Collections-based systematics in the new age of discovery: Celebrating the legacy and life of Professor Wen-Tsai Wang

Professor Wen-Tsai Wang (王文采, June 5, 1926–November 16, 2022) was an academician of the Chinese Academy of Sciences (CAS) and a legendary plant taxonomist at the Institute of Botany of CAS (Fig. 1). Herein, we organize a virtual special issue in Journal of Systematics and Evolution (JSE) to celebrate the legacy and life of Professor Wang, who was a leading plant taxonomist in China and made important contributions toward advancing the understanding of the flora of China, the biogeography of eastern Asia, and biodiversity research in the vast Hengduan Mountains. He served as the Editor-in-Chief of Acta Phytotaxonomica Sinica (now JSE) for 6 years from 1982 to 1988, and trained several generations of plant taxonomists in China (Li, 2001).

Professor Wang graduated from Beijing Normal University in 1949 and joined the Institute of Plant Taxonomy (now Institute of Botany), CAS, as a research assistant in 1950. He was promoted to the professor rank in 1982, and was elected as an academician of CAS in 1993. Professor Wang had a long, productive career at the Herbarium of the Institute of Botany, CAS (Fig. 2), and published more than 250 taxonomic and floristic papers and several monographs (Fig. 3). He described 28 new genera, 303 new taxa at the tribal, sectional, and series ranks, ca. 1370 new species, and 242 new combinations.

Professor Wang was one of the most important participants in the compilation of the enormous 8-volume series Iconographia Cormophytorum Sinicorum (Institute of Botany, CAS, 1972–1983) (Fig. 4). He was first assigned to be in charge of the preparation of the book series Iconographia Cormophytorum Sinicorum in 1965 to set the foundation for preparing Flora Reipublicae Popularis Sinicae (FRPS) and help with plant identifications in China. The book series included 11 000 higher plant species of China with brief descriptions on morphology, ecology, distribution, and uses, 9082 of which had line drawings. He contributed the treatments of several families in this book series, including Boraginaceae, Geraniaceae, Gesneriaceae, Papaveraceae, Proteaceae, Ranunculaceae, Urticaceae, and Vitaceae. This book series has been widely used by scientific institutions, colleges, and universities to train botanists and young students in biology throughout China and became the most important botanical classics from China.

Professor Wang was a taxonomic authority on several difficult plant families in China, including Boraginaceae, Rubiaceae, Ranunculaceae, Gesneriaceae, Urticaceae, and Vitaceae, through his extensive herbarium and field research (Fig. 5). He contributed several treatments to Flora Reipublicae Popularis Sinicae, treating part of the Ranunculaceae (Aconitum, Delphinium, Anemone, and several small genera) (Wang, 1979, 1980), Gesneriaceae (Wang, 1990), Boraginaceae (Kung & Wang, 1989; Wang, 1993), and Urticaceae (Wang & Chen, 1995; Wang, 2014, 2016). Professor Wang retired in 1986, but he continued his research on Ranunculaceae, Boraginaceae, Urticaceae, and Gesneriaceae. From the early 1990s to the early 2000s, he visited several major herbaria abroad in Europe and United States, including BM, E, G, GH, K, LE, MHA, MO, NY, P, S, UPS, and US. He published 77 papers after he turned 85 years old, and only stopped his research quite recently in the spring of 2021 (e.g., Wang, 1993, 1994, 2000,  2002, 2003, 2004, 2006, 2014, 2016, 2018, 2019, 2020, 2021).

Professor Wang also contributed to the collaborative Flora of China project and treated Ranunculaceae (in collaboration with De-Zhi Fu and Liang-Qian Li) and Gesneriaceae (in collaboration with Kai-Yu Pan and Zhen-Yu Li). In 1996, he visited the United States National Herbarium (US) at the Smithsonian Institution, the Gray Herbarium of Harvard University (GH), the New York Botanical Garden (NY), and the Missouri Botanical Garden Herbarium (MO). During this trip, he completed the revision of Gesneriaceae for Flora of China with Dr. Laurence E. Skog (Smithsonian Institution) (Wang et al., 1998).

