Collections‐based systematics and biogeography in the 21st century: A tribute to Dr. Vicki Funk

Abstract

This special issue honors Dr. Vicki Ann Funk (26 November 1947–22 October 2019), who passed away after a battle with an aggressive cancer (Fig. 1). Dr. Funk was a Botanist at the Smithsonian Institution in 1981–2019. Vicki was an inspirational evolutionary biologist and a champion for collections-based systematics and biogeography (Funk, 2018). She quite literally changed the way we perform our collections-based systematics today, and she was consistently a driving force for positive change in botany and beyond. Vicki was one of the most active, enthusiastic, and passionate professional botanists of our time. She combined these qualities with a quick mind and glowing wit, always with new ideas or opinions that she was eager to share with anyone who would listen and be willing to enter an engaging dialog. During her distinguished career, Vicki achieved pre-eminence in the fields of phylogenetic methods, systematics, biogeography, and biodiversity conservation. She was a very active member and leader in several professional societies in systematics and biogeography. Her vision and leadership as well as her passion for mentoring the next generation have had a strong influence on the direction of botanical research and the career development of many colleagues. A detailed biography of Vicki was published recently by Wagner & Specht (2020), and her contributions to systematics and biogeography can also be found in the works of Wagner et al. (2019) and Gillespie & Whittaker (2020). Vicki pioneered the use of cladistics or phylogenetic theory in plant systematics in the late 1970s and the early 1980s (e.g., Funk & Stuessy, 1978; Funk, 1982, 1985a). She was one of the few botanists at the time who actively collaborated with leading zoologists in advocating new phylogenetic approaches in systematics (e.g., Funk & Brooks, 1981; Platnick & Funk, 1983; Wiley et al., 1991). She innovatively developed guidelines to detect hybridization events, which are common in plants, using phylogenetic patterns and extensive case studies (Funk, 1985b). She continued to extensively study the evolutionary diversification and classification of the Compositae using phylogenetics (e.g., Funk et al., 2005, 2009; Nie et al., 2013), and added next-generation phylogenomics to her tool box for phylogenetic systematics in the last few years (e.g., Mandel et al., 2015, 2017, 2019). Vicki was one of the world's leading experts on the systematics and biogeography of the sunflower family, Compositae, the largest family of flowering plants with more than 27 000 species, accounting for 10% of all angiosperm species. She started her career in Compositae at the Ohio State University with her dissertation research on the systematics of Montanoa Cerv. (Funk, 1982) under the direction of Tod Stuessy. In 1981, she spent a postdoctoral year at the New York Botanical Garden, where she studied Compositae systematics with Art Cronquist. During that time, Vicki spent 1 day a week at the American Museum of Natural History to develop her expertise and intellectual leadership among the cladistics community. In the subsequent 35 years, Vicki and her large network of collaborators across the globe generated numerous important studies on the systematics and evolution of this large, diverse, and ecologically important, and taxonomically difficult family. The spectacular Compositae book (Systematics, Evolution, and Biogeography of the Compositae) (Funk et al., 2009) is an outstanding example of Vicki's research and organizational skills, which represents the most extensive synthesis of the largest family of plants. The work won the prestigious Stebbins Medal from the International Association for Plant Taxonomy (IAPT) in 2010 (Fig. 2). In her office at the Smithsonian, Vicki was surrounded by all her favorite objects of Compositae plants (Fig. 3). Vicki was one of the founding members of the International Biogeography Society (IBS), and she also served as the President for IBS (Gillespie & Whittaker, 2020). Early in her career, she advocated innovative approaches for cladistic biogeographic analyses (Funk & Brooks, 1981; Funk, 1982; Platnick & Funk, 1983). In the early 1990s, Vicki teamed with Warren Wagner to organize a symposium for the Honolulu botany meetings that explored the utility of phylogenetics to understand the biogeographic patterns of the Hawaiian archipelago. The proceedings were published in the highly