rather than the previously considered South American origin hypothesis. In addition, the species belonging to the Atta section did not show monophyly. Finally, A. cherimola and A. pruinosa seem to be phylogenetically close species and additional studies are needed to discern the relations between them.
• Impacts of domestication on population genetics of a traditional Chinese medicinal herb, Atractylodes macrocephala (Asteraceae)

  Chuan Chen, Li Zheng, Qing Ma, Wen-Bin Zhou, Yin Lu, Yun-Peng Zhao, and Cheng-Xin Fu

  J Syst Evol. 2019, 57(3): 222-233.
  https://doi.org/10.1111/jse.12446

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  As a medicinal herb, Atractylodes macrocephala Koidz. experienced centuries of cultivation in China, and germplasm resources of all cultivated populations have degraded over time as a consequence of domestication processes. This study used chloroplast DNA and microsatellites to clarify not only the effects of domestication on population genetics, but also determine the geographic origins of landraces. The results revealed that cultivated populations (except the “Pingzhu” landrace) showed higher genetic diversity than their wild counterparts and low levels of genetic differentiation occurred between cultivated and wild groups. Furthermore, STRUCTURE and UPGMA analyses grouped all wild populations into three genotypic clusters, two of which (in Shaanxi and Hunan Province) shared the same gene pool with cultivated A. macrocephala, suggesting that wild populations in Central China have been involved in the origin of cultivated A. macrocephala. Moreover, the wild population from Qimen, Anhui Province and the cultivated “Pingzhu” landrace harbor unique gene pools and rare alleles that could be useful in future breeding efforts. This large‐scale analysis of population genetics on a medicinal herb that has a centuries‐long history of human‐mediated selection will facilitate utilization and conservation of the valuable genetic resources of medicinal species.
• Congruent species delimitation of two controversial gold‐thread nanmu tree species based on morphological and restriction site‐associated DNA sequencing data

  Xin Ding, Jian Hua Xiao, Lang Li, John G. Conran, and Jie Li

  J Syst Evol. 2019, 57(3): 234-246.
  https://doi.org/10.1111/jse.12433

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  Species delimitation is fundamental to conservation and sustainable use of economically important forest tree species. However, the delimitation of two highly valued gold‐thread nanmu species (Phoebe bournei (Hemsl.) Yang and P. zhennan S. K. Lee & F. N. Wei) has been confusing and debated. To address this problem, we integrated morphology and restriction site‐associated DNA sequencing (RAD‐seq) to define their species boundaries. We obtained consistent results from the two datasets, supporting two distinct lineages corresponding to P. bournei and P. zhennan. In P. bournei, higher order leaf venation is more prominent, petioles are thicker, and leaf apex angle is narrower, compared to P. zhennan. Both datasets also revealed that the former putative P. bournei populations from northeastern Guizhou belong to P. zhennan. The two species are now distinct in distributions except in the Wuling Mountains, where they overlap. Phoebe bournei occurs mainly in central Fujian, southern Jiangxi, the Nanling Mountains, and the Wuling Mountains, whereas P. zhennan is found in the adjoining eastern regions of the Qionglai Mountains, the southern Sichuan hills, and the Wuling Mountains. The re‐delimitation of P. bournei and P. zhennan and clarification of their ranges provide a better scientific basis guiding the conservation and sustainable utilization of these tree species.
• Molecular diagnosis for a Tamarix species from two reclaimed lands along the Yellow Sea in Korea inferred from genome wide SNP markers