Beyond his taxonomic and floristic studies, Professor Wang published several important papers on distribution patterns and migration routes in the Eastern Asiatic Region (Wang, 1989, 1992). These papers have inspired many studies on eastern Asian biogeography (Wen et al., 2014; Nie et al., 2016; Liu et al., 2021; Mao et al., 2021; Zhang et al., 2022). The two volumes on vascular plants of the Hengduan Mountains that he edited (Wang et al., 1993, 1994) documented all the plants collected in this vast region based on specimens created by Chinese and western collectors. This was a major achievement at the time when herbarium collections were not easily available online or digitized. The completion of the two volumes set the foundation for systematic, biogeographic, and conservation work in this vast evolutionary hotspot in Asia.

Professor Wang trained numerous students and workers in plant taxonomy through his courses at the Chinese Academy of Sciences and many colleges, universities, and research institutes (Fig. 6). He was always humble, modest, and approachable, and taught many younger colleagues on plant taxonomy informally at the PE Herbarium (Fig. 7). He was well known for training the taxonomists in PE such as Professor De-Zhi Fu, Professor Liang-Qian Li, Professor Zhen-Yu Li, and numerous other students (Fig. 8).

Professor Wang joined the editorial board of Acta Phytotaxonomica Sinica (now JSE) in 1973. In May 1981, as the Deputy Editor-in-Chief, he chaired a standing board meeting to reach some important agreements for the journal, such as publishing research with significant academic value or innovation, soliciting high-quality manuscripts, and adopting a strict peer-review process, which have been implemented for the journal until today. He was the Editor-in-Chief of JSE from 1982 to 1988, and after leaving the position, he continued to serve the journal in various ways. In April 1995, he wrote to the editorial office to suggest that type specimens of new species should be deposited in a recognized herbarium that is committed to long-term maintenance. He helped revise and approve Latin description or diagnosis for some JSE authors even when he was in his 80s.

Professor Wang received numerous awards and honors, such as the most prestigious First Prize of National Natural Science Award of China twice (in 1987 and 2009) (Figs. 9, 10), the Qiu Shi Science & Technologies Foundation in 1996, and the Science and Technology Achievement Award from the Ho Leung Ho Lee Foundation in 1997. In 2018, Professor Wang was named the Lifetime Honorary Professor by the Institute of Botany, CAS. In 2019, he received the Commemorative Badge for Celebrating the 70th Anniversary of the Founding of the People′s Republic of China from the Chinese government.

To honor Professor Wang′s contributions to plant taxonomy, floristics, and eastern Asian biogeography and his efforts to train next-generation taxonomists, herein, we have selected 16 scientific papers recently published in JSE in the last 3 years on collections-based systematics to celebrate his life and legacy. The articles that we have selected showcase the advances in collections-based plant taxonomy, biogeography, and floristics in the new age of discovery (Wen et al., 2015, 2017; Funk, 2018).