influential book Hawaiian Biogeography: Evolution on a Hot Spot Archipelago (Wagner & Funk, 1995). In this volume, Funk & Wagner (1995) articulated the famous progression rule for hotspot archipelagos: clades tend to inhabit older islands first and disperse to younger islands in the order that the islands appear. The large collection of papers in Wagner & Funk (1995) set the foundation for phylogenetic biogeographic research and inspired numerous subsequent studies on the Hawaiian archipelago, the Pacific, and island systems in general (Appelhans et al., 2018a, 2018b). On our expedition to Tibet in 2006 (Fig. 4), Vicki often discussed with the many young participants on the island-like systems on the vast Qinghai–Tibetan Plateau in Asia and inspired many phylogenetic biogeographic studies in that region (e.g., Baird et al., 2010; Wen et al., 2013, 2014; Nie et al., 2013, 2016; Zhang et al., 2019). Vicki was an exceptionally strong advocate for collections-based research (Funk et al., 1999; Funk & Richardson, 2002; Funk, 2004, 2006, 2017, 2018; Wen et al., 2015). She served as Director of the Biological Diversity of the Guiana Shield Biodiversity Program (BDG) for over 30 years and supported collection of diverse organisms from plants to birds, mammals, and insects from the region. Her BDG program was fundamental to document, understand, and conserve the biological diversity of the Guiana Shield area of northeastern South America. The program made more than 60,000 new collections and databased all those plus nearly 100,000 previously collected specimens (Kelloff et al., 2019). The collections and this database are extremely valuable for systematic and biogeographic studies and conservation efforts of a biodiversity-rich region. She made over 15,000 number of collections in her career and brought back important Compositae collections worldwide, especially from South America. She legendarily explored remote areas from the Death Valley to the Roof of the World and targeted her taxa like Bidens orofenensis M.L.Grant in Tahiti via a helicopter (see cover image, this issue). In the genomic era, Vicki was instrumental for establishing the Global Genome Initiative for Gardens (GGI-Gardens) in 2015 with the goal of fulfilling the GGI mission: to preserve and understand the genomic diversity of life on Earth—for the plant tree of life (Fig. 5). Vicki Funk was passionate about mentoring the next-generation biologists, and she mentored more than 40 undergraduate and graduate students and postdoctoral fellows, and inspired numerous interns, students, and visiting scientists through the Botany Department at the National Museum of Natural History at the Smithsonian. Vicki served numerous professional societies in leadership and various other roles. She was the President of the Society of Systematic Biologists in 1998–1999, American Society of Plant Taxonomists 2006–2007, the International Biogeography Society in 2007–2009, the Botanical Society of Washington in 2014, and the International Association of Plant Taxonomists from 2011 to 2017. Vicki received many honors and awards recognizing her achievements in systematics, evolutionary biology, and biogeography. For example, in addition to the Stebbins Medal from IAPT, she was awarded the Rolf Dahlgren Prize in 2014 for her contributions to the systematics and evolution of the flowering plants. In 2018, she won the prestigious Asa Gray Award, the highest honor bestowed to an individual from the American Society of Plant Taxonomists (ASPT). ASPT also established the named Vicki Funk Graduate Student Research Award in her honor at the 2019 Botany Meetings in Tucson, Arizona. Also, in 2019, the Linnean Society of London recognized Vicki with its Linnean Medal for lifetime service to the natural sciences. For this special issue, we invited a broad group of scientists to explore the advances of collections-based systematics and biogeography in the 21st century, to pay tribute to a true leader in our field. We emphasize four major areas that Vicki was passionate about and made significant contributions: Pacific biogeography, statistical phylogenetic biogeography, systematics and evolution of the Compositae (Asteraceae), and collections-based phylogenetic systematics. Three papers in this special issue emphasize plant evolution on oceanic islands. Stuessy (2020) has reviewed the evolutionary processes in plants of oceanic islands (ontogeny of the islands, population divergence, speciation, and hybridization) and argues that the present patterns