  Soo-Rang Lee, John F. Gaskin, and Young-Dong Kim

  J Syst Evol. 2019, 57(3): 247-255.
  https://doi.org/10.1111/jse.12432

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  The taxonomy and phylogenetic relationships of related taxa are important for understanding the biology of a species. Also, spatial distribution of genetic variation may offer insights into history of range shifts and demographic changes. The genus Tamarix L. from the Old World is a taxonomically challenging group that has widely expanded its range in the recent past. We examined genomic diversity patterns and the taxonomic identities of Korean Tamarix species whose taxonomy has remained unresolved. We used a total of 1773 SNP data from genotyping by sequencing for 37 Tamarix plants representing two species; T. chinensis and T. ramosissima to infer species delimitation and the geographic distribution of genomic diversity. Clustering (STRUCTURE; PCA, neighbor joining) and phylogenetic tree results indicated that the two morphologically similar species T. chinensis and T. ramosissima are genetically distinct and the two Korean populations (Sihwa & Songdo) are clustered closely with T. chinensis. Approximate Bayesian Computation based hypothesis testing results suggested that one of the two Korean populations, Songdo might have primarily been derived from the native area, China, followed by range expansion to Sihwa with a secondary admixture event between an established population, Songdo, and a native population, Beijing.
• Exploring the generic delimitation of Phyllagathis and Bredia (Melastomataceae): A combined nuclear and chloroplast DNA analysis

  Qiu-Jie Zhou, Che-Wei Lin, Jin-Hong Dai, Ren-Chao Zhou, and Ying Liu

  J Syst Evol. 2019, 57(3): 256-267.
  https://doi.org/10.1111/jse.12451

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  Phyllagathis Blume and Bredia Blume (Sonerileae?s.l., Melastomataceae) are two closely related Asian genera with similar morphology and overlapping geographical range. Their generic circumscription and phylogenetic relationships are far from fully understood. We present here a molecular phylogenetic investigation for the two genera using nuclear ribosomal internal transcribed spacer and chloroplast (trnV‐trnM) sequence data. Seventeen genera of Sonerileae s.l. were included in the analyses, with Phyllagathis and Bredia densely sampled to cover their geographical range and morphological diversity. We identified 14 well supported species clusters within Sonerileae s.l.–Medinilla. Phylogenetic analyses together with reconstruction of morphological characters clearly indicated the taxonomic mess in generic delimitation of Sonerileae s.l. Many of the characters traditionally used in generic delimitation were highly homoplasious. Bredia and Phyllagathis, as well as Allomorphia, Anerincleistus, Fordiophyton, and Oxyspora, were revealed to be non‐monophyletic. Bredia, as currently defined, contains two groups of species with different phylogenetic affiliations. Bredia should be recircumscribed to exclude the Bredia–Phyllagathis clade I and accommodate the Bredia–Phyllagathis clade II as the type of the genus is included in the latter clade. Most species sampled in Phyllagathis spread across eight well supported clades throughout the phylogenetic tree. The type of Phyllagathis showed no close affiliation with other members of Phyllagathis nor its putative relatives. Phyllagathis, as presently circumscribed, is heterogeneous, encompassing multiple evolutionary lineages. As sequence data of nuclear ribosomal internal transcribed spacer and chloroplast trnV‐trnM failed to resolve the phylogenetic relationships among these lineages, the formal taxonomic adjustment of Phyllagathis is postponed until further evidence can be gathered.
• Analyses of genome‐scale variation reveal divergence of two Sinalliaria species (Brassicaceae) with continuous but limited gene flow