Professor Wang dedicated his career to understanding of the flora of China. We present and discuss four papers that emphasize floristic diversity and assembly in Asia. Hu et al. (2020) provided an updated phylogenetic tree of Chinese vascular plants, generating a mega-phylogenetic tree with 15 092 tips and 14 878 species, including 13 663 species (44.0%) and 2953 genera (95.7%) that are native to China. Beyond the tremendous scientific value of the phylogenetic framework of the Chinese flora, the study also identified hotspots of phylogenetic diversity for the Chinese angiosperms at both the genus and species levels; hence, the paper is also of great conservation significance utilizing information of phylogenetic diversity. Xie et al. (2021) reviewed and analyzed the floristic data from The Species Catalogue of China: Volume 1: Plants (SCCP), a comprehensive inventory of Chinese higher plants. The database is freely accessible at: http://www.sp2000.org.cn/, and includes entries of 478 families, 4052 genera, and 41 687 specific and infraspecific taxa. Mao et al. (2021) reviewed the evolutionary origin of species diversity on the Qinghai-Tibetan Plateau (QTP), a well-known biodiversity hotspot in Asia. The authors discussed issues and advances on circumscribing and naming the QTP, the QTP uplifts, dating of molecular phylogenetic trees, and processes of species diversification and high-altitude adaptation. Low et al. (2021) used a phylogenetic framework of the tropical genus Typhonium s.s. of Araceae to reconstruct the biogeographic origin of the Asian paleotropical flora. Typhonium s.s. was inferred to have originated in Indochina during the early–middle Miocene and subsequent diversification within the genus may have been triggered by the intensification of the Asian monsoons around the middle Miocene. The study provides an important framework as well as a set of hypotheses for studying the origin and evolution of the Asian paleotropical floristic elements.

The tree of life or phylogenetics has become the foundation for classification and taxonomy (Wen et al., 2017). Phylogenetic systematics has progressed tremendously in the last decade with the additional sampling of characteristics (e.g., genomics) as well as taxa, especially with the collaboration of team colleagues (Zimmer & Wen, 2015). We have selected five papers to discuss the advances in phylogenetic systematics, especially in the realm of taxonomy and classification. Soreng et al. (2022) updated the worldwide phylogenetic classification of the large and economically important grass family Poaceae. This revised classification includes 12 subfamilies, 7 supertribes, 54 tribes, 5 supersubtribes, 109 subtribes, and an updated list of the number of species in each of the 787 accepted genera, setting the phylogenetic framework for the conservation and scientific investigations of the grass family. In another landmark paper, Larridon et al. (2021) used phylogenomic data based on target enrichment sequences in conjunction with morphology and other traditional sources of data to propose a classification of the large family Cyperaceae with new tribal rearrangements and re-circumscriptions. Roalson et al. (2021) re-evaluated the infrageneric classification of the large and taxonomically challenging genus Carex using a phylogenetic framework and organizing principles that will serve as a roadmap toward ongoing progress on Carex classification, to reflect the current state of our knowledge while progress is being made. The hybrid classification framework organized Carex into six subgenera, which were then classified into 62 sections plus 49 informal groups. Wang et al. (2021) used target enrichment phylogenomic data, and the species tree and species network approaches to infer the phylogeny of Caprifoliaceae. They also integrated evidence from divergence times and morphology, and described Zabelioideae as a new subfamily in Caprifoliaceae. Jiang et al. (2022) report a case study focused on assessment of the monotypic Pseudobartsia yunnanensis (Orobanchaceae), which is known from a single specimen. The authors obtained chloroplast genome and nuclear ribosome sequence data from the herbarium specimen collected in 1940, and the phylogenetic analyses of Orobanchaceae using plastomes support reinstatement of Pseudobartsia. The study showcases the importance of herbarium collections in today′s phylogenomic and biodiversity research.

Two papers that we have selected provided insights into species delimitations (Li et al., 2021; Lin et al., 2022). One of the major goals of systematics is to discover and describe species; yet, species delimitation has remained highly controversial due to phenotypic plasticity, an indistinguishable morphology, and complex hybridizations (Wiens, 2007; Wen et al., 2018; Hillis et al., 2021). Li et al. (2021) examined the cryptic diversity of the widespread Roscoea tibetica in the Hengduan Mountains using genotyping by sequencing, morphological traits, species distribution models, and simulating demographic history. Phylogenomic and genetic structure inferences supported two distinct lineages within R. tibetica, and the two lineages were also supported by several morphological characteristics discovered from field and common garden observations, as well as ecological divergence based on species distribution models. Phylogenomic, morphological, and ecological evidence was hence in support of two distinct species, but recent contact likely occurred between the two lineages. However, phenotypic plasticity in heterogeneous environments and morphological convergence in similar habitats complicated the variational patterns. Lin et al. (2022) explored the species delimitation of a species complex, the Stewartia sinensis complex (Theaceae), showing the continuum of phenotypic variations. They integrated data from phylogenomics, ecology, and morphology. The multispecies coalescent-based species delimitation using 572 nuclear orthologs based on anchored enrichment supported reciprocal (but not sister) monophyly of the northern lineage (NL) and the southern lineage (SL). Significant climatic niche differentiation was also detected between NL and SL populations, and species distribution modeling further supported their separation. Morphometric analyses also suggested significant differentiation of multiple traits. Hence, two distinct species were suggested: Stewartia gemmata for SL and S. sinensis for NL. The two studies highlight the importance of applying an integrative approach in assessing species delimitations in plants.