of distribution and ecology of species within endemic groups may have little to do with the patterns when the species originated. Thus, understanding these environmental changes is fundamental to infer processes such as founder effect and modes of speciation, with case studies from the Juan Fernández Archipelago and Lord Howe Island. Knope et al. (2020) have explored the radiation of the genus Bidens in the Pacific. Although Bidens is confirmed to be polyphyletic within Coreopsis, the Polynesian Bidens is inferred to be monophyletic, and this morphologically diverse clade has most likely radiated from an ancestor in South America. The initial colonization of the Pacific was either to the Marquesas (43% probability) or the Hawaiian Islands (39% probability). The crown group in the Pacific is estimated to have occurred ~1.63 million years ago (Ma), the youngest and most rapid plant diversification events documented in the Pacific. Within the Pacific, each of the Marquesan and Hawaiian radiations was the result of single colonization events, with the Hawaiian radiation being monophyletic and the Marquesan radiation being paraphyletic with respect to the Society Islands radiation. From the Marquesas, Bidens dispersed to the Society Islands and then to the Austral Islands. The study showcases that relatively rare long-distance dispersal and founder event speciation, coupled with subsequent loss of dispersal potential and within-island speciation, can lead to the repeated, complex, and explosive adaptive radiation of Bidens across the archipelagoes of Polynesia. On the basis of the RADseq data, Appelhans et al. (2020) have reconstructed the Hawaiian radiation of Myrsine L. of the primrose family (Primulaceae), the only one of the ten most species-rich Hawaiian plant lineages that has never been studied in a phylogenetic analysis. Myrsine is likely paraphyletic with the monotypic Macaronesian genera Heberdenia and Pleiomeris nested within it, and the Hawaiian Myrsine is supported to be monophyletic. Hawaiian Myrsine includes three main lineages: one of which contains the majority of species mainly from Kauaʻi and the other two lineages are the few widespread species. Quartet Sampling and HyDe analyses further suggest phylogenetic incongruence throughout the phylogeny and provide evidence of extensive hybridization in the lineage (also see Kleinkopf et al., 2019). Four papers showcase the power of phylogenetics in inferring classical biogeographic patterns. Echeverría-Londoño et al. (2020) have explored the diversification patterns of another major plant radiation in the megadiverse genus Solanum L. (c. 1200 species, Solanaceae). Despite the vast diversity of Solanum lineages in the Neotropics, the Old World lineages are inferred to have diversified more rapidly, with the recent increase in diversification coinciding with a long-distance dispersal event from the Neotropics to regions with active major climatic changes. Two groups of Solanum migrated to Australia independently, with the arid-adapted lineages experiencing significant increases in the diversification rate, as they adapted to the long-term climatic trend toward seasonally dry and arid biomes there. This study represents an excellent case study showing how successful colonization of new areas and niches can drive explosive plant diversifications. Zhu et al. (2020) have conducted a phylogenetic biogeographic analysis on the genus Celastrus L. (c. 30 species, Celastraceae) with a wide disjunct distribution in five continents of both hemispheres. The diversification of Celastrus is suggested to be linked to global warming events during the Miocene. The genus is inferred to have originated in tropical Asia and then dispersed to Central and South America, North America, Oceania, and Madagascar at different time periods via long-distance dispersals. Birds may have facilitated transoceanic migrations of Celastrus, due to its bicolored fruits, which contain red and fleshy arils, highlighting the importance of key morphological innovations and animal-mediated dispersals for the rapid diversification of plant lineages across vast distributional ranges. Zhang et al. (2020) have constructed the origin and diversification of Saxifraga L. sect. Irregulares Haw. (c. 15–20 species, Saxifragaceae), one of the early-diverged lineages in the genus. The results corroborate the monophyly of sect. Irregulares and its sister relationship to sect. Heterisia from North America. Divergence time estimates and ancestral area analysis