  Tian-Jing Wang, Da-Fu Ru, Dan-Zhang, and Quan-Jun Hu

  J Syst Evol. 2019, 57(3): 268-277.
  https://doi.org/10.1111/jse.12461

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  Numerous biogeographic studies have suggested that geographic isolations triggered by Quaternary climatic changes could have contributed greatly to the high species diversity of eastern Asia. However, little is known about how speciation proceeded during the evolutionary divergence of sister species in this region. In this study, we examined genomic divergence and investigated the speciation process of the two species in the genus Sinalliaria endemic to eastern China, S. limprichtiana (Pax) X. F. Jin, Y. Y. Zhou & H. W. Zhang and S. grandifolia (Z. X. An) Huan Hu, com. nov. (Basionym: Alliaria grandifolia Z. X. An (Acta Phytotax. Sin. 23: 396, 1985)). We sequenced the transcriptomes of seven and eight S. limprichtiana and S. grandifolia individuals, respectively. Analysis of transcriptome single nucleotide polymorphism data indicated that both species were well‐delineated with strong genetic differentiation (mean F_ST?=?0.31). A total of 4000 genes showed differential expression between the two species. Based on these genome‐scale nucleotide variations, we used the allele frequency spectrum for modeling analysis with fastsimcoal to gain insights into the speciation process. Our results suggested divergence with continuous gene flow between the two species. These findings will add to our knowledge on the origin of species diversity in eastern Asia.
• Nuclear simple sequence repeat markers are superior to DNA barcodes for identification of closely related Rhododendron species on the same mountain

  Ji Wang, Jian Luo, Ya-Zhen Ma, Xing-Xing Mao, and Jian-Quan Liu

  J Syst Evol. 2019, 57(3): 278-286.
  https://doi.org/10.1111/jse.12460

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  Accurate species delimitation of sampled biological material is critical for a range of studies. Although the DNA barcodes developed in recent years are useful for identifying numerous well differentiated species that have not experienced frequent gene flow, they fail to delimit recently diverged species, especially those with extensive introgressions. Here we use five Rhododendron species growing together on the same mountain as a model system to compare the species delimitation effectiveness of the DNA barcodes (internal transcribed spacer, matK, psbA‐trnH, and rbcL) previously proposed versus 15 pairs of microsatellite markers. Using these markers, we genotyped 129 individuals, which were members of five species according to morphological identification. We identified five simple sequence repeat genetic clusters (independently evolving lineages) corresponding to the morphological identification. However, we found that numerous individuals contained cryptic hybrid introgressions from the other species. The four DNA barcodes could not delimit three out of four closely related species that showed clear morphological differentiation and cryptic introgressions. Even after excluding all cryptic hybrids, two closely related species could not be successfully identified. The low discrimination ability of the DNA barcodes for closely related Rhododendron species could result from two, not mutually exclusive factors: introgressive hybridization and incomplete lineage sorting. Our results highlight the importance of simple sequence repeat markers in delimiting closely related species and identifying cryptic introgressions in the absence of morphological changes.
• Polyphyletic Alyssum cuneifolium (Brassicaceae) revisited: Morphological and genome size differentiation of recently recognized allopatric taxa

  Stanislav Španiel, Karol Marhold and Judita Zozomová-Lihová

  J Syst Evol. 2019, 57(3): 287-301.
  https://doi.org/10.1111/jse.12464

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  Alyssum cuneifolium has been recognized as a perennial alpine species growing in five isolated European mountain ranges: the Pyrenees, Western Alps, Apennines, Pirin Mts and Mt Smolikas. Recent molecular systematic studies revealed that the disjunct populations from distant mountains are not closely related and belong to five independent species: A. cacuminum (Spain, Pyrenees), A. cuneifolium (Italy, Apennines), A. flexicaule (France, Western Alps), A. pirinicum (Bulgaria, Pirin Mts), and A. spruneri (Greece, Mt Smolikas). The present study brings the thorough morphometric analysis of the segregated taxa. We found minor morphological differences between them. Whereas A. pirinicum can be clearly distinguished, the other taxa are recognizable only at the level of population means of investigated characters. The morphological similarity of these distantly related species is obviously the result of adaptation to similar high‐alpine scree habitats. It is not clear, however, whether this adaptation is environmentally controlled or whether it is also genetically fixed and whether it reflects parallel evolution towards similar morphotypes. The observed morphological patterns and their assumed correlation with environmental factors are discussed using examples from other Alyssum taxa. Three different ploidy levels have been reported for the species under study. In the present article, we examine variation in relative nuclear genome size. The Alpine and Pyrenean species have larger relative monoploid genome sizes than the Apennine and Balkan ones, probably reflecting the evolutionary history of the group. A nomenclatural account of the study species is presented, and lectotypes of A. cuneifolium and of two other names are selected.