To honor Professor Wang′s contributions to biogeography, we have selected five recent papers that discussed the biogeographic origin and patterns in Asia and the Northern Hemisphere. Zhou et al. (2021) sequenced 20 single-copy nuclear genes and 14 chloroplast regions of all species in the genus Paeonia of Paeoniaceae to infer the phylogeny and biogeography and document the parents of tetraploids. Paeoniaceae was dated to the late Cretaceous and diverged into two clades, woody and herbaceous clades in the late Oligocene or early Miocene. They survived and diverged in the Pan-Himalaya, from where they migrated to eastern Asia and then further to Northwestern America, Middle Asia, and Europe. The glacial and interglacial cycles in Europe in the late Pliocene and early Pleistocene promoted polyploidy speciation including both allotetraploids and autotetraploids. Xu et al. (2021) used karst endemic genus Primulina as a model to identify hotspot areas in the Nanling Mountains in north Guangdong and northeast Guangxi and southeast Yungui Plateau in north and southwest Guangxi. The categorical analysis of neo- and paleoendemism suggested the karst areas in southern China as both “museums” and “cradles” of plant evolution that deserve conservation priority. Lu et al. (2021) supported the hypothesis that southern Japan–East China probably served as both the ancestral area and the diversification cradle for Carex sects. Confertiflorae and Molliculae. This study highlights the geographic heterogeneity and importance of eastern Asia for Carex diversification. Dong et al. (2022) utilized nuclear SNPs and plastome data to explore the phylogenetics of Magnolia and revealed extensive cytonuclear discordances. Their analyses also suggested hybridization events within sect. Yulania, and sect. Magnolia. Dating and biogeographic inferences suggested three tropical Magnolia disjunctions tracing to the mid to late Eocene, and two temperate disjunctions occurred much later in the Miocene, supporting the boreotropical flora hypothesis of Magnolia (Nie et al., 2008). Yao et al. (2021) constructed the biogeographic history of the holly genus, Ilex (Aquifoliaceae). Ilex was inferred to have originated in subtropical Asia and colonized South America by c. 30 million years ago (Ma), North America by 23 Ma, Australia by 8 Ma, Europe by 6 Ma, and Africa by 4 Ma, with South and North America colonized multiple times. The genus has used efficient seed dispersal mechanisms to rapidly colonize suitable mesic areas. The near-cosmopolitan distribution of the genus reflected the dynamic balance of dispersal, diversification, and extinction, and the significance of long-distance dispersal (Wen et al., 2013).

Professor Wang′s scientific achievements have been well known in the botanical community. Finally, we would like to share what was said about Professor Wang by one of his American friends Hayden Wetzel from Washington, DC: “he was the most delightful guest and friend—gentle, direct, always positive and helpful. Almost every evening when I came home he had prepared dinner (always the same beef dish, which was fine with me). When I was traveling for about a week he told me afterward that while I was gone the house seemed lonely and he always ate at a local Chinese restaurant. What a sweet guy! A few years later, when I visited Beijing, he showed up at my hotel every morning and took me around town, until he tired out in the late afternoon. I have the most fond and pleasant memories of this lovely man.”