suggest a western North American origin of sect. Irregulares with migration into eastern Asia via the Bering land bridge (Graham, 2018) in the middle Oligocene. The development of desert belt in the late Miocene is hypothesized to be important in the subsequent divergence of the north and south lineages within eastern Asia, supporting an emerging important biogeographic pattern in Asia. Wang et al. (2020) have tackled another classical biogeographic pattern in eastern Asia—the Sino-Japanese disjunctions in Diabelia Landrein (four species, Caprifoliaceae; Linnaeoideae). The species diversification within Diabelia dated back to the middle Oligocene, and phylogenomic analysis of the plastomes supported two independent vicariance events leading to the disjunction between Japan and Korea in the middle-to-late Miocene and between eastern China (Zhejiang) and Japan in the early Miocene. Five papers are included in memory of Vicki's important contributions to Compositae systematics and evolution. Watson et al. (2020) have analyzed five closely related tribes of Compositae (Anthemideae, Astereae, Calenduleae, Gnaphalieae, and Senecioneae), which represent over 10 000 species. These tribes form one of the two megadiverse clades within subfamily Asteroideae. Sampling both the nuclear and plastid genomes via the HybSeq approach (Zimmer & Wen, 2015), Watson et al. (2020) have found both concordance and conflicting support in both data sets and documented four ancient hybridization events. With the timing of the early radiation of this five-tribe lineage dated to be shortly before the Eocene–Oligocene extinction event (c. 34 Ma), early lineages were likely lost, hence obscuring the details of their early diversification history. Ackerfield et al. (2020) have tackled the phylogeny of the thistle genus (Cirsium L.), one of the most taxonomically challenging groups of Compositae in North America. This first phylogenetic attempt of the North American thistles suggests that the messy difficulties within Cirsium may be due to (i) previously undescribed taxa, (ii) inadequate representation of taxa from herbarium specimens, (iii) phenotypic convergence, (iv) hybridization, and (v) incipient speciation. Using a phylogenomic approach, Lichter-Marck et al. (2020) have analyzed the rock daisy tribe Perityleae, consisting of seven genera, most of the c. 84 taxa narrowly endemic on rock cliffs throughout the southwest United States and northern Mexico. Discordance between sources of molecular data supports hybridization events in Perityleae. Phylogenies reject the monophyly of the most species-rich genus Perityle Benth. and several of its sections. Pappus elements show a high level of homoplasy, and flower color is found to be conserved. A base chromosome number of x = 18 is suggested to give rise to lower base numbers in subtribe Peritylinae (x = 12, 13, 16, 17, and 19) via descending dysploidization. Most taxa constitute a clade with a base chromosome number of x = 17, but with many polyploidization events inferred. Using a new progenitor-specific amplicon sequencing method, Wan et al. (2020) have tested the hypothesis that allopolyploidization between the same two parental species has led to the origin of two different yarrow species, Achillea alpina L. and A. wilsoniana Heimerl ex Hand.-Mazz., from the same diploid progenitor species pair, A. acuminata (Ledeb.) Sch. Bip. and A. asiatica Serg. On the basis of the sequences of 17 nuclear genes from 21 wild populations of the four Achillea species investigated, this study supports independent allopolyploidy events between the same Achillea parental species that gave rise to two genetically and ecologically distinct taxa. Approximate Bayesian computation suggested that both tetraploid species originated before the Last Glacial Maximum and nearly all diploid lineages went through population declines after the allopolyploidization events. Ma et al. (2020) have explored the origins of cultivated chrysanthemums using chloroplast genomes and the nuclear LEAFY gene. Several wild species of Chrysanthemum L., for example, C. indicum L., C. zawadskii Herbich, C. dichrum (C.Shih) H.Ohashi & Yonek., C. nankingense Hand.-Mazz., C. argyrophyllum Ling, and C. vestitum (Hemsl.) Stapl, were likely directly or indirectly involved as paternal species of most of the chrysanthemum cultivars examined in this study. Yet, the maternal species is supported to be a lineage of an extinct wild Chrysanthemum species and its subsequent cultivars, as all accessions of chrysanthemum cultivars sampled formed a strongly supported clade, distinct from all other species of Chrysanthemum in the plastome tree. Thus, the results support that the spectacular chrysanthemum cultivars originated from multiple hybridizations involving several paternal species rather than only two or a few wild species, with an extinct species and its subsequent cultivars serving as the maternal parents. Phylogenetic systematics has progressed tremendously in the last decade with the additional sampling of characters as well as taxa. DiMichele & Bateman (2020) have updated the reconstruction of the Carboniferous tree-clubmoss Paralycopodites Morey & Morey from disarticulated, anatomically preserved fossils to determine its phylogenetic position and to infer the developmental biology that dictated its remarkable architecture. Their biological and taxonomic conclusions on the phylogenetically basalmost member of the Carboniferous stigmarian lycopsids can be expanded to encompass the more widespread compression mode of plant preservation. Considering that the recently published Pteridophyte Phylogeny Group classification (PPG I, 2016) did not include intergeneric hybrids (nothogenera), Liu et al. (2020) have provided an evaluation of previously proposed nothogenera in the context of a current phylogeny-based pteridophyte classification. They also explore the distribution of nothospecies across the pteridophyte phylogeny. Their results support future efforts to better report and study hybrids in ferns and lycophytes, especially in biodiversity-rich areas. Spooner et al. (2020) have compared next-generation sequencing results of the same accessions of the carrot genus Daucus L. with different genomic regions: (i) the entire plastid genome, (ii) 47 mitochondrial genes, (iii) 94 conserved nuclear orthologs, and (iv) 564 895 nuclear SNPs. Extensive data discordance is detected in all four results using the same accessions analyzed with maximum parsimony, maximum likelihood, and with the nuclear data species trees through a coalescent analysis. The nuclear results show significant areas of discordance as well. The results, thus, raise questions concerning the best data and analytical methods to reconstruct and understand the “true” phylogeny. Thode et al. (2020) have evaluated character partitioning and molecular models in plastid phylogenomics using Amphilophium Kunth (Bignoniaceae) as a case study. They detected incongruences in recovered phylogenetic relationships mainly located in short internodes. They suggest that the selection of appropriate partition strategies and evolutionary models is important to increase accuracy in phylogenetic relationships, even when using plastome data sets. Welker et al. (2020) have proposed a new phylogenetic classification of the grass tribe Andropogoneae Dumort. (14 subtribes, 92 genera, and c. 1224 species), which includes several important crops such as maize, sugarcane, and sorghum, and dominates the tropical grasslands of the world. Their dated phylogeny suggests that Andropogoneae diverged from Arundinelleae in the early Miocene, and the “core Andropogoneae” clade is dated to the late Miocene. The tribe was inferred to have originated in eastern Asia, with many independent dispersal events to Africa and the New World. Soreng et al. (2020) have presented a nuclear ribosomal DNA phylogeny of the grass genus Poa L., characterized the breeding systems and morphology for several species of Poa sect. Nivicolae (Roshev.) Prob., and assessed the taxonomy of these poorly understood taxa in the section. Rabarijaona et al. (2020) have revisited the phylogeny and divergences of Cayratia Juss. of Vitaceae and its close relatives in tribe Cayratieae J.Wen & L.M.Lu (Wen et al., 2018), and for the first time broadly sampled the taxa from Africa and Madagascar. On the basis of the new phylogenetic evidence, the authors have proposed a new genus, Afrocayratia J.Wen, L.M.Lu, Rabarijaona & Z.D.Chen from Africa and Madagascar and have provided a taxonomic revision for the genus. The untimely passing of Dr. Vicki Funk was a big loss to the entire systematics, biogeography, and biodiversity science community. Vicki was a dear friend to both of us, and organizing this special issue was a very emotional process for us. We hope that the collection of papers in the special issue will help inspire many colleagues in carrying on the Vicki Funk spirit to promote collections-based systematics, biogeography, and biodiversity science in the 21st Century (Funk, 2018).